i i ili

Dynamic disequilibrium of t eterrestriaE carbon cycme underglobal changeYiqi Luo and Ensheng Weng

Department of Botany and Microbiology, University of Oklahoma, OK 73019, USA

In this review, we propose a new framework, dynamicdisequilibrium of the carbon cycles, to assess future landcarbon-sink dynamics. The framework recognizes inter-nal ecosystem processes that drive the carbon cycle to-ward equilibrium, such as donor pool-dominated transfer;and external forces that create disequilibrium, such asdisturbances and global change. Dynamic disequilibriumwithin one disturbance-recovery episode causes tempo-ral changes in the carbon source and sink at yearly anddecadal scales, but has no impacts on longer-term carbonsequestration unless disturbance regimes shift. Suchshifts can result in long-term regional carbon loss or gainand be quantified by stochastic statistics for use in prog-nostic modeling. If the regime shifts result in ecosystemstate changes in regions with large carbon reserves atrisk, the global carbon cycle might be destabilized.

thus diminish the C sink over time. Disturbances createdisequilibrium in the C cycle by both individual events andregime shifts. Global change affects both internal process-es and disturbances, potentially leading to complex systemdynamics. Among all types of dynamic disequilibrimncreated by disturbances and global change, the statechange in the C cycle could potentially have the mostprofound impacts on future terrestrial C sink stability.

The need for a unified concept for carbon researchNearly 30% of carbon (C) released by anthropogenic activi-ties has been sequestered by terrestrial ecosystems duringa period in which fbssil-fuel COs emissions increased from2.4 Pg C per year in 1960 to 8.7 Pg C per year in 2008 [1-3].These figures suggest that the rate of land C sequestrationhas accelerated over time. Recent research has identifiedvarious causes of future instability of the land C sink inresponse to global change. For exmnple, it is suggested thatfbrest dieback would trigger a massive C release fi-omAmazonian forests [4], As permafl'ost regions store signifi-cant amounts of C [5], climate warming could also acceler-ate the release of old C stored in such regions [61. Inaddition, disturbances such as fires [7], storms [8], insectoutbreaks [9] and land-use change [10,11] have been esti-mated by many researchers to release huge amounts of'C.

These processes and events have to be evaluated in acohesive li'amework to guide thture research into thestability of terrestrial C storage.

In ÿhis review, we develop a conceptual fi'amework,dynmnic diseqnilibrimn of C cyetes, to gain insights intoterrestrial C sink dynmnics. We first define the dynamicdisequilibrium framework based on two opposite forces: (i)internal ecosystem processes; and (ii) external forcingvariables; and then examine each of the tba'ee major ele-meats of the fi'amework (internal processes, disturbancesand global change). We fbcus on the properties of internalprocesses that gÿ'adually equalize C efttux to influx and

Correspÿmdlnguuthor: Luo, Y, (yluo{!Vuu.edu/.

The dynamic disequilibrium of C cyclingWe propose the dynamic disequilibrium as a central con-eept to quantify the C sink and assess its stability inresponse to global change (Box 1). The dynamic disequilib-rium fl-amework is built upon two opposing forces: theinternal equilibration processes versus external forcingvariables, which act against each other to maintaindynamic disequilibrium. The internal processes involveorganic C metabolism fl-om photosynthetic fixation torespiratory releases by plants, animals and microbes. Theyinclude C transfers among pools and the growth anddecomposition of litter and soil organic matter. The exter-nal fbrcing variables include both disturbances and globalchanges. Disturbances include anthropogenic land use andland-use change (e.g. forest cleaning, urbanization, crop-

ping, pasture management and forestry), natural events(e.g. insect outbreaks, fire and volcanic eruptions) andextreme weather conditions (e.g. floods, droughts andstorms). Global change includes increasing atmosphm'ic[CQ], climate warming, altered precipitation, nitrogen (N)deposition and plant invasion.

External forcing variables influence internal C processesto create dynamic disequilibrium in several ways (Table 1).Some disturbances (e.g. clearing hmwests and fires), forexample, result in reduced C stocks in plant and soil pools(Figure 1). Other disturbances, sudl as hm'ricanes andinsect outbreaks, increase the C stock in litter pools, butdecrease it in plant pools [8,91. All of these disturbancescause C eyc]ing at disequilibrium, from which the internalprocesses facilitate ecosystem recoveW toward equilibrium.After the distm'bances, the plant canopy is usually restoredwithin a few years and so the plant biomass pool sizegradually increases. C pool sizes in the litter and soil mightinitially decline tbllowing a disturbance, but then increaseover time to a level of' stabilized equilibrium [12]. Stonedistttrbances, such as invasive species, can change theecosystem structure, enhance C influx and increase poolsizes [13].

96 0169-5347/$ see front matter © 2010 Elsevier Ltd. All rights reserved, doi:lO,1016/].tree.2010.11.003 Trends in Ecology and Evolution, February 2011, VoL 26, No. 2

Trends in Ecology and Evolution February 2011, Vol. 26, No. 2

ox 1. Elements and predictions of the dynamicdisequilibrium framework

tÿlements

,ÿ C sequestration (or release) occurs only when the C influx is larger(or smaller) than the C effiux (i.e. there is disequilibrium).

• , Ecosystems have internal processes that, without disturbances

and global changes, gradually equalize C effiux to influx and thusdiminish the C sink or source over time to reach equilibrium (i.e.recovery force).

o External forces, such as disturbances and global change, create

disequilibrium by altering internal C processes and pool sizes.,,, The internal C processes and external forces are opposite and act

against each other to maintain dynamic disequilibrium.

Predictions

Global change affects both internal C processes andexternal disturbance regimes, inducing dynamic disequi-librium. Climate warming, for example, can not onlyaccelerate the microbial decomposition of litter and soilorganic C [14], but also alter fire regimes [151. Changesin precipitation not only affect plant gÿ'owth [16], butcan also be conducive to fire and insect outbreaks [9].Thus, global change can induce dynamic disequilibriumvia direct effects on internal C processes or indirectlyvia altered disturbance regimes. In short, the dynamicdisequilibrium concept refers to a time-variant magni-tude of the C-cycle disequilibrimn. While the disequilib-rium is created by disturbances and global change,its varying magnitude with time is driven by internalC processes.

• , Disturbance causes temporal changes in the C sink and source

within one disturbance-recovery episode, but has no impact on

long-term C sink dynamics unless its regime changes.o The realizable C storage is smaller than the equilibrium level when

disturbances occur frequently enough to prevent the ecosystem

from recovering fully under a prevailing regime (Figure 2d-f).,p Ecosystem C storage capacity decreases if global change and

disturbance reduce canopy photosynthetic C influx and residencetimes, and vice versa.

,, Terrestrial C storage capacity decreases, leading to positive

feedback on climate change, if climate change causes more

frequent, severe and extensive disturbances.

,, Instability of the terrestrial C sink becomes globally significantwhen global change and disturbances trigger state changes inregions where vast C reserves are at risk.

Internal processes driving ecosystem C cyclestowards equilibriumThe C cycle in an ecosystem is usually initiated whenplants fix COs via photosynthesis. Photosynthate is usedpartially fbr plant growth and partially for plant respira-tion, releasing COs to the atmosphere. Plant tissues canlive for several months (e.g. leaves and fine roots) up tohundreds of years (e.g. wood). Dead plant material (i.e.litter) is partially decomposed by microbes to release COsand partially incorporated into soil organic matter (SOM).SOM can store C in the soil Cor up to hundreds or thousandsof years before it is oxidized [17,18]. This C cycle in an

Table 1. Applications of the dynamic disequilibrium concept to assess properties of C sink dynamics in five casesCase Equilibrium DisequilibriumEcosystem Annual averages of C influx Diel and seasonal imbalancesover 1 day and efflux are balanced unless of C influx and effiux areand 1 year the ecosystem is at driven by cyclic

disequilibrium owing to environmental changedisturbance or global change

Globalchange

Ecosystem

within onedisturbance-

recovery

episode

Regions withmultipledislurbances

over time

An original equilibrium can bedefined at a reference

condition (e.g. pre-industrial

[C02]) and a new equilibriumat the given set of changedconditions

Multiplestates

C cycle is at equilibrium if theecosystem fully recovers aftera disturbance. The

equilibrium C storage equalsthe product of C influx andresidence time

C cycle is at dynamicequilibrium in a region whenthe disturbance regime does

not shift (i.e. is stationary).The realizable C storage under

a stationary regime is smaller

than that at the equilibriumlevel (Figure 2d-f, main text)

C cycle can be at equilibriumat the org na and alternative

states

Dynamic disequilibriumoccurs as the C cycle shiftsfrom the original to a newequilibrium. Global changefactors gradually alter over

time, leading to continuousdynamic disequilibrium

C cycle is at dynamicdisequilibrium and anecosystem sequesters or

releases C before theecosystem fully recovers tothe equilibrium level

C cycle is at dynamicdisequilibrium and the regionsequesters or releases C when

the disturbance regime in theregion shifts (i.e. is non-

stationary)

Dynamic disequilibriumoccurs as an ecosystemchanges from the original toalternative states

Methods of quantificationDiel and seasonal imbalancesof C influx and efftux cangenerally be simulatedsuccessfully by modelswithout changes inparameterization

Direct effects of global changeon the C cycle can be modeledvia environmental scalars to

estimate dynamicdisequilibrium explicitly

C sequestration or release

under dynamic disequilibriumcan be fully quantified bythree sets of parameters

reÿated to C influx, residencetime and initial pool size

Disturbance regime shifts canbe characterized by a jointprobability distribution ofdisturbance frequency and

severity over space and time.

The joint distribution can becombined with C cycle modelsto estimate regional C sink

dynamics over time

State changes usually resultfrom changed ecosystem

structures to require changes

in structures and parameters

of C models

NoteNo need to apply the dynamicdisequilibrium concept forunderstanding diel andseasonal dynamics of

the C cycle

Dynamic disequilibriumdiminishes with acclimationand adaptation, but amplifieswith changes in ecosystemstructure to new states of the

C cycle

Data assimilation and othertechniques are needed toestimate the three sets of

parameters simultaneously

Single disturbance events

offer no information on

regional C sequestration.

Probability distribution canbe used for prognostic C

modeling by generatingstochastic forcings of

disturbance

State changes can be themajor mechanisms forinstability of futureterrestrial C storage

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(b)

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TRENDS in Ecology & Evoh,'lÿotÿ

Figure 1. Tire forces shaping the dynamic disequilibrium of C cycling. (a) Disturbances usually create disequilibrium by: either depleting or adding C to plant, litter and soilpools; changing plrotosynthetic capacity; and altering residence times. Internal ecosystem processes, such as donor pool-dominated transfer, drive the recovery of theecosystem towards equilibrium. The rate of recovery is determined by the photosynthetic capacity and C residence time. (b) Changes in the recovery trajectory if globalchange alters C influx and residence time. If elevated C02 increases photosynthetic C influx or residence time, for example, ecosystem C content might recover to a newequilibriurn level (red dashed lines) that is higher than the original equilibrium level (black dashed line). If climate warming increases decomposition and decreases the Cresidence time or reduced precipitation decreases C influx, ecosystem C content might recover to an equilibrium lever that is lower (red dashed tina) than the original. (c)State changes of the ecosystem C cycle, which are determined by hydroclimate condition and triggered by disturbance or restoration. When global change and humanactivities substantially alter hydroclimate condition in a region, the ecosystem C cycle might change from a stable to an unstable state or vice versa. Along the moisturegradient in the USA, for example, ecosystems change from a relatively stable state of forest in the east to multiple states on the Great Plains to another relatively stable state ofdesert in the west. If climate change causes shifts in precipitation regimes, boundaries move between the relatively stable and unstable states of ecosystems. Fluman activities interms of fire suppression have resulted in state changes from grasslands to woodlands on the Great Plains. Restoration of natural fire can reverse the state change.

ecosystem can be mathematically expressed [19] byEqnathm 1:

{ d_,ÿ__ ÿ(t)AX(t) -t- BUtt) (1)X(O) =- Xg

where X(t) is the C pool size,A is the C trans['er matrix, Uisthe photosyilthetic input, B is a vector of partitioningcoefficients, X(O) is the initial value of' the C pool andis an etwironmental scalar. Equation 1 adequatelydescribes most observed C processes, such as litter decom-position [20,21] and soil C dynamics, and has been repre-

sented in most ecosystem models [22,23] as well as beingintegrated into Earth system models [4,24].

The C cycle can be characterized by five properties(Box 2), of which the donor pool-dominated transfer is themost hmdamental mechanism that drives C processestowards equilibrium. (In compmqson, prey and predatorpopulations are each regulated by both donor and recipientpopulations, causing complex d)mamics of a predation sys-tem [25].) The equilibration mechanism of the C cycle wasoriginally described by Odum [26] and can be verifiedby using mathematical anMysis and empirical eÿddence.Mathematically, Equation I satisfies the Lyapunov stability

Box 2, Properties of the internal C processes of an ecosystem

• Photosynthesis as the primary pathway of C entering an ecosystemand described by parameter U in Equation 1 {main text}.

., Compartmentalization with clear physical boundaries of differentpools of C in leaf, root, wood, litter and soil. Soil C has been further

compartmentalized into a few conceptual pools in some models to

describe adequately its short- and long-term dynamics. Pools are

represented by vector X(t) with their initial values by X(0) inEquation 1 (main text}.

. Partitioning of C from photosynthesis to various pools as described

by vector B for plant C partitioning and matrix A for C transferamong plant, litter and soil pools (Equation 1, main text}. Each of

the pools has a different residence time, which is the inverse of itstransfer coefficient (i.e. the diagonal element of A). The capacity of

an ecosystem to sequester C is higher if more C is partitioned to

pools with long residence times, such as wood and soil.

• Donor pool-dominated C transfers. C transfer from a plant to litter

pool, for example, is dominated by the amount of C in the plantpool and not the litter pool. In this transfer, the plant is a donor,

whereas the litter pool is a recipient. Although SOM decomposilionis mediated primarily by microorganisms [98,99], C transfer amongsoil pools can be modeled effectively in proportion to donor-poolsizes and not to recipient pool sizes.

• The first-order decay of litter and SOM to release CO2. A first-order

decay function as described by the first term on the right side ofEquation I (main text) can adequately describe the mass remainingof litter with time lapsed based on data from litter decompositionstudies, and SQM decomposition from soil incubation experiments.

The combined property of the donor pool-dominated transfers and

first-order decay function is the fundamental mechanism that drives

the C cycle toward equilibrium.

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Trends in Ecology and Evolution February 2011, Vol. 26, No. 2

conditions with negative eigenvalues of the C transfer ma-trix A linearized near the equilibrinm [271 see supplemen-tary matmdal ratline). Empirically, many studies haveshown that C stocks in plant and soil pools recover towardsequilibrium during secondary forest succession and grass-land restoration following disturbances [28,29].

At equilibrium, C influx equals efflux, C pools are stabi-lized without any thrther change and the net ecosystem Cexchange becomes zero (i.e. there is no C sink or source). Theequilibrated size of C storage in an ecosystem equals theproduct of C influx and residence time [19]. C infltux at theecosystem scale is equals to canopy photosynthesis. Theecosystem residence time of C is determined by partitioningcoefficients in vector b and the transfbr matrixA of Equation1 [30[. A tropical fbrest, for example, has longer residencetimes, and thus a larger C sink capacity, than does a tropicalsavanna, even though both have high C influx. By contrast,C pool sizes in tundra soil are large prinÿarily because Cresidence times in these regions are long [5,6].

When the C pool size is smaller than the equilibriumsize, respiratory CO2 release is less than the photosynthet-ic influx, leading to C sequestration and an increase in theC pool size over time. When the C pool size is larger thanthe equilibÿdum pool size, the ecosystem becomes a net Csource and the pool size diminishes over time, towardequilibrium. This dynamic disequilibrium can be quanti-fied by three sets of parameters related to: (i) C influx; (if) Cresidence time; and (iii) the initial pool size (Figure 2a-e).Traditionally, C cycle models were spun up to equilibriumbefore being used to study C sequestration in response toglobal change [25]. Such an assumption on equilibrium

could result in major discrepancies between obseÿ-ced andmodeled C fluxes and pools [31]. Recently, data assimila-tion techniques have been used to estimate all three sets ofparameters to account for disequilibrium [32].

At least three aspects of'the internal C processes can beaffgcted by disturbance and global change: (i) the pool sizesaltered by disturbances; (if) the equilibrinm levels of Cstorage altered by global change; and (iii) ecosystem struc-ture changed to different states of the C cycle (Table 1).For example, fire depletes C in plant and litter pools butmight not affect the equilibrium level of C storage. Thus,fire effects can be modeled by resetting initial pool sizeswithout changes in parameters related to C influx andresidence time. Increasing atmospheric [COd increasesC influx so that the equilibrium C storage increases(Figure lb). Clfinate warming might increase decomposi-tion and decrease residence time so that the equilibrium Cstorage decreases. Most models have environmental sca-

lars to simulate these direct effects of global change on Cprocesses. If global change and disturbances result inchanges in vegetation structure and soil properties, thestate of the C cycle also might have changed. The C statechange can be simulated by adjusting the parametervalues in and modifying model structures of Equation 1.

Disturbances leading to disequilibriumAn ecosystem is subject to natural and anthropogenic dis-turbances, causing ecosystem C cycling processes to be atdisequilibrium. Disturbances create disequilibrium of the Ccycle by: (i) either depleting or adding C in pools; (if) eitherdecreasing or increasing canopy photos3mthesis; and (iii)

Eo

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2010

0

(d)

,,;, , ',, .

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TRENDS In Ecolo,gy ÿ£ Evolution

Figure 2. Simulated rate of C sequestration as affected by initial values of pool sizes (a), C influx (b), C residence time (e) and ecosystem C storage under disturbance frequencof once every 10 (d), 40 (e) and 400 (f) years. The simulation was performed by using an eight-pool model with three levels of initial ecosystem C content, C influx and residencetime. The baseline values of these parameters were 6.80 Kg C m 2, 1.23 Kg C m 2 per year and 34.7 years, respectively. These values were obtainer/from an inverse analysis ofdata collected at the Duke Forest Free Air Free-Air CO2 Enrichment site [28]. The baseline results are indicated by solid lines of (a-c), whereas the dotted and dashed lines indicatesimulation results with low and higlr values of the three parameters, respectively. The low and high initial pool sizes were zero and five times of the base value, respectively, Thelow and high C influx and residence time were 40% lower and higher than the base values, respectively. Tile disturbance events were assumed to be Poisson events and toremove all biomass. The 20 dark-yellow lines in (d-f) are individual simulations of the eight-pool model with the baseline parameter values, whereas the red lines are the mean of200 simulations. The figure shows that the realizable C storage in an ecosystem decreases with increasing disturbance frequency.

99

Trends in Ecology and Evolution February 2011, Vol. 26, No. 2

altering C residence times via changes in respiration anddecomposition. Each disturbance creates disequilibrium ata different magnitude, spatial scale and frequency.

Land use and land-use changeOf' all types of disturbance, land use is probably mostsignificant in its eftbct because it affects the C cycle inat least two ways, through land-use change and continu-ous land use. Land-use change converts forests and

native grasslands to croplands, pastures and urbanareas. Conversion of tbrests not only results in the re-lease of C to the atmosphere, but also shortens the Cresidence time owing to the elimination of C pools inplant wood biomass and coarse wood debris, and thephysical disturbance of long-term soil C pools [33]. Inthe case of urban development in forests, canopy photo-synttmsis is all but stopped and no C flows into imper-meable areas. Conversion of native grasslands leads toreduced C residence times in soil pools when the land isplowed. Continuous use afÿer land conversion disturbsthe C cycle on a regular basis. For exmnple, in annualcropping systems with tillage, soil is disturbed at leastonce a year. In commercial plantations, forests are usu-

all), harvested once every 10-20 )Tears. Once the land isreleased fi'om human use, the C storage capacity usuallyrecovers. For example, grassland restoration in NorthAmerica increased C storage by 43 g C m 2.per yearduring the first 26 years [291.

Spatially, humans use nearly 50% of the land surface of'the Earth and 23% of net primary production for agricul-ture and domestic animal grazing [10,341. From 1850 to2000, land-use conversion resulted in net C emissions thataccounted for ÿ35% of the total global anthropogenicemissions [11,35]. Currently, human land-use activitiesresult in a net release of 1-2 Pg C per year to the atmo-sphere Ii1]. By contrast, relbrestation, recovery and im-proved management of fbrests and croplands result in Csequestration 136].

ed 374 000 km2 of western North/Mnerican forest killedtrees and transferred C to litter pools, releasing C overtens of years [91. Tornados, volcanic m'uptions and floodsall result in tree mortality and, therefore, release C [41].A Era'ape-wide drought during 2003 resulted in a stronganomalous net release of COs to the atmosphere [42].Drought has also increased tree mortality (and thusdecreased C residence times) in the USA and Amazon[43,44].

Disturbance regimeDisturbances occur at different fi'equencies with varyingseverity on diverse spatial scales in different regions. Forexample, fire disturbs the land C cycle relatively fi'equentlyin dry regions, but rarely occurs in wet regions [451.Repeated distm'bances not only affect C cycles duringthe events themselves, but also substantially reduce therealizable capacity of an ecosystem to store C owing to theshort recovery time [46,47]. Indeed, the realizable C stor-age is lower than the potential capacity at the equilibriumlevel as the disturbance fi-equency and severity increases(Figure 2d-f). Thus, it is crucial to quantify the nonstatio-narity of disturbance regimes to estimate a regional C sinkcapacity. To this end, satellite data have been used todescribe land-use patterns, fire regimes and other distur-bances [48,491. Eddy flux towers [50], forest inventm%s[51] and long-term observations [521 have been used tomeasure disturbance effects on C processes.

Other disturbancesOther episodic events, such as windstorms or insect epi-demics, occur on a less extensive spatial scale than do firesand anthropogenic land use. Windstorms and insect out-breaks both reduce canopy photosynthesis and transfer Cfl'om plant to litter pools. Hurricane Katrina in the Gulf ofMexico in 2005 transtb.rred C fi'om trees so that theybecame a net source ofÿ0.1 Pg C in the years that fbllowed18,401. A pine beetle epidemic that occurred in an estimat-

re

Fire bm'ns live and dead plants, litter, and sometimes C inthe top soil layers, resulting in the removal of C from thesepools to below equilibrium levels. Fire usually reducesecosystem photosynthetic capacity and also alters its phys-ical and chemical properties to influence the decompositionof litter and SOM [371. Hence, C residence time can also beaffected. Globally, wildfires burn 3.5-4.5 million lon2 ofland per year (ÿ4% of the vegetated land surface) and emit2- 3 Pg C per year into the atmosphere [38]. From 1997 to2001, fire-induced COs emissions ranged fi'mn 1.74 to 3.53Pg C per year [391.

Impacts of global change on the terrestrial C cycleGlobal change affects C sink dynamics via direct influenceson C influx and residence time, indirect effects via inducedchanges in ecosystem structure and shifts in disturbanceregimes.

Direct and indirect effects of global change on CprocessesIncreasing levels of atmospheric [COs], [br example, pri-marily stimulate photosynthetic C influx, and usuallyresult in increases in plant biomass growth and, possibly,in soil C storage [531 (Table 2). Instantaneous increases inC influx in response to increasing [COs] can be estimatedfi'om an invariant function [54,55]. However, the long-termsustainabitity of C sequestration depends on N availability[56], which regulates COs stimulation of plant growth[57,58] and net soil C accumulation [591. Changes inlong-term N availability in terrestrial ecosystems havenot been well quantified.

Temperature affects both C influx and residence time. Itis usually assumed that C release is accelerated more (i.e.has a reduced residence time) by c]imate warming than isphotosynthesis. As a consequence, climate warming wouldresult in a net C release, leading to additional warming viapositive feedback [25]. Experimental evidence has shownthat temperature also indirectly affects ecosystem C pro-cesses via changes in phenology and the tengdl of growingseasons, nutrient availability, ecosystem water dynamicsand species composition, with complex effects on C influxand residence time [14].

Increased precipitation usually stimulates C influx intoecosystems as well as increasing decomposition rates (i.e.

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Trends in Ecology and Evolution February 2011, Vol. 26, No. 2

Table 2. I(knowledge base, major gaps, and future needs on responses of C processes to global

Factors

Increasing

atmospheric

ICOn]

Climatewarming

Alteredprecipitation

Nitrogendeposition

Knowledge baseElevated [C02] primarily stimulates Cinflux into ecosystems and creates

potentials for C sequestrationunless N and water strongly

limit plant growth

Warming affects all chemical,physical and biological processesWarming extends growing seasons,increases nutrient availability, alters

species composition and water cyclingVariable responses of photosynthesisand respiration to warming

Knowledge gapsN regulation of long-term C sequestration

Partitioning of additional C to pools withdifferent residence times

Relative sensitivities of various Cprocesses to temperature change

Relative importance of various Cprocesses in different ecosystems

Increases in NPP, respiration and

decomposition with increased

precipitation and vice versa

Increased variability in NPP andrespiration with increased variabilityof precipitation in terms of amounts,

intensity and frequency

Difficult to summarize ecosystemresponses because of the many waysthat their amounts, intensity, frequency

and spatial distributions can be alteredChanges in belowground C dynamicswith precipitation

Stimulates plant growth and NPPLitter produced under high N is ofhigh quality and is easily decomposedSoil C can decrease or increase

depending on the ecosystem type

Relative effects of N on NPPversus decompositionN-induced changes in C partitioning

change

Future research needs

C partitioning to different poolsC sink vs, N relationships as

modified by water availability, claycontent, and temperature regimesC02 effects on residence times

Temperature response functionsand acclimation of photosynthesis,

respiration, SOM decomposition,

species composition, phonology,nutrient availability and soilwater availabilitySpatial and temporal variabilityof key parameters, such as Qÿ0

Response functions of NPP,

respiration, species compositionand decomposition rates withprecipitation or moisture content

Temporal and spatial variability inmajor C processes as related tovariability in precipitation amount,intensity and frequency

N effects on relative C allocation

to belowgroundContribution of aboveground litterproduction to soil C storageDecomposition of litter producedunder high levels of N

decreased (] residence time) [16]. Precipitation as a tbrcingvariable could change in its fl'equency, intensity andamount, each of which has different effects on ecosystemC processes, increases in raint'all variability, for example,de.creased soil respiration and aboveground net primaryproduction [60,611. Precipitation also influences speciescomposition, soil development, nutrient availability andother processes, all ot'whJeh could indirectly affect ecosys-tem C processes [62].

N fertilization and deposition usually stimulate C influxand result in C storage in plant pools [63,64]. Whether theincreased plant growth can lead to net C storage in soil (thelargest pool hÿ terrestrial ecosystems) is controversial [65].N fertilization significantly stimulated soil C gain in someecosystems [66,67], but its loss in other ecosystems [68,69].N usually stimulates litter and SOM decomposition [70]and more abovcground than belowground growth, reduc-ing C input into the soil.

have increased rapidly in recent decades, attributable toregional warming and subsequent increases in water def-icits [75]. Warming and drought stress can contributedirectly to tree mortality [761 and enhance insect andpathogen attacks of trees [77] and wildfires. Yet it is stillchallenging to project tkÿture disturbance regimes in re-sponse to global change.

Effects of global change on disturbance regimesGlobal change can also regulate disturbance regimes,Occurrences of large wildfires in forests in the westernUSA, [br example, increased markedly during the mid-1980 s, owing largely to unusually warmer springs andlonger summer dry seasons [15]. Tight coupling betweenfire activities and climate oscillations has been re'vealed bydendrochronological and observational analyses [71] andsedimentary charcoal records [72]. The projected globalwarming of 1.5-5.8 C during the current century couldincrease extreme fire events [73], leading to sigmificant Closs fl'om affected ecosystems.

Episodic disturbances, such as tbrest dieback and insectoutbreaks, are also influenced by global change [74]. Mor-tality rates of old tbrests in the western USA, for example,

Future C sink dynamics and state changesFuture C sink dynmnies in terrestrial ecosystems wil] bestill governed by these internal processes as described byEquation 1 but also regulated by disturbances and globalchange in at least fore" ways: (i) temporal changes in poolsizes by disturbances; (ii) altered disturbance regimes; (iii)altered C inflax and residence time directly by globalchange; and (iv) state changes in the C cycle caused bydistm'bances and global change (Table 1). Of'these, the statechange is least understood but has the most profound impacton future C stability in the ten'estrial ecosystems [78-84].

The multiple states of ecosystem equilibrium have longbeen documented in ecology [85,861. The state changemight be primarily determined by hydroclimate conditions(Figure lc), regulated by climate-land surface feedback,and triggered by natural distm'bances and human inte>vention. When an ecosystem changes to a new state with alow C sink capacity, a net release of C from the ecosystem tothe atmosphere occurs, leading to positive tbedback onclimate warming. Conversely, a change of an ecosystemto a state with a high sink capacity results in C seqnestraÿtion. When the state change occurs in regions with hugeamounts of C at stake, it can destabilize the global C cycleand enhance the positive C-climate feedback.

C storage in tln'ee regions ot' the' world (Amazonianfbrests, Ati'ican tropic tbrests and permafl'ost) could undergo

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!i[;{:ÿi'ÿ\9.i ÿ: Trends in Ecology and Evolution February 2011 Vol. 26, No. 2

unstable state changes to become major C som'ces. The threeregkms contain a total ofÿ2000 Pg C, fbur to five times thatin the atmosphere. Amazonian forests are cm'rently thelargest tropical fbrests on Earth and affect atmosphericcirculation across continents and hemispheres [87]. Thefbrests themselves contain ÿ86 440 Pg C [88] and an equiv-alent amount in their soils 187]. Climate change could altermoist convection, especially in the boundary between con-vetting and nonconvecting zones [89], leading to a reductionin dry-season rainfall in various parts of Amazonia [84] andtriggering positive fbedback, resulting in ecosystem statechanges [90].

Aft'Jean tropical lbrests are distributed around the equa-tor, away fl'om which are savanna gÿ'asslands and desertsin a sequence to either the north or south. The Sahara washeavily vegetated 6000 years ago and experienced anabrupt change in its vegetation and climate 4000-5000years ago [911, The Sahel region of West Ati'ica has alsogone through state changes [92], resulting partially frominteractions between the atmosphere and vegetation [93].Changes in vegetation properties (e.g. rooting depth andleaf area index) or types (e.g. forest, grassland and desert)can alter the moistm'e gradient in the atmospheric bound-ary layer fl'om the ocean to inland, leading to either posi-tive or negative feedback, which then triggers ecosystemstate changes.

Permafrost in the high latitude regions of the northernhemisphere contains 1672 Pg of organic C [94], ÿ50% of theestimated global belowground C pool. As land surfacetemperatm'es are projected to increase by up to 7-8 °Cin these regions by the end of' the current century [73],ecosystems will shift fl'om permafl'ost to active layers viathawing. Tbe state change will result in substantial C lossand become one of the most significant potential feedbacksfl'om land ecosystems to the atmosphere [95]. The statechanges fl'om permafl'ost to active soil involve changes inphysical, chemical, biological and ecological states. Theinstability of the land C sink could occur as a result of avegetation shift between boreal fbrests and tundra [96],witb dilIbrent snow covers reflecting radiation and regu-lating temperature [97].

theory with biogeochemistry and can be used to generatedisturbance events in prognostic modeling. Third, globalchange not only directly alters C influx and residence time,but also induces changes in ecosystem structure and dis-turbance regimes. Although direct effects of global changeon the C cycle can be simulated by most Earth systemmodels, it is still a major challenge to quantify thtm'echanges in disturbance regimes and ecosystem structureunder global change. Fourth, when the ecosystem struc-ture changes and disturbance regimes shift, the ecosystemC cycle might move to alternative states. State changesamong multiple equilibriums can lead to global instabilityof future land C sink dynamics if they oecur in regions withlarge C resmwes at risk. Innovative methods are neededto examine the conditions and processes leading to statechanges.

AcknowledgmentsWe thank Philippe Ciais, and three anonymous reviewers for theirconstructive comments. The work was financially supported by NSF DBI

0850290, DEB 0840964 and DEB 0743778; by the Office of Science (BEll),Department of Energy, Grant No. DE-FG02-006ER64319 and through

the Midwestern Regional Center of the National institute for ClimaticChange Research at Michigan Technological University, under AwardNumber DE-FC02o06ER64158.

Appendix A. Supplementary dataSupplementary data associated with this article can befbund, in the online version, at doi:10.1016/j.tree.2010.11.003.

Concluding remarksThe dynamic disequilibrium fl'amework provides guidingprinciples on the assessment offhture land C sink dynam-ics in tbur cases. First, dynamic disequilibrium within onedisturbance-recovery episode causes temporal changes inthe C source and sink at yearly and decadal scales. Indi-vidual disturbance events might not have any impacts onlonger-term C sequestration, unless the distm'banceregimes shill Dynamic disequilibrium within the episodecan not be fully quantified until three sets of parametersrelated to C intlux, residence time and initial pool sizes areestimated with data assimilation and other techniques.Second, shifts in disturbance regimes, which are usuallycausc, d by global change and hmnan intervention, canresult in long-term reg%nal C loss or gain. Regime shiftscan be quantified by joint probability distributions ofdisturbance fl'equency, severity and extensity overtime and space. The probability distributions introducestochastic approaches to the integration of disturbance

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