Ecography 37: 1020, 2014 doi: 10.1111/j.1600-0587.2013.00345.x 2013 The Authors.

. Ecography 2013 Nordic Society Oikos Subject Editor: Jens-Christian Svenning. Accepted 14 May 2013

How do disturbances and environmental heterogeneity affect the pace of forest distribution shifts under climate change?
Mark C.Vanderwel and Drew W.Purves
M. C. Vanderwel (mark.vanderwel@u.edu) and D. W. Purves, Computational Ecology and Environmental Sciences Group, Microsoft Research, 21 Station Road, Cambridge, CB1 2FB, UK. MCV also at: Dept of Biology, Univ. of Florida, Gainesville, FL 32611, USA.

Although it is widely predicted that the geographic distributions of tree species and forest types will undergo substantial shifts in future, modelling approaches used to date are largely unable to project the pace at which forest distributions will respond to environmental change. The expansion and contraction of forest distributions act against considerable demographic inertia in the present composition and size-structure of forest stands as climate-induced changes in growth, mortality, and recruitment alter population dynamics through time. We aimed to better understand how shifts in forest distributions reect long-term changes in tree demographic rates and population dynamics, and how such shifts are inuenced by 1) disturbance from forest harvesting and 2) local environmental heterogeneity. Using a simple, data-constrained gap model, we simulated regional forest dynamics in the eastern United States over the next 500 yr. We then compared the geographic distributions of ve dierent forest types through time under present and altered climatic conditions, in scenarios that variously included and excluded forest harvesting and environmental heterogeneity. Although we held climate xed after 100 yr, it took another 160 yr after this for these forest types to collectively experience 90% of their eventual climate-related distribution gains and losses. Competition strongly aected the nature of responses to climate change. Harvesting accelerated and amplied gains by an early-successional forest type at the expense of a late-successional one, but these gains did not occur faster than those for other forest types. Environmental heterogeneity had little eect on distribution gains or losses through time. These ndings indicate that forest distributions should respond quite slowly to climate change, with the leading and trailing edges of dierent forest types shifting over a span of centuries. Disturbances can expedite some transitions, but are unlikely to lead to wholesale changes in forest types in the coming decades.

It is widely predicted that the geographic distributions of tree species and forest types will experience large future shifts in response to altered climatic conditions and increased atmospheric CO2 concentrations (Iverson etal. 2008, Morin etal. 2008, Keenan et al. 2010, Cheaib et al. 2012). However, such projections typically describe the distributions that forests may achieve upon reaching equilibrium with new climatic conditions. Most current modelling approaches are unable to predict the timescale at which leading and trailing edges of forest (or more generally, any species) distributions will respond to environmental change (Thuiller etal. 2008), whereas dynamic models that purport to do so carry serious limitations (Purves and Pacala 2008). The actual pace at which geographic distributions will shift in future thus represents a substantial gap in our understanding of climate change impacts on biodiversity and ecosystem services (Bellard etal. 2012, McMahon etal. 2011). Several approaches have been used to predict future changes in the distributions of tree species and broader plant functional types. Bioclimate envelope models (Iverson and Prasad 1998) capture statistical relationships between current species distributions and environmental factors, but do not describe the dynamical processes through which species track these environmental niches. Process-based biophysical 10

models capture climate dependencies in the components of population tness (Morin etal. 2008), but assume that future distributions will maintain equilibrium with tness. Other techniques capture dynamic responses to climate change, with important limitations. Spatially explicit patch occupancy models (Garca-Valds et al. 2013) simulate species ongoing colonization and extinction at the patch level (e.g. for individual forest plots), but typically do not incorporate any local population dynamics or species interactions (but see Cabral and Schurr 2010). Dynamic vegetation models (Sitch etal. 2008, Tang and Beckage 2010) predict vegetation distributions by scaling up from short-term ecophysiological processes (e.g. daily gas exchange and water balance), but their representations of population-level processes are highly simplied and have not yet been constrained against data (Purves and Pacala 2008). All of these approaches can be useful for particular purposes; however, none are wellsuited for considering the rate at which forest distributions might shift under climate change. Because trees are long-lived organisms, there is a great deal of demographic inertia in the present composition and size-structure of forest stands. Changes in forest distributions must act against this inertia as climate-induced changes in growth, mortality, and recruitment operate to

alter stand and landscape population dynamics over long time scales (Sato etal. 2007). Forest gap models (Bugmann 2001) are appropriate tools for understanding how these changes unfold. Gap models typically consist of sub-models describing tree growth, allometry, mortality, and recruitment as driven by individual tree characteristics, competition for light or other resources, and local environmental conditions. They have long proven successful in representing population dynamics and disturbance impacts in complex, multi-species forest stands (Shugart 1984, Pacala etal. 1996), and recently have been extended to predict geographic distributions and succession at regional scales (Purves etal. 2008, Vanderwel etal. 2013a). Importantly, forest gap models permit consideration of how external processes may facilitate or hinder climatedriven forest shifts through their eects on tree demography. Here we explore two particular examples: 1) the role of disturbance in accelerating stand turnover at the leading and trailing edges of forest distributions; and 2) the role of environmental heterogeneity in supporting local populations in climatically unfavourable landscapes. Disturbances are expected to have a strong inuence on how forests respond to climate change (Dale et al. 2001). Dynamic landscape simulations have shown that forest disturbances can have major impacts on carbon storage and species composition under changing climatic conditions (Scheller and Mladeno 2005). Disturbances provide many opportunities for colonization and establishment, and also aect the competitive balance between early- and latesuccessional species at stand and landscape scales (Xu etal. 2012). Accordingly, we hypothesized that periodic stand disturbances from forest harvesting would accelerate the rate at which forest types gain and lose area at the leading and trailing edges of their distributions, respectively. We also predicted that this eect would be strongest for gains made by early successional forest types under a changing climate. Tree migration is considered to be a strong limiting factor to forest distribution shifts (Iverson et al. 2004), although further work is needed to clearly resolve its implications (Thuiller etal. 2008). One theory suggests that, historically, the persistence of small refuge populations within unfavourable landscapes has dramatically shortened the distance (and velocity at which) trees need to disperse to rapidly extend their ranges (McLachlan etal. 2005, Pearson 2006). Climate refugia may arise where environmental heterogeneity creates conditions that favour local persistence of a given forest type in landscapes that are broadly unsuitable to its growth, survival, or reproduction. This ne-scale environmental heterogeneity can produce considerable variation in species responses to climate change, both locally and when extrapolated to broader scales (Ise and Moorcroft 2010, Liang etal. 2011). We hypothesized that local environmental heterogenenity would increase the rate at which the leading and trailing edges of forest-type distributions shift under climate change. In this paper we use CAIN, an individual-based model of stand dynamics that has been calibrated against extensive data on tree demographic rates across the eastern United States (Vanderwel etal. 2013a), to understand how quickly forest types in this region may shift in response to 100-yr climate change. Rather than making specic predictions

for the future state of these forests, we focus on general principles for how shifts in forest distributions emerge through long-term changes in tree demographic rates, and how such shifts are inuenced by 1) disturbance from forest harvesting and 2) local environmental heterogeneity.

Methods
Forest dynamics model CAIN is a simple, scalable, individual-based model of forest stand dynamics that captures general properties of tree demography in a manner that allows all model parameters to be estimated from forest inventory data and allometric relationships (Caspersen et al. 2011). CAIN has been used previously to understand relationships between stand structure and productivity (Caspersen et al. 2011), demographic limitations on forest-type distributions (Vanderwel et al. 2013a), and the implications of forest disturbance for regional biomass dynamics (Vanderwel etal. 2013b). While CAIN is closely linked with data in the form of tree- and plot-level demographic observations, it is also designed for application as a dynamic simulation tool. When used as a forest simulator, the demographic sub-models in CAIN describe how dierent sizes and types of trees compete with one another and, over time, how the structure and composition of a forest stand is expected to evolve. Simulated stands do not have an explicit spatial extent or model the positions of individual trees; they are considered to represent population dynamics over a localized area with a uniform abiotic environment and canopy structure. Simulated stands that are in close geographic proximity (dened as occurring in the same 0.5 grid cell see Simulations below) are linked through landscape eects on recruitment of new individuals. In the version of CAIN used here, tree growth (G) and mortality (M) rates vary non-linearly with tree size (diameter at breast height, DBH), height-structured competition for light (vertical prole of crown area index, CAIh, a measure of projected shading for a given inventory plot or simulated stand), and climatic variables (mean annual temperature, MAT, and precipitation, MAP):

G d G s ( DBH )Gc (CAI h )G E ( MAT, MAP )

M 1y Lg ( MAT, MAP ) Ls ( DBH ) LC (CAI h )

(1)

Recruitment (or ingrowth, I) rates vary with crown area index, climate, and the basal area in the surrounding landscape (LBA) of each tree species or plant functional type (PFT):

I I c (CAI h ) I c ( LBA ) I E ( MAT, MAP )

(2)

where GS, GC, GE, LE, LS, LC, IC, IL, and IE represent non-linear functions, and d, y, and t represent constants. The functional forms of individual terms were chosen based on successful previous applications in the forest ecology literature (Coates etal. 2009, Lines etal. 2010, Caspersen etal. 2011, Gmez-Aparicio etal. 2011, Hurst etal. 2011). 11

Full details on the models formulation are presented in Supplementary material Appendix 1. We previously parameterized CAIN against data on tree growth, mortality and recruitment from 47 723 0.07-ha Forest Inventory and Analysis (FIA) plots across the eastern United States that had been re-measured after an average of ve years (Vanderwel etal. 2013a). We grouped species into seven PFTs to make it feasible to simulate joint population dynamics within stands, including the eects of competition for light and growing space among dierent PFTs. We classied more than 200 tree species into six PFTs dened by their latitudinal ranges (boreal, northern temperate, southern temperate) and leaf habit (hardwood, conifer), plus a seventh type (southern temperate hydric) that encompassed species primarily associated with coastal plain swamps (Supplementary material Appendix 1, Table 1). Although there is considerable variation in species characteristics within each of these PFTs, our classication allowed us to broadly discriminate early-, mid-, and late-successional groups of species and to capture several major forest cover transitions across the eastern US (Table 1). Calibrated solely from demographic data, dynamic projections derived from model simulations approximate the observed geographic distribution of each PFT, as well as several key transitions between early- and late-successional PFTs in dierent parts of the region (Vanderwel etal. 2013a). Simulations We used the CAIN model to carry out simulations of stand population dynamics across the eastern United States under a variety of scenarios to consider how, and how quickly, forests may respond to future climate change. We divided the region into 0.5 grid cells, within each of which we created 30 simulated forest stands. Within each cell, stands diered in initial cohort structure, climatic conditions, and local environmental eects (each described further below). The 30 stands were therefore not identical replicates, but instead sampled the variability found across each cells forest landscape. Each stand was also subjected to a unique sequence of stochastic harvesting events. Each stand consisted of a set of tree cohorts, where each cohort represented the number of trees per hectare of a given DBH and PFT. We initialized the cohort structure of each stand from a random 0.07-ha FIA plot within the cell (drawn with replacement) or, if there were no plots in the cell, a neighbouring cell. We then applied growth, mortality, and recruitment models to individual tree cohorts, and implemented probabilistic stand harvesting, over a series

of ve-year timesteps. Five-year timesteps are common in many forest dynamics models, and also closely matched the re-measurement interval of FIA data. In each timestep: 1) growth increased the DBH of trees in each cohort; 2) mortality reduced the number of trees per hectare represented by each cohort; 3) recruitment added new cohorts with the minimum DBH (3 cm); and 4) harvesting was executed probabilistically for each stand (as detailed below under the heading Forest harvesting). At the end of each timestep we calculated the average basal area of each PFT in each grid cell from the sets of cohorts that were present. By averaging basal area across 30 individual stands, we obtained a landscape-level abundance for each PFT that incorporated eects of both local environmental variability and a stochastic harvesting process. Simulations were run for 500 yr. At the end of this period the basal area of all PFTs had reached quasi-equilibrium in each grid cell. Stochastic harvesting induced little variation in model output at the grid cell level, and so we present results from a single simulation run per scenario. Model scenarios (summarized in Table 2 and described in detail below) were developed to assess the rate and extent to which PFT distributions may shift as a result of altered population dynamics under climate change. We specically considered how disturbance (in the form of stand harvesting) and environmental heterogeneity may aect the area gained and lost by dierent PFTs over time, and whether recruitment limitation in unoccupied and low-abundance areas could strongly aect colonization dynamics. Climate regimes We dened a xed and a dynamic climate regime. For scenarios with a xed climate regime, we assigned the average mean annual temperature and precipitation from 19601990 to each simulated stand, and held these values constant for the duration of the simulation. Climate data were obtained from the WorldClim database (Hijmans et al. 2005). These climate data were the same as those used in the original parameterization of the demographic models. In the dynamic climate scenarios, we initialized the simulations with the same climate data as the xed climate scenarios, but then applied a linear increase to both temperature and precipitation over the rst 100 yr. We applied median projections of climate change for central and eastern North America under an A1B scenario (Christensen et al. 2007), such that after 100 yr mean annual temperature had increased by 3.5C and mean annual precipitation

Table 1. Description of plant functional types for the eastern United States used in this study. Name Boreal conifer (BC) Boreal hardwood (BH) Northern temperate conifer (NC) Northern temperate hardwood (NH) Southern temperate conifer (SC) Southern temperate hardwood (SH) Southern temperate hydric (SY) Niche description Late-successional Early-successional Late-successional Late-successional Early-successional Mid-successional Edaphic specialist Representative species Abies balsamea, Picea spp., Pinus banksiana Populus spp., Betula papyrifera Pinus spp., Thuja occidentalis, Tsuga canadensis Acer spp., Quercus rubra, Fagus grandifolia Pinus spp., Juniperus virginiana Quercus spp., Liquidambar styraciua, Liriodendron tulipifera Nyssa spp., Taxodium spp.

12

Table 2. Summary of features that were varied in different model scenarios to assess the rate at which forest distributions in the eastern United States may shift under climate change. Scenario description Features Climate change With feature Mean annual temperature and precipitation start at 19601990 means, and increase linearly until they are respectively 3.5C and 5% higher after 100 yr. Climate is constant thereafter. Harvesting applied stochastically using intensity and frequency as shown in Fig. 2ac. Each stand has local growth and recruitment multipliers applied, as summarized in Fig. 2d and Table 3. Recruitment scales with PFT abundance in each grid cell. Without feature Mean annual temperature and precipitation held to 19601990 means throughout simulation. No harvesting or other forms of stand disturbance. No local growth or recruitment multipliers applied. All PFTs have an equal opportunity to establish in each grid cell, based on the overall mean county-level basal area of PFTs within their observed ranges.

Disturbance Environmental heterogeneity Recruitment limitation

had increased by 5% in each stand. Temperature and precipitation were held stable at these elevated levels for the remainder of the simulation period.

Under these altered climatic conditions, our demographic models predicted that most PFTs would exhibit faster growth, particularly in colder parts of the region (Fig. 1). All PFTs were predicted to experience higher mortality in the warmer parts of their ranges, with this eect especially pronounced for boreal and northern temperate conifers. Recruitment rates for boreal and southern temperate PFTs were predicted to increase in colder parts of their ranges and decrease in warmer areas, but neither northern temperate PFT was predicted to experience much change in recruitment. These changes assume that modelled relationships with climate variables represent causal eects. Our approach also implies that the chosen model forms are appropriate for extrapolation outside current PFT ranges. Demographic predictions beyond current PFT distributions are inherently dicult to verify, but appear consistent with dominant trends observed as individual species approach their range limit (Vanderwel et al. 2013a). Uncertainty arising from these assumptions means that the models could well over- or underestimate demographic responses to changes in climate. Nevertheless, they provide a useful means of assessing how modied demographic rates translate into shifts in forest distributions over time. Forest harvesting We estimated the local intensity and frequency of forest harvesting across the region based on records of recent harvesting from 50836 plots in the FIA database. To model harvest intensity in each 0.5 grid cell, we calculated the mean residual basal area of plots that had at least one tree removed by harvesting in the most recent survey interval (average of 5 yr). We then used a thin plate spline model to smooth spatial variation in mean residual basal area between nearby grid cells. For each grid cell, we modelled variance in residual basal area as the mean squared dierence between each FIA plots residual basal area and the smoothed grid cell mean. Again, we used a thin plate spline to smooth the variance in residual basal area across the region (Fig. 2a, b). To model harvest frequency in each grid cell, we estimated annual harvest probability as the number of FIA plots that were harvested in the most recent survey interval, divided 13

Figure 1. Simulated changes in PFT growth, mortality, and recruitment rates following a 3.5C increase in mean annual temperature and 5% increase in mean annual precipitation over 100 yr. All other covariates in CAINs demographic models (DBH, crown area index, and landscape basal area) were xed at mean values. The solid portion of each line indicates the interval between the 1st and 99th percentiles of the temperature range for each PFT; dashed portions represent extrapolations outside this range. PFT abbreviations are given in Table 1.

Figure 2. (ac) Frequency and intensity of forest harvesting in the eastern United States as estimated from recent (19952011) Forest Inventory and Analysis data. Spatial patterns were smoothed across 0.5 grid cells using thin plate spline models for mean residual basal area, variance in residual basal area, and ve-year harvest probability. (d) Histograms for the distribution of growth and recruitment multiplier terms representing local environmental heterogeneity in tree demography across the eastern United States. The scatterplot shows the correlated nature of these eects in a 1% sample of 47723 FIA plots.

by the sum of the survey interval lengths for all plots in that grid cell. We then multiplied this estimate by ve to derive a ve-year harvest probability for each simulation timestep. As with harvest intensity, we used a thin plate spline model to smooth variation among grid cells while capturing spatial trends in the probability of harvest (Fig. 2c). In our simulations we applied a harvesting algorithm to each stand independently. Each timestep, a stand was considered to be harvested if a uniformly-drawn random number (between 0 and 1) was less than the estimated ve-year harvest probability for the stands grid cell. If a stand was to be harvested, we drew a random deviate from a gamma distribution with mean and variance taken from the residual basal area model of harvest intensity for that grid cell. If the stands current basal area exceeded this value, we reduced the density of all tree cohorts by a constant factor to achieve the desired residual basal area. 14

Environmental heterogeneity We sought to quantify the degree to which trees in a given locality experience stand-to-stand variation in growth, mortality, and recruitment attributable to ne-scale dierences in edaphic conditions or other unmeasured environmental factors. These environmental eects can be expressed by a vector {EG, EL, EI} that applies a set of multiplicative eects to the demographic rates of all trees within a given FIA plot or simulated stand: G EG G M (1 exp( E L ) L )1  I exp( E I ) I where G, L, and I represent the growth rate, longevity, and recruitment rate predicted as a function of state variables (3)

such as DBH, crown area index, and climate; G, M, and I represent the corresponding growth, mortality, and recruitment rates predicted after accounting for latent stand-level environmental eects. We developed a hierarchical Bayesian model to characterize the multivariate distribution of these environmental eects. We postulated that all FIA plots within a grid cell would show a multivariate normal (MVN) distribution of environmental eects around a given grid cell mean vector, mc: { EG , E L , E I } MVN ( mc , Sc )  (4)

that site-related factors that would cause a persistent, systematic increase in mortality would produce a corresponding decrease in tree growth; this pattern was not apparent from our analysis. Plot-to-plot variation in mortality could also partly reect sampling artifacts caused by the stochastic nature of mortality and small plot sizes. In addition, preliminary tests showed that persistent dierences in mortality rates often led to unreasonably low or high basal area in simulations for individual stands. Given these concerns, we opted to apply ne-scale environmental variation in growth and recruitment, but not mortality, in our simulations. Sources for recruitment In our recruitment model, the density of new recruits of each PFT increases as a power function of the PFTs average basal area within a given grid cell (LBA in Eq. 2). This eect reects the tendency for recruitment to increase with propagule sources, all else being equal. However, with this positive feedback PFTs may not establish well in grid cells where they are initially at low abundance, and cannot recruit into cells where they are initially absent. To assess the importance of this landscape dispersal eect for recruitment, we developed an alternate scenario where we substituted the current observed mean county-level PFT basal area (5.66 m2 ha1) in the source eect term for recruitment. This no recruitment limitation scenario enabled us to explicitly test the degree to which modelled distribution gains were dependent on current PFT presence and abundance, via eects on recruitment. For simplicity, we only ran this scenario with harvesting and environmental heterogeneity included. Analysis of simulation results We compared PFT distributions under both current and altered climates with their present distributions at the start of each simulation. In dening each PFTs distribution, we applied a 5 m2 ha1 basal area threshold to identify grid cells where a PFT was a locally important component of the forest community. For each scenario factor (disturbance, heterogeneity, and recruitment), gains in PFT distributions attributable to climate change at a given time were dened as grid cells with 1) basal area greater than 5 m2 ha1 in the altered climate scenario, and 2) basal area below this threshold both initially and at the corresponding timestep of the xed climate scenario. Conversely, losses attributable to climate change were dened by cells that, at a given time, had 1) basal area less than 5 m2 ha1 in the altered climate scenario, and 2) basal area above this threshold both initially and at the corresponding timestep of the xed climate scenario. Although all seven PFTs were included in the simulations, our model predicted that two of these (boreal hardwoods and southern temperate hydric) would not maintain a basal area greater than 5 m2 ha1 anywhere in the region in any of the scenarios considered. We have omitted these two PFTs from the presentation of results. 15

where c is a single covariance matrix describing plot variation around the grid cell means. In turn, grid cell means were considered to exhibit a multivariate normal distribution around a global mean vector, mg:

mc MVN m g , S g 

(5)

where g is a covariance matrix describing grid cell variation around the global mean. We estimated {EG, EL, EI} for 47723 FIA plots, mc for 1280 grid cells, and the global parameters c, mg, and g through Bayesian inference using the Infer.NET software library (Minka etal. 2010). Given initial predictions of tree growth, mortality, and recruitment from the CAIN model, Infer.NET estimated the set of parameter values that provided the best t between G, M, I and raw demographic observations from FIA data. We found that spatial environmental eects varied much more within grid cells than among grid cells (Table 3). Growth and recruitment showed a moderate correlation within grid cells, producing up to about two-fold increases and decreases in these rates in individual plots (Fig. 2d). Although longevity was correlated with growth among grid cells, it did not correlate strongly with either growth or recruitment within grid cells. Given the lack of local covariation between growth and longevity/mortality, we believe it is likely that heterogeneity in mortality eects reects transient processes such as local disturbance, rather than persistently higher or lower mortality rates over time (Vanderwel etal. 2013b). We reasoned
Table 3. Standard deviations (s) and correlation coefcients (r) of environmental effects on tree demography across the eastern United States, as derived from the estimated covariance matrices in a multivariate hierarchical Bayesian analysis that partitioned spatial variability in these effects among and within 0.5 grid cells. Parameter1 sG sL sI rGL rGI rLI Covariance among grid cells (Sg)2 0.174 (0.167, 0.180) 0.170 (0.165, 0.177) 0.191 (0.184, 0.198) 0.484 (0.444, 0.523) 0.244 (0.193, 0.294) 0.027 (0.027, 0.078) Covariance within grid cells (Sc)2 0.423 (0.421, 0.426) 0.837 (0.832, 0.843) 0.462 (0.459, 0.465) 0.056 (0.047, 0.065) 0.337 (0.329, 0.345) 0.206 (0.214, 0.197)

1G: growth; L: longevity; I: recruitment. 2First value represents the posterior mean value. Values inside parentheses represent the limits of the 95% credible interval from each covariance matrixs posterior distribution.

hardwoods from their southwestern range margin near the Missouri Ozarks; and northwards expansion of both southern temperate hardwoods and conifers (Fig. 3). Each PFTs distribution additionally showed some areas where the present distribution did not match that predicted at equilibrium under present climatic conditions (for example, locations where a particular PFT is absent or uncommon now, but where our simulations predicted that it could reach moderate abundance in both present and future climates). As transitions in such areas cannot be unambiguously attributed to climate change, we have excluded them from our interpretation of climate-driven range dynamics. We stabilized climatic conditions after 100 yr in our simulations, but changes in forest distributions tended to unfold over a considerably longer period. The distributions of boreal and northern temperate conifers exhibited some of the most rapid dynamics: by the end of the rst century of the scenarios with harvesting, northern temperate conifers had realized nearly all of their eventual gains and boreal conifers had seen about half of their eventual losses (Fig. 4). By contrast, southern temperate hardwoods and conifers achieved about one-quarter of their eventual gains in the rst 100 yr. Northern temperate hardwoods experienced an average of 20% of their eventual total losses over this period. Among all these scenarios and forest types, it took 160 yr after the end of the 100 yr climate change period for 90% of the total climate-related distribution gains and losses to occur. Effects of harvesting Disturbances in the form of harvesting had clear eects on the distributions of several forest types. Harvesting enabled an early-successional PFT, southern temperate conifers, to persist in Atlantic and Gulf Coast regions from which it would otherwise be lost, and also prevented southwards expansion of northern temperate hardwoods and conifers under both present-day and altered climate scenarios (Fig. 3). However, harvesting had mixed eects in terms of responses to climate change. Southern temperate conifers extended their range considerably farther and faster under climate change with harvesting, at the expense of northern temperate hardwoods. The resulting increase in competition accelerated and amplied losses from northern temperate hardwoods distribution (although the losses still occurred over a span of several centuries). By contrast, the rate and magnitude of changes in the distributions of boreal conifers and southern temperate hardwoods were less sensitive to harvesting. Although early-successional southern temperate conifers gained the most area under climate change with harvesting, they took no less time to do so than other PFTs. Our model projected, for example, that it would take 300320 yr for southern temperate conifers to realize 90% of their climatechange gains, but only 200250 yr for southern temperate hardwoods to do the same. Environmental heterogeneity and recruitment limitation Unlike disturbance, environmental heterogeneity had little impact on the rate or magnitude of shifts in forest

Figure 3. Shifts in the geographic distribution of each PFT at the end of 500-yr simulations. Red and dark blue cells represent the areas gained and lost, respectively, from each distribution as a result of climate-related changes in demographic rates. These cells are the focus of our results. Light blue, yellow and green cells indicate areas for which present conditions and equilibrium predictions for the present climate are not in agreement (either because current distributions do not ll their climatic niche, or because of model error). Interpretation of these cells in the context of climate change is less straightforward, and is not considered further. The scenarios depicted here included both environmental heterogeneity and recruitment limitation (Table 1).

Results
Overall patterns With a 3.5C increase in temperature and 5% increase in precipitation, our simulations project, at quasi-equilbrium: replacement of boreal conifers with northern temperate conifers in the upper Lake States; loss of northern temperate 16

Figure 4. Changes in the number of 0.5 grid cells gained and lost by each PFT as a result of climate change over the 500-yr simulations. Cells gained refers to the number of grid cells with 1) basal area greater than 5 m2 ha1 in the altered climate scenario, and 2) basal area below this threshold both initially and at the corresponding timestep of the xed climate scenario. Cells lost refers to the number of grid cells with 1) basal area less than 5 m2 ha1 in the altered climate scenario, and 2) basal area above this threshold both initially and at the corresponding timestep of the xed climate scenario. These denitions correspond to the red and dark blue grid cells in Fig. 3, respectively.

distributions according to our model (Fig. 4). For all PFTs and both harvesting scenarios, the trajectories of distribution gains and losses did not strongly depend on whether or not plots expressed local variation in their demographic rates. Only one PFT (southern temperate conifers) showed evidence of appreciable recruitment limitation in our model. With the density-dependency of recruitment rates removed, southern temperate conifers gained about 30% more area, and did so in a shorter time (200 yr) than when recruitment rates varied with landscape basal area. In this scenario, the additional gains by southern temperate conifers occurred in areas where this PFT is currently absent, rather than areas where it currently has a non-zero abundance below the

5 m2 ha1 basal area threshold. No other PFTs showed a pronounced eect of recruitment limitation on the area added to their distributions under climate change.

Discussion
Long tree lifespans and asymmetric competition for light impart considerable demographic inertia to forest structure and composition. As a result, climate warming over (at least) the next century will certainly outpace the rate at which forest distributions respond to environmental change. Nevertheless, tree growth, mortality, and recruitment 17

are all responsive to climate dynamics in the short term; alterations in these demographic rates inevitably aect forest population dynamics and biogeography through time. To understand how quickly forest distributions may shift in future, we must therefore consider which particular demographic processes may be most strongly aected by changes in climatic conditions (Fig. 1), and how such changes will propagate through forest stands and landscapes. Importance of demography and competition Our simulations showed that northern temperate conifers could replace boreal conifers in the upper Lake States as higher temperatures lead to increases in boreal conifer mortality rates. We considered this area to be partially outside the current distribution of northern temperate conifers (based on a 5 m2 ha1 basal area threshold), but northern temperate conifers were still initially present at low abundances here. Aided by increased growth rates, they could quickly respond to vacant canopy space created by harvesting and become a more substantial component of forests in the upper Lakes States within 100 yr. The cumulative eects of increased mortality were projected to result in the loss of boreal conifers from this area over about 200 yr. In more southerly parts of the region, increases in the recruitment rates of southern temperate hardwoods and conifers allow these PFTs to extend the northern edges of their projected distributions into areas currently dominated by northern temperate hardwoods. Unlike the previous case, these range expansions are not accompanied by a substantial decrease in the performance of the resident forest type. Consequently, it takes a somewhat longer time (200 300 yr) for stand turnover processes to allow southern PFTs to expand in areas where they are presently at low abundance and, as a direct result, for northern temperate hardwoods to nish receding from areas around their current southern margin. Comparison of the timeframes at which northern and southern PFTs shift their distributions northwards in our simulations highlights the importance of competition in understanding forest dynamics under climate change (Clark et al. 2011). Even though northern temperate conifers experience modest changes in their demographic rates near their northern range margin, this PFT is still projected to extend its range relatively quickly because of a decrease in the performance of boreal conifers. On the other hand, southern temperate hardwoods and conifers experience large increases in recruitment (and growth in one instance) near their northern range margin, but it takes considerably longer for them to extend their distributions in our simulations because northern temperate hardwoods remain a strong competitor. Biotic interactions are broadly recognized as a potentially important, yet poorly understood, factor in understanding how species distributions will shift under climate change (Kissling etal. 2012). Our results indicate that in the case of forests, competition may be at least as important as intrinsic demographic changes in determining the rate and extent of distribution shifts. 18

Roles of disturbance, heterogeneity, and recruitment The primary eect of disturbance was to tilt the competitive balance more in favour of early-successional forest types. Among the PFTs considered here, forest harvesting magnied and accelerated a projected transition from northern temperate hardwoods to southern temperate conifers across the central part of the region in accordance with our initial prediction. Harvesting could further enhance these changes by promoting the establishment of individuals that are better-adapted to new climatic conditions (Kuparinen et al. 2010), though such evolutionary eects are not considered in our simulations. However, we also found that harvesting had little eect on distribution shifts that did not involve early-successional forest types (boreal conifers and southern temperate hardwoods), and that gains and losses for these lateand mid-successional PFTs could occur even more quickly than distribution gains made by an early-successional PFT. Although disturbances have strong eects on forest dynamics (Frelich 2002, Scheller and Mladeno 2005), our results suggest that additional factors are important in determining the pace of distribution shifts under climate change. Environmental heterogeneity had no substantive eects on shifts in forest distributions in our simulations, but this is perhaps unsurprising given that our model results showed little eect of initial landscape-level (grid cell) abundance. We applied a 5 m2 ha1 basal area threshold in dening whether a PFTs distribution included a given grid cell; i.e. areas where the PFT formed a substantial part of the community. The initial conditions featured many grid cells where each PFT occurred at lower, non-zero abundances. As climatic conditions became more favourable, PFTs could become more abundant in such areas and thereby incorporate new grid cells in their distributions without any explicit longdistance dispersal. Under the climate change scenario that we imposed, the two southern temperate PFTs added much of the area where they currently occur at low abundance (5 m2 ha1) to their distributions (44 and 23% of the area that became more climatically suitable for conifers and hardwoods, respectively, in the scenario with both harvesting and environmental heterogeneity). Our no recruitment limitation scenario showed that density-dependent recruitment eects did not hamper PFTs from increasing in abundance in areas where they are currently present but uncommon. As a result, environmental heterogeneity was not required to oset the initial disadvantages of low abundance. Our nding that, in general, propagule sources did not limit shifts in forest distributions contrasts with the dispersal limitation predicted by many bioclimate envelope models (Iverson etal. 2004), as well as recent models of wind-driven spread (Nathan etal. 2011). To some extent, our conclusion reects the fact that we dened distributions by the set of grid cells with basal area greater than 5 m2 ha1 (as discussed above). Climate-induced additions to forest distributions occurred in locations where a PFT was already present but below this abundance threshold. These few individuals provided a source for recruitment without the need for dispersal from other cells (at least, granted the fairly coarse spatial and taxonomic resolution of our model). When we removed dispersal constraints and allowed PFTs to establish anywhere,

only one PFT (southern temperate conifers) reached moderate abundance in extensive areas where it is currently absent. Even in this case though, most of the gains to the PFTs distribution occurred in areas where it is now present at low abundance (Fig. 4). In contrast with our approach, bioclimate envelope models typically focus on the absolute range; i.e. locations where the species is present vs. completely absent. As the threshold abundance is lowered closer to zero, colonization processes may take on a more important role than relative performance in a given locality (Garca-Valds etal. 2013). For models that incorporate population dynamics, we consider our threshold approach to be a reasonable one for studying forest PFT distributions because it reects importance in terms of overall forest structure, which is principally determined by PFTs that are common rather than those at low abundance. More generally, it remains an open research question whether species are restricted from becoming locally important by the establishment of a founding population, or by the subsequent growth of such populations (Lockwood etal. 2005, Wirth etal. 2008, Ibez etal. 2009). Caveats and limitations For several reasons, it is inappropriate to regard the extent or precise timing of distribution shifts as specic predictions of the future state of eastern US forests. We have only considered a simplied climate change scenario that represents a median estimate of 100-yr climate model predictions for this region, and unchanging conditions for 400 yr thereafter. We have assumed that climate-related spatial variation in demography represents entirely causal relationships from which we can infer the eects of future climate change. This approach is analogous to that employed in bioclimate envelope modelling (although at the level of demographic processes rather than species presence), but is susceptible to potential confounding with factors that do not change through time in the same manner as mean annual temperature and precipitation. Also, like many other large-scale models of forest and vegetation dynamics (Medvigy et al. 2009, Tang and Beckage 2010), we have carried out simulations for a suite of plant functional types that aggregate the responses of many individual species, each of which may show either a larger or smaller response than a PFT average. The more specialized ecological requirements of individual species could mean, for example, that environmental heterogeneity is more important to range dynamics at the species level than is apparent at the coarser scale of plant functional types. Particular species are also likely to be aected more by disturbance than was the case for their respective PFTs (e.g. shade-intolerant Pinus resinosa or Prunus serotina, which are grouped with predominantly late-successional northern temperate conifers and hardwoods, respectively). Despite such limitations, there are good reasons why our approach is well suited for improving our understanding of how and why forest distributions may shift under climate change. All elements of our model are well-grounded in data, with demographic rates, harvesting regimes, and local environmental heterogeneity all formally parameterized against

extensive forest inventory data. CAIN has already been shown to capture demographic limitations on forest distributions, and to produce credible emergent distributions and successional dynamics for the region (Vanderwel etal. 2013a). By using an individual-based model of population dynamics, we were also able to incorporate many details of the initial forest structure, mechanisms of asymmetric competition for light, impacts of forest harvesting, nature of environmental heterogeneity, and landscape-level recruitment limitation, that would not be possible with other kinds of models. Conclusions We expect the pace at which forest distributions respond to climate change to be relatively slow, with the leading and trailing edges of dierent forest types shifting over a span of centuries. Even a moderately large increase in the mortality rates of boreal species, comparable to that observed over recent decades (Peng etal. 2011), could require 100 yr or longer to displace these species from their southern range limit. Such lags are not necessarily well-captured by physiologically-based vegetation models (Tang and Beckage 2010), and can be attributed to strongly inertial forest dynamics when demographic changes are modelled explicitly. Disturbances (which might include increasing frequency of re or insect outbreaks under climate change) can expedite some foresttype transitions, but are still unlikely to lead to wholesale changes in forest types in the coming decades. Although shifts in forest distributions may unfold slowly, climate-related changes in tree demography will still have shorter-term eects on forest structure and dynamics. As forest structure evolves through time to reect altered demography, we should expect to observe climate impacts on biodiversity and ecosystem services well before particular forest types become or cease to be common in a given area (Dale etal. 2010).
Acknowledgements We are grateful to T. Minka, J. Guiver, and J. Winn for valuable discussions and support in using Infer.NET. We also thank D. Coomes, G. McInerny, S. Pacala and F. Schurr for their helpful comments and advice.

References
Bellard, C. etal. 2012. Impacts of climate change on the future of biodiverisity. Ecol. Lett. 15: 365377. Bugmann, H. 2001. A review of forest gap models. Clim. Change 51: 259305. Cabral, J. S. and Schurr, F. M. 2010. Estimating demographic models for the range dynamics of plant species. Global Ecol. Biogeogr. 19: 8597. Caspersen, J. P. etal. 2011. How stand productivity results from size- and competition-dependent growth and mortality. PloS One 6: e28660. Cheaib, A. et al. 2012. Climate change impacts on tree ranges: model intercomparison facilitates understanding and quantication of uncertainty. Ecol. Lett. 15: 533544. Christensen, J. H. etal. 2007. Regional climate projections. In: Solomon, D. et al. (eds), 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 Univ. Press, pp. 848940.

19

Clark, J. S. etal. 2011. Climate change vulnerability of forest biodiversity: climate and competition tracking of demographic rates. Global Change Biol. 17: 18341849. Coates, K. D. etal. 2009. Above- versus below-ground competitive eects and responses of a guild of temperate tree species. J. Ecol. 97: 118130. Dale, V. H. et al. 2001. Climate change and forest disturbances. BioScience 51: 723734. Dale, V. H. etal. 2010. Modeling transient response of forests to climate change. Sci. Total Environ. 408: 18881901. Frelich, L. E. 2002. Forest dynamics and disturbance regimes: studies from temperate evergreen-deciduous forests. Cambridge Univ. Press. Garca-Valds, R. etal. 2013. Chasing a moving target: predicting climate change-induced shifts in non-equilibrial tree species distributions. J. Ecol. 101: 441453. Gmez-Aparicio, L. et al. 2011. Disentangling the relative importance of climate, size and competition on tree growth in Iberian forests: implications for forest management under global change. Global Change Biol. 17: 24002414. Hijmans, R. J. et al. 2005. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25: 19651978. Hurst, J. M. et al. 2011. Size-specic tree mortality varies with neighbourhood crowding and disturbance in a montane Nothofagus forest. PLoS One 6: e26670. Ibez, I. etal. 2009. Estimating colonization potential of migrant tree species. Global Change Biol. 15: 11731188. Ise, T. and Moorcroft, P. R. 2010. Simulating boreal forest dynamics from perspectives of ecophysiology, resource availability, and climate change. Ecol. Res. 25: 501511. Iverson, L. R. and Prasad, A. M. 1998. Predicting abundance of 80 tree species following climate change in the eastern United States. Ecol. Monogr. 68: 465485. Iverson, L. R. et al. 2004. How fast and far might tree species migrate in the eastern United States due to climate change? Global Ecol. Biogeogr. 13: 209219. Iverson, L. R. et al. 2008. Estimating potential habitat for 134 eastern US tree species under six climate scenarios. For. Ecol. Manage. 254: 390406. Keenan, T. et al. 2010. Predicting the future of forests in the Mediterranean under climate change, with niche- and process-based models: CO2 matters! Global Change Biol. 17: 565579. Kissling, W. D. etal. 2012. Towards novel approaches to modelling biotic interactions in multispecies assemblages at large spatial extents. J. Biogeogr. 39: 21632178. Kuparinen, A. etal. 2010. Increased mortality can promote evolutionary adaptation of forest trees to climate change. For. Ecol. Manage. 259: 10031008. Liang, Y. etal. 2011. Are plot data eective for landscape prediction? A simulation study of tree species response to climate warming under varying environmental heterogeneity. Ann. For. Sci. 68: 899909. Lines, E. R. etal. 2010. Inuences of forest structure, climate and species composition on tree mortality across the eastern US. PLoS One 5: e13212. Lockwood, J. L. et al. 2005. The role of propagule pressure in explaining species invasions. Trends Ecol. Evol. 20: 223228.

McLachlan, J. S. etal. 2005. Molecular indicators of tree migration capacity under rapid climate change. Ecology 86: 20882098. McMahon, S. M. etal. 2011. Improving assessment and modelling of climate change impacts on global terrestrial biodiversity. Trends Ecol. Evol. 26: 249259. Medvigy, D. etal. 2009. Mechanistic scaling of ecosystem dynamics in space and time: Ecosystem Demography model version 2. J. Geophys. Res. 114: G01002. Minka, T. etal. 2010. Infer.NET 2.4. Microsoft Research Cambridge, http://research.microsoft.com/infernet. Morin, X. et al. 2008. Tree species range shifts at a continental scale: new predictive insights from a process-based model. J. Ecol. 96: 784794. Nathan, R. etal. 2011. Spread of North American wind-dispersed trees in future environments. Ecol. Lett. 14: 211219. Pacala, S. W. etal. 1996. Forest models dened by eld measu rements: estimation, error analysis and dynamics. Ecol. Monogr. 66: 143. Pearson, R. G. 2006. Climate change and the migration capacity of species. Trends Ecol. Evol. 21: 111113. Peng, C. etal. 2011. A drought-induced pervasive increase in tree mortality across Canadas boreal forests. Nat. Clim. Change 1: 467471. Purves, D. and Pacala, S. 2008. Predictive models of forest dynamics. Science 320: 14521453. Purves, D. W. et al. 2008. Predicting and understanding forest dynamics using a simple tractable model. Proc. Natl Acad. Sci. USA 105: 1701817022. Sato, H. etal. 2007. SEIB-DGVM: a new dynamic global vegetation model using a spatially explicit individual-based approach. Ecol. Model. 200: 279307. Scheller, R. M. and Mladeno, D. J. 2005. A spatially interactive simulation of climate change, harvesting, wind, and tree species migration and projected changes to forest composition and biomass in northern Wisconsin, USA. Global Change Biol. 11: 307321. Shugart, H. H. 1984. A theory of forest dynamics: the ecological implications of forest succession models. Springer. Sitch, S. et al. 2008. Evaluation of the terrestrial carbon cycle, future plant geography and climate-carbon cycle feedbacks using ve dynamic global vegetation models (DGVMs). Global Change Biol. 14: 20152039. Tang, G. and Beckage, B. 2010. Projecting the distribution of forests in New England in response to climate change. Divers. Distrib. 16: 144158. Thuiller, W. etal. 2008. Predicting global change impacts on plant species distributions: future challenges. Perspect. Plant Ecol. 9: 137152. Vanderwel, M. C. etal. 2013a. Climate-related variation in mortality and recruitment determine regional forest-type distributions. Global Ecol. Biogeogr. in press. Vanderwel, M. C. et al. 2013b. Quantifying variation in forest disturbance, and its eects on aboveground biomass dynamics, across the eastern United States. Global Change Biol. 19: 15041517. Wirth, C. etal. 2008. White spruce meets black spruce: dispersal, postre establishment, and growth in a warming climate. Ecol. Monogr. 78: 489505. Xu, C. etal. 2012. Importance of colonization and competition in forest landscape response to global climatic change. Clim. Change 110: 5383.

Supplementary material (Appendix ECOG-00345 at www.oikosoce.lu.se/appendix). Appendix 1.

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