North American tree migration paced by climate in the West,lagging in the East

Tree fecundity and recruitment have not yet been quantified at scales needed to anticipate biogeographic shifts in response to climate change. By separating their responses, this study shows coherence across species and communities, offering the strongest support to date that migration is in progress with regional limitations on rates. The southeastern continent emerges as a fecundity hotspot, but it is situated south of population centers where high seed production could contribute to poleward population spread. By contrast, seedling success is highest in the West and North, serving to partially offset limited seed production near poleward frontiers. The evidence of fecundity and recruitment control on tree migration can inform conservation planning for the expected long-term disequilibrium between climate and forest distribution.

Effective planning for the redistribution of habitats from climate change will depend on understanding demographic rates that control population spread at continental scales. Mobile species are moving, some migrating poleward (1, 2) and/or upward in elevation (3, 4). Species redistribution is also predicted for sessile, long-lived trees that provide the resource and structural foundation for global forest biodiversity (5–7), but their movement is harder to study. Contemporary range shifts are recognized primarily where contractions have followed extensive die-backs (8) or where local changes occur along compact climate gradients in steep terrain (9, 10). Whether migration capacity can pace habitat shifts of hundreds of kilometers on decade time scales depends on seed production and juvenile recruitment (Fig. 1A), which have not been fitted to data in ways that can be incorporated in models to anticipate biogeographic change (11–13). For example, do the regions of rapid warming coincide with locations where species can produce abundant seed (Fig. 1B)? If so, does seed production translate to juvenile recruitment? Here, we combine continent-wide fecundity estimates from the Masting Inference and Forecasting (MASTIF) network (13) with tree inventories to identify North American hotspots for recruitment and find that species are well-positioned to track warming in the West and North, but not in parts of the East.Open in a separate windowFig. 1.Transitions, hypothesized effects on spread, and sites. (A) Population spread from trees (BA) to new recruits is controlled by fecundity (seed mass per BA) followed by recruitment (recruits per seed mass). (B) The CTH that warming has stimulated fecundity ahead of the center of adult distributions, which reflect climate changes of recent decades. Arrows indicate how centroids from trees to fecundity to recruitment could be displaced poleward with warming climate. (C) The RSH that cold-sensitive fecundity is optimal where minimum temperatures are warmer than for adult trees and, thus, may slow northward migration. The two hypotheses are not mutually exclusive. B and C refer to the probability densities of the different life stages. (D) MASTIF sites are summarized in SI Appendix, Table S2.2 by eco-regions: mixed forest (greens), montane (blues), grass/shrub/desert (browns), and taiga (blue-green).Suitable habitats for many species are projected to shift hundreds of kilometers in a matter of decades (14, 15). While climate effects on tree mortality are increasingly apparent (16–19), advances into new habitats are not (20–23). For example, natural populations of Pinus taeda may be sustained only if the Northeast can be occupied as habitats are lost in the South (Fig. 2). Current estimates of tree migration inferred from geographic comparisons of juvenile and adult trees have been inconclusive (2, 7, 21, 24, 25). Ambiguous results are to be expected if fecundity and juvenile success do not respond to change in the same ways (20, 26–29). Moreover, seedling abundances (7, 30) do not provide estimates of recruitment rates because seedlings may reside in seedling banks for decades, or they may turn over annually (31–33). Another method based on geographic shifts in population centers calculated from tree inventories (3, 34) does not separate the effects of mortality from recruitment, i.e., the balance of losses in some regions against gains in others. The example in Fig. 2 is consistent with an emerging consensus that suitable habitats are moving fast (2, 14, 15), even if population frontiers are not, highlighting the need for methods that can identify recruitment limitation on population spread. Management for forest products and conservation goals under transient conditions can benefit from an understanding of recruitment limitation that comes from seed supply, as opposed to seedling survival (35).Open in a separate windowFig. 2.Suitable habitats redistribute with decade-scale climate change for P. taeda (BA units m² /ha). (Suitability is not a prediction of abundance, but rather, it is defined for climate and habitat variables included in a model, to be modified by management and disturbance [e.g., fire]. By providing habitat suitability in units of BA, it can be related it to the observation scale for the data.) Predictive distributions for suitability under current (A) and change expected from mid-21^st-century climate scenario Representative Concentration Pathway 4.5 (B) showing habitat declines in the Southwest and East. Specific climate changes important for this example include net increases in aridity in the southeast (especially summer) and western frontier and warming to the North. Occupation of improving habitats depends on fecundity in northern parts of the range and how it is responding. Obtained with Generalized Joint Attribute Modeling (see Materials and Methods for more information).We hypothesized two ways in which fecundity and recruitment could slow or accelerate population spread. Contemporary forests were established under climates that prevailed decades to centuries ago. These climate changes combine with habitat variables to affect seeds, seedlings, and adults in different ways (36, 37). The “climate-tracking hypothesis” (CTH) proposes that, after decades of warming and changing moisture availability (Fig. 3 A and B), seed production for many species has shifted toward the northern frontiers of the range, thus primed for poleward spread. “Fecundity,” the transition from tree basal area (BA) to seed density on the landscape (Fig. 1A), is taken on a mass basis (kg/m² BA) as a more accurate index of reproductive effort than seed number (38, 39). “Recruitment,” the transition from seed density to recruit density (recruits per kg seed), may have also shifted poleward, amplifying the impact of poleward shifts in fecundity on the capacity for poleward spread (Fig. 1B). Under CTH, the centers for adult abundance, fecundity, and recruitment are ordered from south to north in Fig. 1B as might be expected if each life-history stage leads the previous stage in a poleward migration.Open in a separate windowFig. 3.Climate change and tracking. (A) Mean annual temperatures since 1990 have increased rapidly in the Southwest and much of the North. (Zero-change contour line is in red.) (B) Moisture deficit index (monthly potential evapotranspiration minus P summed over 12 mo) has increased in much of the West. (Climate sources are listed in SI Appendix.) (C) Fecundity (kg seed per BA summed over species) is high in the Southeast. (D) Recruits per kg seed (square-root transformed) is highest in the Northeast. (E and F) Geographic displacement of 81 species show transitions in Fig. 1A, as arrows from centroids for adult BA to fecundity (E) and from fecundity to recruitment (F). Blue arrows point north; red arrows point south. Consistent with the RSH (Fig. 1B), most species centered in the East and Northwest have fecundity centroids south of adult distributions (red arrows in E). Consistent with the CTH, species of the interior West have fecundity centroids northwest of adults (blue arrows). Recruitment is shifted north of fecundity for most species (blue arrows in F). SI Appendix, Fig. S2 shows that uncertainty in vectors is low.The “reproductive-sensitivity hypothesis” (RSH) proposes that recruitment may limit population growth in cold parts of the range (Fig. 1C), where fecundity and/or seedling survival is already low. Cold-sensitive reproduction in plants includes late frost that can disrupt flowering, pollination, and/or seed development, suggesting that poleward population frontiers tend to be seed-limited (40–44). While climate warming could reduce the negative impacts of low temperatures, especially at northern frontiers, these regions still experience the lowest temperatures. The view of cold-sensitive fecundity as a continuing rate-limiting step, i.e., that has not responded to warming in Fig. 1C, is intended to contrast with the case where warming has alleviated temperature limitation in Fig. 1B. Lags can result if cold-sensitive recruitment naturally limits growth at high-latitude/high-altitude population frontiers (Fig. 1C). In this case, reproductive sensitivity may delay the pace of migration to an extent that depends on fecundity, recruitment, or both at poleward frontiers. The arrows in Fig. 1C depict a case where optimal fecundity is equator-ward of optimal growth and recruitment. The precise location of recruitment relative to fecundity in Fig. 1C will depend on all of the direct and indirect effects of climate, including through seed and seedling predators and disturbances like fire. Fig. 1C depicts one of many hypothetical examples to show that climate variables might have opposing effects on fecundity and recruitment.Both CTH and RSH can apply to both temperature and moisture; the latter is here quantified as cumulative moisture deficit between potential evapotranspiration and precipitation, D=∑m=112(PETm−Pm) for month m, derived from the widely used Standardized Precipitation Evapotranspiration Index (45). Whereas latitude dominates temperature gradients and longitude is important for moisture in the East, gradients are complicated by steep terrain in the West, with temperature tending to decline and moisture increase with elevation.We quantified the transitions that control population spread, from adult trees (BA) to fecundity (seeds per BA) to recruitment (recruits per kg seed) (Fig. 1A–C). Fecundity observations are needed to establish the link between trees and recruits in the migration process. They must be available at the tree scale across the continent because seed production depends on tree species and size, local habitat, and climate for all of the dominant species and size classes (13, 46). These estimates are not sufficient in themselves, because migration depends on seed production per area, not per tree. The per-area estimates come from individual seed production and dispersal from trees on inventory plots that monitor all trees that occupy a fixed sample area. Fecundity estimates were obtained in the MASTIF project (13) from 211,000 (211K) individual trees and 2.5 million (2.5M) tree-years from 81 species. We used a model that accommodates individual tree size, species, and environment and the codependence between trees and over time (Fig. 1C). In other words, it allows valid inference on fecundity, the quasisynchronous, quasiperiodic seed production typical of many species (47). The fitted model was then used to generate a predictive distribution of fecundity for each of 7.6M trees on 170K forest inventory plots across the United States and Canada. Because trees are modeled together, we obtain fecundity estimates per plot and, thus, per area. BA (m² /ha) of adult trees and new recruits into the smallest diameter class allowed us to determine fecundity as kg seed per m² BA and recruitment per kg seed, i.e., each of the transitions in Fig. 1A.Recruitment rates, rather than juvenile abundances, come from the transitions from seedlings to sapling stages. The lag between seed production and recruitment does not allow for comparisons on an annual basis; again, residence times in a seedling bank can span decades. Instead, we focus on geographic variation in mean rates of fecundity and recruitment.We summarized the geographic distributions for each transition as 1) the mean transition rates across all species and 2) the geographic centroids (central tendency) for each species as weighted-average locations, where weights are the demographic transitions (BA to fecundity, fecundity to recruitment, and BA to recruitment). We analyzed central tendency, or centroids (e.g., refs. 3 and 34) because range limits cannot be accurately identified on the basis of small inventory plots (21). If fecundity is not limiting poleward spread (CTH of Fig. 1B), then fecundity centroids are expected to be displaced poleward from the adult population. If reproductive sensitivity dominates population spread (RSH of Fig. 1C), then fecundity and/or recruitment centroids will be displaced equator-ward from adult BA. The same comparisons between fecundity and recruitment determine the contribution of recruitment to spread.