Four Decades of Plant Community Change Along a Continental Gradient of Warming

Received: 7 May 2018 | Revised: 10 October 2018 | Accepted: 2 December 2018 DOI: 10.1111/gcb.14568

PRIMARY RESEARCH ARTICLE

Four decades of plant community change along a continental gradient of warming

Antoine Becker‐Scarpitta | Steve Vissault | Mark Vellend

Département de Biologie, Université de Sherbrooke, Sherbrooke, Québec, Canada Abstract Many studies of individual sites have revealed biotic changes consistent with climate Correspondence Antoine Becker‐Scarpitta, Département warming (e.g., upward elevational distribution shifts), but our understanding of the de Biologie, Université de Sherbrooke, tremendous variation among studies in the magnitude of such biotic changes is mini‐ Sherbrooke, Québec, Canada. Email: [email protected] mal. In this study, we resurveyed forest vegetation plots 40 years after the initial surveys in three protected areas along a west‐to‐east gradient of increasingly steep Funding information Natural Sciences and Engineering Research recent warming trends in eastern Canada (Québec). Consistent with the hypothesis Council of Canada, Grant/Award Number: that climate warming has been an important driver of vegetation change, we found 5804 an increasing magnitude of changes in species richness and composition from west to east among the three parks. For the two mountainous parks, we found no significant changes in elevational species’ distributions in the easternmost park (raw mean = +11.4 m at Forillon Park) where warming has been minimal, and significant upward distribution shifts in the centrally located park (+38.9 m at Mont‐Mégantic), where the recent warming trend has been marked. Community Temperature Indices (CTI), reflecting the average affinities of locally co‐occurring species to temperature conditions across their geographic ranges (“Species Temperature Indices”), did not change over time as predicted. However, close examination of the underpinnings of CTI values suggested a high sensitivity to uncertainty in individual species’ tempera‐ ture indices, and so a potentially limited responsiveness to warming. Overall, by test‐ ing a priori predictions concerning variation among parks in the direction and magnitude of vegetation changes, we have provided stronger evidence for a link be‐ tween climate warming and biotic responses than otherwise possible and provided a potential explanation for large variation among studies in warming‐related biotic changes.

KEYWORDS biodiversity, climate changes, community ecology, forest, historical ecology, legacy data, long‐term monitoring, plant community, resurvey, understory vegetation

1 | INTRODUCTION & Yohe, 2003; Rooney, Wiegmann, Rogers, & Waller, 2004; Urban, 2015), phenology (Cleland, Chuine, Menzel, Mooney, & Schwartz, Climate is a dominant driver of large‐scale plant distributions 2007; Menzel et al., 2006), distributions (Bertrand et al., 2011; Kelly (Pearson & Dawson, 2003). On smaller spatial and temporal scales, & Goulden, 2008; Lenoir, Gegout, Marquet, de Ruffray, & Brisse, changes in local climatic conditions can lead to modifications of spe‐ 2008), and local adaptation (Aitken, Yeaman, Holliday, Wang, & cies’ abundances (Vellend et al., 2017), risks of extinction (Parmesan Curtis‐McLane, 2008). Although many such changes have been

Glob Change Biol. 2019;1–13. wileyonlinelibrary.com/journal/gcb © 2019 John Wiley & Sons Ltd | 1 2 | BECKER‐SCARPITTA et al. observed in previous studies, the magnitude of response varies tre‐ the 1970s, during the time that many provincial parks were being mendously from study to study, and we have only a limited under‐ planned and established in Québec. Plots were widely distributed standing of the processes underlying this variation. throughout each park and were typically placed in mature forest Most of the world's natural vegetation is dominated by long‐ stands. Since the time of the original surveys, these forests have lived perennial plants (Grime, 1977), and so we expect vegetation not experienced any major anthropogenic disturbances (National responses to environmental change to occur slowly relative to the Capital Commission‐Commission de la Capitale National, 2005; Parc time span of a few years (or less) typical of ecological studies (Tilman, Canada, 2010; Parc National du Mont‐Mégantic, 2007), thus mini‐ 1989). A key strategy used to assess longer term temporal changes in mizing possible confounding causes of vegetation change. plant communities is the resurvey of plots initially surveyed decades The province of Québec (Canada) spans >1,000 km east–west, ago, often referred to as “legacy” studies (Chytrý, Tichý, Hennekens, & over which there is a marked gradient of warming over the past Schaminée, 2014; Hédl, Bernhardt‐Römermann, Grytnes, Jurasinski, ~60 years (see Appendix S1 and Yagouti, Boulet, Vincent, Vescovi, & Ewald, 2017; Perring et al., 2017; Vellend, Brown, Kharouba, & Mekis, 2008). At the tip of the Gaspé Peninsula, the location of McCune, & Myers‐Smith, 2013). An important limitation of such our most easterly site, Forillon National Park (Figure 1), warming has studies is their constrained ability to test the ecological mechanisms been least pronounced, likely due to the climatic buffering effect of underlying temporal community change. Indeed, most legacy stud‐ the Atlantic Ocean (see Appendix S1). In contrast, Gatineau Park in ies pertain to a single site or region, meaning a set of plots within an continental western Québec has experienced marked warming, with area sharing a similar climate and history, in which case community Mont‐Mégantic Provincial Park in between both geographically and change might be caused by many local changes, such as ongoing land in terms of the magnitude of warming (Figure 1 and S1, Yagouti et al., use (Hermy & Verheyen, 2007; Kampichler, van Turnhout, Devictor, 2008). To the best of our knowledge, very few studies have used & van der Jeugd, 2012; Newbold et al., 2015), historical management legacy data to specifically test for contrasting vegetation responses legacies (Becker, Spanka, Schröder, & Leuschner, 2016; Perring et al., in sites with variable warming trends but otherwise similar ecological 2017; Vanhellemont, Baeten, & Verheyen, 2014), nitrogen deposi‐ conditions and history (but see Steinbauer et al., 2018 and Menzel tion (Becker‐Scarpitta, Bardat, Lalanne, & Vellend, 2017), or grazing et al., 2006). (Frerker, Sabo, & Waller, 2014; Vild et al., 2016). Our core hypothesis is that areas with greater warming will Causes of community change at a single site are often assessed have experienced stronger vegetation changes than areas with less by comparing observed changes in community composition across warming (Chen, Hill, Ohlemuller, Roy, & Thomas, 2011; Wang, Wen, space or time with predictions based on drivers of interest, such as Farnon Ellwood, Miller, & Chu, 2017). We take advantage of this climate warming. For instance, as predicted by the climate warming unique combination of original studies along a warming gradient to hypotheses, many species have experienced a shift in distribution perform a regional‐scale analysis of temporal change in forest plant toward higher elevations (Gottfried et al., 2012; Pauli et al., 2012; communities. Results for Mont‐Mégantic, including significant up‐ Sproull, Quigley, Sher, & González, 2015; Stockli, Wipf, Nilsson, & ward elevational distribution shifts and increased local species rich‐ Rixen, 2012) or latitudes (Boisvert‐Marsh, Périé, & Blois, 2014; ness, were reported in a previous paper (Savage & Vellend, 2015), to Hickling, Roy, Hill, Fox, & Thomas, 2006; Parmesan et al., 1999 but which we here add data for Gatineau Park (stronger warming trend) see VanDerWal et al., 2012). Given that plant species richness tends and Forillon Park (weaker warming trend). We tested the following to be greater in warmer areas, a local‐scale increase in richness is specific predictions: (a) The magnitude of upward shifts in eleva‐ also predicted due to warming, at least in the absence of severe tional distributions is stronger at Mont‐Mégantic (already observed) moisture stress (Vellend et al., 2017). Finally, if each species is first than at Forillon Park (tested in this paper). (Elevational variation in characterized by its geographic affinity with different temperature Gatineau Park is minimal—insufficient to test for temporal shifts in conditions (using a “Species Temperature Index” [STI]), then the av‐ species distributions.) The magnitude of (b) the temporal change in erage affinity across species in a local community (the “Community species richness, (c) the temporal change in community composi‐ Temperature Index” [CTI]) is predicted to increase in response to tion (R2 from the “time” effect in a multivariate analysis), and (d) the warming (Devictor, Julliard, Couvet, & Jiguet, 2008; Devictor et al. magnitude of temporal increase in the CTI vary in magnitude among 2012). Although there have been considerable advances in testing parks as follows: Forillon (the least warming)

(a) (b) 2,000 km 200 km

950 mi 100 mi

N N

Forillon

Gatineau Québec Mont-Mégantic

FIGURE 1 Location of study sites in (a) Canada and (b) the Province of Québec. The red box in (a) shows the area used for extraction of species occurrences in the calculation of Species Temperature Indices (STI): 60˚-90˚W; 30˚- 60˚N. The provincial capital Québec City is indicated as a spatial reference point of the province (Figure 1). The three study sites are located either 2.2 | Dataset in federal Canadian National Parks or in Québec Provincial Parks, where forest exploitation is prohibited (National Capital Commission‐ All original vegetation surveys were conducted using phytosociologi‐ Commission de la Capitale National, 2005; Parc Canada, 2010; Parc cal methods (Chartrand, 1976; Majcen, 1981; Marcotte & Grandtner, National du Mont‐Mégantic, 2007). 1974). In fixed‐area square plots (see below), authors made a full Forillon National Park, located at the eastern extremity of the list of vascular plant species in different strata (i.e., canopy trees, Gaspé peninsula (48°54′N, 64°21′W), was created in 1970 and shrubs, herbs) with abundance coefficients per species assigned fol‐ covers 245 km2, with our study plots ranging in elevation from ~50 lowing the scale of Braun‐Blanquet, Roussine, and Nègre (1952). In to 500 m a.s.l. The vegetation at Forillon is characterized in large our analyses, we pooled shrubs and herbs into a single “understory” part by boreal species, such as Abies balsamea (L.) Mill., Picea glauca stratum and given the limited representation of the tree community (Moench) Voss, and Betula papyrifera Marshall. At low elevation, in smaller plots (90 m2, see below), we focused all analyses on the temperate deciduous or mixed forests are dominated by Acer sac‐ understory data. For analyses, Braun‐Blanquet classes were con‐ charum Marsh. and Betula alleghaniensis Britt. (Majcen, 1981). verted to a percentage value representing the midpoint of a given Mont‐Mégantic Provincial Park is located in the Eastern abundance class. Townships region of Québec (45°27′N, 71°9′W), about 650 south‐ None of the original survey plots were permanently marked, but west of Forillon Park and 15 km north of the US borders with New for all three parks plot coordinates were reported in maps and/or Hampshire and Maine. The park was created in 1994 (logging ceased tables. As such, plots are considered “semi‐permanent”, which in‐ in the 1960s prior to park planning) and covers ~55 km2. Our study troduces the possibility of pseudo‐turnover due to relocation un‐ plots range in elevation between ~460 and 1,100 m a.s.l. Vegetation certainty (Hédl et al., 2017; Kapfer et al., 2017; Stockli et al., 2012; patterns are very similar to Forillon, with a somewhat more visually Vellend, Brown, et al., 2013). However, previous studies have shown evident elevational gradient: at low elevations, temperate decidu‐ that conclusions are robust to uncertainty in plot relocation, which ous forests are dominated by A. saccharum Marsh., Fagus grandifolia adds statistical noise but not systematic bias (Kopecký & Macek, Ehrh., and B. alleghaniensis Britt., while at high‐elevation boreal for‐ 2015). In our study, original surveyors tended to sample mature ests are composed largely of A. balsamea (L.) Mill. and Picea rubens forest stands where spatial heterogeneity was relatively low, thus Sar. (Marcotte & Grandtner, 1974). reducing any effects of plot relocation uncertainty. We used origi‐ Gatineau Park is located in southwestern Québec (45°35′N, nal plot maps and environmental descriptions (elevation, slope, as‐ 76°00′W), in the Outaouais region, 360 km west of Mont‐Mégantic. pect) to select potential locations for resurvey plots in a GIS (QGIS The park was established in 1938, covers 361 km2, with relatively Development Team 2016, Open Source Geospatial Foundation little elevational variation compared to the other parks (250 m ele‐ Project). Potential locations were visited in the field, with the final vational range). Contrary to Forillon and Mont‐Mégantic, our vege‐ location of a given plot determined by the best match to the orig‐ tation sampling was not spread throughout the entire park (access inal location and description. Logistical limitations prevented us to certain sectors of the part is restricted). Our study area (~30 km2) from resurveying all original plots in Forillon and Gatineau. At is largely dominated by A. saccharum Marsh and F. grandifolia Ehrh., Mont‐Mégantic, all plots within the current park boundary were sur‐ with a few more southerly tree species such as Tilia americana L., veyed in 2012 (see Savage & Vellend, 2015). Plot selection for our Quercus rubra L., Quercus alba L., or Fraxinus americana L. as well. recent surveys followed several criteria: (a) plots occurred in forest, 4 | BECKER‐SCARPITTA et al. excluding swamps or bogs; (b) plots were accessible via <3–4 hr hik‐ was calculated as the abundance‐weighted average of the STI across all ing off of trails (abandonment of old forest roads and trails since the species in a given plot. The STI for a given species is the median of the 1970s has reduced accessibility); (c) plots had not obviously expe‐ long‐term (1960–2010) mean annual temperatures calculated across rienced recent major natural disturbances (e.g., storms, fire, or in‐ all known occurrences of the species (methodology adapted from sect outbreaks); (d) in the original survey the plots were sampled in Devictor et al., 2008). To calculate STIs, we compiled an independ‐ mature stands that have since maintained forest cover (i.e., no early ent dataset by extracting all recorded occurrences for each species in successional dynamics in the intervening period). the Botanical Information and Ecology Network (BIEN—http://bien. At Forillon, the original survey was conducted in June–September nceas.ucsb.edu/bien/; Enquist, Condit, Peet, Schildhauer, & Thiers, 1972 in 256 vegetation plots of 500 m2 distributed throughout the 2016) in eastern North America: 60° to 90°W; 30° to 60°N (red box park (Majcen, 1981). We resurveyed 49 plots during July and August of Figure 1). We excluded occurrences further west, in order to control of 2015. At Mont‐Mégantic, the vegetation was originally surveyed in the range of variation in precipitation (precipitation decreases mark‐ 1970 in 94 plots, almost half of which were outside of the current park edly to the west of the deciduous forest biome). Our STIs thus reflect boundaries. The plot size was 400 m2 in coniferous forest and 800 m2 temperature affinities under precipitation conditions most comparable in broadleaved forests (Marcotte & Grandtner, 1974). Among the 94 to those found in our study region. For each occurrence point, we ex‐ original plots, 48 were revisited within the current park limits at Mont‐ tracted the annual mean temperature from ANUSPLIN, a model devel‐ Mégantic in 2012, with results reported in Savage and Vellend (2015). oped by Natural Resources Canada (http://cfs.nrcan.gc.ca/projects/3; In Gatineau Park, surveys were conducted in 33 plots of 90 m2 during McKenney, Pedlar, Papadopol, & Hutchinson, 2006). The abundance‐ the summer in 1973 (Chartrand, 1976) and 28 plots were resurveyed in weighted version of CTIw was calculated for each plot j as: summer 2016. We harmonized taxonomy across all three parks and two S = × time periods (see below), so the Mont‐Mégantic data are not precisely CTIwj (STIi RAij) (1) the same as reported in Savage and Vellend (2015). The study design i = 1 was perfectly balanced within parks for statistical analysis (i.e., there is the same number of plots between the original and recent surveys). The STI of species i is weighted by the relative abundance (RA) of species i in plot j (RA = the species local abundance divided by the sum of all S species’ abundances in that plot). Given some surprising 2.3 | Taxonomy results (a decrease over time of CTIw), we also explored analyses Our taxonomical reference for vascular plants was the Taxonomic of the unweighted version: CTIuw (median STI across species with Name Resolution Service v4.0 (assessed in Feb 2017: http://tnrs.ip‐ no weighting for abundance), thus focusing on which species were lantcollaborative.org). present in a given plot rather than their RAs. Our dataset was collected by five different survey teams, one Species Temperature Index values were calculated only for spe‐ for each of the three original surveys: Forillon: Majcen (1981); Mont‐ cies identified at the species level and with more than 50 occur‐ Mégantic: Marcotte and Grandtner (1974); Gatineau: Chartrand (1976), rences in the BIEN database (see Appendix S3—STI database). We one for the recent Mont‐Mégantic survey: Savage and Vellend (2015), chose a minimum of 50 occurrences as a balance between having and one for the recent Forillon and Gatineau surveys (A. Becker‐ sufficient data per species for estimates of STI and retaining as many Scarpitta and assistants). Most plants were identified to the species species in the analysis as possible. Note that compared to Savage level in the same way across surveys, such that the only harmoniza‐ and Vellend (2015) we used improved climate data (ANUSPLIN in‐ tion step for these taxa was to standardize names, which may have stead of WORLDCLIM) and updated distribution data (BIEN instead changed over time. In many cases, however, coarser levels of tax‐ of GBIF), thus leading to the potential for different results. onomic resolution (e.g., a pair of similar species not identified to the species level) were used in some but not all surveys, or the timing of 2.5 | Statistical analysis different surveys created doubt about the likelihood of comparable de‐ tection abilities (e.g., for spring ephemeral plants) (see Appendix S2 for All statistical analyses were performed in R v.3.4.2 (R Core Team 2017). details on taxonomic standardization). In these cases, the coarser level To test for upward elevational shifts in species distributions at Forillon of resolution was applied to all datasets, or species were removed to and Mont‐Mégantic, we selected species occurring in at least four plots maximize comparability. We deposited all specimens identified at the per survey in a given park. For each species in each park we calculated species level in the Marie‐Victorin herbarium (Institut de Recherche en the average abundance‐weighted elevation across occurrences. We Biologie Végétale, Université de Montréal, Canada) and all locations then conducted linear mixed effect models (LMM, function lmer, pack‐ were entered into the GBIF database (GBIF—https://www.gbif.org). age ‘lme4’ v.1.1‐14, Bates, Mächler, Bolker, & Walker, 2015) testing for a fixed effect of time period on abundance‐weighted mean elevation, with species as a random effect to account for the paired sampling 2.4 | Community Temperature Index structure of the data (each species observed in each time period). A predicted response of communities to warming is a temporal in‐ We first studied the relationship between α‐diversity (spe‐ crease in the CTI, which we calculated for all plots in each survey. CTI cies richness) and time using LMMs including time, elevation, BECKER‐SCARPITTA et al. | 5 and the time × elevation interaction (if significant) as fixed ef‐ 3 | RESULTS fects, and plot ID as a random effect. Because Gatineau has a negligible elevation gradient, we used a model for this park with 3.1 | Species elevational distributions only time and plot ID as a random effect. Coefficients of deter‐ In Forillon, where there has been the least warming in recent dec‐ mination were expressed as marginal R2 (R2 ), measuring the pro‐ m ades, there was no significant temporal change, on average, in under‐ portion of variance explained by fixed effects and conditional R2 story species’ elevational distributions (raw mean change = +11.4 m, (R2 ), giving the proportion of variance explained by both fixed c original survey mean = 195.4 ± 12.3 (SE) m; recent = 206.8 ± 12.3 m, and random effects. Both coefficients were computed using the t = 0.85, p = 0.41, Figure 2a, see Appendix S4 for species‐by‐spe‐ function r.squaredGLMM, package ‘MuMIn’ v.1.40.0 (Nakagawa & cies data). In contrast, a significant upward elevational shift was Schielzeth, 2013). observed at Mont‐Mégantic, which has experience marked warm‐ We then explored temporal change in β‐diversity (i.e., the vari‐ ing (mean change = +38.9 m, original mean = 622.1 ± 10 m, recent ability in species composition among communities) using permu‐ mean = 660.94 ± 10 m, t = 4.67, p < 0.001, Figure 2b). At Mont‐ tational analysis of multivariate dispersion. This analysis assessed Mégantic, on average species’ distributions have shifted 39 m to‐ the multivariate homogeneity of group dispersions based on Bray– ward higher elevations (~10 m per decade), and this was consistent Curtis distances (also called percentage‐difference distance), with along the spatial gradient (Figure 2b; see also Savage & Vellend, significance testing via permutation (function betadisper, package 2015). ‘vegan’ v.2.4‐4, Anderson, Ellingsen, & McArdle, 2006). A decrease in the multivariate distance between plots and the time‐specific centroid is interpreted as biotic homogenization, while an increase 3.2 | Species richness indicates biotic differentiation. To examine changes in community composition over time, At Forillon, for plot‐level species richness (α‐diversity) we found no we used permutational analysis of variance (PERMANOVA, significant temporal change (Tables 1a and 2), and the weak nega‐ with Bray–Curtis distances) using 999 permutations (func‐ tive trend of richness with elevation was not significant (Figure 3d, tion adonis, package ‘vegan’) (Anderson, 2001). We used the Table 1a). Across all plots we observed 18 fewer understory species R2 values from the PERMANOVA models as quantification of in the recent survey (65 species) than in the original survey (83 spe‐ the magnitude of temporal change in order to compare among cies); 27 species present in original survey were not found in the parks. We used nonmetric multidimensional scaling (NMDS) recent one, while we found nine new species (Table 2). It is impor‐ with Bray–Curtis distances for visualization (function metaMDS, tant to note that these are not likely to be gains and losses to and package ‘vegan’). from the entire park, but only to and from this set of semipermanent Temporal changes in the CTI were tested using LMMs for both plots. weighted and unweighted versions of CTI (CTIw and CTIuw, respec‐ At Mont‐Mégantic, richness declined significantly with ele‐ tively). Model structure was identical to the model for species rich‐ vation in both time periods (original: t = −6.97, p < 0.001; recent: ness. We included the interaction between time and elevation only if t = −6.91, p < 0.001, Figure 3e and Table 1a). Similar numbers of significant. understory plant species overall were found in the recent and

) (a) Forillon (b) Mégantic 400 900

800 300

700

200 600

100 500 Species mean elevation, recent (m 100 200 300 400 500 600 700 800 900 Species mean elevation, original (m)

FIGURE 2 Changes over time in species’ elevational distributions at (a) Forillon, n = 35 species, F = 0.70, p = 0.41 – no significant shift in elevation (raw mean change = +11.4 m), and (b) Mont-Mégantic, n = 50 species, F = 22.72, p < 0.001 – significant upward shift in elevation (mean change = +38.9 m). The diagonal line (1:1) represents no elevational change over time. Each point represents one species (occurring in minimum four plots per survey); see Appendix S4 for data 6 | BECKER‐SCARPITTA et al.

(a) (b) (c)

ns ****** 40

Species richness 20

FIGURE 3 Temporal changes in 60 (d) (e) understorey species richness. (a-c) Box plots of original and recent species richness per plot in the three parks. (d-e) Linear relationships between species 40 richness and elevation in the original Original survey and recent surveys at Forillon (n = 49*2 Recent survey plots, no significant relationship for either 20 original or recent surveys, see Table

Species richness 1a), and Mont-Mégantic (n = 48*2 plots, significant relationship for both original and recent surveys, see Table 1a). The 0 colored polygons around each regression 100 200 300 400 500 600 8001000 line represent 95% confidence intervals. Plot elevation (m) ***p < 0.001

TABLE 1 Results of linear mixed Coefficient F value df Pr(>|t|) R2 m R2c models (LMMs) predicting species (a) Plot richness (α diversity) richness and community temperature 2 2 Forillon Intercept 19.68 indices (CTIw). R m is the marginal R , measuring the proportion of variance Time −1.87 3.19 47 0.08 0.04 0.41 explained by fixed effects; R2c is the Elevation −0.01 1.26 46 0.27 conditional R2, giving the proportion of Mégantic Intercept 51.19 variance explained by both fixed and random effects. Values in bold are Time 5.77 26.77 47 <0.001 0.54 0.74 significant, p < 0.05 Elevation −0.04 68.14 46 <0.001 Gatineau Intercept 11.54 Time 4.39 17.15 27 <0.001 0.16 0.50 b) Community Temperature Index (CTIw) Forillon Intercept 6.42 Time −0.04 0.01 47 0.74 0.01 0.16 Elevation 0 0.57 46 0.46 Mégantic Intercept 7.74 Time 1.52 7.02 46 0.01 0.13 0.36 Elevation 0 4.57 46 0.04 Time × Elevation 0 9.57 46 0.003 Gatineau Intercept 8.14 Time 0.25 1.49 27 0.23 0.01 0.56 BECKER‐SCARPITTA et al. | 7

TABLE 2 Temporal changes in total species numbers and plot‐level species richness (α‐diversity). The total number of species observed across all plots is broken down into those shared, lost, or gained between the original and recent surveys. For plot‐level richness, means ± SE are reported. Values in bold are significant (p < 0.05, see Table 1a for statistical tests)

Total species number α‐diversity

Original Recent Shared Losted Gained Original Recent

Forillon 83 65 56 27 9 18.2 ± 1 16.4 ± 0.8 Mégantic 87 92 79 8 13 21.2 ± 1.5 27.0 ± 1.5 Gatineau 70 90 58 12 32 11.6 ± 0.8 15.9 ± 0.8

TABLE 3 Tests for temporal shifts in β‐diversity (PERMDISP) and community composition (PERMANOVA) of understory communities between original and recent surveys. β‐diversity is the mean distance between each plot and the time‐specific centroid in multivariate space (Bray–Curtis distances). R2 is the proportion of variation in community composition explained by time. Statistical significance levels were calculated with 999 permutations. Values in bold are significant, p < 0.05

β‐diversity Community composition

Original Recent F Pr(

Forillon 0.50 0.54 3.53 0.06 0.052 5.26 <0.001 Mégantic 0.53 0.50 2.56 0.11 0.076 7.78 <0.001 Gatineau 0.56 0.60 3.52 0.70 0.096 5.71 <0.001

FIGURE 4 Non-metric multidimensional scaling (NMDS) ordination of understorey community composition of all plots from all parks together for both original and recent surveys; stress=0.96. Ellipses show 75% confidence limits for each time survey within each park. We used two dimensions and Bray-Curtis distances 8 | BECKER‐SCARPITTA et al. original surveys (92 and 87 species, respectively); eight species shifts (R2) increased from Forillon (5%) to Mont‐Mégantic (8%) to from the original survey were not found, while we recorded 13 new Gatineau (10%) (Table 3). Appendix S5 reports the list of species species in recent survey (Table 2). Mont‐Mégantic showed a sig‐ frequencies. nificant increase over time in the plot‐level richness of understory species (27% increase on average, see Figure 3b and Tables 1a and 3.4 | Community Temperature Indices 2), and this increase was consistent across the elevational gradient (Figure 3e). The only significant temporal change in CTI (CTIw, the weighted Finally, in Gatineau Park, plot‐level species richness increased version) was found at Mont‐Mégantic, and the change showed significantly by an average of 38% (t = 4.14, p < 0.001, Figure 3c, a decrease in CTIw over time, the opposite of the predicted Tables 1a and 2). Overall, we found 20 more species in the recent sur‐ direction (Figure 5b,e and Table 1b). We detected no signifi‐ vey than in the original survey. Gatineau showed the largest study‐ cant changes in CTIw in Forillon or Gatineau (Figure 5a,d,c and wide gain in species, with 32 new species observed in the recent Table 1b). At Forillon, there was no significant relationship be‐ survey and 12 species from the original survey not observed in recent tween CTIw and elevation for either the original or recent survey one (Table 2). (Figure 5d and Table 1b), nor was there any relationship for the original survey at Mont‐Mégantic (Figure 5e and Table 1b). For the recent survey at Mont‐Mégantic, there was a significant nega‐ 3.3 | Understory community composition and tive relationship between CTIw and elevation (t = −3.1, p = 0.003, heterogeneity Figure 5e and Table 1b), suggesting a decrease over time in the At none of the three sites was there significant temporal change CTIw at high elevations but not low elevations (Figure 5e). When in β‐diversity (Table 3). However, we observed highly signifi‐ using the unweighted CTI (CTIuw), results were qualitatively the cant shifts in understory community composition for all study same for Forillon and Gatineau. At Mont‐Mégantic, however, we sites (Table 3). For Gatineau and Mont‐Mégantic, the shifts are found no effect of time and a clear and significant decrease in clearly visible in the NMDS run on all plots from all parks to‐ CTIuw with elevation for both the original and recent surveys (see gether (Figure 4). The magnitude of the understory compositional Appendix S6).

Forillon Mégantic Gatineau 10 (a) (b) (c)

6 Recent CTIw (°C)

4 468 10 468 10 46810 Original CTIw (°C) 10 (d) (e)

Original survey Recent survey

6 Plot CTIw (°C)

100 200 300 400 500 600 800 1000 Plot elevation (m)

FIGURE 5 Community Temperature Indices (CTIw) during the two-time periods and across the elevational gradient. (a-c) Abundance- weighted indices (CTIw) at Forillon, Mont-Mégantic, and Gatineau, with the 1:1 line indicating no temporal change between two times. (d-e) Relationships between CTIw and elevation for each time period at Forillon and Mont-Mégantic. Red and blue illustrate original and recent surveys, respectively. Each point is a plot in all panels BECKER‐SCARPITTA et al. | 9

4 | DISCUSSION complicated by different degrees of warming over the relevant time frames in different places. Moreover, there have been relatively few Many studies at single sites have revealed temporal changes in studies in North America, making our study not only a novel general species distributions, community composition, or phenology that contribution to global change biology but also a valuable regional‐ are consistent with predictions based on climate warming (Ash, scale contribution to our knowledge of changes in species distribu‐ Givnish, & Waller, 2017; Bernhardt‐Römermann et al., 2015; tions along elevation gradients in eastern North America. Bertrand et al., 2011; Lenoir, Gégout, Pierrat, Bontemps, & Dhôte, 2009; Rogora et al., 2018; Sproull et al., 2015). However, with ob‐ 4.2 | Species richness, composition, and servational data (i.e., most long‐term studies) it is always difficult heterogeneity to rule out alternative causes of temporal community change, such that comparative multisite studies are needed to strengthen Since warm areas tend to have higher local plant diversity than cold tests of the general hypothesis that biotic change over time has areas, climate warming is predicted to increase local plant diversity been influenced by climate warming (Verheyen et al., 2017). In this in many regions (Vellend et al., 2017). Consistent with our predic‐ study, we have taken advantage of a natural gradient in the degree tion, there was no significant temporal change in species richness of climate warming and of a protected area network in eastern over ~40 years at Forillon but significant increases were found at Canada, combining three resurvey efforts totaling >100 plots to Mont‐Mégantic and Gatineau. Some other studies in regions that test whether greater warming has led to more marked changes have experienced warming have also found increases of local vascu‐ in species distributions and community properties. Results were lar plant diversity (Klanderud & Birks, 2003; Steinbauer et al., 2018; mostly consistent with our predictions, with the magnitude of Stockli et al., 2012; Walther, Beißner, & Burga, 2005), although biotic changes (i.e., elevational distributions, species richness, temporal changes in species richness are highly variable (Vellend, composition) most often increasing from Forillon Park in eastern Baeten, et al., 2013; Verheyen et al., 2012). Québec, where the warming trend has been relatively weak, to We found significant temporal shifts in understory commu‐ Mont‐Mégantic where warming has been moderate, to Gatineau nity composition in all three parks, consistent with many studies Park in western Québec where the warming trend has been the in the literature showing species turnover through time (Dornelas strongest. Results for CTI were difficult to interpret, as discussed et al., 2014; Magurran et al., 2010; Shi et al., 2015). Comparisons further below. among parks were consistent with our predictions, with the mag‐ nitude of community shifts (R2) following the gradient of warm‐ ing: Forillon < Mont‐Mégantic < Gatineau. However, we found no 4.1 | Species’ elevational distributions evidence of biotic homogenization, in contrast to many studies in As predicted, species’ mean elevations shifted significantly upward literature (Jurasinski & Kreyling, 2007; Keith, Newton, Morecroft, at Mont‐Mégantic but not at Forillon. There is no elevational gradi‐ Bealey, & Bullock, 2009; Zwiener, Lira‐Noriega, Grady, Padial, & ent in Gatineau Park. On average, species at Mont‐Mégantic moved Vitule, 2018). In fact, our earlier study of Mont Mégantic reported toward higher elevations, as predicted if species are at least partially significant biotic homogenization (Savage & Vellend, 2015), and the spatially tracking their temperature optima in response to warming difference with the present study appears to be largely due to differ‐ (Kelly & Goulden, 2008; Savage & Vellend, 2015; Sproull et al., 2015). ences in data processing and analysis. The raw community data were Although the gradients in Forillon and Mont‐Mégantic cover sim‐ slightly different given our taxonomic standardization across sur‐ ilar elevational ranges (~500–600 m), the vegetation gradient is less veys in different parks and a few differences in which woody plants pronounced in Forillon Park than at Mont‐Mégantic. For instance, were considered part of the understory vs. canopy (e.g., Acer spica‐ Forillon's high‐elevation summits are not as predictably dominated tum was included in the understory in the current study but not the by boreal forest as they are at Mont‐Mégantic. This can be seen in earlier one). More importantly, Savage and Vellend (2015) first used the weaker relationships between plot richness and CTI with eleva‐ a fourth‐root transformation of abundance data prior to calculating tion at Forillon compared to Mont‐Mégantic (Figures 3d,e and 5d,e, Bray–Curtis differences (a recommendation in the PRIMER soft‐ Appendix S6). Despite these differences, the clear absence of any ware; Anderson, Gorley, & Clarke, 2008), whereas we saw no clear shift in elevational distributions in Forillon Park is consistent with justification for this in the present study. Applying the same trans‐ the hypothesis that climate warming is the probable cause of eleva‐ formation to our data revealed significant biotic homogenization for tional distribution shifts at Mont‐Megantic (and elsewhere). Mont Mégantic, but not for the other two parks (results not shown). The rate of elevational shift for the understory plants at Mont‐ This is of negligible consequence for the present study, given that Mégantic (~10 m per decade) is close to the global average of 11 m we did not have strong a priori predictions concerning beta diversity, per decade reported in the meta‐analysis of Chen et al. (2011), al‐ although it is clear that the earlier result of biotic homogenization though individual studies have reported higher values (e.g., ~22 m was not robust to alternative methods of analysis. per decade in southern California; Kelly & Goulden, 2008) and lower All observational studies involve uncertainty in making inferences values (e.g., no shift in elevation in Montana; Klasner & Fagre, 2002). about the cause of changes over space or time. Among potentially However, direct comparison among studies in different regions is confounding factors that can underlie temporal community changes, 10 | BECKER‐SCARPITTA et al. succession is of potentially high importance. However, our study was was not particularly abundant at high elevation in the original surveys designed specifically to minimize strong successional dynamics. We but became very abundant in the recent surveys. The contribution of resurveyed plots originally surveyed in mature stands that have main‐ D. carthusiana to CTIw for plots at high elevation (>800 m) increased tained closed canopies throughout the period of study. Importantly, from 9.5% to 47%. At Mont‐Mégantic, O. acetosella is more strongly we have no reason to suspect that forest dynamics (driven by factors associated with high‐elevation forests (i.e., colder sites) than is D. car‐ other than climate) varies among our three parks in a way that aligns thusiana, and so their changes in abundance are in one sense consis‐ with the gradient of climate warming. As such, the best supported hy‐ tent with the hypothesis that warming is a major driver of vegetation pothesis for explaining the temporal changes we observed along the change. But since the estimated STI (using independent data) was east–west gradient is that climate warming is a key driver. actually higher for O. acetosella than D. carthusiana, the changes in Resurvey studies also raise questions about the comparability abundance caused a decline in high‐elevation CTIw. In sum, the high of surveys in different years and in different parks (Vellend, Brown, sensitivity of CTI to the dynamics of individual species, combined et al., 2013). In this study, in order to minimize differences between with uncertainty in STI values (see also below), may reduce the de‐ the six surveys, we paid close attention to taxonomic homogeni‐ gree to which CTI acts as an indicator of climate warming. zation, and we consulted with botanists active in the 1970s (e.g., The calculation and interpretation of CTI has several limitations. Colette Ansseau, a collaborator of M. Grandtner's, and Z. Majcen) First, STI are calculated based on recorded species occurrences, in order to reproduce the exact same field survey methods used in but for many species we have limited knowledge of geographic the original studies. One difference among parks we could not avoid distributions, especially in northern regions or at high elevation. was plot size, with smaller plots in Gatineau than in Forillon and Furthermore, the method used in this study (using occurrence points) Mégantic. It is predicted that in small communities, the importance differs slightly from the original methodology described by Devictor of drift (stochastic changes in abundance) in driving community dy‐ et al. (2008) (using range maps). Second, the assumption that median namics should be relatively high (Ricklefs & Lovette, 1999; Vellend, temperature represents a species’ optimum is unverified and could 2016). As such, all else being equal, one might have expected re‐ be influenced by species attributes or other environmental factors duced detectability of deterministic community change over time in (Bowler & Böhning‐Gaese, 2017; Rodriguez‐Sanchez, De Frenne, Gatineau, yet we found the opposite: a stronger temporal increase & Hampe, 2012). As mentioned above, STI is greater (warmer) for in α‐diversity and a stronger directional shift in composition. Thus, Oxalis than for Dryopteris due to the more northern distribution if anything, we may have underestimated the difference between of Dryopteris. However, in eastern North America, Oxalis is known Gatineau and the other parks. to be more abundant in coniferous forests at high elevation while Dryopteris is more widely distributed along elevation gradient. Thus, if we used data from occurrences along elevational gradients (i.e., 4.3 | Community Temperature Indices at Mont‐Mégantic), Oxalis would have a lower STI than Dryopteris. The results for CTIw diverged most strongly from our predictions. In other studies, CTI has been shown to increase as predicted by Specifically, we failed to detect any temporal increase of CTIw in warming (Bowler et al., 2015; Devictor et al., 2008; Lindström, Gatineau, and contrary to our prediction, we found a significant de‐ Green, Paulson, Smith, & Devictor, 2012). In our study system, STIs crease in CTIw for high‐elevation plots at Mont‐Mégantic (see Figure 5e and therefore CTIs come with considerable uncertainty. and Table 1). This result suggests a “cooling” in terms of community af‐ In sum, we have provided empirical evidence of vegetation finities to temperature at high elevation, which has actually been previ‐ changes in eastern Canada that are largely consistent with the east– ously observed in the European Alps (Roth, Plattner, & Amrhein, 2014). west gradient in warming. Explicit comparisons of community change The fact that there was no such trend when using CTIuw indicates that among regions with variable climatic histories appear to be a powerful changes in particular species’ abundances drove the result for CTIw. method for increasing the confidence with which biotic trends can be In particular, two of the most abundant species experienced attributed to climate warming. To date, the magnitude of vegetation major temporal changes: (a) Oxalis acetosella L. (known also as Oxalis changes has been modest relative to the magnitude of warming itself montana Raf.) decreased in average abundance and (b) Dryopteris car‐ (Savage & Vellend, 2015), and climatic variation within (e.g., elevation) thusiana (Vill.) H.P. Fuchs increased in abundance (see Appendix S7). and among (e.g., latitude) protected areas appears to provide suitable Oxalis acetosella had a STI of 8.6°C. This species was often found at conditions for species with shifting distributions. Many unknowns re‐ unusually high abundance in the original surveys at Mont‐Mégantic, main, such as the functional attributes of “loser” and “winner” species, especially at high elevation (>800 m). On average, O. acetosella con‐ and the extent to which adaptive changes within species might also tributed ~74% to CTIw values for high‐elevation plots in the origi‐ contribute to warming responses. Continuing to exploit historical data nal survey, while contributing only ~8% in the recent survey (see sources of all kinds can help advance global change science. Appendix S7). Given abundance reductions at high elevation, the abundance‐weighted elevation of this species declined more than ACKNOWLEDGEMENTS any other, which represents an exception among the full set of spe‐ cies (O. acetosella is the rightmost point in Figure 2b), but which has a We thank the field and lab assistants who contributed to this pro‐ major effect on CTIw values. In contrast, D. carthusiana (STI = 7.6°C) ject: Diane Auberson‐Lavoie, Melissa Paquette, and Sara Gaignard. BECKER‐SCARPITTA et al. | 11

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