Partitioning Phylogenetic and Functional Diversity Into Alpha and Beta Components Along an Environmental Gradient in a Mediterra

Journal of Vegetation Science 24 (2013) 877–889 SPECIAL FEATURE: FUNCTIONAL DIVERSITY Partitioning phylogenetic and functional diversity into alpha and beta components along an environmental gradient in a Mediterranean rangeland Maud Bernard-Verdier, Olivier Flores, Marie-Laure Navas & Eric Garnier

Keywords Abstract Beta dissimilarity; Calcareous rangelands; Community assembly; Environmental gradient; Questions: To what extent is the functional structure of plant communities Functional traits; Phylogenetic community captured by phylogenetic structure? Are some functional dimensions better rep- structure; Trait phylogenetic signal resented by phylogenetic relationships? In an empirical study, we propose to test the congruence between phylogenetic and functional structure at the alpha and Nomenclature the beta scale along an environmental gradient. Bernard (1996) Location: Causse du Larzac, southern France. Received 1 April 2012 Accepted 12 December 2012 Methods: We measured species abundances and eight key functional traits in Co-ordinating Editor: Francesco de Bello 12 plant communities distributed along a gradient of soil depth and resource availability in a Mediterranean rangeland. A phylogenetic super-tree of the species was assembled, and after quantifying the degree of phylogenetic signal pres- Bernard-Verdier, M. (corresponding author, ent in each trait, we quantified taxonomic (TD), phylogenetic (PD) and [email protected]): Universite´ functional (FD) diversity both within (alpha scale) and among (beta scale) com- Montpellier 2, Centre d’Ecologie Fonctionnelle munities, taking species abundances into account. We tested for trends in diver- et Evolutive (UMR 5175), 1919 route de Mende, sity along the environmental gradient, and looked for congruence among 34293 Montpellier, France different facets of diversity, both at the alpha and the beta scale. Garnier, E. ([email protected]): CNRS, Centre d’Ecologie Fonctionnelle et Evolutive Results: We found a significant phylogenetic signal for seven out of eight traits. (UMR 5175), 1919 route de Mende, 34293 However, when accounting for trends in taxonomic diversity (i.e. richness and Montpellier, France evenness), PD did not capture the strong functional structure observed within Flores, O. (olivier.fl[email protected]): UMR Peuplements Veg etaux et Bioagresseurs en and among the communities. At the alpha scale, we found an overall pattern of Milieu Tropical, UniversitedelaR eunion, phylogenetic convergence of abundant species, which did not reflect the 97715, St Denis Messageries, France observed functional divergence. At the beta scale, despite some congruence Navas, M.-L. ([email protected]): between betaPD and betaFD for three individual traits, phylogenetic dissimilari- Montpellier SupAgro, Centre d’Ecologie ties did not capture the overall environmental and functional sorting of species Fonctionnelle et Evolutive (UMR 5175), 1919 according to habitats. route de Mende, 34293 Montpellier, France Conclusions: We show that even when traits display a significant phylogenetic signal, PD does not capture the complex functional structure of communities in response to environmental gradients. Nevertheless, results suggest that phylogenetic relationships may partially capture differences in the beta niche of species and provide additional insights on assembly processes not captured by the set of measured functional traits. Only by accounting for patterns in taxonomic diversity were we able to disentangle the functional and evolutionary determinants of species assembly along the gradient.

netic structure, deﬁned as the pattern of phylogenetic Introduction relatedness among species in communities (Cavender- Recent years have seen a growing interest in the use of Bares et al. 2009), has been used as a tool to understand phylogenetic information in community ecology (Webb community assembly (Webb 2000; Mayﬁeld & Levine et al. 2002; Mouquet et al. 2012). Community phyloge- 2010), as well as to predict ecosystem functioning (Cadotte

Journal of Vegetation Science Doi: 10.1111/jvs.12048 © 2013 International Association for Vegetation Science 877 Partitioning phylogenetic and functional diversity M. Bernard-Verdier et al. et al. 2009; Flynn et al. 2011). These approaches originally studies have investigated PD within communities, where stem from the concept of ecological niche conservatism processes of species co-existence, such as limiting similar- (reviewed in Wiens et al. 2010), a hypothesis stating that ity, are expected to shape local alpha diversity (Webb closely related species should share more ecological and 2000; Cavender-Bares et al. 2009). However, recent stud- functional similarities than distantly related ones. Based ies suggest that phylogenetic diversity may better capture on this assumption, a number of studies have interpreted assembly processes at the beta scale than at the alpha scale phylogenetic diversity (PD) as a surrogate for functional (Emerson & Gillespie 2008; Graham & Fine 2008; De Vic- diversity (FD) in communities (Webb 2000; Cadotte et al. tor et al. 2010). According to one line of reasoning, traits 2009; Violle et al. 2011). However, some authors have related to habitat preferences (i.e. beta niche traits) may be questioned this assumption (Cavender-Bares et al. 2004; more phylogenetically conserved within lineages than Silvertown et al. 2006; Losos 2008), and a consensus now determinants of local co-existence within communities seems to emerge from the literature stating that PD cannot (i.e. alpha niche traits), due to processes of sympatric niche in fact be considered as a simple proxy for FD (Mouquet differentiation among close relatives (Silvertown et al. et al. 2012). Studies comparing FD and PD tend to show 2001; Prinzing et al. 2008). Thus, phylogenetic differences an overall lack of consistency between phylogenetic and among communities, i.e. phylogenetic beta diversity, may functional patterns (Losos 2008; Swenson & Enquist 2009; reveal niche-based processes such as environmental but see Baraloto et al. 2012). Even in cases where clear sorting of species across habitats (Graham & Fine 2008; patterns of phylogenetic clustering or over-dispersion are Cavender-Bares et al. 2009). Although this hypothesis has detected, interpretations of assembly mechanisms are not found unequal support in the literature (Emerson & straightforward because different assembly processes may Gillespie 2008), quantifying phylogenetic beta diversity, create the same phylogenetic patterns (Losos 2008; May- and comparing it to the turnover in species and functional field & Levine 2010). traits along gradients, is a promising way to understand If PD cannot be interpreted as a simple proxy for FD, how ecological and evolutionary processes shape biodiver- then what do the non-random patterns of phylogenetic sity across landscapes and environmental gradients structure, consistently reported in very different systems (Graham & Fine 2008; Vamosi et al. 2009; Pavoine & (reviewed in Pavoine & Bonsall 2011), capture exactly? Bonsall 2011). One hypothesis is that PD may be related only to a few In this study, we investigate the functional information phylogenetically conserved traits. In this case, PD should captured by phylogenetic relationships both within and capture only assembly processes acting upon these traits among communities in a Mediterranean rangeland of (e.g. Cavender-Bares et al. 2004). However, if different southern France. To do this, we quantified and compared phylogenetically conserved traits display opposite patterns taxonomic, phylogenetic and functional diversity along a of convergence or divergence within a community, as seen gradient of soil depth and resource availability, along in recent trait-based studies (e.g. Cornwell & Ackerly which plant communities have been found to exhibit 2009; Spasojevic & Suding 2012; Bernard-Verdier et al. strong taxonomic and functional structures in previous 2012), then PD cannot be expected to capture such a mul- studies (Bernard-Verdier et al. 2012; Perez-Ramos et al. tiplicity of information. Another hypothesis is that PD may 2012). Using data for eight key functional plant traits, phy- be related to a complex combination of multiple ecological logenetic information from the latest published phyloge- traits capturing whole plant strategies, rather than individ- nies, and local species abundances, we aimed to answer ual traits (Flynn et al. 2011). In this case, one would the following questions: (i) can we detect phylogenetic expect PD to be more closely correlated to a multivariate structure, both within and among plant communities, in diversity score based on relevant traits, than to individual response to the environmental gradient; (ii) do phyloge- traits. A third hypothesis is that PD may in some cases cap- netic and functional diversities show congruent distribu- ture some ‘hidden’ aspects of plant functioning that are tions at the alpha and/or the beta scale; and (iii) is the not captured by any of the functional traits commonly existence of phylogenetic signal in traits a good indicator of measured in community studies (e.g. pathogen sensitivity; the correlation between PD and FD both within and Webb et al. 2006), and thus may show no congruence among communities? To answer these questions, we first with the measured FD. quantified the phylogenetic signal in each trait, and then Moreover, relationships between PD and FD are used a unified framework based on Rao’s quadratic expected to shift with increasing spatial scale (Emerson & entropy (Rao 1982) to partition phylogenetic and func- Gillespie 2008). PD may capture different processes of tional diversity within and among communities. We then assembly as one moves from diversity within communities tested the congruence between these different facets of (alpha scale) to diversity among communities (beta scale; diversity along the gradient, while accounting for patterns Graham & Fine 2008; Cavender-Bares et al. 2009). Most in species richness and evenness in communities.

Methods Trait data Study site and environmental gradient Eight plant traits were chosen to characterize different dimensions of the functional niche with respect to species The study was carried out on dry calcareous rangelands of morphology, phenology and chemical composition. Spe- southern France, at the INRA La Fage experimental station cies trait values were measured in a previous study (Ber- (43°55′N, 3°05′E, 790 m a.s.l.), located on a limestone pla- nard-Verdier et al. 2012) using standardized protocols teau (Larzac Causse), 100 km northwest of Montpellier, (Cornelissen et al. 2003). Traits were measured on 42–61 France. The plateau has a sub-humid mediterranean cli- species depending on traits, but always representing more mate, with cool wet winters and warm dry summers. For than 90% of the biomass in each plot (Pakeman & Quested the past 35 yr, the 260 ha of rangelands that constitute the 2009). Leaf traits – leaf dry matter content (LDMC; in mg experimental station have been grazed by a sheep herd dry mass per gram leaf fresh mass), specific leaf area (SLA; raised outdoors all-year-round for meat production. m2kg 1), leaf blade thickness (LT; lm), leaf nitrogen con- For our purpose, 12 plots of grassland (6 9 9 m) were centration (LNC; % leaf dry mass) and leaf carbon isotope selected to span the widest possible range of soil depth and ratio (d13C) – were chosen for their relationship to resource texture across the 160 ha of dolomitic rendzinas in the use and growth strategies (Grime 1977; Westoby et al. study site. Plots were dispersed over the study site without 2002; Wright et al. 2004), while seed mass (SM; mg) and any particular spatial or topological organization (Appen- the onset of flowering (OFL; day of year) were chosen to dix S1). Geographical distances between plots ranged from represent regenerative strategies and temporal reproduc- ca. 10 m to ca. 1.5 km, such that we consider dispersal lim- tive niches (Grubb 1977; Thompson 2000). Reproductive itations to be unlikely among plots. Environmental vari- height (Hrep; cm) was chosen as a trait pertaining to both ables (soil depth, texture, pH, total organic carbon, plant competitive and reproductive strategies (Garnier & available phosphorus, C/N ratio, nitrogen nutrition index, Navas 2012). Hrep and SM were log-transformed prior to spring soil water content) were measured and analysed analyses to meet normality. We chose to normalize the using a principal components analysis (PCA; see details traits showing exponential distributions (i.e. size-related Bernard-Verdier et al. 2012). The first axis (PC1) of the traits: SM and Hrep) to make them more comparable with PCA explained over 67% of the variability and was used in other traits and to be able to standardize their distribution all subsequent analyses as a single variable representing before including them with other traits in a multivariate the environmental gradient. Along PC1, plots varied from diversity index. shallow (ca. 10-cm deep) dry soils with low nitrogen availability, to deeper (ca. 1-m deep) and moister soils with higher nitrogen availability. Standing biomass increased Taxonomic and functional structure of communities from ca. 50 gm 2 on the shallow soils (with 10% bare ground) to ca. 250 gm 2 on the deeper soils (no bare In a previous study investigating community assembly in ground). There was no correlation between the environ- these same communities, Bernard-Verdier et al. (2012) mental gradient (PC1) and geographical distances (see found a clear pattern of species turnover and functional Appendix S1, Fig. S1.2). community structure in response to the soil gradient. No trend in species richness was observed, but a steep decrease Vegetation data in the evenness of species abundances was detected towards the deeper and more productive soils (trend in Species abundances Gini–Simpson index; r = 0.76, P < 0.001). A strong turn- In June 2009, the abundances of vascular plant species over in species taxonomic composition was also detected were estimated using the pin-point method (Levy & Mad- along the gradient. Perennial grasses dominated all 12 den 1933) along five 3-m transects in each of the 12 plots communities, but the identity of the dominant grass (see Bernard-Verdier et al. 2012). We recorded species shifted as one moved from deep to shallow soils: Bromus abundance as the total number of times the pin hit a live erectus, the main dominant on deeper soils, gave way to organ belonging to a given species, across the 150 pin- Stipa pennata at intermediate soil depths, which was points distributed in each plot. The pin-point method of replaced by Festuca christianii-bernardii on the shallower botanical survey estimates the percentage cover of species, soils. Dicotyledonous species also became more abundant which also relates to relative biomass in grasslands (Jonas- on the shallower soils (Fig. 1), with dwarf shrubs such as son 1988). A total of 73 angiosperm species were recorded Helianthemum canum and Thymus dolomiticus becoming across the entire gradient, with plot (=local community) major co-dominant species. This taxonomic response to species richness ranging from 15 to 33 species (average the soil gradient was associated with a strong functional 19.7). response of communities. At both ends of the gradient,

100 Phylogenetic signal in traits

80 Phylogenetic signal, deﬁned as the tendency for related species to resemble each other more than they resemble 60 species drawn at random from the phylogenetic tree (Blomberg & Garland 2002), was tested for each trait using a range of metrics. Blomberg’s (Blomberg & Garland 40 K 2002) was used as an index to rank trait phylogenetic signals: the higher the K value, the stronger the signal, with 20 K = 1 corresponding to trait evolution according to a

Relative abundance (% cover) Brownian motion model. Because the K metric may be 0 Shallow Deep misleading for low samples, significance of the phyloge- Soil gradient (PC1) netic signal was also tested using the variance of PICs (phylogenetic independent contrasts; Felsenstein 1985). As a Other lineages Fabaceae Graminoids means of comparison, we also calculated two other met- Fig. 1. Relative abundance of lineages in communities along the soil rics: Moran’s I (Moran 1950) and Pagel’s Lambda (Pagel gradient. Graminoids represent species from the Poaceae and Cyperaceae 1999). PIC variances and K values (function phylosignal families, other lineages correspond to all other monocotyledon and non- in R package picante; R Foundation for Statistical Com- Fabaceae dycotyledon families. puting, Vienna, AT) were compared to null distributions obtained by shuffling (999 times) species labels at the processes of habitat filtering restricted the range of differ- tip of the phylogeny: observed values in the upper fifth ent traits, such as Hrep, SLA, LNC, LDMC, LT and SM. Leaf quantile of the null distribution indicated significant traits values (LDMC, LNC, d13C) tended to be divergent phylogenetic signal (Blomberg & Garland 2002; Kraft & within communities at shallow to intermediate soil depth, Ackerly 2010). Observed values of Moran’s I were tested but tended to converge on plots with deeper soils. By con- using a two–sided test as described in Gittleman & Kot trast, reproductive traits (SM and OFT) tended to be more (1990; function Moran.I in R package ape). Pagel’s divergent towards plots with deeper soils. Other leaf traits lambda was tested against a Brownian motion hypothe- (SLA and LT) tended to diverge only at intermediate soil sis using a maximum likelihood ratio test (function depths. phylosig in R package phytools; Revell et al. 2008). Due In the above-mentioned previous study, FD within local to an incomplete trait data set, the number of spe- communities, defined as functional divergence, was cies included in the phylogeny varied depending on assessed by calculating community-weighted variance traits, ranging from 45 for leaf thickness to 61 for the (CWV) and comparing it to a null model (identical to that onset of flowering. To check the bias induced by these used in the present study; see below). In the present study, unequal samples, we also tested trait phylogenetic signal we chose to use Rao’s quadratic entropy as a measure of on the subsample of 40 species common to all eight trait dispersion in order to have a common measure for traits. functional and phylogenetic diversity. Both indices are quite similar in calculation (de Bello et al. 2009), and Partitioning diversity using Rao’s entropy yielded comparable trends in FD within communities along the gradient (see Appendix S2). Rao’s quadratic entropy (Rao 1982) can be used to partition diversity within and among communities, into alpha, Phylogenetic data beta and gamma components (Pavoine et al. 2004; Hardy & Senterre 2007). Being distance-based, it provides a very Phylogenetic super-tree flexible framework that can be adapted to quantify and We assembled a phylogenetic super-tree for the 73 species compare different facets of diversity, such as taxonomic, recorded along the gradient, based on recently published phylogenetic or functional diversity among species (de molecular phylogenies and dated according to published Bello et al. 2010). It should be noted that we use the term fossil records and molecular ages (see Appendix S3). The ‘taxonomic diversity’ to refer to the diversity in species super-tree was well resolved (only 7/64 nodes were left as identity or composition, according to its recent use and def- unresolved polytomies) and spanned major angiosperm inition by de Bello et al. (2010) and other authors (e.g. De families (24 families), with their oldest common ancestor Victor et al. 2010; Richardson et al. 2012), and not accord- dating back to the divergence between eudicots and mono- ing to previous definitions referring to taxonomic hierar- cots, estimated as 322 million years ago. chy diversity.

Alpha diversity Distance measures Within each community k, the among-species diversity Several distance measures can be used to calculate Rao’s (alpha) was calculated using Rao’s coefﬁcient of diversity diversity index, depending on the facet of diversity under (Rao 1982; Pavoine et al. 2004): consideration. Taxonomic diversity was calculated using a

distance measure defined as dij = 1 when i ¼6 j,anddij = 0 Xn Xn when i = j, which is equivalent to calculating the Gini– aRaoðkÞ¼ dijpikpjk ð1Þ i¼1 j¼1 Simpson diversity index (Pavoine et al. 2004). Phyloge- netic distances were calculated for each pair of species as with pik the relative abundance of species i in commu- the age of their most recent common ancestor (in million nity k,and(dij) the distance between species i and j, years; Webb 2000). Euclidean distances were used to cal- which can be taxonomic, functional or phylogenetic (see culate functional distances between species. Multivariate below). This abundance-weighted formulation of alpha functional distances (i.e. Euclidean distances in the multi- diversity represents the expected distance between two trait space created by all eight traits), as well as single-trait individuals chosen randomly from the community. In functional distances were calculated. Euclidean properties other words, because it is weighted by abundances, it were ensured using R function quasieuclid (package ade4), represents the convergence or divergence of abundant when needed. To calculate multivariate Euclidean dis- species within communities. It is a generalization of the tances, species with at least data missing for one trait Gini–Simpson index of evenness that includes differences were removed from the analysis, which brought the among species. number of species to 40 in multivariate analyses. To check if the missing data introduced significant bias, we re-ran all single-trait and phylogenetic diversity analyses Beta dissimilarity on this subsample of 40 species and found similar Beta dissimilarity classically represents the turnover in results to those obtained with the larger sets of species species composition across communities and along envi- (results not shown). This was expected, given the fact ronmental gradients (Simpson 1949), but this notion has that Rao indices are abundance-weighted, and that the recently been extended to describe phylogenetic and func- missing species were all rare species in these communi- tional beta dissimilarities (Pavoine et al. 2004; Hardy & ties. Senterre 2007; Graham & Fine 2008). Rao’s dissimilarity As recommended in de Bello et al. (2010), in order to coefficient (Rao 1982) was used to compute taxonomic, make taxonomic, functional and phylogenetic distances functional and phylogenetic pair-wise beta dissimilarities comparable, we scaled all distances between 0 and 1 by between communities. This dissimilarity index represents dividing each type of distance by its maximum value in the expected distance (e.g. phylogenetic, functional) our data set prior to all analyses. between two individuals chosen randomly from two dis- tinct communities. It is based on the additive partitioning of the overall gamma diversity into within (alpha) and Statistical analysis among (beta) community diversity, and can be calculated Using a single framework such as Rao’s quadratic for each pair of communities, k and l, with the following entropy has the advantage of making different facets of equation (Pavoine et al. 2004): diversity more comparable, but may introduce mathe- cð þ Þ að ; Þ matical artifacts when comparing these facets (De b ð ; Þ¼ k l k l ð Þ Raopairwise k l c 2 ðkþlÞ Victor et al. 2010; Pavoine & Bonsall 2011; see also Pavoine et al. 2013). Through construction of the Rao with ck+l the gamma diversity of the pair of communities diversity index, FD and PD are both influenced by spe- (calculated with equation (1) using the mean of species cies richness and evenness (i.e. TD), at the alpha and relative abundances across the two communities) and the beta scale. As a consequence, a strong signal in TD a(k, l) corresponding to the mean alpha diversity of the along the gradient (e.g. due to differences in evenness two communities. Following recommendations from de among communities) may overwhelm any possible Bello (2010), to accurately quantify beta diversity inde- more subtle functional or phylogenetic patterns in com- pendently of alpha diversity, we applied Jost’s correction munities, and create an apparent strong correlation (Jost 2007) to c and a values prior to calculations between indices. Thus, in order to compare the pat- (see de Bello et al. 2010). Calculations were performed terns of FD and PD along the gradient, we needed to using the R function ‘rao’ provided in de Bello et al. control for the effect of TD, both at the alpha and the (2010). beta scale.

Alpha diversity along the gradient on beta dissimilarities along the gradient (Appendix S1, Fig. S1.3). We used a Mantel test to quantify the corre- Variation in the different facets of alpha diversity was lation of bTD, bFD and bPD with environmental dissimi- investigated along the environmental gradient. First, we larities (999 permutations). Environmental dissimilarity tested the correlation of taxonomic (aFD), functional was calculated as the absolute pair-wise difference in (aFD; univariate and multivariate) and phylogenetic (aPD) plot scores along the soil gradient (PC1). Furthermore, alpha diversities among themselves and against plot scores to control for dissimilarities in bTD, we tested functional on PC1. Preliminary analyses showed no influence of geo- and phylogenetic turnover along the gradient with par- graphic distances on alpha diversity along the gradient tial Mantel regressions using the permutation method (Appendix S1). recommended by Legendre & Fortin (2010) for small To control for trends in aTD along the gradient, we stan- sample sizes (method 1: permutations within the dardized aPD and aFD using a null model that shuffled response matrix; Legendre & Fortin 2010). Similarly, we abundances 999 times among species within each commu- used a partial Mantel test to measure the congruence nity (Bernard-Verdier et al. 2012). This null model main- between bFD and bPD while controlling for the effect of tained the observed community evenness and species bTD. richness constant (i.e. a constant aTD), while breaking all possible ties between traits (or phylogeny) and local species Results abundances. This standardized index was calculated as an effect size (ES) based on the proportion of null values infe- Phylogenetic signal rior to the observed value (scaled from 1to1;seemeth- We found significant phylogenetic signal (PS) in all traits ods in Bernard-Verdier et al. 2012), with negative except specific leaf area (SLA; Table 1), although all had a (alternatively positive) ES indicating a trend towards func- PS lower than expected under a Brownian model (K < 1; tional or phylogenetic convergence (alternatively diver- Blomberg & Garland 2002). According to Blomberg’s K, gence). We tested for overall positive (or alternatively the trait with the highest phylogenetic signal was the leaf negative) effect sizes across all 12 communities using non- d13C isotope ratio (d13C), followed by leaf nitrogen concen- parametric two-sided Wilcoxon rank tests. We also tested tration (LNC), seed mass (SM) and leaf dry matter content for trends in alpha diversity along the gradient by testing (LDMC). These four traits were also loosely correlated the correlation between effect sizes and the soil gradient among themselves (Table S1). Reproductive height (Hrep), (PC1). onset of flowering (OFL) and leaf thickness (LT) had a lower but still significant phylogenetic signal in our regio- nal species pool. It should be noted that the phylogenetic Taxonomic, functional and phylogenetic turnover along the signal measured in this study, and the ranking among gradient traits, is contingent on the pool of species under study, and We used pair-wise beta dissimilarities (bRao) to investi- may not be extrapolated to a broader range of angiosperm gate the turnover in taxonomic, phylogenetic and func- species and families. Down-sampling the trait data set to tional diversity along the soil gradient. Preliminary include only the 40 species common to all traits slightly analyses showed no influence of geographic distances modified trait phylogenetic signals, with the PS of leaf

Table 1. Phylogenetic signal in eight functional traits according to four different metrics: Blomberg’s K index, phylogenetic independent contrasts (PIC) variance across the phylogenetic tree, Moran’s I and Pagel’s lamda. Traits are ranked by increasing values of K, i.e. by increasing phylogenetic signal. Bold font indicates signiﬁcant phylogenetic signals (P < 0.05; see details in Methods). The number of species indicates the size of the species pool used to calculate the phylogenetic signal for each trait.

Trait nb. species Blomberg’s K PIC variance Moran’s I Pagel’s lambda

KPDPIC PI P k P

SLA 52 0.242 0.147 0.726 0.164 0.019 0.857 0.001 0.998 LT 48 0.302 0.016 106.66 0.016 0.083 0.002 0.228 0.033 Hrep 50 0.315 0.024 0.002 0.013 0.121 <0.001 0.38 <0.001 OFL 61 0.339 0.001 16.82 0.002 0.051 0.008 0.725 <0.001 LDMC 52 0.408 0.003 120.14 0.002 0.103 <0.001 0.579 <0.001 SM 48 0.412 0.002 0.006 0.001 0.096 <0.001 0.553 0.010 LNC 45 0.431 0.002 0.383 0.002 0.110 <0.001 0.705 <0.001 d13C520.4330.001 0.019 0.002 0.087 <0.001 0.528 <0.001

Journal of Vegetation Science 882 Doi: 10.1111/jvs.12048 © 2013 International Association for Vegetation Science M. Bernard-Verdier et al. Partitioning phylogenetic and functional diversity thickness and the onset of flowering becoming non-signifi- than in the deeper soils (mostly Poaceae; Fig. 1, Appen- cant, but it did not change the ranking of traits according dix S2). to the K index (results not shown). By contrast, null model testing of multivariate functional alpha diversity (aFD) revealed no pattern of overall Alpha diversity convergence: we observed a decreasing trend in effect sizes, with functional divergence in communities on inter- Variation in alpha diversity along the gradient mediate to shallow soil depths, and convergence on the As previously reported in Bernard-Verdier et al. (2012), deepest soils only (Fig. 2e). When considering the diversity we found a strong trend in taxonomic alpha diversity of each trait individually, d13C, LDMC, SM and LNC were (aTD) along the gradient (Fig. 2a), representing a decrease the only traits with a significant linear trend in aFD in evenness towards the deeper soils. We found similar along the gradient, which decreased towards deeper soils decreasing trends in phylogenetic (aPD) and multivariate (Table 2). However, as reported in a previous study functional (aFD) alpha diversity along the gradient (Bernard-Verdier et al. 2012), null model testing (Fig. 2b,c). revealed more contrasted patterns of trait diversity along However, null model testing to control for the effect of the gradient, with leaf traits diverging on shallow to evenness revealed different phylogenetic and functional intermediate soils, and converging on deep soils, trends along the gradient (Fig. 2d,e). We detected an over- whereas reproductive traits had opposite trends (Appen- all significant signal of phylogenetic convergence in all dix S3). communities along the gradient (significant one-sided Wil- coxon signed-ranks test; Fig. 2d). Nevertheless, results fur- Congruence between aPD and aFD ther suggest that this phylogenetic convergence may be less strong towards the shallower plots (less negative effect Overall, we found no congruence between phylogenetic size; Fig. 2d), where abundant species belonged to a wider and functional alpha diversities (Table 2). This was mostly array of families (Cistaceae, Rosaceae, Lamiaceae, Poaceae) due to the incongruence between aPD and aFD at interme-

(a) αTD (b) αPD (c) αFD 0.9 0.7 r2 = 0.76*** r2 = 0.68*** 0.35 r2 = 0.63** 0.8 0.6 0.30

0.7 0.25 0.5 0.20 0.6 0.4 0.15 0.5 0.10 Shallow Deep Shallow Deep Shallow Deep Soil gradient (PC1) Soil gradient (PC1) Soil gradient (PC1)

(d) αPD Effect size (e) αFD Effect size 1.0 1.0

r = –0.25 ns r = –0.6* 0.5 W : obs < null** 0.5 W : ns

0.0 0.0

–0.5 –0.5

–1.0 –1.0 Shallow Deep Shallow Deep Soil gradient (PC1) Soil gradient (PC1)

Fig. 2. Alpha diversities within communities along the gradient. (a–c)Variationintaxonomic(aTD), phylogenetic (aPD) and multivariate functional (aFD) alpha diversities along the soil gradient, tested using a linear regression. (d, e) Variation of standardized values of aPD and aFD along the gradient. Positive effect sizes indicate phylogenetic/functional divergence, while negative effect sizes indicate phylogenetic/functional convergence. Variation in effect size along the gradient is tested with a linear correlation (r), and overall signal of convergence or divergence is tested with one-sided Wilcoxon tests (W). (ns: P > 0.05, *P < 0.05, **P < 0.01, ***P < 0.001).

Table 2. Variation in functional diversity within (aFD) and among (bFD) Congruence of functional and phylogenetic dissimilarities communities along the environmental gradient, and correlations with phylogenetic diversity (PD). Pearson correlations were used to test for the Partial Mantel tests revealed no correlation between bPD variations in aFD along the gradient and its correlation with aPD. Partial and multivariate bFD (Table 2). However, when consid- Mantel tests were used to test the correlation of bFD with environ- ering traits individually, three single trait bFD did show a mental dissimilarities (D gradient) and with bPD, while controlling for bTD. significant correlation with bPD: LNC, SM and Hrep (*P < 0.05, **P < 0.01, ***P < 0.001). (Table 2). These three traits had a significant phyloge- Trait Alpha diversity Beta dissimilarity netic signal, but not necessarily the strongest (see aFD bFD Table 1). In fact, it is interesting to note that some traits with stronger PS and a significant turnover along the gra- ~Gradient ~a PD ~D gradient ~b PD dient, such as d13C, showed no correlation at all with Multivariate 0.79** 0.43 ns 0.65*** 0.17 ns bPD. These contrasting responses among traits may LNC 0.61** 0.43 ns 0.25 ns 0.04 ns explain the absence of correlation observed between bPD d13C 0.89*** 0.78** 0.33* 0.03 ns b b LDMC 0.81** 0.57 ns 0.2 ns 0.55 ns and the multivariate FD, or between PD and the envi- SM 0.66* 0.29 ns 0.34* 0.58*** ronmental gradient. Hrep 0.55 ns 0.41 ns 0.60*** 0.55*** OFL 0.27 ns 0.21 ns 0.29* 0.08 ns Discussion LT 0.48 ns 0.15 ns 0.53** 0.39** SLA 0.49 ns 0.17 ns 0.44** 0.11 ns In this study, we investigated how phylogenetic diversity relates to functional and taxonomic diversity in plant communities, both at the alpha and the beta scale. We found diate soil depths, in which phylogenetic clustering co- communities were strongly structured in terms of taxo- existed with functional divergence (Fig. 2d,e; see also nomic, functional and phylogenetic diversity along a gradi- Bernard-Verdier et al. 2012). This finding concerned uni- ent of soil depth and resource availability. Among the variate as well as multivariate measures of FD, except for eight functional traits under study, seven displayed signifi- d13 one single trait, C, whose alpha diversity was positively cant phylogenetic signal in our species pool. Despite these a correlated to PD (Table 2). Nevertheless, once compared results, we show that the different facets of diversity are d13 to the null model, even C did not show a pattern of con- not equivalent and may capture different processes of com- vergence congruent with phylogenetic convergence at munity assembly along the gradient. By taking care to con- intermediate soil depths (Appendix S3). trol for the effect of species richness and evenness on diversity indices, we were able to discriminate the subtle Beta dissimilarities among communities patterns of mismatch and congruence among functional Correlation between beta dissimilarities and environmental and phylogenetic diversities, both at the alpha and the beta differences scales. Taxonomic pair-wise beta dissimilarities (bTD) were signif- Phylogenetic convergence and functional divergence icantly correlated to environmental dissimilarities within communities (Fig. 3a), confirming the influence of environmental factors in driving a turnover in species composition and abun- At the alpha scale, we detected an overall phylogenetic dances (see Bernard-Verdier et al. 2012). Phylogenetic convergence within communities, a pattern frequently dissimilarities (bPD) showed a similar trend (Fig. 3b), but reported in the literature (reviewed in Vamosi et al. 2009). multivariate functional dissimilarities (bFD) presented an Given the significant phylogenetic signal detected in seven even stronger correlation with environmental dissimilari- out of eight key functional traits under study, one could ties (Fig. 3c). This tighter link between functional dissimi- have expected an overall functional convergence within larities and environmental factors was confirmed in the communities (Webb et al. 2002; Cavender-Bares et al. partial Mantel tests controlling for the effect of bTD, which 2009). However, functional diversity within communities detected no significant correlation for bPD, but a signifi- did not reflect this phylogenetic convergence. On the cant correlation for the multivariate bFD (Fig. 3d,e). When contrary, complex patterns of functional divergence and considering single-trait beta dissimilarities, we found con- convergence were observed all along the gradient, both for trasting patterns depending on traits (Table 2): six traits – the multivariate functional index and for individual traits Hrep, SLA, LT, d13C, SM and OFL – had dissimilarities sig- (Fig. 3e, Appendix S2). Our results thus support the idea nificantly correlated with the environmental variations, that phylogenetic diversity cannot be used as a simple while LNC and LDMC showed no turnover associated with proxy for functional diversity (Emerson & Gillespie 2008; the gradient. Mouquet et al. 2012).

β = β = β = (a) TD rM 0.69*** (b) PD rM 0.68*** (c) FD rM 0.81*** 50 20 20

40 15 15 30 10 10 20 5 5 10

0 0 0 0246 0246 0246 Environmental dissimilarity Environmental dissimilarity Environmental dissimilarity

= = (d) PD residuals rM 0.17 ns (e) FD residuals rM 0.65***

4 4

2 2

0 0

–2 –2

–4 –4

0246 0246 Environmental dissimilarity Environmental dissimilarity

Fig. 3. Pair-wise beta dissimilarities among communities along the environmental gradient. (a–c) Taxonomic (bTD), phylogenetic (bPD) and multivariate functional (bFD) pair-wise beta dissimilarities are tested against pair-wise environmental dissimilarities using a Mantel test on Pearson coefﬁcients (rM). Environmental dissimilarities are the differences in plot scores along the axis of the soil gradient. (d, e) Graphical representation of partial regressions of bPD and bFD against environmental dissimilarities, while controlling for bTD; the residuals of the regressions bFD ~bTD (FD residuals) and bPD ~bTD (PD residuals) are plotted along environmental dissimilarities. Statistics for the partial Mantel test (rM) are indicated in the upper right corner of panels (ns: P > 0.05, ***P < 0.001).

This mismatch between phylogenetic and functional as the result of the overwhelming dominance of grami- diversity within communities was mostly apparent at noids (i.e. representing over 70% of cover on average; intermediate soil depths: communities were phylogeneti- Fig. 1), particularly at intermediate soil depths. It is well cally convergent but, at the same time, harboured the known that the general success of graminoids in grazed highest functional diversity of the gradient (Fig. 2e, ecosystems is related to traits conferring better tolerance to Appendix S3; see also Bernard-Verdier et al. 2012). These grazing and trampling (e.g. capacity for tillering, heavy results suggest that closely related species may successfully sympodial rhizome system, basal leaf meristems; Gibson co-exist at intermediate levels of stress and productivity by 2009), which were not measured in this study. Such traits diverging functionally, mainly in terms of reproductive are not easily quantifiable with continuous measures height and resource acquisition strategy (captured by leaf (Weiher et al. 1999), and would need to be added as dis- traits such as LDMC and SLA; Westoby et al. 2002). This is crete or binary variables in a diversity index using more consistent with recent findings suggesting that intermedi- flexible distance indices (such as the Gower distance; Pavo- ate abiotic environments play an important role in main- ine et al. 2009). In such an analysis, we would expect a taining and generating the striking trait diversity present convergence of these traits on intermediate to deep soils, within certain lineages (Hermant et al. 2012). consistent with the dominance of graminoids, and thus If none of the eight functional traits taken individually, congruent with the phylogenetic convergence. or the multivariate index, reflect the strong pattern of phylogenetic convergence at the alpha scale, then it is possible Phylogeny only partially captures the beta niche in these that phylogenetic relationships may capture some other communities unmeasured functional feature that converges within these rangeland communities. Indeed, phylogenetic con- Contrary to hypotheses from the literature (Silvertown vergence within these communities can easily be identified et al. 2001; Graham & Fine 2008), we did not detect strong

Journal of Vegetation Science Doi: 10.1111/jvs.12048 © 2013 International Association for Vegetation Science 885 Partitioning phylogenetic and functional diversity M. Bernard-Verdier et al. patterns of phylogenetic differentiation among communi- expectations from the literature, stating that traits related to ties in response to the gradient (i.e. at the beta scale). Phy- habitat preferences (i.e. beta niche traits) may be better cap- logenetic dissimilarities among communities were not tured by PD than traits involved in processes of local co-exis- related to environmental dissimilarities (Fig. 3d), despite tence (Silvertown et al. 2001; Emerson & Gillespie 2008). the existence of a strong turnover in species abundance and composition (Fig. 3a; see also Bernard-Verdier et al. Beyond phylogenetic signal in traits 2012). In contrast, we detected a strong functional turnover, Significant phylogenetic signal in traits was necessary but which supports the existence of environmental sorting of not sufficient to predict a correlation between PD and FD species according to habitat preferences (i.e. beta niche at any scale (Losos 2008; Swenson & Enquist 2009). For traits) along the gradient. Functional turnover along the instance, a trait such as LDMC had one of the highest phy- gradient was driven by dissimilarities in six traits, related to logenetic signals, but was never correlated to PD, either at both the reproductive (Hrep, SM, OFL) and the vegetative the alpha or at the beta scale (Table 2). As pointed out by (SLA, LT, d13C) phases (Table 2). These results are consis- previous authors (e.g. Losos 2008), this is not really sur- tent with a previous study (Bernard-Verdier et al. 2012) in prising, because testing the congruence between FD and which these traits were found to be filtered, i.e. restricted PD can be understood as investigating a phylogenetic sig- in range, within these communities. These traits can thus nal at the community scale, and not at the species scale (as be interpreted as traits relevant to the beta niche of species in PS). At the community scale, relationships between PD along this gradient in soil resources (Emerson & Gillespie and FD integrate a more complex signal, which takes into 2008). account both the phylogenetic signal of traits across spe- Because we chose to use abundance-weighted diversity cies, but also the effect of species sorting among communi- indices, beta dissimilarity measures were largely influ- ties, as well as the local distribution of abundances. The enced by the most abundant species, in particular the dom- very discrepancies observed between the signal at the com- inant grasses Bromus erectus, Stipa pennata and Festuca munity scale and the PS among species may provide addi- christianii-bernardii, which gradually replace each other tional information concerning community assembly (e.g. along the soil gradient (see Appendix S2). The fact that Cavender-Bares et al. 2004). these dominants belong to the Poaceae family certainly Moreover, although seven out of eight traits had a sig- contributes a large part to the low and non-significant phy- nificant phylogenetic signal, our multivariate index of logenetic turnover observed along the gradient. But diversity was never well correlated to phylogenetic diver- despite belonging to the same family, these species did sity. This does not support the hypothesis that phyloge- show clear functional differences, especially in terms of netic diversity may be more related to a multivariate index leaf and phenological traits, thus participating in the signif- of functional diversity (e.g. Flynn 2011). However, these icant functional turnover detected along the gradient. This conclusions may depend on the list of functional traits illustrates how a phylogenetic approach may be inade- selected. The multivariate index used in this study may not quate to capture the subtle functional turnover occurring be the best multidimensional descriptor of species niche in among dominant grasses, and driven by soil resource het- these communities, and different multivariate indices erogeneity in this rangeland. would probably show different patterns depending on the Nevertheless, although phylogenetic and functional dis- selected traits. Although the eight functional traits mea- similarities were not congruent when considering a multi- sured in this study were chosen to cover a wide array of variate functional index, we did find significant functional dimensions, from vegetative growth to regener- correlations when considering, individually, three traits ative strategies, and showed a strong response to the gradi- related to the beta niche in these communities: Hrep, SM ent in our communities, we did not include potentially and LT (Table 2). In this case, phylogenetic dissimilarities crucial traits pertaining to underground foraging and stor- did capture part of the beta niche of species, but not all of age strategies, such as root traits (Kembel & Cahill 2011). It its dimensions. Indeed, the turnover of other important would be interesting to investigate the diversity of under- beta niche traits along this gradient, such as SLA or d13C, ground traits in future analyses, which may provide a bet- were not captured by phylogenetic dissimilarities, which ter understanding of the processes creating functional, and likely explains the absence of phylogenetic beta structure phylogenetic, convergence within communities. detected along the environmental gradient. Overall, we found that the relationship between FD and Conclusions PD shifted from the alpha to the beta scale, with a slightly better congruence at the beta scale than at the alpha scale Overall, our results show that investigating the phylogenetic when considering single-trait diversity. This tends to support structure of communities can be used as a complement,

Journal of Vegetation Science 886 Doi: 10.1111/jvs.12048 © 2013 International Association for Vegetation Science M. Bernard-Verdier et al. Partitioning phylogenetic and functional diversity but not a substitute, for trait-based approaches of plant understand patterns of plant community productivity. PLoS community assembly. We show that, even when traits ONE 4: e5695. have a significant phylogenetic signal, phylogenetic diver- Cavender-Bares, J., Ackerly, D.D., Baum, D.A. & Bazzaz, F.A. sity is not a good indicator of functional structure within 2004. Phylogenetic overdispersion in Floridian oak commu- communities. Moreover, moving from the alpha to the nities. The American Naturalist 163: 823–843. beta scale revealed that beta niche traits in our communi- Cavender-Bares, J., Kozak, K.H., Fine, P.V.A. & Kembel, S.W. ties were only partially captured by phylogenetic dissimi- 2009. The merging of community ecology and phylogenetic – larities, thus limiting the power of PD to detect ecological biology. Ecology Letters 12: 693 715. sorting of species along an environmental gradient. Cornelissen, J.H.C., Lavorel, S., Garnier, E., Dıaz, S., Buchmann, N., Gurvich, D.E., Reich, P.B., Ter Steege, H., Morgan, H.D., However, phylogenetic convergence within these commu- Van der Heijden, M.G.A., Pausas, J.G. & Poorter, H. 2003. A nities did capture a pattern of community assembly (i.e. handbook of protocols for standardised and easy measure- the dominance of graminoids) that had not been detected ment of plant functional traits worldwide. Australian Journal with our functional approach. Confronting different facets of Botany 51: 335–380. of diversity provides a promising approach bringing Cornwell, W.K. & Ackerly, D.D. 2009. Community assembly together community ecology and evolutionary ecology, a and shifts in plant trait distributions across an environmental crucial issue in fields of research such as conservation gradient in coastal California. Ecological Monographs 79: 109– biology (Mouquet et al. 2012). Environmental gradients 126. provide an ideal context to disentangle the functional and de Bello, F., Thuiller, W., Leps, J., Choler, P., Clement, J.-C., evolutionary determinants of the alpha and the beta niche Macek, P., Sebastia, M.-T. & Lavorel, S. 2009. Partitioning of of species. functional diversity reveals the scale and extent of trait convergence and divergence. Journal of Vegetation Science 20: 475 Acknowledgements –486. de Bello, F., Lavergne, S., Meynard, C.N., Leps, J. & Thuiller, W. This work was funded in part by the ANR programme 2010. The partitioning of diversity: showing Theseus a way O2LA (09-STRA-09) and by the DIVHERBE project (ACI out of the labyrinth. Journal of Vegetation Science 21: 992– ECCO, ECOGER programme). M.B.V. was supported by a 1000. doctoral fellowship from the French Ministry of Education De Victor, V., Mouillot, D., Meynard, C., Jiguet, F., Thuiller, W. and Research. We thank J. Richarte for his invaluable help & Mouquet, N. 2010. Spatial mismatch and congruence in the field and B. Testi for help correcting species names between taxonomic, phylogenetic and functional diversity: in the phylogeny. We also thank C. Violle, M. Vellend, the need for integrative conservation strategies in a changing J. Ruffault, F. de Bello and three anonymous referees for world. Ecology Letters 13: 1030–1040. helpful discussions and comments on earlier versions of Emerson, B.C. & Gillespie, R.G. 2008. Phylogenetic analysis of the manuscript. community assembly and structure over space and time. Trends in Ecology & Evolution 23: 619–630. Felsenstein, J. 1985. Phylogenies and the comparative method. 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