Biodivers Conserv (2016) 25:1133–1149 DOI 10.1007/s10531-016-1113-y ORIGINAL PAPER

How soil and elevation shape local plant biodiversity in a Mediterranean hotspot Rafael Molina-Venegas1,2 • Abelardo Aparicio1 Se´bastien Lavergne3 • Juan Arroyo1

•

Received: 16 November 2015 / Revised: 5 April 2016 / Accepted: 16 April 2016 / Published online: 26 April 2016 Ó Springer Science+Business Media Dordrecht 2016

Abstract Elucidating how evolutionary and ecological factors drive the assemblage of communities in biodiversity hotspots remains an important challenge. This currently impedes our ability to predict the responses of communities to the ongoing global changes in these major world’s biodiversity reservoirs. Here, we focus on the Sierra Nevada mountain range, a core region of the Baetic-Rifan biodiversity hotspot in the western Mediterranean, and explore the relative importance of soil properties and elevation in shaping phylogenetic and functional diversity of shrub communities. We recorded the total number of each species in community transects across elevation gradients and contrasting soil conditions, and measured some ecologically relevant functional traits (specific leaf area, leaf carbon:nitrogen ratio, plant height and blooming duration). Phylogenetic distances among species were inferred from a genus-level time-calibrated molecular phylogeny. Elevation was the main factor predicting phylogenetic and functional alpha diversity of plant communities. Species in high-elevation communities were phylogenetically distant but functionally similar, being relatively smaller and having relatively short blooming durations, whilst species in low-elevation communities showed the opposite pattern. Beta diversity in SLA and leaf C:N ratio based on species incidences were positively correlated with a soil pH and micronutrient gradient. Specifically, communities that

Communicated by Daniel Sanchez Mata. Electronic supplementary material The online version of this article (doi:10.1007/s10531-016-1113-y) contains supplementary material, which is available to authorized users. & Rafael Molina-Venegas [email protected] 1

Departamento de Biologı´a Vegetal y Ecologı´a, Universidad de Sevilla, Apartado 1095, 41080 Seville, Spain

2

Present Address: Departmento de Ciencias de la Vida, Universidad de Alcala´, Alcala´ de Henares, Madrid, Spain

3

Laboratoire d’E´cologie Alpine, CNRS Universite´ Grenoble Alpes, BP 53, 38041 Grenoble Cedex 9, France

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develop on soils of high pH and low micronutrient concentrations showed low SLA values and high leaf C:N ratios, whilst communities on soils of lower pH and high micronutrient concentrations showed the opposite pattern. We conclude that soil properties and elevation simultaneously shape the structure of Mediterranean shrub communities by differentially acting on the different dimensions of the species niches. Elevation seems to filter plant height and phenology-related traits whereas nutrient-related functional traits are more related to soil properties. Our study illustrates the primary role of environmental heterogeneity for the maintenance of diversity in Mediterranean mountain ecosystems. Keywords Alpha and beta diversity  Baetic-Rifan range  Community ecology  Environmental filtering  Functional diversity  Phylogenetic structure

Introduction Despite the ‘renaissance’ of community ecology that occurred over the past decade (Mouquet et al. 2012), elucidating how evolutionary and ecological factors drive the assemblage of communities in biodiversity hotspots remains an important challenge (Mason and de Bello 2013). Much of the work focused on elucidating causes of high diversity in the hotspots has been achieved at regional scales, whereas community level studies are less frequent (but see Kembel and Hubbell 2006; Comita et al. 2010). Importantly, many ecological and evolutionary processes that ultimately shape biodiversity occur at the community scale (McIntire and Fajardo 2014; Valiente-Banuet et al. 2015), and therefore community-level studies are of paramount relevance for applied conservation. Further, understanding the mechanisms driving the assemblage of communities in biodiversity hotspots is critical if we are to predict their response to ongoing global changes (Ho´dar et al. 2011; Matı´as et al. 2012). The incorporation of phylogenetic information into community assembly studies has permitted the evaluation of the effect of the ancestor–descendant relationship on the present distribution of species in communities (Webb et al. 2002). Besides shedding light on the drivers of community assembly, phylogenetic data may also be highly valuable for conservation (Mouquet et al. 2012; Tucker et al. 2016), particularly in preserving the evolutionary potential of floras in biodiversity hotspots (Forest et al. 2007) and predicting ecosystem functioning (Srivastava et al. 2012). However, despite the advantages of incorporating phylogenetic information, there is evidence that phylogenies may be unable to capture all aspects of community structure (Carboni et al. 2013) given the varied evolutionary trajectories of the species’ niches (Ackerly and Cornwell 2007; Devictor et al. 2010). A solution to this problem consists in analyzing functional trait distributions within and among communities and along varied environmental gradients (de Bello et al. 2013; Mason et al. 2013). Thus, understanding the drivers of community structure requires quantifying species’ ecological differences based on either functional traits and phylogenetic information (Chalmandrier et al. 2013, 2015; de Bello et al. 2013), and studying community patterns along varied environmental gradients (Bernard-Verdier et al. 2012; Gross et al. 2013). Plant assemblages in the Mediterranean are characterized by a high turnover of narrowranging species and vegetation types along sharp environmental gradients (Thompson 2005; Molina-Venegas et al. 2013; Jime´nez-Alfaro et al. 2014). At regional scales, glacial refugia have played an important role in structuring the exceptional concentration of biodiversity in these ecosystems (Me´dail and Diadema 2009), allowing the long-term

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persistence of extant representatives of the flora that once existed under past climatic conditions (Herrera 1992; Postigo-Mijarra et al. 2009). At local scales, the enormous spatial heterogeneity that characterize Mediterranean ecosystems is a key factor for understanding the distribution of biodiversity in these species-rich biomes (Thompson 2005). Specifically, elevation gradients have been shown to be an important factor in structuring Mediterranean plant assemblages (Fontaine et al. 2007; Loidi et al. 2015; Molina-Venegas et al. 2015). However, less attention has been paid to the effects that soil properties have on the functional and phylogenetic structure of Mediterranean plant communities (but see Ojeda et al. 2010; Escudero et al. 2015). Mediterranean landscapes show a high incidence of stressful substrates that characterize the spatial heterogeneity of the region (Mota et al. 2008, 2011; Pe´rez Latorre et al. 2013). This lithological heterogeneity could be acting as local environmental filters that ultimately would lead to ‘clustered’ local trait variation compared to that of the surrounding habitats (Diamond 1975; de Bello et al. 2012). As well, strong phylogenetic clustering may be observed in such stressful environments due to deep phylogenetic signal in species niches (Kraft and Ackerly 2014; Molina-Venegas et al. 2015; Chalmandrier et al. 2015). However, because species do not coexist in isolation from one other, the resulting local species pool and observed composition of communities will be the result of both environmental filters and biotic interactions (Webb et al. 2002). Incidence-based functional composition of communities may mainly inform about environmental filters selecting species based on their physiological tolerance, whereas the abundance-weighted functional composition could be more related to the effect of biotic interactions (Chalmandrier et al. 2015). Thus, considered in tandem, diversity indices based on species’ incidence-only and abundance can provide evidence for different processes of community assembly. Moreover, the mosaic-like pattern of Mediterranean plant landscapes suggests a high diversity turnover in communities, and thus the decomposition of diversity into within-community (alpha diversity) and among-community (beta diversity) components should tease apart processes driving species coexistence within local sites and species distributions along environmental gradients (Hardy and Senterre 2007). In this study, we analyzed patterns of species incidence and abundance in vegetation surveys, along with multiple traits and phylogenetic information in order to assess the relative importance of soil properties and elevation gradients in shaping phylogenetic and functional diversity of Mediterranean shrub communities. We focused on the Sierra Nevada, a core range of the Baetic-Rifan biodiversity hotspot located between the southern part of the Iberian Peninsula (mostly in Andalusia) and northwest Africa (north Morocco) (Me´dail and Que´zel 1997; 1999) in the western Mediterranean. The Sierra Nevada provides an ideal eco-historical setting for assessing the role of elevation and soil properties in shaping shrub communities in Mediterranean mountain ecosystems. Indeed, this mountain range is one of the highest ranges in the Mediterranean Basin, and encompasses a wide array of edaphic conditions, thus harboring a great floristic and community diversity (Blanca et al. 1998).

Methods Study area The Sierra Nevada is among the highest mountain ranges in the Mediterranean basin and it also includes the tallest peak in the Iberian Peninsula (Mulhace´n, 3482 m a.s.l.). Its rugged

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topography harbours a heterogeneous lithology, with a broad central mica-schist core that extends linearly west-southwest-to-east-northeast for about 100 km. This siliceous central core is surrounded by a discontinuous Triassic limestone border (along with other less abundant substrates) that forms the middle and lower slopes of the sierra, and an extensive dolomite outcrop along its western edge (Martı´n et al. 2008). Dolomite is a sedimentary rock in which a good deal of calcium has been replaced by magnesium (Jones 1951), which implies high toxicity levels for plants (Brady et al. 2005; Venkatesan and Jayaganesh 2010) and may impose a severe restriction for grow and establishment (Mota et al. 2008). The whole area has been deeply eroded by generally north-to-south-flowing rivers, particularly in the southern slope. The climate is predominantly Mediterranean with precipitation concentrated in spring and autumn (mean annual precipitation in the range 200–900 mm), while the warmest season coincides with effective drought in summer. Although there is no clear cut rule for trends in precipitation in Sierra Nevada with increasing elevation, its west-to-east alignment means that, due to the prevailing Atlantic fronts, the western and northern valleys are generally more humid than the eastern and southern ones.

Vegetation survey We conducted fieldwork in Jun–Jul 2013. To cover the main array of soil conditions in Sierra Nevada, as well as the altitudinal and longitudinal variation in environmental characteristics, we selected two south-oriented elevation gradients for each of the three main types of bedrocks present in Sierra Nevada (mica-schist, limestone and dolomites, n = 6 elevation gradients), being separated from one other along the west-to-east axis of the range (Fig. 1). The dolomite elevation gradients were located towards the western edge of the Sierra Nevada since no large outcrops of this nature exist in the eastern part of the range. Within each elevation gradient, we drew at random three 75-m-long and 1-m-wide transects at three different elevations (*1300, *1650 and *1950 m a.s.l.) that passed through shrub vegetation (chamaephytes, nanophanerophytes and a few phanerophytes) on sunny slopes beyond the edge of the tree canopy (when present). We only selected one transect site on the dolomites at *1950 m because there is only one dolomitic peak over 1900 m in the Sierra Nevada. We avoid sampling at locations where there was clear evidence of recent disturbance, such as fires or pine plantations. Within each transect, we counted the total number of adult plants of each species and subspecies, and collected five healthy individuals (or part of them) of each species growing in full sunlight for functional trait measurements (see Appendix 1 in supplementary material for details). All plants collected were pressed and preserved for taxonomical identification following nomenclatural criteria in Blanca et al. (2009). Our dataset consisted of 11,316 individual plants belonging to 77 woody species.

Soil survey and analyses We took five soil samples at random along each transect at a depth of 10–20 cm and mixed them into a single bulk sample. We left these samples to dry for 24 h at room temperature and then passed them through a 2-mm sieve. The following physicochemical parameters were obtained: granulometry (% of sand, silt and clay), pH (at 25 °C 1:5), electric conductivity (lS/cm, at 25 °C 1:5), carbonates (%), oxidizable organic matter (%), concentrations of macronutrients (mg/kg of N-Kjeldahl and Olsen P) and micronutrients (mg/kg of Cu, Fe, Mn, Zn and Bo), and assimilable cations (meq/100 g of Ca, Mg, K and Na).

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Fig. 1 Map of Sierra Nevada in southern Iberian Peninsula, showing the location of the study transects (n = 17) along the elevation gradients. Circles, squares and diamonds represent the sampled communities on limestones, mica-schists and dolomites, respectively. The arrow in the inset shows the location of the Sierra Nevada in the western Mediterranean. The pictures show typical Mediterranean shrub communities in Sierra Nevada growing at high and low elevations (top and bottom pictures, respectively) on contrasting bedrocks (from left to right, limestones and mica-schists)

In order to avoid redundant information (collinearity) we applied principal components analysis (PCA) to soil parameters and retained the first two principal components as explanatory variables, which accounted for 42.9 % (PC1) and 25.5 % (PC2) of the soil

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Fig. 2 Graphical representation of the two principal components of the PCA analysis conducted on soil physicochemical parameters. Samples are displayed as numbered symbols and variables as vectors. Vector length represents the relative weight of the variables in the analysis, and were expanded to tweak the scaling of the two sets to a physically comparable scale. The numbers within the symbols represent elevation belts (1 = low elevation; 2 = medium elevation; 3 = high elevation). Variable labels: sand sand fraction; clay clay fraction; silt silt fraction; Mg magnesium; EC electric conductivity; Ca calcium; CO3 carbonates; P phosphorus; N nitrogen; OOM oxidizable organic matter; K potassium; Zn Zinc; Na sodium; Cu cooper, Mn manganese; Fe iron; Bo boron

parameter variance across the study transects, respectively. Negative scores of PCA1 were mainly related to carbonated and silty soils with high concentrations of Ca and N, and high electric conductivity, whereas positive scores corresponded to sandy soils. Negative scores of PCA2 were mainly due to high concentrations of micronutrients (Cu, Fe and Mn), whereas positive scores were related to high pH values (see Fig. 2; Tables S2, S3).

Functional traits In order to characterize the functional structure of communities, we measured the average specific leaf area (SLA) and the leaf carbon:nitrogen ratio (leaf C:N ratio) of each population of the species within transects using standardized protocols (Cornelissen et al. 2003, see Appendix 1 in supplementary material for details). We also obtained information about plant height and blooming duration of each species from the literature. These four traits reflect key components of plant fitness and biotic interactions (Cornelissen et al. 2003; Lavergne et al. 2003; Gross et al. 2009). In particular, plant height is associated to competitive ability and to trade-offs in tolerance and avoidance of environmental stress (Cornelissen et al. 2003; Ko¨rner 2003), SLA and leaf C:N ratio are related to soil resourceprocessing and maximum photosynthetic rate across species (Wright et al. 2004), and blooming duration is related to plant-pollinator interactions (Primack 1985).

Phylogenetic tree We used the genus-level time-calibrated phylogeny as described in Molina-Venegas and Roquet (2014). This phylogeny was inferred using a Maximum Likehood approach with a multilocus supermatrix of chloroplastic and nuclear DNA sequences (rbcL, matK, ndhF,

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trnL-F, ITS1 and ITS2) available in Genbank (accessed in September 2011) following the pipeline of Roquet et al. (2013). Node support was estimated using bootstrap values, and nodes with values less than 50 % were collapsed into soft polytomies (see Molina-Venegas and Roquet 2014 for full details on the phylogenetic procedure). The phylogeny includes all the genera in the dataset (n = 47). Species and subspecies were inserted as polytomies at the midpoint of the corresponding genus and species terminal branches, respectively.

Alpha and beta diversity and community-mean values We used the framework developed by de Bello et al. (2010) that partitions species diversity into independent a-, b- and c-components using Rao’s quadratic entropy index (Rao 1982). Because it is distance-based, it provides a very flexible framework that can be used to quantify different facets of diversity such phylogenetic and functional diversity of communities (de Bello et al. 2010). The Rao index can also incorporate species’ relative abundances and is thus highly suitable for detecting changes in the phylogenetic and functional composition of communities across environmental gradients. We used multiplicative partitioning to separate diversity components of pairwise transects (cpair) into within-transect (a) and among-transect (b) components. Here, c-diversity (cpair) was defined as cpair ¼

s X s X

dij pi pj

ð1Þ

i¼1 j¼1

where S is the total number of species in the two transects, Pi and Pj are the relative abundances of species i and j in the two transects, and dij is the dissimilarity (phylogenetic or functional) between the two species i and j. When considering species incidence rather than abundances, Pi and Pj are equal to 1 if species i and j are present in the transects, otherwise they are equal to 0. Likewise, a-diversity was defined as a¼

s X s X

dij pi pj

ð2Þ

i¼1 j¼1

where S is the total number of species within a given community, Pi and Pj are the relative abundances of species i and j, and dij is the dissimilarity between each pair of coexisting species i and j. Finally, b-diversity was multiplicatively partitioned as b¼

cpair  amean  100 cpair

ð3Þ

where amean is the mean local diversity of the pair of communities. We used the corrected computation of the Rao quadratic entropy index proposed in de Bello et al. (2010), along with an additional correction based on equivalent numbers proposed by Jost (2007), in order to avoid negative beta diversity values, which are biologically counterintuitive. We used a phylogenetic distance matrix of the recorded species based on the cophenetic distances of a hierarchical clustering and a Euclidean distance matrix of the species for each functional trait separately. Alpha and beta components of functional diversity indicate whether species are close to each other in the morpho-functional space within and between communities, respectively (de Bello et al. 2010). However, they are not informative about the magnitude of trait

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values. Thus, community-mean values (i.e. the mean of species trait values in each transect) were calculated to further characterize trait distributions in the communities.

Null model testing Raw values of phylogenetic and functional diversity are not highly informative because they may be affected by the number of taxa present in the communities. Therefore, we used effect size values to assess whether the observed diversity values differed from those expected given the extant phylogenetic and functional dissimilarities among all species (or populations) in the dataset (Kembel 2009). To do so, we compared the observed functional diversity of communities for each trait with their respective null distributions, generated by randomly shuffling trait values across populations in the whole dataset. Similarly, the observed phylogenetic structure of communities (i.e. phylogenetic distances) was compared with a null distribution of phylogenetic distances generated by randomly shuffling taxa labels across the tips of the phylogeny. Effect size values were calculated on the basis of the one-side probability (P) that the observed value is lower than expected by comparing with a null distribution of values (9999 runs): p¼

numberðnull\obsÞ þ numberðnull¼obsÞ 2 10000

ð4Þ

This one-side probability was used to calculate effect size values by subtracting 0.5 to P and multiplying by 2 (Kelt et al. 1995; Chase et al. 2011; Bernard-Verdier et al. 2012). This non-parametric calculation of effect sizes was preferred to the widely used standardized effect size (SES; e.g. Kembel 2009; Verdu´ et al. 2009) due to the asymmetry and lack of normality of most of the null distributions in the study. Effect size values vary between -1 and 1, with values close to -1 and 1 indicating that the observed values are lower and higher than expected based on the null distributions, respectively.

Statistical analysis Alpha diversity We investigated the effects of soil parameters (PCA1 and PCA2) and elevation on phylogenetic and functional alpha diversity of communities using both incidence-based and abundance data. We fitted multiple linear regressions with PCA1, PCA2 and elevation as predictors. In order to account for spatial trends in the data, we also included the longitudinal geographical coordinates of transects (x coordinates) as a predictor. The derived global model is as follows: a-diversity component  PCA1 þ PCA2 þ elevation þ longitude

ð5Þ

For each of the global models, we created a model set based on the global model (Eq. 5) up to a model including only the intercept, and compared the performance of the models within each set using Akaike’s information criterion (AIC). We retained the model with the lowest AIC score as the most likely combination of predictors. All models were fitted using maximum likelihood (ML) to allow for comparisons with AIC (Grueber et al. 2011).

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Beta diversity To investigate changes in phylogenetic and functional beta diversity with changes in soil properties (PCA1 and PCA2) and elevation among the study transects, we conducted Partial Mantel tests controlling for the geographical distance between transects (Legendre and Legendre 1998). The geographical coordinates of transects (x and y coordinates) were Z-transformed and the distance between transects was estimated as the Euclidean distance between each pair of coordinates. We tested the significance of the partial Mantel tests by permuting rows and columns of the response matrix 10,000 times. All analyses were carried out in R 2.15.1 (R Development Core Team 2012) with the software packages NLME (Pinheiro et al. 2012), NCF (Bjornstad 2013), PHYTOOLS (Revell 2012) and the R code implemented in de Bello et al. (2010).

Results Alpha diversity Elevation was the main factor predicting phylogenetic alpha diversity and some aspects of functional alpha diversity of communities. Specifically, phylogenetic alpha diversity was positively correlated with elevation (i.e. clustering at low elevations and overdispersion at higher elevations), whilst functional alpha diversity showed a negative correlation—albeit only for plant height and blooming duration (Table 1). Thus, species in high-elevation communities were phylogenetically distant but functionally similar, being relatively smaller and having relatively short blooming durations, whilst species in low-elevation communities showed the opposite pattern (Figs. 3, 4). Functional alpha diversity in SLA Table 1 Effects of soil parameters (PCA1 and PCA2), elevation and geographical longitude on phylogenetic and functional alpha diversity of communities (PD and FD respectively) a-Diversity component

Dataset

Significant effect

PCA1

PCA2

Elevation

Longitude

R2

PD

Abund.

Yes

–

–

0.001 *

-0.120

0.28

Inc.

No

0.28

FD—SLA FD—leaf C:N ratio FD—blooming duration FD—height

Abund.

No

Inc.

No

Abund.

No

Inc.

No

Abund.

Yes

–

–

20.001*

–

Inc.

Yes

–

–

20.001**

–

0.40

Abund.

Yes

–

0.057

20.001**

–

0.47

Inc.

Yes

–

0.087

20.002***

–

0.65 2

Estimators from the model with the lowest AIC score and the coefficient of determination (R ) are given. Significant regression estimators are in bold Abund. abundance data; Inc. incidence data. The column labelled ‘‘significant effect’’ indicates whether the corresponding a-diversity component showed a significant relationship with at least one of the explanatory variables *** P \ 0.001; ** P \ 0.01; * P \ 0.05

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Fig. 3 Scatterplots displaying community-mean values for plant height and blooming duration along elevation (top panels) and those for SLA and leaf C:N ratio along a gradient of soil pH and micronutrient concentrations (PCA2 of the principal components analysis of the soil parameters, bottom panels)

Fig. 4 Schematic representation of phylogenetic and functional alpha and beta diversity patterns in shrub communities along elevation and soil gradients in Sierra Nevada. Communities at low elevation show phylogenetic clustering, while communities at high elevation show phylogenetic overdispersion. Functional alpha diversity (tree silhouettes) decreases at high elevation (functional clustering) towards lower heights and shorter blooming durations. The double black arrow represents differences in beta-niche between communities of high SLA and low leaf C:N ratio growing in soils of relatively low pH and high micronutrient concentrations (grey background) and communities that show the opposite strategy in basic soils with low micronutrient concentrations (white background)

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and leaf C:N ratio showed no significant relationships with either elevation or soil properties.

Beta diversity Functional turnover in SLA and leaf C:N ratio based on species incidences displayed a positive correlation with changes in soil pH and micronutrient concentrations (PCA2) (Table 2). Specifically, communities that develop on soils of high pH and low micronutrient concentrations showed low SLA values and high leaf C:N ratios, whilst communities on soils of lower pH and high micronutrient concentrations showed the opposite pattern (Figs. 3, 4). Turnover in plant height and blooming duration based on both incidence and abundance data were positively correlated with elevation, whilst they showed a negative correlation with PCA2.

Discussion Elevation gradients have long been claimed as a decisive factor in shaping diversity patterns (von Humboldt 1849; Lomolino 2001) and particularly in the Mediterranean (Arroyo and Maran˜o´n 1990; Molina-Venegas et al. 2015). Also, the edaphic factor is known as a key determinant of evolutionary diversification and species distributions (e.g. Kruckeberg 1986; Rajakaruna 2004). In this study, we show how elevation and soil properties simultaneously shape the functional and phylogenetic structure of plant communities in a western Mediterranean biodiversity hotspot. Elevation was the main factor predicting the phylogenetic and functional alpha diversity of plant communities—albeit only for plant height and blooming duration. However, they varied in opposite directions, with phylogenetic and functional diversity increasing and decreasing towards high elevations, respectively. Further, the correlations between

Table 2 Correlation coefficients from Partial Mantel test investigating the effects of physicochemical soil parameters (PCA1 and PCA2) and elevation on phylogenetic and functional beta diversity among communities (PD and FD respectively) a-diversity component PD

Dataset

PCA1

PCA2

Elevation

Abund.

ns

ns

ns

Inc.

ns

ns

-0.17*

Abund.

ns

ns

ns

Inc.

ns

0.30**

ns

FD—leaf C:N ratio

Abund.

ns

ns

ns

Inc.

ns

0.23*

ns

FD—blooming duration

Abund.

-0.20 *

-0.22*

0.29**

Inc.

ns

-0.17

0.49**

Abund.

ns

-0.29***

0.32**

Inc.

ns

-0.19*

0.30**

FD—SLA

FD—height

Correlations were controlled by the geographical distance between transects Abund. abundance data; Inc. incidence data *** P \ 0.001; ** P \ 0.01; * P \ 0.05

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functional alpha diversity in plant height and blooming duration with elevation are expected to be even stronger at the population level, because high-elevation populations usually show smaller sizes and shorter blooming durations than those inhabiting lower elevations (Primack 1980; Ko¨rner 2003). Furthermore, these phylogenetically distant but functionally similar species were also dominant within the communities, since we found the same pattern using both incidence-based and abundance data. These results suggest that drastic environmental filtering is driving the assemblages in high-elevation communities in these mountains through phylogenetically convergent traits, that is, species harbouring similar trait syndromes in distant lineages. Small-size individuals necessarily keep buds and apical shoots near ground level to protect them from desiccation and frost during the adverse periods of the year (Cornelissen et al. 2003; Ko¨rner 2003). Also, favourable blooming durations of high mountain populations are usually constrained and overlap due to both abiotic (short growing seasons) and biotic factors (short pollinator activity periods) (Primack 1980; Arroyo et al. 1982). Overall, the high phylogenetic and lower functional diversity of high-elevation communities is very much in line with the known history of Mediterranean floras, where adaptation and endemism has repeatedly emerged through the local adaptation of distinct, globally distributed cosmopolitan families (Lavergne et al. 2013 and references therein). Nevertheless, the specific mechanisms of species interactions (i.e. competitive exclusion, facilitation) cannot be inferred from these analyses and may also be at stake in our study system. For example, it is expectable that increasing phylogenetic diversity observed at higher elevations would be a sub-product of positive interactions increasing with environmental stress (Butterfield and Callaway 2013; ValienteBanuet and Verdu´ 2013). We also found that communities at low elevation tended towards phylogenetic clustering. This pattern suggests that other non-considered functional traits may be driven the assemblage of communities through environmental filtering at lower elevations of the range, since close relatives in many plant groups tend to share similar phenotypic traits (Kraft and Ackerly 2014). It is known that environmental severity can be very high at lower elevations in montane habitats of Mediterranean-type climate zones due to summer drought (Cavieres et al. 2006). Overall, low elevation communities of the Sierra Nevada are dominated by few related species in the Lamiaceae (e.g. Rosmarinum officinalis, Teucrium capitatum subsp. capitatum, Lavandula lanata, Thymus vulgaris) and the Cistaceae (e.g. Cistus clusii subsp. clusii, Helianthemum syriacum, Fumana ericoides, Helianthemum cinereum subsp. rotundifolium) that develop on low-nutrient-stressed soils such us those derived from limestones and dolomites (Mota et al. 2008). Many of these species show a high accumulation of phenolics compounds, particularly during the summer drought, which has been hypothesized to be a general response of plants to stressful environments such us gypsum soils (Boscaiu et al. 2010). On the other hand, low elevation communities growing on mica-schists are dominated by a few species in the Fabaceae (e.g. Adenocarpus decorticans, Genista cinerea, Genista umbellata subsp. umbellata). These species are well-known by their ecological role in nitrogen fixation (Moro et al. 1996; West et al. 2005), which has been shown to be an evolutionary key innovation with a single origin in the evolution of angiosperms (Soltis et al. 1995). Thus, these species may have advantage over non-fixing species in soils derived from mica-schists, which showed relatively low availability of organic nitrogen in comparison with carbonated soils (see Fig. 2). Phylogenetic clustering driven by evolutionary key adaptations to stressful environments may also occur in other low elevation perennial plant communities in southeast Iberian Peninsula, such us inland salt marshes. These communities are dominated by few

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salt-resistant species in the Chenopodiaceae and other close related families such as Tamaricaceae, Plumbaginaceae and Caryophyllaceae (Rogel et al. 2000). As expected, we found significant relationships between beta diversity and the environmental gradients of the sierra. Functional turnover in plant height and blooming duration were positively correlated with elevation, whilst they showed a negative correlation with PCA2 (soil pH and micronutrient gradient). This result further remarks the importance of elevation gradients in shaping species distributions in Mediterranean mountain ecosystems. The negative relationship between functional turnover in plant height and blooming duration and the soil pH and micronutrient gradient is not surprising, since edaphic conditions varied independently of elevation and were more related to bedrock type (see Fig. 2). On the other hand, both SLA and leaf C:N turnover based on species incidences were positively related to changes in soil conditions (i.e. soil pH and micronutrient gradient, PCA2). Specifically, communities that develop on basic soils with low micronutrient concentrations (such as those derived from dolomites) harboured species with low SLA and high leaf C:N ratios, whilst communities on soils of lower pH and high micronutrient concentrations (such as those derived from mica-schists) showed the opposite pattern. Low SLA tends to reflect low growth rates due to slow nutrient capture and longer tissue turnovers in resource-poor habitats (Westoby et al. 2002; Wright et al. 2002). In fact, the relationship between SLA and soil fertility has been shown to be particularly significant in other Mediterranean shrublands suffering from harsh climatic conditions (Anacker et al. 2011). High leaf C:N ratios may indicate a lower investment in photosynthetic machinery and an increase of leaf thickness and dry matter content, which also may reflect low relative growth rates (Cornelissen et al. 2003). Additionally, plant growth is constrained under low-nutrient conditions but photosynthesis is less affected, which may lead to a re-allocation of carbon from growing to the building-up of carbonbased secondary metabolites (Tuomi et al. 1984; Bryant et al. 1985). This carbon reallocation may help to explain the high production of secondary metabolites in closely related species that develop on low-nutrient-stressed soils (Boscaiu et al. 2010). Nevertheless, turnover in SLA and leaf C:N ratio based on species abundances were nonsignificant, most likely because abundant species which seemed tolerant to various edaphic conditions (e.g. Ulex parviflorus subsp. parviflorus, Arenaria armerina subsp. armerina, Helianthemum apenninum subsp. suffruticosum, Bupleurum spinosum). This contributed to subtle differences between communities of different floristic composition. In conclusion, soil properties and elevation seem to simultaneously shape the structure of Mediterranean shrub communities by differentially acting on the different leading dimensions of the species niches. Elevation seems to filter plant height and phenologyrelated traits whereas nutrient-related functional traits are more related to soil properties. Our results illustrate the primary role of environmental heterogeneity for the maintenance of diversity, and highlight the importance of preserving not only species, but the variety of communities and landscapes that sustain biodiversity in species rich ecosystems on Earth (Hoekstra et al. 2005). Moreover, conserving ecological heterogeneity may not only help preserve greater species richness but also conserving the processes driving species differentiation as the basic engine of biodiversity. Acknowledgments We would like to thank the whole Sierra Nevada National Park staff and Juan Lorite (University of Granada) for help in the field; Juan Carlos Rubio (IGME) for providing lithological information; Mike Lockwood for revision of the English style; Jose M. Iriondo and Adrian Escudero for their comments on the sampling design; AGRAMA S.L. laboratory for the soil sample analyses; the University of Seville Microanalysis Service for the leaf sample analyses and to the EVOCA discussion group (http:// grupo.us.es/grnm210/web/index.htm). This work was supported primarily by the Spanish Organismo

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Auto´nomo de Parques Nacionales via grant 296/2011 and secondarily by the Regional Government of Andalusia (Grant P09-RNM-5280).

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