We analysed two different plant communities hosting Ionopsidium savianum (Brassicaceae), a species of EU interest included in the Habitats Directive 92/43/CEE annexes, for which specific studies on the ecology of communities where the species grows are lacking and more in-depth knowledge is needed. We examined two important sites of occurrence of this species in Tuscany with different soil types, namely limestone (Mt. Calvi) and serpentine (Mt. Pelato), to determine the structural and functional profile of the communities hosting this species in such different contexts. At each site, we surveyed the plant communities with I. savianum in ten 1 m² quadrats to determine information on communities' species composition and total plant cover, as well as taxonomic (species richness, and Shannon H’ index), phylogenetic (phylogenetic diversity, mean nearest taxon distance and mean pairwise distance) and functional diversity (focusing on Rao’s Q, leaf functional traits and adaptive strategies community weighted mean). We took into account site location, soil type, slope aspect and microrelief as plot-level environmental factors. The two communities were highly diverging from multiple points of view. Differences were in species composition, richness and diversity, with Mt. Calvi hosting higher diversity. The indices of phylogenetic diversity were influenced significantly by site and microrelief, allowing the presence of peculiar niches occupied by the fern Asplenium ceterach. From the functional point of view, communities at Mt. Calvi showed a higher functional diversity and a higher specific leaf area. Plant height was influenced by the slope aspect and was higher on north-facing slopes. In terms of Grime’s adaptive strategies, the Mt. Pelato communities resulted to be more stress tolerant than those surveyed at Mt. Calvi. Here, a decrease in stress-tolerant strategy associated with an increase in ruderal strategy was detected in communities on north-facing slopes.

Assembly rules, community ecology, CSR plant strategy, plant traits, serpentine soils, phylogeny

Ionopsidium savianum (Caruel) Ball ex Arcang. is a species belonging to Brassicaceae family, that occurs only in Northern Spain and in a few regions of Central Italy, namely Tuscany, Umbria and Latium (Gigante et al. 2014). It is a small annual species with erect habit, branched stems at the base, and an average height between 3 and 10 cm (Pignatti 1982). The genus Ionopsidium Rchb., which includes nine recognized species, constitutes the western Mediterranean clade (opposite to the central and northern European/arctic clade of Cochlearia L.) of the tribe Cochlearieae, a well-defined monophyletic lineage of Brassicaceae. These two genera resulted from a deep evolutionary split dating to the middle Miocene and separating the tribe into two clades with very different evolutionary dynamics (Kock et al. 2012). In Italy, I. savianum is categorized as Least Concern according to IUCN standards (Gigante et al. 2014). Moreover, it is considered a species worthy of conservation in the European Community, being included in the Habitats Directive 92/43/CEE, Annexes I and II, and according to the Geneva Convention. This species can be found on different substrates, as it grows mainly on limestone substrates but also on ultramafic outcrops (Gigante et al. 2014). In these different contexts it can be found predominantly in open communities like meadows, mountain and hill grasslands, path edges and edges of Mediterranean scrub vegetation, between 300 and 1.600 meters a.s.l.

Important hints to help fill the picture of relationships among species in a community can be offered by the evaluation of phylogenetic diversity. Indeed, the use of molecular phylogenies may help analyze the forces that influence patterns of biodiversity and biogeography, and in depicting the interactions among co-occurring species (Selvi et al. 2016). Especially when supported by data on functional diversity, phylogenetic information can be used in the study of the phylogenetic overdispersion or clustering of the community in relation to the variation of the habitat conditions (Erickson et al. 2014, Qian and Jiang 2014, Selvi et al. 2016, Mugnai et al. 2022).

Moreover, considering that soil type is one of the most important ecological factors for plant communities’ evolution and development, and is often pivotal in plant species diversification (Rajakaruna 2018), we compared the structure and functional profile of the communities hosting this species on limestone and serpentine. Particularly to the latter, it should be noted that serpentine outcrops are chemically extreme substrates, extraordinarily challenging for plant life (Lefèbvre and Vernet 1990). They are characterised by a multifaceted source of stress, linked to high concentrations of trace elements (namely Ni, Co, and Cr), along with other edaphic constraints, including high Mg concentration, low Ca/Mg ratio, high pH values, and heat stress (Brooks 1987; Gonnelli and Renella 2012; Kazakou et al. 2008; Rajakaruna and Boyd 2009). While taxonomic features are generally used to provide a description of plant communities, it is widely recognised that much more information can be evaluated by adopting a multifaceted approach, including functional traits (Garnier et al. 2004, Chase et al. 2019). In this sense, functional traits and their universal approach may inform on ecosystem multifunctionality and services, also providing insights into the plant communities' direct response, often easily interpretable, to environmental changes (Violle et al. 2007, 2014). Accordingly, trait-based metrics may be used together with taxonomic ones, as they may better depict biodiversity patterns across different spatial scales (de Bello et al. 2013, Mugnai et al. 2022), and for this reason, trait-based studies have become extremely common in plant ecology (Chelli et al. 2019). Despite this, through the review of trait-based ecological studies performed in Italy (Chelli et al. 2019), some gaps have been highlighted, such as the Mediterranean ecosystems are still poorly represented (e.g., Bricca et al. 2020, Stanisci et al. 2020, Mugnai et al. 2021). Moreover, Pierce et al. (2016) recently showed that the measurement of only three leaf functional traits: leaf area (LA), leaf dry matter content (LDMC) and specific leaf area (SLA), may be useful to assess the position of individuals in the framework of Grime's Competitive Stress-tolerant Ruderal (CSR) theory (Grime 1977, Grime and Pierce 2012).

In this study, we aimed at examining differences in taxonomic, phylogenetic and functional diversity of plant communities hosting I. savianum in two distant areas with limestone and serpentine substrates. This information is helpful in filling important gaps in the knowledge of the ecology of I. savianum, considering that specific studies on communities where the species grows are lacking and only phytosociological information can be usually found (Gigante et al. 2014). Particularly we expected a polarization of the communities of serpentine sites towards the Stress-tolerant strategy, and this should be reflected in the functional traits of the plant in the communities, based on the premises expresses above on the harsh conditions linked to the serpentine substrate. Moreover, we aimed to assess whether local micro-site conditions may affect the different facets of diversity in addition or in contrast to soil type.

The sampling resulted in 97 species (Suppl. Material 1, Table S1), with 14 shared species among the two habitats, 57 species exclusive of Mt. Calvi and 26 of Mt. Pelato. Plot-level environmental variables sampled or calculated are shown in Suppl. Material 2, Table S2.

According to the CCA, the species composition of plots resulted largely different among the two sites (p-value < 0.001, variance explained 17.5%, see Fig. 2), and also significantly influenced by northerness (p-value = 0.039, variance explained = 6.6%). Conversely, the effect of microrelief was not significant. The total variance was 4.51 and explanatory variables accounted for 29%. Axis 1 was linked to site, while the effect of northerness and microrelief (which appeared correlated) lay on Axis 2 (Fig. 2). The ISA (Table 1) confirmed a high differentiation among the plant communities at the two sites, with Mt. Calvi showing a higher number of indicators species than Mt. Pelato (14 and 9 significant indicator species, respectively).

The indices of taxonomic diversity were all significantly affected by the Site (which showed significant coefficients and generally high importance scores), but not by the plot-level conditions (Table 2). All the indices, i.e. species richness, total plant cover on the plot and species diversity expressed as Shannon H’ index, were higher at Mt. Calvi (Fig. 3).

All the indices of phylogenetic diversity resulted influenced by site and microrelief. Indeed, the effect of the latter changed among the two different sites (in all cases the interaction term site:microrelief was highly significant and with high importance scores; Table 3). At Mt. Pelato all phylogenetic diversity indices increased drastically as the plot's microrelief values increase, while almost no effect was detected for Mt. Calvi (Fig. 4).

Functional diversity expressed as Rao’s quadratic entropy was significantly different among the two sites (the term site was highly significant and showed a very high importance score; Table 4), and resulted higher at Mt. Pelato (Fig. 5A). Among the leaf functional traits, only SLA varied significantly among the two sites, with an interaction effect with northerness (p-value = 0.049; Table 4), although site was by far the more important term. Generally, SLA was smaller at Mt. Pelato, where no significant changes were recorded due to northerness, while at Mt. Calvi SLA appeared greater, and increased with the northerness (Fig. 5B). Plant height within communities was affected by northerness (p-value = 0.046; Table 4), indeed at both sites, it increased with the north exposition (Fig. 5C). Looking at the CSR adaptive strategies coordinates (Fig. 5D), both communities showed low participation of competitive species (Mean CWM C component: Mt. Calvi 13.31%, Mt. Pelato 10.12%), being dominated by stress-tolerant species (Mean CWM S component: Mt. Calvi 49.58%, Mt. Pelato 82.29%), but with an important contribution of ruderal species at Mt. Calvi (Mean CWM R component: Mt. Calvi 37.11%, Mt. Pelato 7.6%). The two communities were quite differentiated as to S- and R-strategies, and resulted both influenced by an interaction effect of northerness and site (p-value = 0.014 in both cases, see Table 4). In general, Mt. Pelato was characterized by a high contribution of the S strategy irrespective of slope aspect (no variation with northerness), while at Mt. Calvi the importance of the S strategy decreased at increasing northerness, with R-strategy importance increasing (Figs 5E and F).

Figure 2. 

Canonical correspondences analysis (CCA) ordination plot based on species composition of the communities at Mt. Calvi and Mt. Pelato. Site, northerness and microrelief are used as explanatory variables. Blue empty triangles represent the species, while filled red triangles represent plot centroids according to the site. Only 30 best-fitting species are shown (the first 30 species showing the highest correlation with the first CCA axis). See Suppl. Material 2, Table S2 for species names abbreviations.

Figure 3. 

Effect of the site on A) Species richness, B) Total plant cover and C) species diversity expressed as Shannon H’ index. Sites: C = Mt. Calvi, P = Mt. Pelato.

Figure 4. 

Effect of site and microrelief on the indices of phylogenetic diversity. A) standardized effect size of phylogenetic diversity (PD.ses); B) standardized effect size of mean nearest taxon distance (MNTD.ses); C) standardized effect size of mean pairwise distance (MPD.ses). Sites: red circles = Mt. Calvi, blue triangles = Mt. Pelato.

Figure 5. 

A) Functional diversity expressed as Rao’s quadratic entropy in function of site. B-F) Community weighted mean for the tested traits B) Specific leaf area (mm2/mg) and C) Plant mean height in function of site and northerness, D) Ternary diagram reporting the Grime's Competitive Stress-tolerant Ruderal (CSR) adaptive ecological strategies at the plot level, E) Stress-tolerant and F) Ruderal strategy in function of site and northerness. Sites: red circles = Mt. Calvi, blue triangles = Mt. Pelato.

Within this contribution, we aimed at analyzing the taxonomic, phylogenetic and functional features of two diverse plant communities hosting Ionopsidium savianum, growing at two important sites of occurrence of this species in Tuscany, with very different soil types: limestone (Mt. Calvi) and serpentine rocks (Mt. Pelato). The two communities investigated resulted to be different from multiple points of view.

Firstly, they differed taxonomically in terms of species composition, species richness, total cover and Shannon diversity, with Mt. Pelato showing lower values for all these indices. Such differentiation appears mainly explained by the different types of substrate in the two sites. Indeed, the substrate can affect substantially also the same vegetation types, like in the case of species-rich Nardus stricta grasslands hosting a higher vascular plant diversity on calcareous than on siliceous bedrock (Pittarello et al. 2017). This differentiation appears greater considering the specifity of the vegetation growing on serpentine substrate. Indeed, it should be noted, that even if from a structural and physiognomic point of view the two communities that we analyzed are somehow similar (i.e. open garrigues/grasslands with sparse shrublets and abundant rockiness), they are quite different from the phytocoenological point of view. In both areas annuals (Tuberarietea guttati class), succulents (Sedo-Schleranthetea class) and semi-mesophilous grasses and herbs (Festuco-Brometea class) are present, but Mt. Calvi communities are rich in small chamephytes such as Satureja montana and Helianthemum apenninum, typical of some Apennine hilly and montane garrigues (mainly attributable to Artemisio albae-Brometalia erecti suborder, but see also Mucina et al. 2016 and Terzi et al. 2016), recently also proposed as a new habitat of conservation importance (Casavecchia et al. 2021), while in Mt. Pelato's coenoses the relevant species are those typical of serpentine substrates (which resulted also as indicator species for Mt. Pelato), either strictly endemic or preferential, such as Odontarrhena bertolonii, Centaurea aplolepa subsp. maremmana, Sesleria pichiana, Plantago subulata, Iberis umbellata, Onosma echioides (mainly attributable to Alyssion bertolonii alliance); also these communities are important as a habitat of conservation relevance according to the Habitats Directive (Biondi and Blasi 2015, Casavecchia et al. 2021). These communities showed a lower taxonomic diversity, probably due to the harshness of the environmental conditions typical of the serpentine substrate. Indeed, already Selvi (2007) found for the serpentine flora of Tuscany a relatively low species diversity, but a considerable taxonomic distinctiveness, resulting from the selective pressure of serpentine soils.

Interestingly, microrelief resulted as the only factor shaping the phylogenetic structure of communities, though in a different way in the two sites. While at Mt. Calvi there was almost no variation in the indices of phylogenetic diversity, at Mt. Pelato there was in all three indices a significant positive correlation with microrelief. This pattern may be the result of the occurrence of particular ecological conditions linked to more rugged soils (i.e. with higher microrelief), which allows the establishment of different phylogenetic groups. Indeed, the two sites with higher microrelief at Mt. Pelato are the only ones hosting a fern (Asplenium ceterach L.). It has already been shown that the presence of a single species characterized by a deep separation in the phylogeny of the communities may raise substantial differences in phylogenetic trends (Lazzaro et al. 2020).

Finally, the two communities showed significant differences in the level of functional diversity and displayed a differentiation in terms of leaf traits and dominant CSR strategy. Noteworthy, the higher mean species richness detected at Mt. Calvi was paralleled by a higher functional diversity. This is consistent with studies on the relationship between species diversity and functional diversity, which generally predict that increasing species diversity results in increasing functional diversity (Biswas and Mallik 2011). Moreover, the lower functional diversity retrieved at Mt. Pelato may be explained by a stronger environmental filter acting on plant communities (Götzenberger et al. 2012). In this case, the harsh soil conditions (low water availability and heavy metals abundance) represent a strong environmental filter which led to strong functional adaptation to survive in such an environment (i.e., lower SLA; see Kandlikar et al. 2022). Conversely, the more favorable conditions of Mt. Calvi, in terms of resources availability and soil composition, result in weaker environmental filters on communities and allow the coexistence of multiple adaptations to survive and reproduce, determining a higher functional diversity (de Bello et al. 2013).

The higher SLA detected on Mt. Calvi, may be linked to the higher abundances in this site of species with a resource-acquisition strategy, which usually show high growth rates and photosynthetic efficiency (Wright et al. 2004). On the other hand, plant size (i.e. in our case plant height) was mainly linked in both sites to the plot aspect. The importance of the slope aspect on vegetation is well known (see for instance the effect of the slope aspect on Mediterranean vegetation in Kutiel 1992, Sternberg and Shoshany 2001). In our case, it is conceivable that the northern expositions buffer aridity and sun exposure in both sites, allowing the establishment of bigger plants and fostering their dominance within the communities. Moreover, it has been recently shown that Mediterranean serpentine communities on northern-facing slopes display reduced plant mortality after extreme heat events (Coppi et al. 2022). Regarding the dominant CSR adaptive strategies, as expected, the Mt. Pelato communities were polarized towards an S-type ecological strategy. Again, this is in agreement with the harsher environmental conditions at Mt. Pelato, leading to the selection of plants with stress-tolerant functional traits, such as small size, thick leaves, and low stature, which confer slow resource acquisition and low growth rates (Damschen et al. 2012, Fernandez-Going et al. 2012, Rajakaruna 2018 for traits evolution in serpentinophytes, and Lazzaro et al. 2021 for variation at the intraspecific level on Silene paradoxa L.). In contrast, the Mount Calvi community presented a trend toward an R-type ecological strategy. This strategy is likely linked to the presence of grazing in the area, which is used as sheep pastureland. Thus, species presented a conservative strategy on serpentine substrata and an exploitative strategy on grazed areas, in agreement with previous studies on the leaf economic spectrum (Adamidis et al. 2014).

In conclusion, our results revealed important differences between the communities analysed, highlighting quite different features in taxonomic, phylogenetic and functional diversity, as well as in the dominant ecological strategies. Our data bring evidence for the capability of this species to be part of communities that can highly differ from the ecological point of view even if are structurally and physiognomically similar. These indications may be useful from a conservation point of view as they indicate the need of maintaining the structure of vegetation, for instance with a recursive disturbance, to allow the presence of this protected species. Nevertheless, further studies, including also non-Tuscan occurrence sites, are needed in order to better depict the ecological preferences of this species, considering that Latium and Umbria sites cover a wider range of biogeographical and ecological conditions.