1. Introduction
Taxonomy and phytosociology are two long-established tools that underlie the correct interpretation of vegetation and habitats [
1,
2]. There are numerous studies in these two fields (often as combined works or reviews) that confirm their importance and in which new plant taxa and syntaxa are described (e.g., [
3]). Among the many types of vegetation that have been given special importance, we must consider the communities of nitrified grasslands that have been studied by different authors. Gutte [
4] proposed the
Malva neglecta communities in the
Malvenion neglectae suballiance, and later Rivas-Martínez [
5] proposed the
Malvenion parviflorae suballiance; years later, Rivas-Martínez et al. [
6] included the
Urtico urentis-Malvetum neglectae communities in the suballiance described by Gutte and eight different associations in
Malvenion parviflorae, subordinating both suballiances to the
Chenopodion muralis alliance. Both authors carried out exhaustive studies from a phytosociological point of view but did not provide edaphic data. Subsequently, a group of associations of nitrophilic character [
7] were studied from the phytosociological and edaphic points of view; among the syntaxa studied, there are the grasslands with
Malva neglecta,
M. parviflora,
Chyrsanthemum coronarium (=
Glebionis coronaria), and
Hordeum murinum subsp.
leporinum. More recently, Cano-Ortiz [
8] carried out a study on the
Hordeion leporini alliance in the Western Mediterranean area, providing relevés from Greece, Italy, Morocco, Spain, and Portugal. In this study, due to the similarity in the ecology and distribution of
Malva neglecta and
M. parviflora, the authors state that, taking into account the edaphic parameters and distribution of both
Malva species and having priority in the name of the suballiance described by Gutte, the suballiance
Malvenion neglectae should be maintained with its new alliance rank
Malvion neglectae.The importance of the communities of G. coronaria and G. discolor is based on two aspects. Firstly, by acting as indicators of edaphic nutrients and presenting requirements in soil texture and oxidizable organic matter (MOO), and secondly, by acting as CO2 sinks and presenting a high biomass. Considering these functions, these communities provide magnificent ecosystem services. Consequently, it is necessary to study the diversity of associations dominated by Glebionis, since this is the basis for managers to be able to apply the ecosystem services offered by these communities.
The grassland communities dominated by
G. coronaria and
G. discolor were included by several authors [
5,
9,
10,
11,
12,
13,
14,
15,
16,
17] in the
Hordeion leporini alliance, which is composed of grasslands of Mediterranean optimum, subnitrophilous or nitrophilous character, and spring growth. Grasslands that reach sub-Mediterranean and central European territories with sub-nitrophilous communities were included by different authors in alliances such as
Taeniathero-Aegilopion geniculatae [
7,
18], while the nitrophilous communities of
Hordeion leporini and
Malvion neglectae were studied by Rivas-Martínez [
9], and more recently by Cano-Ortiz et al. [
8], who proposed the suballiance
Resedo albae-Chrysanthemenion coronariae Cano Ortiz et al., 2014 [
8]. Once the taxonomy of
Glebionis spp. was established [
19,
20], as an objective, we set out to adapt the syntaxonomic nomenclature, using the new taxonomy according to the International Code of Phytosociological Nomenclature (ICPN), making the appropriate corrections of names, and incorporating new syntaxa [
21].
These ruderal communities have been ignored over time, when in fact they contain great edaphic and thermoclimatic information since G. coronaria is always located in thermo-mediterranean environments, not reaching the meso-mediterranean, contrary to what happens with G. discolor.
2. Results
2.1. Cluster Analysis
The cluster analysis for the 81 samples from Spain and Portugal (
Figure 1) reveals the difference between 5 plant associations: ArGc (20 relevés)
Anacyclo radiati-Glebionetum coronariae; KaGc (8 relevés)
Klaseo alcalae-Glebionetum discoloris; RtGc (8 relevés)
Reichardio tingitanae-Glebionetum coronariae; AvG (11 relevés)
Anacyclo valentinae-Glebionetum coronariae; and CbGc (34 relevés)
Centaureo baeticae-Glebionetum discoloris. These 34 relevés of the cluster CbGc correspond to samples taken by Cano Ortiz [
8] (CbGc1 to CbGc21), while the samples from CbGc22 to CbGc34 were obtained by García Fuentes and Cano [
22,
23], García Fuentes et al. [
24], and Rivas Martínez et al. [
11]. The five groups are corroborated by phytosociological analysis.
The 101 relevés taken in Italy and Greece are separated in the cluster into three clearly distinct groups: A, B, and C (
Figure 2). Group A consists of 4 subgroups: A1 (relevés 1–10),
Malvo parviflorae-Chrysanthemetum coronarii, published by Brullo et al. [
25] for Aspromonte massif (Reggio Calabria, Southern Italy); A2 (relevés 73–77)
Hordeo-Centauretum macracanthae; A3 (relevés 78–82)
Chrysanthemo-Silybetum mariani; and A4 (relevés 83–92),
Malvo parviflorae-Chrysanthemetum coronarii, published by Brullo [
26] for Sicily (Italy). The four subgroups are closely related to each other. Group B presents subgroup B1 (relevés 44–62),
Malvo parviflorae-Chrysanthemetum coronarii, published by Ferro [
27] for Sicily, and subgroup B2 published by Ferro [
28] for the Aeolian Islands (Sicily, Italy) (relevés 63–72), which is included in the association
Lavatero creticae-Chrysanthemetum coronarii. Finally, group C is composed of subgroup C1 (relevés 11–43), which is separated from the rest of the groups, thus constituting a new syntaxon, and subgroup C2 (relevés 93–101), which contains the most separated samples from all the others due to the fact that they correspond to Greek territories, far from the others.
2.2. Results of the Multivariate Analysis
The statistical analysis according to Cano-Ortiz reveals that the
Glebionis communities are very close to those of
Malvion, which is the fundamental reason for including them in this alliance and not in
Hordeion leporini, as has been the case over time. In addition to presenting a high value as an ecosystem service, they can be used as an indicator of nutrients and as a sink for CO
2. As can be seen in
Figure 3, the plant communities included in
Malvion neglectae present a variability in their floristic composition, largely explained from the nutritional point of view of the soil. In this case, these communities respond well to an increasing gradient in terms of silt content, CE, pH, and Mg and do not desolubilize in sand-rich soils. In contrast, in the plant communities grown in the
Hordeion leporini alliance, the edaphic variables that best define these communities are sandy soil texture as well as low pH and CE.
Once the differences between the two main groups of
Hordeion leporini and
Malvion neglectae communities were established, the structure of the different communities studied, dominated by
Glebionis coronaria s.l., was analyzed. The result of the exploratory PCA shows the correlation between the floristic composition of the communities studied in the two countries and their relationship with the different edaphic and bioclimatic parameters. The first two factors explain 58.79% of the variability of the plant communities, and the different relationships between the factors and the samples can be seen in
Figure 4.
At first, it can be observed that AdGc is a more or less generalist community, but with a preference for high values of Itc, this bioclimatic parameter provides information about the thermicity of the area where this community develops. The low values of cosine squared (r2) in the PCA once rotated (0.07 for F1 and 0.068 for F2) suggest that this is a generalist community in the study area.
For the AvGc community, a high correlation can be observed (r
2 = 0.104 for F2) with the variables related to humidity. These communities are located in
Figure 4, totally opposite to the variables that present an increasing humidity gradient; therefore, they are located in dry and sunny places, in addition to having a certain positive correlation with the apparent density of the soil with the C/N ratio.
The communities called CbGc show high negative correlations with Itc and Tp, as well as correlating positively with soils with high CEC, carbonates, clays, and high pH. This shows the appetence of this floristic combination for calcareous loamy-clay soils in cold places; in fact, they are distributed in the southernmost inland areas of the Iberian Peninsula.
The sampling of CnGc in Italy clearly shows a positive correlation with a gradient of increasing humidity or water content. They are located in rainier and relatively warm places, making the bioclimatic parameters the ones that best explain the floristic composition of this community. A negative correlation can also be observed with edaphic parameters related to high pH values or high carbonate content (r2 = −0.47).
KaGc correlates positively with the variable C/N and negatively with Ic, and the continentality index provides information about the annual thermal oscillation. This community also correlates significantly with low N contents, compared to other communities, as well as with low moisture or water content indices.
Finally, the RtGc community presents similar affinities and correlations to KaGc in the same variables, although with slightly higher squared cosines; therefore, these variables have greater relevance in the distribution of this plant community.
2.3. Canonical Correspondence Analysis Results
Once the phytosociological importance value of each of the species forming the different phytochorions under study was calculated, those taxa whose modified IVI was included in the top 5% (5% percentile) were selected. With these species selected according to their importance within the community, a CCA was carried out with the aim of observing the possible correlations between environmental variables and the presence and abundance of these species. The first two factors account for 39.84% of the variability. Although it is true that this explained variance is a priori low, it should be noted that the CCA seems to be sensitive to the relationship between the number of species and the number of samplings, so much so that in the different simulations and model adjustments carried out, when the number of species to be analyzed was reduced, the explained variance increased because all the variance was explained by a few species. However, it was decided to observe the behavior of the 62 species with the highest IVI, since the bioindicator character of the species is largely preserved.
In principle, differences can be observed in the inclination of various species depending on the country. As can be seen in
Figure 5, the CCA clearly shows 5 groups of species. On the one hand, there are species with an inclination for carbonate-rich soils, high pH, and clay soils that are negatively correlated with high Tp, PE, and Iar values, such as
Centaurea baetica,
Sinapis mairei,
Diplotaxis catholica, or
Phalaris minor. These species characterize the so-called CbGc communities.
Another group of species has an inclination for clay soils that are poor in sand, rich in carbonates, have a high bulk density, high C/N ratios, and are negatively correlated with variables such as Ic, PEs, and Ios2. These species are Klasea alcalae, Hyparrhenia sinaica, Centaurea pullata, Crepis vesicaria, and Asteriscus acuaticus. These species characterize the phytochorions called KaGc.
On the other hand, there is another cluster of species strongly correlated with the variables associated with high temperatures (Itc) and negatively correlated with Io and Ioe. Partial negative correlations can also be seen with other variables related to soil carbonate content and high pH. Species such as Reichardia tingitana, Brassica repanda, and Tetragonia tetragonioides are characteristic of RtGc communities. These three species clusters correspond to plant communities present in the Iberian Peninsula, which are well characterized from the point of view of species co-occurrence (floristic composition) as well as from a bioclimatic and edaphic point of view. Another grouping of species responds, with positive correlations, to the variable continentality (Ic), as well as being partially correlated with the variables related to water availability both at annual (Io) and summer (Ioe) levels. From an edaphic point of view, they are negatively correlated with variables such as the C/N ratio (CN) or soil bulk density. Species such as Astragalus drupaceus and Sinapis dissecta define these communities. These phytochorions correspond to the so-called AdGc, distributed in the central-eastern Mediterranean belt in Greece, being the eastern-most community studied in this manuscript.
Finally, in the analysis of canonical correspondences, a well-defined cluster of plant species with a clear appetence for arid or low humidity climates and high temperatures can be observed. They are positively correlated with variables such as the aridity index (Iar), the positive annual temperature (Tp), or summer evapotranspiration (PEs). From the edaphic point of view, they correlate negatively with variables such as clay content, pH, or carbonate content. Species such as Anacyclus valentinus, Carrichtera annua, and Lophocloa pumila are examples. These phytochorions, or plant co-communities, correspond to AvGc in this manuscript and are located in the most arid areas of Western Europe.
Within this last cluster, we can distinguish a subcluster of species that are not very correlated with edaphic and bioclimatic variables in general, although with an inclination for warm and relatively arid climates, showing a certain correlation with variables such as PE, Iar, or Tp. From the edaphic point of view, they seem to exclude soils rich in carbonates, with a clayey texture, or with a high pH. The species with these appetences are characteristic of the communities sampled in Italy, maintaining a certain relationship with AvGc. Species such as Centaurea napifolia, Calendula fulgida, Lotus ornithopodioides, and Galactites elegans (synonym of Galactites tomentosus Moench) respond to these characteristics in the Glebionis coronaria communities in Italy. These phytochorions have been referred to as CnGc.
3. Discussion
The communities dominated by
Glebionis coronaria,
G. discolor, and
Hordeum leporinum have structural, edaphic, and floristic differences. According to Cano-Ortiz et al. [
8], at the edaphic level,
Glebionis communities present soil parameter values of MO, Nt, P, K, and Mg that are closer to those of
Malvenion neglectae Gutte 1966 communities than to those of
Hordeion leporinii. The frequent presence of
Malvenion neglectae species in
Glebionis communities and the structure of
Malvenion neglectae [
4] were reason enough for Cano-Ortiz et al. [
8] to propose the new suballiance
Resedo albae-Chrysanthemenion coronarii and subordinate it to
Malvion neglectae (Gutte 1966) Cano Ortiz et al. 2014, whose name we now correct according to the newly established taxonomy
Resedo albae-Glebionenion coronariae (Gutte 1966) Cano Ortiz et al. 2014
corr. (
Table 1).
All the communities of the genus
Glebionis are of great interest for land management, so it has been necessary to describe them phytosociologically. These plant associations have a narrow edaphic ecology in that they are bioindicators of edaphic nutrients [
8], and it is necessary for managers to know the associations described with the abundance of the species. The communities dominated by
G. coronaria for the thermo-Mediterranean environments of southwestern Iberia (Spain and Portugal) were published by Cano-Ortiz et al. [
7] with the name
Anacyclo radiati-Chrysanthemetum coronarii (Rivas-Martínez 1978) Cano-Ortiz et al. 2009, making it necessary to correct the name in all syntaxa (ICPN article 44)
Anacyclo radiati-Glebionetum coronariae (Rivas-Martínez 1978) Cano-Ortiz et al. 2009 corr., since this association included the suballiance
Resedo albae-Chrysanthemenion coronarii Cano Ortiz et al. 2014 and the alliance
Malvion neglectae (Gutte 1966), whose name we now correct according to the newly established taxonomy
Resedo albae-Glebionenion coronariae (Gutte 1966) Cano Ortiz et al. 2014 corr. Because Cano-Ortiz et al. [
8] do not give the type for the suballiance, it is typified in this work, and we propose as typus
Resedo albae-Glebionetum coronariae O. Bolòs & Molinier 1958 nom. corr. Indeed, due to the doubts raised about the taxonomy of
G. coronaria, Cano et al. [
19] carried out a taxonomic study on both
Chrysanthemum coronarium var.
concolor and var.
discolor and distinguished the taxa of
G. coronaria and
G. discolor. Based on this new taxonomy, we establish a new syntaxonomy for the
Glebionis s.l. communities being included in the suballiance
Resedo albae-Glebionenion coronariae (Cano-Ortiz et al., 2014)
nom. corr., which is subordinate to
Malvion neglectae. However, these authors do not propose the type of the suballiance, so we designate as type the association
Resedo albae-Glebionetum coronariae O. Bolòs & Molinier 1958
nom. corr.Based on the results obtained for Spain and Portugal for the association Anacyclo radiati-Glebionetum coronariae, we propose the following new associations:
Centaureo baeticae-Glebionetum discoloris Cano-Ortiz
ass. nova (
Table 2, Relevés 1–21,
holotypus rel. 6), an upper thermo-mediterranean and lower meso-mediterranean grassland growing on nitrified basic substrates in the Betic territories, characterized by
G. discolor and
Centaurea pullata subsp.
baetica differential species compared to
Resedo albae-Chrysanthemetum coronarii, described by Bolòs and Molinier [
29,
30] for the thermo-mediterranean areas of Mallorca, and extending its area to the thermo-mediterranean areas of Valencia [
31]. Three types of grasslands dominated by
G. coronaria develop in southeastern Iberian thermo-mediterranean territories on basic and neutral substrates.
Klaseo alcalae-Glebionetum discoloris ass. nova (
Table 3, Relevés 1–8,
holotypus rel. 8), a very frequent plant community in the Malacitano-Almijarense biogeographic sector (Malaga province, Spain), which develops on nitrified neutro-basic substrates of anthropized areas such as roadsides and abandoned places. Its dominant species are
G. coronaria,
Klasea alcalae, and
Sinapis alba subsp.
mairei.
In the Alpujarreño-Gadorense biogeographic unit (Granada province, Spain), the
Glebionis coronaria-dominated grassland continues to prevail, with a similar ecology to the previous one but with a different floristic composition:
Reichardio tingitanae-Glebionetum coronariae ass. nova (
Table 4, Relevés 1–9,
holotypus rel. 4).
Finally, in the semi-arid thermo-mediterranean territories on basic substrates rich in organic matter of the Almerian sector, there is a community of
G. coronaria differentiated from the previous ones by the presence of
Anacyclus valentinus Beta vulgaris and
Carrichtera annua among other species, which allows us to propose the association
Anacyclo valentinae-Glebionetum coronariae ass. nova (
Table 5, Relevés 1–11,
holotypus rel. 2).
In previous research by Cano et al. [
19], we established the species
G. coronaria (L.) Cass. ex Spach for exclusively thermo-mediterranean environments and
G. discolor (d’Urv.) Cano, Musarella, Cano-Ortiz, Piñar Fuentes, Spampinato & Pinto Gomes for thermo- and meso-mediterranean environments. The morphometric study confirmed different dimensions of achene wings and different arrangements of their glands (
Figure 6).
This work was carried out due to several previous taxonomic errors that have remained uncorrected since the time of Linnaeus. Unfortunately, attempts at lectotypification of
Chrysanthemum coronarium L. by Dillon were made erroneously. However, Turland [
30] confirmed two varieties and proposed a new combination under the name
Glebionis coronaria var.
discolor (d’Urv.) Turland, using
Chrysanthemum coronarium var.
discolor d’Urv. as a basionym. After the morphometric study and bioclimatic distribution, different authors have reported both taxa with specific ranks: Cueto et al. [
32] for Spain and Bertolucci et al. [
33,
34] for Italy.
The morphometric differences between
G. coronaria and
G. discolor are supported by the phytochemical study of Ivashchenko et al. [
35], which concludes that there are differences in the amounts of carotene, vitamins, and other molecules present in both species due to the influence of environmental factors. Recently, Gallucci et al. [
20] carried out a study of the genetic diversity between
G. coronaria and
G. discolor through AFLP markers, using material from Spain, Italy, and Portugal, and reached the conclusion that, using the mentioned markers, there are genetic differences between both species.
Taking into consideration articles 40–45 of the ICPN [
21], it is not possible to maintain the syntaxonomy that is based on the species
C. coronarium, when a vast majority of researchers support
G. coronaria and
G. discolor. For these reasons, we propose the correction of the names.
Although Álvarez de la Campa [
37] described the association
Asphodelo fistulosi-Hordeetum leporini A. & O.Bolòs in O.Bolòs 1956 and the sub-association
chrysanthemetosum coronarii Álvarez de Campos 2003, the only differential being the taxon
Chrysanthemum coronarium L. [=
Glebionis coronaria (L.) Cass. ex Spach], due to its thermo-mediterranean environment and similar floristic composition, it could be assimilated to the new AvG association. All these associations are distributed in the south and east parts of the Iberian Peninsula (
Figure 7).
In Italian territories, several authors have followed the Spanish and Portuguese syntaxonomy with respect to nitrophilous and sub-nitrophilous communities [
25,
26,
27,
28,
39,
40,
41,
42,
43,
44,
45,
46]. For Italy and Greece, Ferro [
27] described the association
Malvo parviflorae-Glebionetum coronariae Ferro 1980 corr. for Sicily (B1), which is corroborated by Brullo [
26] in Sicily, together with the new associations described by this author,
Hordeo-Centauretum macracanthae (A2) and
Glebiono-Silybetum mariani Brullo 1983 corr. (A3). However, Brullo et al. [
25] studied these
Glebionis communities in southern Italy and included them in
Malvo parviflorae-Glebionetum coronariae. Community (A1) in the cluster (
Figure 2) is very far from the one described by Ferro, being closer to (A2), (A3), and (A4), so these grasslands should be included in the syntaxa described by Brullo [
26] (
Figure 8).
Group B is constituted by relevés published by Ferro [
27,
28] for Sicily and for the Aeolian Islands, broken down in the cluster into two subgroups: (B1)
Malvo parviflorae-Glebionetum coronariae and (B2)
Lavatero creticae-Glebionetum coronariae Ferro 2004 corr., described for the Aeolian Islands. Both associations have strong floristic differences with respect to the group (C1) of the cluster, which allows us to propose a new association (Relevés 1–33) for the territories of Reggio Calabria, characterized by species absent in the association
Lavatero creticae-Glebionetum coronariae (B2), these being the differences of the new association
Centaureo napifoliae-Glebionetum coronariae ass. nova (
Table 6, Relevés 1–19,
holotypus rel. 16), an association differentiated from
Centauretum napifoliae Brullo 1983. This association grows in dry environments on basic substrates in the thermo-mediterranean belt. The subgroup (B2)
Malvo parviflorae-Glebionetum coronariae published by Brullo [
26] for Sicily differs from the same (A1) communities published by Brullo et al. [
25] for Reggio Calabria. The group (C1) based on relevés from Sicily and Reggio Calabria belongs to a new syntaxon, floristically differentiated from the rest of the relevés of C1 by the presence, among other species, of
Calendula suffruticosa subsp.
fulgida,
C. suffruticosa subsp.
fulgida x Calendula arvensis, and
Valeriana graciliflora (=
Fedia graciliflora). This community is present on basic and loamy substrates in dry-subhumid environments of the lower thermo- and meso-mediterranean territories, which allows us to propose the new subassociation
Centaureo napifoliae-Glebionetum coronariae calenduletosum fulgidae subass. nova (
Table 6, Relevés 20–33,
holotypus rel. 31), while the grasslands dominated by
G. coronaria in Greece belong to subgroup (C2), which establishes a new syntaxon named
Astragalo drupacei-Glebionetum coronariae ass. nova (
Table 7, Relevés 1–9,
holotypus rel. 2), an association located on thermo-mediterranean basic substrates (
Figure 9).
Proposed syntaxonomical scheme
Stellarietea mediae Tüxen, Lohmeyer & Preising ex von Rochow 1951
Chenopodio-Stellarienea Rivas Goday 1956
Sisimbrietalia officinalis J. Tüxen in Lohmeyer et al. 1962 em. Rivas-Martínez, Báscones, T. E. Díaz, Fernández-González & Loidi 1991
Malvion neglectae (Gutte 1966) Cano Ortiz, Biondi, Pinto-Gomes, Del Río & Cano 2014
Resedo albae-Glebionenion coronariae Cano-Ortiz, Biondi & Cano ex Cano Ortiz, Biondi, Pinto-Gomes, Del Río & Cano 2014 corr.
Resedo albae-Glebionetum coronariae O. Bolòs & Molinier 1958 nom. corr.
Anacyclo radiati-Glebionetum coronariae (Rivas-Martínez 1978) Cano-Ortiz et al. nom. corr.
Malvo parviflorae-Glebionetum coronariae Ferro 1980 nom. corr.
Lavatero creticae-Glebionetum coronariae Ferro 2004 nom. corr.
Glebiono-Silybetum mariani Brullo 1983 nom. corr.
Reichardio tingitanae-Glebionetum coronariae ass. nova (Spain)
Anacyclo valentine-Glebionetum coronariae ass. nova (Spain)
Centaureo baeticae-Glebionetum discoloris ass. nova (Spain)
Klaseo alcalae-Glebionetum coronariae ass. nova (Spain)
Astragalo drupacei-Glebionetum coronariae ass. nova (Greece)
Centaureo napifoliae-Glebionetum coronariae ass. nova (Italy)
Centaureo napifoliae-Glebionetum coronariae calenduletosum fulgidae subass. nova (Italy)