Floristic–Vegetational Features of Geranium argenteum, an Alpine–Apennine Species at Its Limit of Distribution in the Apennines

We present a floristic–vegetational study on a plant community dominated by Geranium argenteum in the Sibillini Mountains (Central Apennines), at the southern limit of its distribution in the Apennines. It is a rare pioneer community located at an elevation of about 2100 m a.s.l. with northern exposure on the fractured rocky ridges and at the edges of the rocky detrital valleys on lithosol, with a prolonged presence of snowpack and gelifraction processes. The results of the phytosociological analysis allow us to propose the new Festuco italicae-Geranietum argentei association referred to as the Leontopodio nivalis-Elynion myosuroidis alliance (Carici rupestris-Kobresietea bellardii class). The comparison with the Alpine and the Northern Apennines phytocoenoses characterized by Geranium argenteum allows us to provide a new interpretation of the syntaxonomical framework concerning the Geranium argenteum communities within its Alpine–Apennine range in light of the new data presented in this paper. The new Festuco italicae-Geranietum argentei association represents a further contribution to the knowledge of the relict alpine vegetation of the Leontopodio nivalis-Elynion myosuroidis alliance in the Sibillini Mountains and thus in the Central Apennines. Finally, habitat monitoring will be essential for assessing the impacts of climate change on this fragile and narrowly restricted plant community.


Introduction
Geranium argenteum is a rare Italian subendemic species distributed in the Alps (from Southeast France to Slovenia) [1] and within the Apennines ridges [2] (Figure 1).It is a small perennial herbaceous plant (8-15 cm) with all basal leaves arranged in a rosette and with a long and robust rhizome [2].Geranium argenteum is a pioneer species that grows in open grasslands in neutral to alkaline conditions at nutrient-poor sites in high mountain environments [3,4], with the highest elevation in Val di Fassa (Dolomites Alps), where the species was found in a dolomitic scree at 2350 m a.s.l.[5].The species occurs in ridge positions more or less exposed to the winds but also on scree slopes thanks to the long rhizome that can penetrate crevices and debris rock [6].Geranium argenteum prefers calcareous substrate but is also present on siliceous lithologies in the Northern Apennines [7,8].
The origin and biogeographical history of this species are controversial, partly due to the absence of specific phylogenetic data in the literature.On the one hand, some authors indicate G. argenteum as a tertiary species (Gams 1933;Pignatti and Pignatti 2014;Chiarugi 1937) [5,9,10] with an Alpine-Mediterranean distribution, where the current discontinuity of geographic distribution should be considered a direct consequence of the glacial period that fragmented the primitive range of the species [5].On the other hand, other authors indicate G. argenteum as a species of Alpine origin that migrated southward during the Quaternary glaciations (e.g., Ansaldi et al., 2008) [7].
Life 2023, 13, x FOR PEER REVIEW 2 of 16 glacial period that fragmented the primitive range of the species [5].On the other hand, other authors indicate G. argenteum as a species of Alpine origin that migrated southward during the Quaternary glaciations (e.g., Ansaldi et al. 2008) [7].In the Northern Apennines, the species has a scattered distribution in a few highaltitude sites [6,7,11], to the extent that it is listed as a protected species at the regional level [12,13].Regarding the Central Apennines, lg.Ottaviani (in Bertoloni (1847): vol.VII pp.224-225 [14]) reports the presence of G. argenteum "ex Umbria in montibus delle Fonti prope il Sasso Borghese" in the Sibillini Mountains group (Mt.Argentella).This record has not been confirmed in subsequent floristic studies; thus, for a long time, the Northern Apennines were indicated as the southernmost distribution limit of G. argenteum [2].Only recently has the species been confirmed for the Central Apennines [15,16]; thus, this area automatically becomes the new southern distribution limit of G. argenteum in the Apennines.
Published literature data on plant communities with or dominated by G. argenteum mainly concern the Eastern Alpine chain (e.g., Surina 2005a; Sutter 1969) [17,18], while the published works on the Apennines exclusively concern the distribution and the size of populations at the regional level (e.g., Ansaldi et al. 2008) [7], except for a recent phytosociological study [19] on Mt.Cimone in the Northern Apennines (Figure 1).However, seven unpublished phytosociological relevés characterized by G. argenteum are reported in a thesis [11] for three Northern Apennines Mountain groups, one of which is from the Apuan Alps.Notably, a single relevé from the Apuan Alps (only one station, in the area of Pania della Croce) was also published in Ferrarini 1967 [6] (rel.n. 64 carried out on 14 September 1963).
From the syntaxonomic point of view, the phytosociological associations containing G. argenteum in their epithet currently recognized and sampled within the native range of the species are reported below with the original references at alliance and class levels: Salici retusae-Geranietum argentei Surina 2005 (Soldanello-Salicion retusae alliance, Thlaspietea rotundifolii class) for the Julian Alps in Slovenia [20,21]; Sesleria sphaerocephala-Geranium argenteum ass.prov.Sutter 1969 (Oxytropido-Elynion alliance; Elyno-Seslerietea class) (Sutter 1969), later reported as Seslerio sphaerocephalae-Geranietum argentei Sutter 1969 for the Dolomites [21,22] and as Seslerio caeruleae-Geranietum argentei Sutter 1969 prov for the Hautes In the Northern Apennines, the species has a scattered distribution in a few highaltitude sites [6,7,11], to the extent that it is listed as a protected species at the regional level [12,13].Regarding the Central Apennines, lg.Ottaviani (in Bertoloni (1847): vol.VII pp.224-225 [14]) reports the presence of G. argenteum "ex Umbria in montibus delle Fonti prope il Sasso Borghese" in the Sibillini Mountains group (Mt.Argentella).This record has not been confirmed in subsequent floristic studies; thus, for a long time, the Northern Apennines were indicated as the southernmost distribution limit of G. argenteum [2].Only recently has the species been confirmed for the Central Apennines [15,16]; thus, this area automatically becomes the new southern distribution limit of G. argenteum in the Apennines.
Published literature data on plant communities with or dominated by G. argenteum mainly concern the Eastern Alpine chain (e.g., Surina 2005a; Sutter 1969) [17,18], while the published works on the Apennines exclusively concern the distribution and the size of populations at the regional level (e.g., Ansaldi et al., 2008) [7], except for a recent phytosociological study [19] on Mt.Cimone in the Northern Apennines (Figure 1).However, seven unpublished phytosociological relevés characterized by G. argenteum are reported in a thesis [11] for three Northern Apennines Mountain groups, one of which is from the Apuan Alps.Notably, a single relevé from the Apuan Alps (only one station, in the area of Pania della Croce) was also published in Ferrarini 1967 [6] (rel.n. 64 carried out on 14 September 1963).
From the syntaxonomic point of view, the phytosociological associations containing G. argenteum in their epithet currently recognized and sampled within the native range of the species are reported below with the original references at alliance and class levels: The objectives of this research are: (i) the floristic-vegetational and ecological characterization of the communities dominated by G. argenteum in the Sibillini Mountain group (Central Apennines) at the southern limit of distribution of the species; (ii) to provide a new interpretation of the syntaxonomical framework concerning the G. argenteum communities within its Alpine-Apennine range in light of the new data presented in this paper.

Study Area
The study area is located on Mount Argentella in the Sibillini Mountain range and lies within the Natura 2000 Special Areas of Conservation (SAC IT5210071 "Monti Sibillini (versante umbro)"), included in the Monti Sibillini National Park.The substrate is exclusively calcareous, belonging to the Umbrian-Marche limestone succession and specifically to the Massive Limestone Formation [24].The morphology is very rugged, with rocky bumps and ridges, scree, sinkhole systems, rocky detrital valleys, and snow beds (Figure 2).[19].The objectives of this research are: (i) the floristic-vegetational and ecological characterization of the communities dominated by G. argenteum in the Sibillini Mountain group (Central Apennines) at the southern limit of distribution of the species; (ii) to provide a new interpretation of the syntaxonomical framework concerning the G. argenteum communities within its Alpine-Apennine range in light of the new data presented in this paper.

Study Area
The study area is located on Mount Argentella in the Sibillini Mountain range and lies within the Natura 2000 Special Areas of Conservation (SAC IT5210071 "Monti Sibillini (versante umbro)"), included in the Monti Sibillini National Park.The substrate is exclusively calcareous, belonging to the Umbrian-Marche limestone succession and specifically to the Massive Limestone Formation [24].The morphology is very rugged, with rocky bumps and ridges, scree, sinkhole systems, rocky detrital valleys, and snow beds (Figure 2).The bioclimatic classification sensu Rivas-Martínez et al. (2011) [25] indicates a temperate macrobioclimate, oceanic bioclimate, and upper orotemperate thermotype [26].The vegetation is represented by various types of high-altitude grassland communities depending on the morphology and stability of the substrate (Figure 2) and mainly referable to the following habitats of 92/43/EEC Directive Annex I: 6170 "alpine and subalpine calcareous grasslands" with plant communities belonging to the Apennine alliances Leontopodio nivalis-Elynion myosuroidis, Seslerion apenninae, and Ranunculo pollinensis-Nardion strictae; 8120 "Calcareous and calcshist screes of the montane to alpine levels (Thlaspietea rotundifolii)" with plant communities belonging to the Apennine alliance Linario-Festucion dimorphae; and 8210 "Calcareous rocky slopes with chasmophytic vegetation" with plant communities belonging to the Apennine alliance Saxifragion australis (Asplenietea class).
A total of 106 phytosociological relevés were used for the comparisons with the literature data.Four of these were unpublished and were performed in the study area.
The plant collections of the new association are preserved at Herbarium Universitatis Camerinensis, School of Biosciences and Veterinary Medicine, University of Camerino, Via Pontoni 5, 62032 Camerino, Italy.

Statical Analysis
Braun-Blanquet's cover-abundance values were transformed according to the van der Maarel scale [33] and then subjected to multivariate analysis through the use of the VEGAN community ecology package [34] for R software version 4.2.3 [35].In order to assess the degree of similarity between the surveys carried out in the study area and those already published on plant communities in the alpine and subalpine planes of the Central Apennines, a cluster analysis was carried out by applying Ward's minimum variance method to the stratified similarity matrix calculated using the Bray-Curtis index.To analyze the changes in species composition between the different G. argenteum communities, principal component analysis (PCA) was performed.Furthermore, the "indicspecies" R package [36] was used to perform the indicator species analysis [37], in order to identify the species significantly associated with the different G. argenteum communities.
It is an extremely rare and fragmentary pioneer community dominated by G. argenteum (mean cover 44%) with Festuca violacea subsp.italica and Silene acaulis subsp.bryoides that develops exclusively near the summit sector of Monte Argentella (2201 m a.s.l.) in the northern aspects and at an elevation between 2040 and 2080 m a.s.l.(Figures 2 and 3).It is present on the fractured rocky ridges (Figure 4) and at the edges of the rocky detrital valleys on lithosol, in conditions of prolonged presence of the snowpack and gelifraction processes.Thanks to its long and robust rhizome, G. argenteum creeps into the cracks of the pebbles up to the consolidated soil also associated with Silene acaulis subsp.bryoides.The elaboration of the phytosociological relevés and the comparison with the plant communities occurring in the alpine and subalpine belts of the Central Apennines, which exhibit floristic similarities with the G. argenteum community in the study area (Table S1), highlight the floristic-vegetational autonomy of the G. argenteum community under investigation, for which the new Festuco italicae-Geranietum argentei association is proposed (Table 1).The elaboration of the phytosociological relevés and the comparison with the plant communities occurring in the alpine and subalpine belts of the Central Apennines, which exhibit floristic similarities with the G. argenteum community in the study area (Table S1), highlight the floristic-vegetational autonomy of the G. argenteum community under investigation, for which the new Festuco italicae-Geranietum argentei association is proposed (Table 1).The elaboration of the phytosociological relevés and the comparison with the plant communities occurring in the alpine and subalpine belts of the Central Apennines, which exhibit floristic similarities with the G. argenteum community in the study area (Table S1), highlight the floristic-vegetational autonomy of the G. argenteum community under investigation, for which the new Festuco italicae-Geranietum argentei association is proposed (Table 1).The specific combination that is characteristic of the new association includes: Geranium argenteum, Festuca violacea subsp.italica, Gentianella columnae, Achillea barrelieri, and Potentilla brauneana.Geranium argenteum is an Alpine-Apennine subendemic species at its southern limit of distribution in the Apennines, and F. violacea subsp.italica, G. columnae, and A. barrelieri subsp.barrelieri are endemic Italian species restricted to the Central Apennines.Finally, P. brauneana is an Alpine-Pyrenaic species first reported in the Sibillini Mountains and new to the Umbrian flora; this species is very rare in the Central Apennines, reaching the southern limit of its distribution in the Mainarde Mountain group (Molise Region) [38].All these species testify to the high biogeographic value of the new association, which has a strong component of Italian endemic species and subendemic species (25%) (Table S2).The boreal species including Arctic-Alpine species, such as Potentilla crantzii subsp.crantzii, are well represented (15%).Also important is the role of the south-European orophytes (38%), including Southeast European orophytes species exhibiting a strict amphi-Adriatic distribution, such as Carex kitaibeliana.The Mediterranean species such as Sesleria juncifolia are represented well in terms of richness and frequency (11.7% and 9.8%, respectively) but negligible in cover percentage (1.8%)(Table S2).
The results of the classification are in accordance with the list of the syntaxa of the Central Apennines reported in the Leontopodio nivalis-Elynion myosuroidis alliance [31], with the exception of the Seslerio apenninae-Dryadetum octopetalae association, which in this classification (Figure S1) is included in the floristic context of the Seslerion apenninae alliance, confirming the original interpretation of the authors [41] and the subsequent revision of Lancioni et al. (2011) [40].The plant communities included in the Leontopodio nivalis-Elynion myosuroidis alliance (Table S1) may be interpreted as relict communities of the primary alpine tundra on the summits of the highest mountains in the Central Apennines [31], which show an evident alpine belt, such as Gran Sasso [41][42][43] and Majella [39,44,45], while in the Sibillini Mountains, as in other mountain groups in the Central Apennines where the alpine belt is reduced, they appear to be very fragmentary [46,47].The new Festuco italicae-Geranietum agentei association referred to the Leontopodio nivalis-Elynion myosuroidis represents a further contribution to the knowledge of the alpine vegetation in the Sibillini Mountains and thus in the Central Apennines.

Comparison between the Geranium argenteum Communities in the Alpine-Apennine Biogeographical Range
In order to provide a new interpretation of the syntaxonomic framework concerning the communities of G. argenteum within its Alpine-Apennine range and to identify their ecological and floristic characteristics, the new association Festuco italicae-Geranietum argentei from the study area was compared with Salici retusae-Geranietum argentei from the Julian Alps in northwestern Slovenia, Sesleriello sphaerocephalae-Geranietum argentei from the Dolomites Alps, Geranio argentei-Caricetum rupestris from the Tuscan-Emilian Apennines, and the Geranium argenteum group from the Northern Apennines (six relevés, from the Tuscan-Emilian Apennines on siliciclastic substrate, and one from the Apuan Alps (Pania della Croce) on calcareous substrate).

Topography and Geranium argenteum Cover
The Alpine-Apennine communities characterized by G. argenteum are present on snow-covered scree slopes, snow valleys, and windy rocky ridges in an elevation range from 1450 to 2130 m a.s.l., with the highest average values (always above 2000 m a.s.l.) in the pioneer communities of Sesleriello sphaerocephalae-Geranietum argentei (original name: Sesleria sphaerocephala-Geranium argenteum Sutter 1969 ass.prov.(nom.inv.Art.1)) in the Dolomites and Festuco italicae-Geranietum argentei in the Central Apennines (Table 2).The substrate is calcareous, except for the Geranio argentei-Caricetum rupestris association and Geranium argenteum group in the Northern Apennines (Tuscan-Emilian sector), which are siliciclastic (Table 2).It should be noted that the G. argenteum group includes six relevés from the Tuscan-Emilian Apennines on a siliciclastic substrate and one relevé from the Apuan Alps on calcareous lithologies.On average, the total cover of the species is 75% (the highest in Sesleriello sphaerocephalae-Geranietum argentei), while the average number of species is 26 (the highest in the G. argenteum group).The coverage of G. argenteum (Table 2) reaches significantly high average values in the communities of Festuco italicae-Geranietum argentei followed by that of Salici retusae-Geranietum argentei, while the lowest value was recorded in Geranium argentei-Caricetum rupestris.

Floristic-Vegetational Features with Syntaxonomical Notes
The PCA of the groups of relevés, belonging to the five Alpine-Apennine communities characterized by G. argenteum (Figure 5), underlines the floristic, biogeographic, and syntaxonomic context of the plant communities even more clearly.
Salix retusa and Bistorta vivipara guide the floristic variation along the main PC1 axis (Figure 5A) and characterize the alpine cenoses on calcareous substrates of Salici retusae-Geranietum argentei, differentiated by boreal species and European and south-European orophytes of the Soldanello minimae-Salicion retusae alliance (Arabidetalia coeruleae order), whose association is originally referred to by the authors [17].
Carex rupestris guides the floristic variation along the PC2 axis, with the clear separation of the cenosis of the windy summit ridges of the Northern Apennines (Tuscan-Emilian sector) on a siliciclastic substrate of Geranio argentei-Caricetum rupestris, characterized by the high coverage of Carex rupestris of the Carici rupestris-Kobresietea bellardii class and silicicolous species of the Juncetea trifidii class, including Festuca riccierii, a species endemic to the Northern Apennines [19].
In addition to the boreal species of the Carici-Kobresietea class, such as P. crantzii subsp.crantzii and Sedum atratum, the Italian endemic (Achillea barrelieri) and subendemic species (Leontopodium nivale), Mediterranean elements (Erigeron epiroticus), and south-European orophytes species (Omalotheca diminuta, Carex kitaibeliana) that do not reach the Alps are significantly linked to the pioneer calcicolous communities of Festuco italicae-Geranietum argentei (Tables 1 and 3) in the Central Apennines that, in turn, are also characteristics and differentials of the Leontopodio nivalis-Elynion myosuroidis Central Apennines alliance to which the association refers.
Regarding the G. argenteum group communities of the Northern Apennines (Tuscan-Emilian Apennines and Apuan Alps sectors), ranging from the upper supratemperate to the lower orotemperate thermotype, there are significant species (Table 3) of the Festuco-Seslerietea (e.g., Sesleria juncifolia complex) and Festuco-Brometea classes (e.g., Cerastium arvense subsp.suffruticosum).To these, exclusively on siliciclastic substrate (Tuscan-Emilian sector), the species of Nardetea strictae classes are added (e.g., Antennaria dioica), and those of the Juncetea trifidi classes (e.g., Agrostis rupestris) and Loiseleurio-Vaccinietea classes (e.g., Vaccinium uliginosum), which indicate the connection with the cenoses of Geranium argentei-Caricetum rupestris of the highest elevation.An exception is the only relevé from the Apuan Alps [11], on a calcareous substrate in which the acidophilic species typical of siliciclastic rocks of the Nardetea strictae, Juncetea trifidi, and Louseleurio-Vaccinetea classes are practically absent.Table 3. Species significantly linked to the plant communities characterized by Geranium argenteum deriving from the indicator species analysis (p value < 0.05, significance codes: *** ≤ 0.001, ** ≤ 0.01, * ≤ 0.05; column A is the positive predictive value of the species as indicator of the site group; column B is the sensitivity of the species as indicator of the target site group).The diagnostic species indicated in the original description of the association are underlined.Climate change has a high negative impact on high-altitude habitats, especially in the Mediterranean area where the few isolated mountain peaks host plant associations characterized by endemic and rare species (e.g., Pauli et al., 2003) [48] with a narrow and fragmented areal [49].The potential impact of climate change on the fragile and narrowly restricted G. argenteum plant association in the study area could alter its floristic composition and lead to its extinction.As observed in the short and long term (e.g., Frate et al., 2018) [50], climatic warming has determined the reduction in typically cryophilous species and the upward shift of thermophilous species from the lower vegetation belt (e.g., Korner 2021) [51], a process described as thermophilization (e.g., Stanisci et al., 2011) [52].Recently, the decline of the alpine cushion plant Silene acaulis at its southern limit of distribution in the Apennines was documented by Bonanomi et al., 2023 [53] as being strongly linked to particularly intense heatwaves.The vulnerability of high-altitude species such as G. argenteum is also amplified by the high fragmentation of the species at its southern limit of distribution and the absence of specific dispersal mechanisms (mean dispersal distance <1 m) [54].Dispersal distance can play a key role in the persistence and survival of rare species confined to particular microhabitats, as demonstrated by seven endangered and vulnerable taxa in the central Apennines [49].In order to conserve the microhabitats that host the G. argenteum plant community in the study area, it will be essential to monitor over time any changes in the floristic composition of the community

Figure 1 .
Figure 1.Geographical distribution map of Geranium argenteum.Circles (•) indicate the presence of G. argenteum, the triangles (▲) indicate the current position of the sites where the communities have been described.

Figure 1 .
Figure 1.Geographical distribution map of Geranium argenteum.Circles (•) indicate the presence of G. argenteum, the triangles ( ) indicate the current position of the sites where the communities have been described.

Figure 2 .
Figure 2. Plant landscape of the study area (the red stars indicate the locations of the relevés).

Figure 2 .
Figure 2. Plant landscape of the study area (the red stars indicate the locations of the relevés).

Figure 3 .
Figure 3.The typical habitat of the G. argenteum in the study area.

Figure 4 .
Figure 4. G. argenteum close-up of flowering (a) and G. argenteum community in the study area on the fractured rocky ridges (b).

Figure 3 . 16 Figure 3 .
Figure 3.The typical habitat of the G. argenteum in the study area.

Figure 4 .
Figure 4. G. argenteum close-up of flowering (a) and G. argenteum community in the study area on the fractured rocky ridges (b).

Figure 4 .
Figure 4. G. argenteum close-up of flowering (a) and G. argenteum community in the study area on the fractured rocky ridges (b).