A new association with Patzkea paniculata on serpentine substrates at low elevations in the western Alps (Italy)

Patzkea paniculata usually dominates grassland communities in the subalpine and alpine belts. The analysis of a unique vegetation community found at low altitudes growing on serpentinitic substrates in the North-Western Alps (Italy) dominated by P. paniculata , is hereby presented. These communities are substantially different from already described alpine communities, framed in the alliance Festucion variae (class Caricetea curvulae , order Festucetalia spadiceae ) and typical of higher elevations. Syntaxonomic and ecological investigations were performed to provide a correct phytosociological framework for these grasslands. The new association Potentillo albae-Patzkeetum paniculatae ass. nova is here described, with two different variants, one co-dominated by Bromopsis erecta and the second with co-dominance of Molinia arundinacea . It is a secondary grassland of arid environments attributable to the alliance Bro-mion erecti (class Festuco valesiacae-Brometea erecti ), and characterized by the presence of numerous species, both rare and typical of serpentinitic substrates.


Introduction
Patzkea paniculata is a gregarious grass species scattered in the main mountain ranges of southern Europe, as far as Morocco (Vittoz et al. 2005). Patzkea paniculata grasslands are found in rather restricted areas (Sburlino et al. 1996) and are characterized by high biodiversity (Garde 1996), indeed they are included in the habitat 6150 (Siliceous alpine and boreal grasslands) according to European Natura 2000 habitat classification (Biondi et al. 2009).
These grasslands are apparently indifferent to the substrate, on soils with an acid to weakly acid reaction and prefer steep southern-facing slopes (Sburlino et al. 1996). The origin of these stands, mainly occurring in the upper mountain and subalpine belt, seems to be in most cases derived from the cutting down of the natural woody cover. Only in a few cases they can be considered of natural origin: at higher altitudes, where they constitute a stage of recolonisation after the glaciation (Négre 1950), as colonizing formations of stony ground (Barbero 1970), in the lower alpine belt (Guinochet 1938) and in areas subject to avalanche disturbance (Braun-Blanquet 1972).
Patzkea paniculata at low altitudes tend to be a subordinate species to other more competitive ones (Vittoz et al. 2005), and has been found at exceptionally low altitudes (500-800 m a.s.l.) in the outer Cottian Alps by Mon-dino (1975Mon-dino ( , 1997. Based on the information by Mondino, several new coenosis dominated by P. paniculata were found in the colline and montane belts on shallow soils on serpentine substrates, which probably act as a selective agent on the flora (Mota et al. 2017). The aim of this work was to describe and characterize these low altitude P. paniculata dominated communities, contributing to the knowledge and phytosociological characterization of this species on Italian territory.

Study area
The investigated grasslands are located in the outer Cottian and Graian Alps of Piemonte Region (North-West Italy) at an altitude of 450-1200 m a.s.l. (Fig. 1). Some areas fall in protected areas: Zone of Special Conservation "Laghi di Avigliana" (IT1110007) and Natural Park of Monte San Giorgio.
The substrate is characterized by serpentinites (Piana et al. 2017a(Piana et al. , 2017b, a metamorphic rock predominantly composed of magnesium and iron silicates, highly resistant to alteration (D'Amico et al. 2014). These characteristics affect the soil chemical and physical properties leading to stress or even toxicity in plant species that are not adapted to the substrate, indeed several endemic species exist on serpentinites (Kruckeberg 1984). The resistance to alteration of the parent rock and the steepness of the slopes determines the formation of shallow, scarcely evolved soils, subject to sheet erosion. Moreover, the centuries-long anthropic exploitation, especially through grazing, has favored the erosive processes leading to deterioration of the already poor soils (Mondino 1975(Mondino , 1997. Two weather stations represent the studied area (Avigliana and Lanzo). The average annual temperatures range from 11.2 °C to 12.2 °C (Table 1). Rainfall ranges from 871.1 mm to 1334.2 mm (Table 1; ARPA Piemonte 2021).
As reported in Figure 2, Avigliana, in the Cottian Alps, shows a drought period during summer. Contrarily, Lanzo does not show any drought period.

Methods
In spring 2021, 15 phytosociological surveys were carried out according to the phytosociological method in grasslands dominated by P. paniculata, using the abundance-dominance values proposed by Braun-Blanquet (1928) and Westhoff and Van der Maarel (1978). These relevés were localized in four sites, three were in the Cottian Alps and one in the Graian Alps. The localization of relevés is reported in Appendix I. While the minimum area for surveys on grassland ecosystems is 16 m 2 (Chytrý and Otýpková 2003), we used a slightly higher size, 25 m 2 , to better detect the variability of our grasslands.
Abundance-dominance values were transformed into numerical values according to van der Maarel (1979), which were used to classify the 15 vegetation surveys by hierarchical cluster analysis (option for clustering: UP-GMA; resemblance coefficient: Bray-Curtis coefficient). The results of the analysis were compared with the syntaxonomical classification (classes, orders, alliances and associations) indicated by Mucina et al. (2016), Biondi et al. (2014), Theurillat et al. (1995), Royer and Ferrez (2020), for the attribution of the characteristic and differential species. This allowed the attribution of the studied grasslands to the proper syntaxa. In the final table, the relative frequencies of occurrence of each species in the surveys indicated by I to V were calculated according to Poldini and Sburlino (2005) (I 0-20%, II 21-40%, III 41-60%, IV 61-80%, V 81-100%).
All statistical analyses were performed using the software Past 4.04 (Hammer et al. 2001). The species nomenclature follows Bartolucci et al. (2018) and subsequent updates. The phytosociological nomenclature follows the Vegetation Prodrome of Italy (Biondi et al. 2014) and the rules of the fourth edition of the International Code of Phytosociological Nomenclature (Theurillat et al. 2020).

Results
According to the 15 vegetation surveys, the stands examined have fallen into the class Festuco valesiacae-Brometea erecti Br.-Bl. & Tuxen ex Br.-Bl., 1949. This syntaxonomical classification has been identified on the basis of the presence of 18 characteristic and differential species of this class and its subordinate units (Table 2). Despite the dominance of P. paniculata, no other species characteristic of the class Caricetea curvulae Br.-Bl., 1948, order Festucetalia spadiceae Barbero, 1970em. Grabherr 1993 and specifically of the alliance Festucion varie Guinochet, 1938 were present, confirming that these swards are different from typical P. paniculata grasslands located in the subalpine and alpine belt. Thus, the coenosis have been placed in the order Brometalia erecti Koch, 1926, suborder Leucanthemo vulgaris-Bromenalia erecti Biondi, Ballelli, Allegrezza & Zuccarello, 1995, alliance Bromion erecti Koch, 1926, due to the number and cover of characteristic species of these two subordinate syntaxa (Theurillat 1995(Theurillat , 2020Royer and Ferrez 2020;Terzi 2016).
According to the floristic list identified by the phytosociological surveys (Table 2), it has not been possible to   Walter and Lieth (1960). The average values refer to the 30-year period from 1991 to 2020.  place the coenosis object of the study in an association already described. The present work proposes the new association Potentillo albae-Patzkeetum paniculatae ass. nova (holotypus: rel. n. 7, Table 2). Characteristic species of association are: P. paniculata, Potentilla alba, Vincetoxicum hirundinaria, Campanula bertolae, Oreoselinum nigrum, Pentanema hirtum, and Cervaria rivini. The dendrogram resulting from the cluster analysis (Fig. 3) has divided the surveys into two groups, which, however, couldn't be elevated to the rank of subassociation, due to the absence of differential species between the two groups. As shown in Table 2 the subgroup A, was characterized by the presence of Molinia arundinacea, with high cover values, comparable to those of P. paniculata. Thus, a variant (Poldini and Sburlino 2005) with M. arundinacea (group A) has been proposed within Potentillo albae-Patzkeetum paniculatae ass. nova. The other group, B, formed by the surveys 7-15, could for the same reason be considered a variant with Bromopsis erecta.
The Principal Component Analysis (PCA) has highlighted the ecological differences between the two defined groups, in which most of the variance (62.56%) could be explained by the first component. The Landolt indicator values (Landolt et al. 2010) that appear to be of greatest importance in differencing the groups were F and H, positively correlated with component 1, and K and D, negatively correlated with the same component (Fig. 4).

Physiognomy and structure
The communities are distributed in patches into a matrix of oak forests on serpentine rocks. These grasslands are rich in perennial herbaceous species, with P. paniculata as the dominant one even if never exceeds 50% cover in the surveys (Table 2).
Several shrub species tend to encroach these grasslands, primarily Rosa canina, Rubus fruticosus aggr. and Prunus spinosa.

Syntaxonomy
Clear ecological affinities exist between coenosis dominated by P. paniculata in the subalpine and alpine belts and those described in the present work: they are both located on south-facing steep slopes. In spite of the dominance of P. paniculata, comparable to the cover observed in the high-elevation stands usually attributed to the Festucion variae alliance (order Festucetalia spadiceae, class Caricetea curvulae), the absence of other species charac-teristic of these syntaxa led to the exclusion of this attribution. The species that characterize the study area, indeed, make them clearly more similar to the arid grasslands of lower altitudes of the class Festuco valesiacae-Brometea erecti. In particular, these stands can be placed in the order Brometalia erecti, suborder Leucanthemo vulgar- Figure 3. Cluster dendrogram. Two separated groups can be distinguished from the dendrogram, group A is highlighted with blue, while group B is highlighted with red. is-Bromenalia erecti, alliance Bromion erecti. At high elevations, the stands dominated by P. paniculata are typically placed in Caricetea curvulae, but some exceptions exist e.g. in the Lucanian Apennines, where some P. paniculata dominated coenosis are placed in the class Festuco valesiacae-Brometea erecti and more precisely in the alliance Phleo ambigui-Bromion erecti Biondi, Ballelli, Allegrezza & Zuccarello ex Biondi & Galdenzi, 2012, of Scorzonero-Chrysopogonetalia Horvatic et Horvat in Horvatic, 1963(Sburlino et al. 1996. It should be noted that the high altitude coenosis can also contain some species characteristic of Festuco valesiacae-Brometea erecti, but with much more limited cover; these include e.g. Carex caryophyllea, Festuca ovina aggr., Prunella grandiflora (Négre 1950;Vittoz et al. 2005;Lonati and Siniscalco 2006).
The coenosis described in the present study have a unique species composition compared to the other associations of the alliance Bromion erecti, primarily due to the high abundance of P. paniculata, a gregarious species that tends to be dominant when present (Pignatti et al. 2017(Pignatti et al. -2019. Alongside it, B. erecta and Brachypodium rupestre are often present, in most cases with high cover values, and are characteristic of Bromion erecti and Festuco valesiacae-Brometea erecti, respectively. The presence of these two species, defined by Mondino et al. (2007) as initiators of Bromion communities, is considered consistent with membership of the alliance and its higher-ranking syntaxa.

Diagnostic species
Among the characteristic species of the new association, P. alba grows in arid grasslands and deciduous scrublands, in hilly and mountainous areas. It can be found in the Brometalia erecti communities but is also frequent in the Quercetalia pubescenti-petraeae Klika, 1933(Pignatti et al. 2017-2019. According to Oberdorfer (1983) it is also characteristic of the association Potentillo albae-Quercetum petraeae Libbert, 1933, described for Central Europe, and reported for the Piemonte Region (NW-Italy) on ultrabasic soils in the pre-Alpine belt (IPLA 2020). Campanula bertolae is endemic to the ophiolitic areas of the Western Piedmontese Alps (Pignatti et al. 2017-2019, Fenaroli et al. 2013). The remaining characteristic species, V. hirundinaria, O. nigrum, P. hirtum, and C. rivini, are ingressive species from the class Trifolio medii-Geranietea sanguinei, giving a good representation of the patchy landscape of open and woody areas typical of these semi-natural grasslands.
Like most of the Bromion communities (Calaciura and Spinelli 2008), these P. paniculata grasslands show a high plant diversity (36 ± 2.8 species in Group A and 40 ± 3.6 species in Group B). Additionally, some species are interesting and worthy of conservation. The uncommon Daphne cneorum is usually found on serpentinite soils, while Odontarrhena argentea is considered endemic to serpentine (Mondino et al. 2007;D'Amico et al. 2014).
Other rare species found in the surveys are Pulsatilla montana and Gentiana pneumonanthe both protected at regional level and the latter also vulnerable according to the IUCN list.

Synecology and synchorology
Between the two groups identified through the cluster analysis, Group A, characterized by the co-dominance of M. arundinacea, was observed in the Graian Alps, at an altitude between 1050 and 1200 m a.s.l. This variant has high values of freshness, due to the annual rainfall (Table 1, Fig. 2), and high humus content, probably linked to deeper soils. In addition to M. arundinacea, other species indicative of mesophilic conditions confirm the ecology of this variant: Anemonoides nemorosa, Calluna vulgaris, G. pneumonanthe, Potentilla erecta, Serratula tinctoria, etc. As indicated by Pignatti et al. (2017Pignatti et al. ( -2019, M. arundinacea can also colonize grasslands belonging to Bromion and is considered a pyrophytic species (Stampfli et al. 1994). It is also considered a stress-tolerant competitor adapted to nutrient-poor soils (Taylor et al. 2001): this advantage in competition seems to be due to high clonal growth and adaptation to low phosphorus concentrations (El-Kahloun et al. 2000;Øien and Moen 2001;Güsewell and Koerselman 2002). Indeed, as reported by Mota et al. (2017), low phosphorus concentration is a selective factor for vegetation evolution on serpentine rocks. In addition, early in the growing season, M. arundinacea can store nutrients inside its roots (Pfadenhauer and Twennhöven 1986;El-Kahloun et al. 2000). These characteristics could be the reasons for its strong competitiveness also on these limiting substrates.
The variant with B. erecta (group B) is localized in the Cottian Alps at a lower altitudinal range between 450 and 950 m a.s.l., characterized by a drier climate, highlighted by the summer drought period (Fig. 2). This variant was observed on shallow, poorly structured soils, on very steep slopes, as confirmed by the graph resulting from the PCA (Fig. 4). Patzkea paniculata and B. erecta are associated with a high cover also of B. rupestre. This variant differs from the previous one in the lack of M. arundinacea and of other mesophilic species.

Syndynamics
Potentillo albae-Patzkeetum paniculatae ass. nova is dynamically linked to the vegetation of the downy oak forests (Quercion pubescenti-petraea), forming an alternating woodlands/grasslands pattern. This balanced landscape is maintained by disturbances like grazing, that keep P. paniculata dominated grasslands open. Indeed, in a state of complete abandonment these communities could be limited to the driest and steepest rocky outcrops, where they could be identified as primary. Although the evolution of these secondary grasslands into scrublands and eventual-ly woodlands is considerably slowed down by the harsh environmental conditions, the absence of grazing management could progressively lead towards the downy oak woodlands. Some neighboring areas probably already underwent this change, as indicated by the presence of single tufts of P. paniculata in the surrounding woody areas. The natural dynamism of the vegetation is highlighted by the great abundance of ingressive species of both thermophilic forest edge communities (Trifolio medii-Geranietea sanguinei) and meso-xerophilic shrub communities (Rhamno catharticae-Prunetea spinosae), causing the probable loss of grasslands over time in case the disturbances stop (Table 2). Shrub species such as Crataegus monogyna, P. spinosa and Ligustrum vulgare are also considered species of low intrinsic value, because they are very common, responsible for further loss of open habitats and their biodiversity, both in terms of plant species, entomofauna and avifauna (Calaciura and Spinelli 2008).
In the variant with M. arundinacea, located on less rocky soils with higher water availability, the coexistence of other species with M. arundinacea is threatened by its vigorous growth. The abundant dead dry matter accumulates, forming a very thick layer of litter (Stampfli et al. 1994) that favor fires, which are frequent in winter, particularly in dry areas of Piemonte Region, NW-Italy (Regione Piemonte 2021). Its resistance to fire and its competitiveness in deeper soils make M. arundinacea a potential threat to species of these grasslands. It is realistic to assume that frequent fires and lack of management could also lead to the disappearance of P. paniculata. Moreover, the abundant litter accumulation can slow down the succession towards the woodlands. Indeed, the absence of ingressive species of the class Rhamno catharticae-Prunetea spinosae in the variant with M. arundinacea could indicate a less mature evolutionary stage, compared to the variant with B. erecta.

Conclusions
The new association Potentillo albae-Patzkeetum paniculatae ass. nova describes the P. paniculata coenosis of low altitudes on serpentine substrate in North-West Italy, in the Cottian and Graian Alps. These communities are original due to the lower altitudes than the associations previously described in the Alps, in the alpine and subalpine belts. Moreover, they fall within the phytosociological class Festuco-Brometea, order Brometalia erecti, alliance Bromion erecti in analogy with some coenoses described for the Lucanian Apennines (Sburlino et al. 1996). Two variants were identified, one with B. erecta and one with M. arundinacea, differentiated by pedo-climatic characteristics. These communities are included in the habitat 6210 in the Natura 2000 classification (Biondi et al. 2009) and host some rare species, particularly those endemic to serpentine. They are therefore worthy of conservation. This work contributes to the knowledge of the syntaxonomy of the western italian Alps, where further research could be performed to report and describe similar coenoses.