New plant communities to define the southern boundary of the European Atlantic Province in mainland Portugal

This study identifies and analyzes the plant communities that allow the definition of the geographic limits between Temperate and Mediterranean macrobioclimates, for the center of Portuguese mainland. The altitude of Serra da Estrela, Açor and Lousã, combined with the increase in atmospheric humidity, allows the presence of vegetation typical of a Temperate macrobioclimate. Thus, based on the phytosociological methodology, floristic relevés were carried out in order to identify the series of vegetation existing in these territories. Through these relevés carried out, four new plant associations were identified: Cytisetum grandifloro-striati ass. nova, Scro-phulario grandiflorae-Sambucetum nigrae ass. nova, Pruno lusitanicae-Coryletum avellanae ass. nova that lives in the submediterranean bioclimatic variant, mesotemperate humid to hyper-humid. A new association namely Genisto falcatae-Quercetum broteroanae ass. nova with two subassociations were also identified. Based on the vegetation distribution, new biogeographic limits are proposed. Thus, it was intended to identify the southern limits of the European Atlantic Province (Atlantic Orolusitania Subrovince) based on the vegetation cover, namely the distinction between the Estrela Sierran District and a new Biogeographical District, the Alvo-Gardunhense.


Introduction
Despite the Temperate macrobioclimate's presence on all continents, it's more expressive in Eurasia and in North America (Rivas-Martínez et al. 2011).In the Iberian Peninsula, the Atlantic European Province has its southern limit in mainland Portugal, corresponding to the transition from the temperate macrobioclimate to the Mediterranean macrobioclimate.The distinction between Temperate and Mediterranean macrobioclimates is identified by the lack of aridity during at least two consecutive months in the summer as well as the higher mediterranean aridity during least two consecutive months (Rivas-Martínez et al. 2017a).In general, the European Atlantic Province is characterized by the dominance of a Temperate macrobioclimate, where most of the natural potential forests of Quercus robur L. and Fagus sylvatica L. develop (Rivas-Martínez et al. 2017b).
In the southernmost part of Portugal, the European Atlantic Province is delimited by the Estrela Sierran District, which is characterized by the submediterranean variant.This variant, although inserted in the temperate macrobioclimate, is defined by the existence of at least one month during the summer's quarter with an average precipitation in millimeters that is 2.8 tenths lower than the average temperature in degrees Celsius (Rivas-Martínez et al. 2017a).
Due to the terrain's elevation, the submediterranean variant extends to the central part of Portuguese mainland, through the Serra da Estrela, Açor and Lousã mountain ranges, constituting a block to the humid Atlantic winds that favor the precipitations of the relief (Pisani et al. 2019;Santos et al. 2017).Thus, the increase in humidity favors the occurrence of Quercus robur subsp.broteroana O. Schwartz, whose natural potential vegetation has been represented by the Viburno tini-Querco broteroanae sigmetum (Costa et al. 2015;Raposo et al. 2021).Although there are several works on the mountains' flora of central Portugal (Costa et al. 2012;Santos-Silva 1985;Silveira 2007;van der Knaap and van Leeuwen 1995), information on the plant communities that can be used as bioindicators of the temperate macrobioclimate is still lacking.
On the other hand, there is some difficulty in defining the boundaries for the Estrela Sierran District, considering the frequent erosion of the schist substrates at the lowest levels, due to strong slopes, promoting soil thiness and even the occurrence of outcrops.In these substrates, typical temperate plant communities (more demanding in terms of moisture) find it difficulty in settling, taking refuge in deep soils and north facing slopes exposed to the north quadrant (Connor et al. 2012).Although the Estrelense District was defined by Holco mollis-Quercetum pyrenaicae, Teucrium salviastri-Quercetum rotundifoliae, Frangulo alni-Prunetum lusitanicae and Viburno tini-Quercetum broteroanae (Costa et al. 2015;Rivas-Martínez et al. 2017b), there is a clear separation at 900/1000 meters of altitude between the series of potential vegetation.The temperature's reduction, signaled by the rise in altitude to the supertemperate, has resulted in the Quercus broteroana with Prunus lusitanica L. is disappearance and its alteration to Quercus pyrenaica Willd.groves.In terms of vegetation cover and landscape, this clear separation led us to study this territory's vegetation landscape in greater depth, as plant bioindicators can be a very useful tool in distinguishing and characterizing the environment, regarding thermicity, shoulder climate, edaphology and even the biogeographic limits of a given territory (Cano-Ortiz et al. 2022;Rivas-Martínez 2005).
Thus, since the main ecological characteristic of plants and plant communities is fidelity, based on plant bioindicators (Burger 2006;Parmar et al. 2016), we seek to improve the southern boundary of the European Atlantic Province.To achieve this objective, we tried to identify existing plant communities (with special attention to relics) and characterize them from a chorological, bioclimatic and edaphic point of view in order to select plant bioindicators to identify the submediterranean bioclimatic variant.Second, based on the distribution of identified taxa and syntaxa, we seek to identify the cartography that expresses the southern limit of the new biogeography for the European Atlantic Province.

Materials and methods
The studied territory is part of the mountains of the center of mainland Portugal, whose maximum elevation is located at 1,993 meters of altitude, including the Lousã-Açor-Estrela mountain range.It is a territory dominated by the Mediterranean pluviseasonal oceanic bioclimate and temperate oceanic, meso to supra, humid to ultrahyperhumid, semi-hyperoceanic to euoceanic (Rivas-Martínez et al. 2017).At the substrate level, siliceous rocks dominate, composed of greywacke, schist and granite at higher levels (Rodríguez Fernández et al. 2015).At the hydrographic level, Serra da Estrela gives rise to the two largest rivers that have their source in Portugal, the Mondego and the Zezere river.In Serra da Estrela, the river Alva is the most representative within the study area and flows into the Mondego.The Serra do Açor has its highest elevation in Pico da Ceboça, at 1,418 m a.s.l. and gives rise to the Ceira river, which flows into the Mondego.Serra da Lousã has its maximum elevation in Trevim, at about 1,205 m a.s.l.These three mountains are part of the Montejunto-Estrela mountain range and have a southwest-northeast orientation, crossing the national territory diagonally (Crispim 2008).
Taxonomic and syntaxonomic nomenclature follows up the work of Costa et al. (2012), complemented with Rivas-Martínez et al. (2002) and Rivas-Martínez (2011).Coutinho (1939), Franco (1971Franco ( , 1984)), Franco and Rocha-Afonso (1994) and Castroviejo et al. (1986) are used for plant identification.Plants with a subspecific epithet appear for the first time in the document in full and accompanied by the respective classifier.In the rest of the document they are abbreviated and presented only with the name of the genus and the subspecific epithet.For the syntaxa comparison tables, the caracteristic plants at the level of the association and higher units were used.In the relevé table, the plants' scientific name was abbreviated to the subspecific epiptet.The biogeographical and bioclimatic framework follows up the work of Rivas-Martínez et al. (2017a, 2017b).This work is conducted according to the the phytosociological method proposed by Braun-Blanquet (1979), Géhu and Rivas-Martínez (1981), Rivas-Martínez (2005) and updated by Biondi (2011).The International Code of Phytosociological Nomenclature (4 th Editions) was used for the description of new plant communities (Theurillat et al. 2021).
For the numerical analysis, we collected 18 field relevés, which were compared with another 106 relevés from the literature review (Table 1).Due to the relict character of some communities, it was not possible to carry out more phytosociological relevés.For each community, from a floristic and biogeographic point of view, the closest associations existing in the Iberian Peninsula were used.
For the hierarchical analysis, the characteristic plants at the association level were used.One hundred twenty-four relevés were submitted to hierarchial cluster analysis using Ward´s method with Euclidean distance to measure dissimilarity, using the software RStudio (Rodríguez- Guitián et al. 2007).The transformation of the cover-abundance values followed up Van der Maarel (1979).

Results and discussion
The fieldwork allowed a more detailed recognition of the Montemuro and Estrela Sierras Sector southern zone floristic identity (Atlantic Orolusitania Subprovince, European Atlantic Province).With the relevés and floristic analyzes four new plant communities and two subassociation of climatophilous oak forests of Genisto falcatae-Quercetum broteroanae were identified.These plant communities are typical of climatophilous and tempori-hygrophilous positions and have their own geographic identity, which contributes to the definition of biogeographical boundaries.Most of the identified associations belong to ecological positions of deep soils, taking into account the dynamics of the climatophilous oak forest series.1).In order to highlight the floristic differences between the Cytisus striatus associations, the characteristic plants are presented in Table 3. Synchorology: The soil's strong erosion has reduced the potential area for this gyestal occurrence; however, the new Alvo-Gardunhense District here defined is its ecological optimum.This association is well represented in Serra do Açor, as well as in the União de Freguesias de Vide e Cabeça.

Analysis and description of plant communities
Syndynamics and catenal contacts: This broom constitutes a replacement stage and integrates the edge of the climatophilous series of oak-alvarinho of Viburno tini-Querco broteroanae sigmetum.It frequently comes into contact with the Portuguese-laurel of Frangulo alni-Prunetum lusitanicae and with the heliophilous communities of the Calluno-Ulicetea class´s degraded soils.

SCROPHULARIO GRANDIFLORAE-SAMBUCETUM NIGRAE ass. nova hoc loco
Synecology and Synstructure: Siliceous community dominated by Sambucus nigra that develops along water courses and surface runoff of nitrophilous water, on deep soils with high organic matter.It occurs in territories influenced by a submediterranean bioclimate, with a meso to supratemperate thermotype, a humid to hyper-humid shoulder type and a semi-hyperoceanic continentality.In its composition, the presence of several elements of the Galio-Urticetea class, namely Urtica dioica L., Scrophularia grandiflora DC. and Alliaria petiolata (M.Bieb.)Cavara & Grande (Holotypus associationis hoc loco: Table 4, relevé 3).It is distinguished from Clematido vitalbae-Sambucetum nigrae by the absence of taxa such as Cornus sanguinea L., Rubus caesius L., Euonymus europaeus L. and Hedera helix L., as well as being distributed throughout the northeast of the Iberian Peninsula, at a chorological level (Bolòs 1978).More recently, Rubo vigoi-Sambucetum nigrae was described for the Serra de Sintra and Portalegre, growing on slightly nitrified siliceous substrates and in a humid thermomediterranean bioclimate (Silva et al. 2012).However, several taxa distinguish these associations, especially the presence of elements with a more temperate hue such as Scrophularia grandiflora, Hypericum androsaemum L., Prunus lusitanica, Ilex aquifolium L., Quercus broteroana, Primula acaulis L. and Salix salviifolia Brot.
(Figure 2).In order to highlight the floristic differences between the Sambucus nigra L. associations, the characteristic plants are shown in Table 5.
Synchorology: This syntaxon has a reduced distribution area due to anthropic action over the last decades, which is why only three phytosociological relevés could be carried out.This syntaxon occurs in the mountains of central Portugal, corresponding in biogeographic terms to the Montemuro and Estrela Sierras Sector, having its ecological optimum in Mata da Margaraça-Serra do Açor.
Syndynamics and catenal contacts: The Sambucus nigra community occurs in conditions very similar to the position of Ulmus glabra Huds., and may represent the first stage of this forest's replacement that is currently very altered.In the study area, it was observed in the most hygrophilous variants of the edges of the new potential oak groves of Quercus broteroana here proposed (Genisto falcatae-Querco broteroanae), also integrating the boundary of the ammias of Scrophulario scorodonae-Alno glutinosae sigmetum.(Bolòs 1956;Lara et al. 2007;Raposo et al. 2021).However, their biotopes are distinguished by greater need for water, need for shade and greater cold resistance of hazel trees.On the other hand, these communities must be considered relicts, once they are hardly recoverable after being destroyed.The few known spontaneous hazel nuclei are found in limit that are physiographically protected from fires, such as embedded valleys or rocky slopes.
Synchorology: The new association develops in the Montemuro and Estrela Sierras Sector, with its main population centres in the Municipality of Seia (Portugal).These hazel trees correspond to the southern limit of associations dominated by Corylus avellana for mainland Portugal.
Syndynamics and catenal contacts: In dynamic terms, this syntaxon represents the first stage of replacement or forest edge of the oak-alvarinho communities of Genisto falcatae-Querco broteroanae sigmetum and of riparian galleries of white borrazeira riparian galleries of Salico salviifoliae minorisigmetum.The tree cover's destruction promotes the appearance of a thicket of the association Lonicero hispanicae-Rubetum ulmifoliae.Catenally, it comes into contact with the temporary-hygrophilous Portuguese-laurel of the association Frangulo alni-Prunetum lusitanicae and with the alders of Galio broteriani-Alno glutinosae sigmetum.1956).However, the geographical and floristic differences allowed this subassociation to be raised to the Viburno tini-Quercetum broteroanae (Costa et al. 2012).It has been described as a thermotemperate (submediterranean) humid hyperoceanic syntaxon, occurring up to 500 m altitude (Rivas-Martínez et al. 2002).However, the oak groves that occur in the upper accounts have an original floristic composition, enriched with plants such as Genista falcata, Quercus pyrenaica, Eryngium juresianum (Laínz) Laínz, Prunus lusitanica and Veronica micrantha Hoffmann.& Link.Thus, based on 11 phytosociological relevés, we propose Genisto falcatae-Quercetum broteroanae ass.nova hoc loco (Holotypus associationis hoc loco: Table 8, relevé 3) for mesotemperate territories, occasionally reaching the supratemperate (submediterranean) humid to hyperhumid, semihyperoceanic, occurring from 500 to 800 meters in altitude, more thermal slopes at an altitude of 1,000 meters, on acid substrates formed by greywacke, schist or granite.
In view of the anthropic action, the best oak groves are found on north facing slopes.As a southern series of Quercus broteroana, influenced by the submediterranean subtype, the presence of elements of Quercetea ilicis is frequent.Of all the associations of Quercus robur, the one that most closely resembles it is the Viburno tini-Quercetum broteroanae by the absence of thermal elements, such as Smilax aspera and Asparagus aphyllus L., and the presence of Prunus lusitanica in climatophilous position, Genista falcata and Quercus pyrenaica (Table 9).Though having some plants in common, the remaining associations, have their own taxa that allow them to be distinguished at the floristic level (Figure 4).
For Serra da Gardunha we point out the subassociation asphodeletosum bento-rainhae (Holotypus associationis hoc loco: Table 8, relevé 11), marked by the presence of Asphodelus bento-rainhae P. Silva and also by the strong presence of Quercus pyrenaica.This subassociation marks the southeast limit of this series distribution area of potentially climatophilous vegetation.As this is an ecological limit, the oak groves in this territory have low ecological resilience, being found only on the north facing slopes.A good part of Serra da Gardunha has been transformed into Castanea sativa forests, so the oak groves are generally poorly preserved.
Synchorology: Both subassociations have their ecological optimum in the new Alvo-Gardunhense District (Montemuro and Estrela Sierras Sector Montemuro-Estrelense, Atlantic Orolusitania Subprovince, European Atlantic Province).The typus association occurs in Serra da Estrela, Açor and Lousã, while asphodeletosum bento-rainhae occurs from the northern slope of Serra da Gardunha to Sertã.The Genisto falcatae-Quercetum broteroanae ass.nova distribution area corresponds to the southern limit of the Atlantic European Province.

Syndynamics and catenal contacts:
The forests of Genisto falcatae-Quercetum broteroanae represent the climatic stage (Figure 5).The first replacement stage is formed by the azereira of Frangulo alni-Prunetum lusitani-  cae or by the avenal of Pruno lusitanicae-Coryletum avellanae ass.nova, which differs from the azereira grove due to the greater water requirement, need for shade and greater resistance to cold of Corylus avellana, although in this territory both associations have a relict character.However, Pruno lusitanicae-Arbutetum unedonis is more common and grows in less humid areas.On the edges of the forest and as a second replacement stage, a gyestal of Cytisetum grandifloro-striati ass.nova.Still on the forest edges, there is sometimes a herbaceous community of Omphalodo nitidae-Linarietum triornithophorae.In addition, on deep soils there are the perennial meadows of Avenella flexuosa (L.) Parl., which are currently quite altered, preventing the proper relevés performance.In clearings, slopes and roadsides there is a meadow dominated by Brachypodium phoenicoides (L.) Roem.& Schult., maintained through shrub vegetation grazing or cutting.With soil erosion, the heath and gorse of Erico umbellatae-Pterospartetum tridentati appear and with the decapitation of the soil, the association Pterosparto lasianthi-Ericetum cinereae appears.The last replacement stage is formed by a therophytic meadow of Galio parisiensis-Logfietum minimae.
In catenal terms, they come into contact at lower levels with oak groves of Viburno tini-Quercetum broteroanae and at higher levels with the oak woods of Holco mollis-Quercetum pyrenaicae.At the valley´s bottom, it comes into contact with the edapho-hygrophilous series of the alder of Scrophulario scorodoniae-Alno glutinosae sigmetum and with the ash trees of Omphalodo nitidae-Fraxino angustifolae sigmetum.
Synchorology: In the study area, one of the best places to observe this species is Mata da Margaraça, but it has also been observed along streams, namely in Vale de Loriga, Lapa dos Dinheiro (Seia), Cascata da Forja (Vide) and near Donas (North slope of Serra da Gardunha).Thus, we think that the presence of Ulmus glabra can help define the Alvo-Gardunhense District boundaries.

Syndynamics and catenal contacts:
The communities of Ulmus glabra are in contact catenally with the climatophilous oaks of Genisto falcatae-Quercetum broteroanae and with the edaphohygrophilous amylias of Scrophulario scorodoniae-Alnetum glutinosae.As the main replacement step, we identified a community of Sambucus nigra from Scrophulario grandiflorae-Sambucetum nigrae ass.nova.

COMMUNITY OF BETULA CELTIBERICA
Synecology and Synstructure: Although not very representative, some forest fragments of Betula celtiberica were identified in the study area.From an ecological point of view, the Betula forests form secondary communities that descend at 450 meters.Although their presence is residual, they are of great interest due to the coexistence with characteristic plants of Quercetea ilicis, namely, Viburnum tinus, Ruscus aculeatus, Erica arborea, Rubia peregrina and Phillyrea angustifolia L., which could represent a new syntaxon.This occurs in the semihyperoceanic to euoceanic hyperhumid mesotemperate level.Due to the low expression it was not possible to carry out phytosociological relevés.Frequent plants: Betula celtiberica, Quercus broteroana, Prunus lusitanica, Ilex aquifolium, Viburnum tinus, Frangula alnus, Dryopteris affinis, Viola riviniana, Pteridium aquilinum, Hedera hibernica, Rubus ulmifolius, Castanea sativa, Rubia peregrina, Ulex minor, Brachypodium sylvaticum, Teucrium scorodonia, Polystichum setiferum, Avenella flexuosa, Genista falcata, Crataegus monogyna, Daphne gnidium and Prunus avium.
This birchwood is geographically close to the association Saxifrago spathularidis-Betuletum celtibericae, however, they are differentiated through the thermotype, normally occurring above 1,000 meters, in the above supra to orotemperate thermotypes of the Estrela and Oresano-Sanabriense territories, as well as by the absence taxa of lauroid, Quercetea ilicis and Saxifraga spathularis (L.) Link, Taxus baccata L., Sorbus aucuparia L., Festuca elegans Boiss.and Cytisus oromediterraneus Rivas-Mart., T.E.Díaz, Fern., Prieto, Loidi & Penas.Synchorology: These relict communities occur in the low altitudes of the Estrela and Açor mountains, corresponding to the southern limit of the Betula celtiberica's natural distribution area in mainland Portugal.In biogeographic terms, they help to define the Alvo-Gardunhense District.

Biogeographic proposal for the study area
The improvement knowledge of the syntaxa's range has made it possible to identify a new territorial domain with its own identity and to distinguish it from surrounding biogeographic territories.Within the Montemuro and Estrela Sierras Sector, depending on the orientation of the slopes, the vegetation change occurs, on average, between 900 and 1,000 m a.s.l.This altitude is close to the work by Costa et al. (1998), when he refers to the Montemuro and Estrela Sierras Sector's altitudinal limit.The altitudinal limit of the Alvo-Gardunhense District can reach a minimum level of 400 m a.s.l., especially on coasts exposed to the north quadrant.Other works published on the biogeography of Serra da Estrela also followed the series of natural potential vegetation (Rivas-Martínez et al. 2017).However, the new Alvo-Gardunhense District now corresponds to the southernmost part of the former Estrela Sierran District (Rivas-Martínez et al. 2017).Below this altitude the natural potential vegetation is formed by the humid to hyper-humid meso to supratempered alvarinho oak series of Genisto falcatae-Querco broteroanae sigmetum, which is represented by the Alvo-Gardunhense District (Figure 6).Thus, it is a District influenced by the  submediterranean variant, mesotemperate humid to hyper-humid.At elevations above 1,000 meters, the natural potential vegetation is represented by the series of black oak from Holco mollis-Querco pyrenaicae sigmetum, corresponding to the Estrelense District.This District is influenced by the submediterranean variant, supra to orotemperate hyper-humid to ultra-hyper-humid.In order to differentiate and consequente definition of the adjacent sectors' biogeographic boundaries, the potential climatophilous vegetation corresponding to each territory is presented in Table 10.
Based on the ecological fidelity of plants and plant communities, it was possible to improve the Atlantic European Province´s southern limits definition in mainland Portugal, which now corresponds to the Alvo-Gardunhense District.The potential climatophilous forests that best define this District are Genisto falcatae-Quercetum broteroanae subass.typicum and subass.asphodeletosum bento-rainhae.These territories, mostly mesotemperate, are thus separated from the Estrelense District characterized by the supra and orotemperate thermotypes, where Quercus broteroana communities are absent.However, it is necessary to conduct more studies in order to understand the real distribution of the Viburno tini-Quercetum broteroanae, since the thermotempered territories are outside the European Atlantic Province and belong to the Portuguese Divisive Sector.
In order to help characterize this new Biogeographic District, the main stages of replacement of the series of potential climatophilous vegetation were identified, some of which were new to the scientific community.Although other syntaxa may help this biogeographic territory´s definition, the humanization of the landscape and climate change may contribute to its limits's redution, due to the tendency of future lower precipitation.Therefore, Genisto falcatae-Quercetum broteroanae ass.nova must be considered a relict vegetation series that needs urgent special conservation measures.

Table 1 .
Origin of the used relevés.
Synecology and Synstructure: Oak groves of Quercus broteroana from central Portugal were initially described as a subassociation of Rusco aculeati-Quercetum roboris, belonging to viburnetosum tini (Braun-Blanquet et al.

Table 10 .
Main series of potential vegetation that allow to distinguish the different biogeographical sectors.