Cyperus-dominated vegetation in the eastern Po river

The ephemeral vegetation dominated by Cyperus sp. pl. was surveyed and analyzed along the eastern trait of the Po River (Po Plain, Italy). Two formerly described communities were recognized: Cyperetum esculenti and Amaranthus tuberculatus-phytocoenon. A third greater cluster is assigned to a new association: Cyperetum micheliano-glomerati. It is characterized by Cyperus glomeratus, C. michelianus, C. odoratus and C. squarrosus, that have been detected on over 75 % of the relevés. The main floristic and ecological traits of these detected vegetation types are discussed.


Introduction
The biodiversity changes caused by human activities are global-scale phenomena; invasive alien species (IAS) threat the diversity in the European countries from a biological and ecosystemic perspective. Following the milestone set by the DAISIE Project (an overview is in Lambdon et al. 2008), many European researchers have been involved in expanding the knowledge of local and national invasive alien plants (e.g. for Italy, Galasso et al. 2018). The invasiveness of a single alien species may cause different impacts, due to the different degrees of resistence or resilience shown by habitats and phytocoenoses (Richardson and Pyšek 2006). Nowadays a major challenge is to clarify the impact of invasive alien plants on the natural habitats, merging the data on number and invasiveness of the alien species and relating them to the vulnerability of those habitats.
The Po Plain, in Northern Italy, is one of the European territories most invaded by alien plant species (EEA 2015). The Po river bed acts as habitat corridor, so that many alien pioneer species easily become invasive. Many alien plants are typical of riverine environments and cannot expand beyond the embankments; other ruderal and synanthropic entities are characteristic of the crops, located either between the embankments or out of them, e.g. the poplar clone crops.
Some case studies showed that riparian invasive plants can change the natural habitats: fast-growing trees and shrubs can affect river biodynamics, sedimentation and erosion processes (van Oorschot et al. 2017). Perennial tall herbs as Reynoutria spp. and annual vines as Humulus japonicus or Sicyos angulatus can create dense canopies that outcompete other species (Gerber et al. 2008;Balogh and Dancza 2008;Zhao et al. 2019).
The late summer vegetation of the Po river bed is composed of a set of generalist, nitrophilous species, mixed with other taxa that show peculiar ecological preferences, especially about water availability and substrate texture. These surfaces are free from running waters only for few months or weeks a year: therefore, the plants colonizing them need to start and complete their life cycle during this short time available. The weather trends and the sediments storage caused by floods influence the extent and duration of water-free surfaces from year to year, as well as the cover of late-summer pioneer vegetation. This is a suitable environment for therophytes, like annual Cyperus species, Echinochloa crus-galli, Eragrostis pectinacea, Lindernia dubia, Panicum dichotomiflorum, Portulaca oleracea, Rorippa palustris. These taxa release a stable seed stock in the ground, that is ready to germinate as soon as possible (van der Walk 1981;Assini 2001). Despite the relate dynamics of spreading and recolonisation are various and unpredictable, a significant advantage is given by the ability to germinate before the water fully recedes (Abernethy and Willby 1999).
The genus Cyperus in Italy includes about 30 species. Many of these are expanding their distribution range, favoured by global warming. These taxa develop late in the season, when the river bed partially emerge from the water due to the decreasing flow, and/or when the waters of the rice-fields are heated enough by the sun. Ten Cyperus species grow along the Po river in the study area (Pellizzari and Verloove 2017). Among them C. flavescens, C. fuscus and C. michelianus are native. C. eragrostis, C. odoratus and C. squarrosus are neophytes from tropical America (Petrik 2003;Verloove 2014). C. microiria is native to eastern Asia (Verloove 2014). C. difformis, C. esculentus and C. glomeratus are paleo-subtropical species, native in some Mediterranean areas, but considered as aliens in Italy . They are spreading in temperate areas.
This work aims to analyse the ephemeral late-summer vegetation dominated, or mainly characterized, by Cyperus sp.pl. Those types are threatened by a pool of Invasive Alien Species (Janssen et al. 2016) and poorly known in the study area. Few types of ephemeral vegetation of river beds are recognized in the Po Plain, representing the main vegetation aspects at the minimum river flow (Sartori and Bracco 1995). These types develop on stretches of the river bed, like oxbows, that are submerged during most of the year, but that in summer are separated from the main course by islands or sand banks, so that they completely dry. Some of these communities are dominated by low-grown species and mainly ascribed to the Cyperetum flavescentis (Nanocyperetalia, Isoëto-Nanojuncetea) (Biondi et al. 1997;Assini et al. 2010). Other communities are featured by medium and tall-size therophytes and were framed in the Bidentetalia tripartitae and Bidentetea (Biondi et al. 2003;Bolpagni 2013b). Outside the Po Plain, the main studies to the hygro-nitrophilous annual vegetation are focused on communities dominated by native species, in which the flatsedges and galingales usually play a minor role (Felzines and Loiseau 2005;de Foucault 2013 a, b;Rennwald 2000;Schneider-Binder 2020). The scheme of Brullo and Minissale (1998) for the Western Palaearctic region needs to be upgraded by a large amount of new data, mainly for France and Spain, but also for the Italian Peninsula (Deil 2005). Only few papers, however, refer to the Po river traits.

Study area
The Po river stretches for 652 km in Northern Italy, from Western Alps to the Adriatic Sea. It receives the last left tributary (Mincio river) 156 km upstream of the mouth, while the final right-handed tributary (Panaro river) 107 km upstream of the mouth. In this trait the river has flooded six times in the last two centuries (Turitto et al. 2004). After the last disastrous flood occurred in 1951, the main river bed has been permanently embanked and periodically dredged. The bends, banks and oxbows located in the upstream traits of the Po river can foster the natural ephemeral vegetation; the downstream river management as a stabilized channel, partially precludes spatial heterogeneity and habitats diversity (Shankman 1996). The relevés were carried out along the main course of the Po river, between Sermide and Panarella, upstream to the river channelization into the Po Delta branches (Fig. 1). The riverine environment is very homogeneous, due to the stabilization of the embankments, which are over 10 m high. It is distinct from the surrounding plain, lower in elevation and widely ploughed and cultivated. In the final portion of the Po river, two annual maximums are detectable in the water flow, in May and in November, respectively. From the end of May the hydrometric levels start decreasing to the minimum, which is usually reached in August, and then grow back. The decrease in solid transport due to decreasing flow significantly affects the fluvial ecosystem, causing a strong lowering of the river bed, and a widespread coastal erosion by the Adriatic Sea. The restrained summer flow and the increasing groundwater pumping for agricultural and industrial uses have led to the intrusion of salt groundwater up to 20 km in the inland (Tornatore 2008).
Following the application to Italy of the wordlwide bioclimatic classification (Rivas Martinez et al. 2011), the study area belongs to the Temperate (steppic) Macrobioclimate. The Bioclimate shifts from continental westwards to steppic eastwards. The ombrotype is lower subhumid and the thermotype is upper mesotemperate (Pesaresi et al. 2017).

Field survey
132 original relevés were done from August to October 2016, according to the phytosociological approach (Braun-Blanquet 1964;Biondi 2011). Date and location of each relevé are listed in Appendix I. Species names follow the italian checklists (Bartolucci et al. 2018;Galasso et al. 2018). Syntaxonomy follows Biondi et al. (2014).

Data analysis
The species that appeared only in 1 or 2 relevés were removed from the original matrix. The two matrixes were compared through Euclidean distance, then the reduced matrix (132 relevés for 45 species) was subjected to cluster analysis using an average-linkage algorithm in the software Cluster, version 3.0 (Stanford University 1999). The corresponding dendrogram was obtained using Java-TreeView (Saldanha 2004).
To underline the main ecological features of each observed vegetation type, the Ellenberg indicator values were calculated for each obtained cluster, and then the ecograms and the mean indicator values were compared (Pignatti et al. 2005). Life forms (Raunkiaer 1934) and chorological spectra were also calculated for each one of the three groups. The chorotypes follow Pignatti et al. (2017Pignatti et al. ( -2019. Archaeophytes (A) and neophytes (N) were detected according to Galasso et al. (2018).

Results
Three main groups were obtained from the cluster analysis, each one corresponding to a distinct vegetation type (Fig. 2).
The groups 1 and 2 are distinct from the last big cluster. The group 1 includes relevés dominated by Cyperus esculentus, with a constant presence of Amaranthus tuberculatus, Xanthium italicum and Portulaca oleracea (Tab. 1). This vegetation type develops mainly along the sand bank borders, that are uncovered by the water and hard dried in summer. C. esculentus is able to colonize this environment defending from surface dryness by means of deep and long rhyzomes. These stands develop further high from the water than those of the Polygono lapathifolii-Xanthietum italici, which grows in the same sandy substrates (Bolpagni 2013b). Annual flatsedges, like other silty-clay substrate species (e.g. Lindernia dubia, Eclipta prostrata) are almost absent. These communities are ascribable to the Cyperetum esculenti, present in the middle-European river beds, e.g. in Germany (Wisskirchen 1995), and France (Felzines and Loiseau 2005). In Italy it was detected along the Po river in Lombardy and Emilia-Romagna (Bolpagni 2014;Braghiroli and Bolpagni 2016), and along the Tiber river (Lastrucci et al. 2012).
The group 2 gathers 32 relevés dominated by Amaranthus tuberculatus, a north-American dioecious amaranth, that has recently become invasive in Italy, where it grows in many disturbed habitats (Iamonico 2015). Its distribution is not influenced by sediment texture, though it often grows on sandy substrates. Similar communities were considered as a form of the pebbly-sandy shore community Polygono hydropiperis-Bidentetum tripartitae (Pellizzari 2009). In the present analysis, we follow the attribution to an Amaranthus tuberculatus-phytocoenon, characterized by this species and a pool of alien pioneer entities, much of them are typical of Bidentetalia (Bolpagni 2013b;Braghiroli and Bolpagni 2016). The cluster is characterized also by the high frequence of four flatsedge species (Cyperus squarrosus, C. michelianus, C. esculentus and C. odoratus) (Tab. 2).
The last big cluster (group 3) is interpretable as a single vegetation type, able to grow on medium-fine substrates. This cluster is very homogeneous, especially in its central part. The most frequent species of this group is Cyperus glomeratus (100 %), followed by C. odoratus, Echinochloa crus-galli, C. michelianus, C. squarrosus and Amaranthus tuberculatus, all reaching over 75 %.
The average species number of the whole group results in 11.5; some relevés, to the left side of the group, are slightly different based on the higher average number (12.6), due to the presence of Amaranthus tuberculatus, Eragrostis pectinacea, Portulaca oleracea and other species that document a major disturbance, while other Cyperus species play a minor role.
The central part of the cluster represents the typical aspect of the community: C. odoratus, C. michelianus and C. squarrosus may show equal or higher cover than C. glomeratus. Lindernia dubia and Panicum dichotomiflorum are also frequent species, when Amaranthus tuberculatus decreases and runs out (Tab. 3).
The main ecological traits of the observed vegetation types are confirmed by the comparison of the mean Ellenberg values calculated for each group of relevés (Tab. 4). The ecograms are basically similar, with all the vegetation types showing high values for light, temperature and moisture; the indicator values for continentality, soil reaction and nutrients are lower (Fig. 3). The Amaranthus tuberculatus-phytocoenon shows the highest N value (6.25), due to the presence of a pool of summer-annual weeds, that also colonize crops and poplar plantations of the Po plain.
The Cyperetum micheliano-glomerati shows the highest moisture index (7.89). It is characterized also by high light and temperature, due to its tendency to grow in the lowest parts of the dried river bed, that are far from temporary shading effects.
The three recognized vegetation types show the typical traits of the pioneer ephemeral vegetation, as it is clearly showed by the life form spectra, that are dominated by therophytes (Fig. 4). Cyperus glomeratus, often a helophyte in reedbeds, behaves as annual in the surveyed environments, spreading from the spring seed stock. The bar graph data include the sporadic species. If these are neglected, the therophyte rate rises on Cyperetum micheliano-glomerati from 64% to 89.2%.

Character species
Cyperus glomeratus L. 2 3 2 3 3 4 1 3 2 3 2 1 5 5 4 4 4 4 3 4 4 2 3 2 2 1 1 2 Cyperus odoratus L. 3 2 2 3 2 2 3 3 2 2 1 1 2 1 3 2 . . . 1 1 2 2 3 3 2 4 3 Cyperus michelianus (L.) Delile 3 2 3 2 1 3 2 2 4 4 5 5 1 . 2 . 1 . 1 2 1 . 1    but it is difficult to identify a clear combination of constant species. Due to its size (sometimes over 2 m) and invasiveness, that weed outcompetes the dominant and characteristic species of all Bidention-communities, whose cover values seem underestimated. C. michelianus and C. squarrosus are able to grow under the thick layers of Amaranthus, unlike, for instance, C. glomeratus. To assign this community to a subassociation or variant of Polygono hydropiperis-Bidentetum tripartitae could mean to underrate the role of A. tuberculatus; conversely, to tipify a new association could mean too emphasize it. The relatively low number of Bidention different communities is related to a large variation of each type, under the aspect of species composition, physiognomy and anthropic pressures (Neacşu and Arsene 2017). Further data and a comparison with other situations outside of the river bed (such as crops or disturbed areas, in which A. tuberculatus is equally invasive), are needed for the institution of a new syntaxon (Costea et al. 2005). The palaeosubtropical species Cyperus glomeratus and C. michelianus give the name to the newly described association Cyperetum micheliano-glomerati, for which also the American neophytes C. odoratus and C. squarrosus are listed as character species. The highlighting of the palaeosubtropical entities (Fig. 5) is seen as an opportunity for reconsidering the status of Cyperus glomeratus compared to C. michelianus. Both are native from Eastern European/Western Asian areals, and nowadays the first is also considered native in Italy by Euro+Med Database (Jimenez-Mejas and Luceño 2011) and IUCN (Kavak 2014). The European distribution ranges of the first two flatsedges are considerably overlapping. Outside Europe, C. michelianus is nowadays widespread in Africa and southern Asia (Lansdown 2014), while C. glomeratus is common further north, up to Korea and Japan (Kavak 2014). Linnaeus (1756) described C. glomeratus based on an Italian specimen (Peruzzi et al. 2008); C. australis Schrad. is a later synonymous of C. glomeratus (Govaerts and Simpson 2007). The species was widespread, although rare, and not strictly linked to rice fields. Indeed, this habitat favoured different species as C. difformis and C. fuscus, both assigned to subgenus Anosporum: their C3 photosynthetic pathway gives them an ecological advantage in habitats flooded for long time (Matsunaka 1983;Pellizzari and Verloove 2017).
C. glomeratus has a wide ecological amplitude. In addition to the presence in the studied late summer vegetation, it plays an active role in building helophytic fringes of Phragmition, along rivers and around lakes, in fresh or brackish waters (Bragato et al. 2006;Biondi et al. 2009). Along the Chienti river (Marche), a C. glomeratus-dominated community was framed into the Magnocaricion (Crisanti and Taffetani 2015). Another C. glomeratus-community found along the Po river was framed into the Chenopodion rubri (Sartori and Bracco 1996;Pellizzari 2009;Assini et al. 2010). Other C. glomeratus-dominated communities were ascribed either to the Bidention or to the Nanocyperion, e.g. along the Po river up to the Venetian Delta (Marconato et al. 2014). At Lake Pistono (Piedmont), some seasonally flooded muddy shores host flatsedge communities: Cyperetum flavescentis close to the water and a Bidention-community with C. glomeratus in less flooded sites (Tisi et al. 2007). A C. glomeratus-community of Nanocyperion can be found in two sites in Lombardy; it is dominated by C. glomeratus, C. fuscus and C. michelianus (FLA 2008). In these cases native species are dominant, unlike along the Po river. In Slovakia, C. glomeratus was reported in the Danube river beds in the middle 19 th century, and was recently rediscovered in few sites. Here the species characterizes an ephemeral, two-layered vegetation type, with features of both Nanocyperion and Bidention, interpreted as a highly ruderal facies of Cyperetum micheliani (see below: Meleckova et al. 2016). Downstream along the Danube river, from the Eastern Wallachia to the Delta, both C. glomeratus and C. michelianus are characteristic of the macrophytes riparian vegetation (Stankovic et al. 2015).
The second characteristic species of Cyperetum micheliano-glomerati is another linnean species from Italy, Cyperus michelianus. It is diagnostic of several European plant communities. Lacking of Western taxa, some of these (Cyperetum micheliani, Lindernio-Dichostylidetum michelianae) are clearly continental, known from Central and Eastern Europe (Trpin et al. 1996;Jasprica et al. 2003;Šumberová 2011;Dubina et al. 2015). Except for Cyperus fuscus, the diagnostic species of Cyperetum micheliani sensu Šumberová (2013) are rare or completely missing along the Po river. Other communities characterized by C. michelianus develop in the Atlanto-Mediterranean range, i.e. in France and Spain (Corillion 1971;de Foucault 2013b;Cochard and Guitton 2014;Renaux 2014;Rivas-Martinez et al. 1980 ;Camacho et al. 2009). In Emilia-Romagna, along and near the Secchia river, the Crypsio schoenoidis-Cyperetum micheliani grows on siltyclay soils (EGPB Emilia Centrale 2013). Within the study area of this work, a C. michelianus-community of Heleochloo-Cyperion was detected at first (Pellizzari 2009). Based on the results of this study, it can be assigned to the new described association, that reports in the same habitat C. glomeratus and C. michelianus together with C. squarrosus and C. odoratus. The last one peculiar species was recently discovered during an investigation of the Po river bed, and in several herbarium specimen (Verloove 2014). In particular, some of them were correctly identified after a former attribution to Cyperus strigosus (Lastrucci et al. 2016;Pellizzari and Verloove 2017). C. odoratus is naturalizing at least in three different European areas (Verloove 2014): a) the Po river in Italy; b) along the Danube river in Serbia, and in its Delta in Romania (Anastasiu and Negrean 2006); c) in NE Spain, along the Segre river down to the confluence with the Ebro. Nowadays C. odoratus is rather common in the Po river beds of Lombardy (Galasso and Banfi 2015), Emilia-Romagna (Verloove 2014), Veneto (Masin et al. 2015) and Tuscany (Lastrucci et al. 2016;. The last species, C. squarrosus, reached the Po plain in the late 19 th century (Cavara 1899), but its spread began in the muddy river beds and ponds only in the last years (Bolpagni 2013 a,b).
Despite a resemblance with the Cyperetum micheliani identified along the Danube river in Slovakia and Hungary, the Cyperetum micheliano-glomerati is rather different. In fact, the communities that grow along the Po river have a higher total cover (often 100 %) and are characterised by a pool of Cyperus species. This is a peculiarity of such vegetation. Along the Po river, near Mantua, no aspects simultaneously dominated by different Cyperus species were found: similar situations were dominated by a larger neophyte set, mainly composed by graminoid grasses (Echinochloa crus-galli, Panicum sp. pl., Paspalum distichum) (Bolpagni 2013b). The only abundant flatsedge was C. squarrosus, and that suggested to frame those communities, in which C. glomeratus and C. difformis played a minor role, in the Nanocyperion. Communities of the Nanocyperion flavescentis are composed of native species and clearly different from the newly typified community.
Here, only C. flavescens is characteristic of alliance, while C. fuscus and C. michelianus are characteristic of order (Brullo and Minissale 1998).
The following observations support the inclusion of the Cyperetum micheliano-glomerati in the Bidention (Bidentetea): 1. A major role, together with Cyperus spp., played by characteristic species of Bidention and of higher syntaxonomic units (Echinochloa crus-galli, Amaranthus tuberculatus, Lindernia dubia, Persicaria lapathifolia, Panicum dichotomiflorum, Bidens connata, B. frondosa, etc.); 2. The alien origin of some pioneer species, that witness both high soil eutrophication and disturbance of the regular flooding, able to carry seed stocks; 3. The fine particle size of silty-clay substrates, compared with that of contact communities of Chenopodion rubri. According to Biondi et al. (2012), communities of Cyperetum micheliano-glomerati are referable to the habitat 3270 "Rivers with muddy banks with Chenopodion rubri p.p. and Bidention p.p. vegetation" (CORINE Biotopes 22.33 and 24.52; EUNIS C3.52 and C3.53). In Italy this habitat is widespread and typically invaded by alien plants, much of which are of tropical and subtropical origin (Zivkovic and Biondi 2010). The next goal will be to clarify the synecology of these alien, often invasive entities (Assini et al. 2010).
The human impacts drastically changed the final stretch of the Po River bed, so that it is very homogeneous and artificial. The late summer ephemeral vegetation is easily replaced by long-lasting secondary vegetation or directly destructed. That underlines the rareness and fragility of such habitat (Bolpagni 2013b;Ditetova et al. 2016). The typified Bidention-community expresses an aspect of conservation interest, in spite of its alien species richness. Anyway it is lower, if compared with the other aspects framed in the Chenopodion rubri. The Cyperetum micheliano-glomerati preserves the natural traits and plays an important ecological role when compared to the artificially managed river beds and river banks.