Hydrocharis laevigata in Europe

Hydrocharis laevigata (Humb. & Bonpl. ex Willd.) Byng & Christenh. [= Limnobium laevigatum (Humb. & Bonpl. ex Willd.) Heine], Hydrocharitaceae, is a floating-leaf aquatic plant that is native to inland South America. It is an invasive species in several parts of the world. Reports of its presence in Europe have been recently published: naturalised populations occur in three locations on the Iberian Peninsula. The literature also contains records of the species in Hungary and Poland. In addition, it has been observed in Sweden, Belgium, and the Netherlands. H. laevigata is highly adaptable and can profoundly transform habitat conditions in its invasive range, causing major issues for ecosystem conservation and human activities. Until recently, H. laevigata was not to be found in natural environments in Europe. Factors explaining its spread include its use as an ornamental plant, the eutrophication of inland waters, and the effects of global warming. With a focus on Europe, this short communication provides information on the species’ distribution, taxonomy, biology, habitat, and negative impacts.


Introduction
The major decline in freshwater species biodiversity has become one of the most important alterations in ecosystems around the world [1,2]. Pollution, water flow restrictions, and climate change are transforming conditions in freshwater habitats, favouring the establishment of invasive species [3][4][5].
There is a common consensus, supported by the Red List of European Habitats [6], that the key threats to European aquatic and wetland habitats are alterations to hydrological systems, climate change, pollution, and invasive species [7]. In Europe, native freshwater biota are facing increasing competitive pressure due to the arrival and spread of floating-leaf aquatic plants (e.g., Azolla filiculoides and Eichhornia crassipes) in inland water bodies [8][9][10][11][12][13][14][15]. Of particular concern is the recent appearance of an aggressive invasive alien species (AIS), Hydrocharis laevigata, whose common names include South American spongeplant, smooth frogbit, or Amazon frogbit. Newly established in a range of European ponds, rivers, and reservoirs, the species serves as yet another warning about the deterioration of Europe's freshwater habitats. Its invasive dynamics are reminiscent of those of Eichhornia crassipes, including its striking colonisation abilities. This short communication describes H. laevigata's history in Europe, including its emergence in distinct continental regions. It also provides key information about the species' taxonomy, biology, habitat, and negative impacts. To this end, it will facilitate prevention efforts aimed at invasive species, help control the spread of H. laevigata, and bolster the preservation of Europe's native biodiversity.
Phylogenomic, morphological, and anatomical evidence strongly suggest a new vision of the genus Hydrocharis L. [16,17], one that includes the species of Limnobium Rich., usually considered to be a separate genus by World Flora Online (WFO) [18]. Assuming the species' reclassification, there are currently five known members of the genus Hydrocharis L. Three are spread throughout Afro-Asia, and the other two are found from Mexico to northern Argentina and in the Caribbean. Those previously classified in Limonium are native to the Americas and utilise wind pollination. The original members of Hydrocharis are autochthonous from the Old World and are insect pollinated [19]. Those differences aside, all five species have a close phylogenetic relationship and display similarities in their vegetative traits [19,20]. Hydrocharis

Species Description
According to [21][22][23][24], H. laevigata is an aquatic stoloniferous plant whose stems are floating on or suspended in the water. They develop floating or emergent leaf rosettes, which are sometimes rooted. The species' differentiated leaves are petiolate, laminate, cordate to reniform, or orbiculate, stipulate, and dimorphic. The aerial leaves have flat, leathery blades and long erect petioles measuring up to 40 cm; the floating leaves have thick spongy tissue on the lower surface and shorter petioles (minimum of 12 cm). Flowers are about 15 mm wide, unisexual, pedicelled, and enclosed in a spathe. Staminate flowers often occur in clusters of two or three; have three (rarely four) sepals and petals each; possess a variable number of stamens, whose filaments form a single column; and usually exhibit staminodes. Pistillate flowers are solitary; have rudimentary sepals and petals, although the latter may be lacking; and possess a unilocular ovary with six carpels, six styles, and divided linear stigmas that are longer than the perianth segments. Furthermore, female flowers may sometimes exhibit staminodes. The species' fruit consists of globose or ellipsoid fleshy berry-like capsules (~1.5 cm long and 0.4-3.5 mm wide) that contain as many as 100 ellipsoid seeds measuring around 10 mm long.

Habitat
Found in the tropics and subtropics [22,25], H. laevigata grows in a variety of freshwater habitats, such as shallow ponds; lakes; dams; reservoirs; pools; and the margins of slow shady rivers, canals, and ditches; environments with a high degree of eutrophication are particularly hospitable [26,27]. The species occurs at elevations from sea level all the way up to 2800 m. It is absent from fast-flowing watercourses [21,22,26,28], and cold temperatures limit its distribution [25].

Reproduction
Hydrocharis laevigata reproduces vegetatively via the fragmentation of the stolon segments connecting the leaf rosettes. The floating rosettes send out stolons bearing ramets on Plants 2023, 12, 701 3 of 10 their ends [29]. The rosettes are easily dislodged by waterfowl or large mammals in the species' native range [26], as well as by water currents or other types of water movement in general. Consequently, H. laevigata is able to rapidly and efficiently colonise suitable new habitats [28].
After pollination, the pedicel of female flowers tips downwards, such that the fruit develops submerged in water; once it reaches maturity, it breaks open, releasing a mucilaginous mass of about 100 seeds [21].

Global Distribution
The native range of H. laevigata extends across the tropics of Central and South America. Naturalised populations can now be found on all continents, with the exception of Antarctica.
According to [22,24,30], this species is naturally found in water bodies in parts of the Americas with tropical, subtropical, and, sometimes, temperate climates. More specifically, these locations are the CARIBBEAN: Antigua and Barbuda, Cuba, the Dominican Republic, Guadeloupe, St. Lucia, Montserrat, Martinique, Trinidad and Tobago, and Puerto Rico; CENTRAL AMERICA: Mexico, Costa Rica, Guatemala, Nicaragua, Panama, and El Salvador; and SOUTH AMERICA: French Guiana, Guyana, Suriname, Venezuela, Brazil, Colombia, Ecuador, Peru, Argentina, Paraguay, and Uruguay. It should also be noted that there may exist some problematic records for South America. For example, although [31] stated that the species is native to the Southern Cone, this assertion is questionable in the case of Chile, as [26] indicates that the country's oldest herbarium specimen dates back to 1954. The same is likely true for Argentina: while the species' native range is thought to extend across most of the country, it certainly appears to be invasive in the southernmost regions of Argentina, where it has recently appeared for the first time [32].
As noted in [25,29,[33][34][35][36], H. laevigata has become naturalised and spread across ASIA: Japan, Taiwan, and Indonesia; AFRICA: Zambia and Zimbabwe; AUSTRALIA: New South Wales and Queensland; NORTH AMERICA: southern Canada as well as the north-eastern and western US; and EUROPE.

Populations in Europe
Based on the scientific literature and the GBIF database, H. laevigata is known to occur in six European countries: Belgium, Hungary, The Netherlands, Poland, Spain, and Sweden.
The first record of its presence (as Limnobium laevigatum) was in hot springs located in Komárom-Esztergom County, northern Hungary [37]. In September 2018, the species was observed in the area of Fényes springs, north of Tata. At this location, the plants were mainly in a vegetative state, although some did bear flowers. One month later, the plants had spread to the Ferencmajori fishponds, traveling a distance of about 1.3 km. In October 2018, the species turned up at another site within the same county: Dunaalmás, a stream fed by warm water [37]. It was observed that the H. laevigata populations became established near hot springs (temperatures = 21-23 • C), which do not freeze in the winter. Recently, Dr. Riezing (pers. comm.) has indicated that these populations in northern Hungary have persisted, likely because of mild winter conditions and the warm water temperatures. However, the plants occur in small groups.
On the Iberian Peninsula, the species seems to have rapidly expanded its range. Since 2018, it has been found at three locations that are quite distant from each other. The first published record for this species (as Limnobioum laevigatum) was associated with a reservoir near Madrid [38]. A few years later, it was observed in a stream next to a dam near Córdoba [39]. Finally, it was also reported to occur in the Guadaira, a tributary of the Gualdalquivir, near Seville [40] (Figure 1). There are no indications that H. laevigata has disappeared from any of these locations in Spain.
Gualdalquivir, near Seville [40] (Figure 1). There are no indications that H. laevigata has disappeared from any of these locations in Spain.
In 2020, H. laevigata was observed in southern Poland, in an artificial pond near Agatowa Street in the district of Bieżanów-Prokocim in eastern Kraków [15]. It was noted [15] that the species (as L. laevigatum) is likely a sporadic invader in Poland, given that other similar invasive species display constrained ranges due to the country's cold winter temperatures. Dr. Pliszko (pers. comm.) recently confirmed that this population has disappeared because of the species' vulnerability to low temperatures. It cannot survive winter conditions in Poland, outside of the habitat found in greenhouses or residences (Figure 1).  In 2020, H. laevigata was observed in southern Poland, in an artificial pond near Agatowa Street in the district of Bieżanów-Prokocim in eastern Kraków [15]. It was noted [15] that the species (as L. laevigatum) is likely a sporadic invader in Poland, given that other similar invasive species display constrained ranges due to the country's cold winter temperatures. Dr. Pliszko (pers. comm.) recently confirmed that this population has disappeared because of the species' vulnerability to low temperatures. It cannot survive winter conditions in Poland, outside of the habitat found in greenhouses or residences (Figure 1).
The GBIF lists nine geographical records for H. laevigata in Europe [41], which include Ganshoren, Belgium; the outskirts of Stockholm, Sweden; and Aalsmer and Bleiswijk in the Netherlands. Only in the latter country are the records associated with herbarium specimens. In the other cases, there are only photographs, no herbarium samples (Appendices A and B). Two of these locations represent artificial habitats: a greenhouse in Aalsmeer in the Netherlands and the Bergianska Botanick Garden in Sweden. The remaining records for Belgium and the Netherlands were one-time events. Consequently, Plants 2023, 12, 701 5 of 10 they can be viewed as sporadic occurrences that have not resulted in H. laevigata becoming naturalised. The same is true for the record in Poland. Therefore, at present, the only naturalised H. laevigata populations in Europe are in Hungary and Spain ( Figure 2). Ganshoren, Belgium; the outskirts of Stockholm, Sweden; and Aalsmer and Bleiswi the Netherlands. Only in the latter country are the records associated with herbar specimens. In the other cases, there are only photographs, no herbarium samples (Ap dixes A and B). Two of these locations represent artificial habitats: a greenhous Aalsmeer in the Netherlands and the Bergianska Botanick Garden in Sweden. The rem ing records for Belgium and the Netherlands were one-time events. Consequently, can be viewed as sporadic occurrences that have not resulted in H. laevigata becom naturalised. The same is true for the record in Poland. Therefore, at present, the only uralised H. laevigata populations in Europe are in Hungary and Spain (Figure 2).

Figure 2.
Locations where Hydrocharis laevigata has been observed in Europe. Blue d sporadic presence. Red dots: naturalised populations. When the name of the city h different spelling of the English alphabet, it appears below in its original spelling. M created using The Geospatial Conservation Assessment Tool.

Invasiveness
As noted in the introduction, H. laevigata displays invasive dynamics reminiscen those of Eichhornia crassipes, including its marked capacity for colonisation [25,32,42] deed, like other invasive aquatic plant species, it is fast growing and thrives in still wa containing high concentrations of nutrients [43]. Under these conditions, it can outc pete native aquatic plant species and profoundly transforms the habitats it invades. W the impacts of this species have yet to be fully described, past observations [22,25,28 indicate that the floating rosettes block light from reaching the water below, indire fostering anoxic conditions. H. laevigata can thus reduce the abundance and diversit

Invasiveness
As noted in the introduction, H. laevigata displays invasive dynamics reminiscent of those of Eichhornia crassipes, including its marked capacity for colonisation [25,32,42]. Indeed, like other invasive aquatic plant species, it is fast growing and thrives in still waters containing high concentrations of nutrients [43]. Under these conditions, it can outcompete native aquatic plant species and profoundly transforms the habitats it invades. While the impacts of this species have yet to be fully described, past observations [22,25,28,44] indicate that the floating rosettes block light from reaching the water below, indirectly fostering anoxic conditions. H. laevigata can thus reduce the abundance and diversity of aquatic plants and animals (e.g., fish, phytoplankton, submersed plants) by rendering water bodies unsuitable for other organisms. The species can also generate mats that cause damage to human infrastructures (e.g., by clogging irrigation pipes or sewers, by damaging pumps or generators in hydroelectric power stations). Consequently, H. laevigata is considered to be one of the most harmful weeds in the United States and Australia, given its high degree of invasiveness combined with its negative impacts on water quality and aquatic biodiversity [25,29,42,44].

Control
Typical methods for controlling H. laevigata are mechanical harvesting and herbicide treatments [45,46]. In the Sacramento-San Joaquin Delta, diquat dibromide has been used, either on its own or in tandem with low levels of glyphosate [46]; this work yielded unclear results. Another study [47] evaluated the performance of the herbicides imazamox, penoxsulam and topramezone. Imazamox (with 1% methylated seed oil surfactant) was found to control all the growth stages of H. laevigata; penoxsulam was particularly effective in targeting seedling and rosette growth. Research is currently lacking on potential biological control methods. However, [36] points out that certain North American herbivores display a dietary specialisation for American frogbit (H. spongia). They might therefore be candidate biological control agents.

Discussion
In summary, H. laevigata is an invasive plant species that poses a significant threat to ecosystems and certain human activities in its non-native range. Its likelihood of establishment is considerably elevated in nutrient-rich, slow-moving freshwater systems subject to mild winter temperatures [25][26][27][28], such as those found in southern Europe or the northern Mediterranean. Its invasion dynamics are similar to those of Eichhornia crassipes [25,32,42].
As indicated earlier, the ornamental plant trade is the main source of H. laevigata (and Eichhornia crassipes) introductions. This fact explains how the species has spread so far from its native range to parts of the world as diverse as Australia, Zimbabwe, Japan, and Spain.
The range expansion of H. laevigata within Europe underscores the deterioration of the continent's inland aquatic ecosystems. Such is, above all, the result of eutrophication, but other causal factors include changes to hydrological regimes (i.e., reduced levels of water flow), decreasing degrees of water transparency, and global warming, which are simultaneously transforming natural aquatic environments [5,[48][49][50][51][52][53]. These ecological shifts are harmful to native aquatic plant populations while promoting the establishment of invasive species such as H. laevigata, leading to profound transformations in European ecosystems [12,14,[54][55][56][57].
It is curious to note that, while the invasive H. laevigata has begun to expand its range in Europe, the native H. morsus-ranae, a close relative, is experiencing decline. While the latter has always been patchily distributed across western Europe, populations are shrinking in certain regions [58]. For example, on the Iberian Peninsula, H. morsus-ranae now occurs in a single area [59], a range constriction that took place over the last century. Probable causes include habitat degradation due to farming and industrial activities as well as changes in the hydrochemical characteristics and hydrological regimes of water bodies [58]. At the same time, H. morsus-ranae has become an AIS in the north-eastern USA and southern Canada [60,61].
Hence, given the plant's recent range expansion in Europe, it is crucial to maximise efforts to rapidly detect its presence. By acting now, during the early stages of the invasion, it is more likely that H. laevigata can be controlled [62,63]. At particular risk is the Mediterranean, where conditions in rivers, streams, lakes, ponds, reservoirs, and canals favour the arrival and establishment of H. laevigata. In this regard, it should be added that the introduction and spread of IAS are a major concern for the European Union; for those reasons, Regulation (EU) No 1143/2014 of the European Parliament and of the Council of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species was published, which is being developed and updated through different implementing regulations and which establishes rules to prevent, minimize, and mitigate the adverse effects of IAS. This regulation is associated with a list of IAS: "the Union list", which is the fundamental instrument for implementing the aforementioned regulation. Hydrocharis laevigata is not included in this list. Taking into account the problems that this species causes to native biodiversity and to human activities in other parts of the world, it is hoped that the information contained in this brief note will serve as a starting point to initiate actions to include Hydrocharis laevigata in the "the Union list", something that will undoubtedly benefit the conservation of European biodiversity and reduce its harmful effects on human activities.

Materials and Methods
This study was based on an extensive literature analysis, data from field surveys, and the examination of herbarium specimens (at MA, SEV, COFC; see Appendix A).
The Geospatial Conservation Assessment Tool (http://geocat.kew.org/, accessed on 1 November 2022) was used to create the map (Figure 2) showing where H. laevigata has been observed (location descriptions: Appendices A and B).
Funding: This research was funded by the Andalusian Regional Government Research Group PLACCA (RNM116).

Data Availability Statement: Not applicable.
Acknowledgments: The author thanks Norbert Riezing from Hungary and Artur Pliszko from Poland for providing information about H. laevigata occurrence in those two countries. The author also expresses his appreciation to Artur Pliszko for furnishing photos of the Polish population.

Conflicts of Interest:
The author declares no conflict of interest.