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Article

Waterbodies in the Floodplain of the Drava River Host Species-Rich Macrophyte Communities despite Elodea Invasions

Department of Biology, Biotechnical Faculty, University of Ljubljana, Jamnikarjeva 101, 1000 Ljubljana, Slovenia
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(10), 870; https://doi.org/10.3390/d14100870
Submission received: 28 September 2022 / Revised: 10 October 2022 / Accepted: 11 October 2022 / Published: 14 October 2022

Abstract

:
The contribution discusses macrophyte communities in natural and man-made waterbodies located on the active floodplain along the Drava river (Slovenia). We presumed that these different types of wetlands host a great number of macrophyte species, but this diversity may be affected by the presence of alien invasive species Elodea canadensis and E. nuttallii. Presence, relative abundance, and growth forms of plant species along with selected environmental parameters were monitored. Correlation analyses and direct gradient analyses were performed to reveal the possible relations between the structure of macrophyte community and environmental parameters. Number of macrophytes in surveyed water bodies varied from 1 to 23. Besides numerous native species we also recorded Elodea canadensis and E. nuttallii, which were present in 19 out of 32 sample sites, with E. nuttallii prevailing. The less invasive E. canadensis was absent from ponds and oxbow lakes but relatively abundant in side-channels, while E. nuttallii was present in all types but dominant in ponds. The most abundant native species were Myriophyllum spicatum and M. verticillatum, Ceratophyllum demersum and Potamogeton natans. Correlation analyses showed no negative effect of the invasive alien Elodea species to the species richness and diversity of native flora. Positive correlation between the abundance of E. nuttallii and temperature of the water was obtained.

1. Introduction

Rivers are complex ecosystems that change in time and space due to ecological and hydro-morphological processes [1]. River flow determines processes that affect the shape and distribution of habitats, and thus associated biotic communities [2]. The diversity of river channel and floodplain wetlands support the diversity of biotic communities. These habitats enable the establishment and dispersal of organisms, which ultimately affects biodiversity patterns [3], especially in macrophytes that have relatively low dispersal ability [4].
The global increase in energy and water demand of the human population resulted in alterations of river channels that affected the function of rivers and adjacent floodplains, as well as wetlands along these rivers such as oxbow lakes, side channels, backwaters, ponds etc. [5]. Williams et al. [6] emphasized that such small waterbodies can contribute significantly to regional biodiversity, including macrophyte communities [7], and are important for the conservation and management of the local biodiversity [8,9,10]. Oxbow lakes may be especially rich since they represent a transition between lotic and lentic ecosystems [11]. Sustainable catchment management should be based on the knowledge of the biodiversity in different water bodies within these catchments [12] and its vulnerability. Such water bodies have a great potential for the conservation of biological diversity and are recognised for their importance for ecosystem services [13], even though they have received relatively little attention. This situation is different along the Danube river, where these water bodies were studied by many researchers (e.g., Otahelová et al. [14]; Schmidt-Mumm and Janauer [15]; Vukov et al. [16]; Gyosheva et al. [17]). The increase in the proportion of urban and agricultural land-use within the catchment areas of mentioned habitats results in a decrease in species richness, thus, for efficient conservation of their biodiversity, actions at a local and regional spatial scale are required [18].
Macrophytes are an important element of the aquatic ecosystem since they are the basis for energy flow and nutrient cycling, and they affect sedimentation processes [19,20]. Macrophyte stands are habitats, refugia and a source of organic material for a range of other organisms [21,22]. Brysiewicz et al. [23] also discovered that species occurrences and abundances of fish fauna in small waterbodies were associated with the amount of macrophytes growing in them. High macrophyte abundance may significantly alter the chemical and biological structure of the ecosystem [24], while degradation of macrophyte communities may cause a reduction in diversity of organisms dwelling in these macrophyte stands [25]. By nutrient uptake from water and sediment, macrophytes ameliorate water quality and affect the quality water and sediment [20,21]. The affinity for specific water and sediment properties in different species make them valuable indicators of water and sediment quality [26,27,28,29].
Small sized water bodies are often subjected to extreme water level fluctuations, which are more pronounced in hydrologically isolated systems, where accelerated succession often occurs [30]. These water level fluctuations may also cause the dieback of some plant species, and consequently a release of nutrients [31], and a decrease in biodiversity. They effect aquatic vegetation, the trophic state of the ecosystem, and consequently affect the diversity and abundance of macroinvertebrates within the macrophyte stands [32]. Another threat to local biodiversity, especially diversity of freshwater biota, is the spread of alien invasive species that is often reported as one of the major factors for its decline [33]. Vukov et al. [16] report that Elodea canadensis and E. nuttallii have been rapidly spreading along the whole Danube, which was documented in [34]. However, the negative influence of these species is not always significant and there may also be some positive effects on target ecosystems [35,36], like new habitat formation for aquatic fauna or cyanobacterial blooms prevention, especially in lentic waterbodies. The extent of the effect of a certain invasive species for the functioning of target ecosystems largely depends on its abundance [37].
In this paper, we studied macrophyte communities in natural and man-made shallow waterbodies located on the active floodplain along the Drava river in Slovenia, within the section with generally preserved morphological conditions but with modified hydrology, to estimate their potential for the conservation value for macrophyte biodiversity. Since these habitats represent different types of wetlands, we hypothesised that they harbour a great number of macrophyte species and so mitigate their loss in other sections of the river, which are affected by numerous hydropower-plants and their impoundments. We also hypothesised that species diversity may be affected by the presence of invasive alien species of the genus Elodea. Deeper understanding of such water bodies will facilitate effective conservation and management of floodplains and support their ecosystem services.

2. Materials and Methods

2.1. Study Area

Studied wetlands are found within the active floodplain of the Drava river in northeast Slovenia, between the town Maribor and the state border with Croatia (Figure 1). The river Drava is among the biggest tributaries of the Danube river and gathers water from Italy, Austria, Slovenia, Croatia and Hungary. The hydrological regime of the surveyed section of the river has been modified, since a great proportion of the water from the river Drava is diverted into artificial channels that supply the water for Hydropower-plants. The advantage of this fact is that there have been no major changes in the morphological conditions of the old river channel and adjacent floodplain, where the studied wetlands occur. As the reference habitats, four reaches in the main channel of the Drava river were also surveyed. Beyond the edges of the floodplain, the land use is characterized by intensive agriculture with cultivated and uncultivated land mosaic.

2.2. Macrophyte Data Set

Surveys were carried out in the years 2015–2016. Since we surveyed different types of the waterbodies the approaches were combined [22]—in ponds, the entire length (<100 m) was examined, whereas in oxbows, side-channels and the river we examined at least 100 m long sections. We recorded emergent, floating-leaved and submerged vascular plants, bryophytes and charophytes. The presence and abundance of macrophytes were evaluated from the boat or from the bank and collected with a stick with hooks. Macrophyte species abundance was estimated as a relative plant biomass using a five-degree scale, namely 1—very rare, 2—rare, 3—commonly present, 4—frequent, and 5—predominant, as proposed by Kohler and Janauer [38]. These values were transformed by the function x3, as suggested by Schneider and Melzer [27]. The plants that were sampled in the phenological phase, which prevented identification to the species level, were only recorded on the genus level (e.g., Carex, Callitriche). Species names followed the nomenclature of Euro+Med Plantbase [39].
We classified the macrophytes into the following growth forms: natant (leaves or whole plants floating at the water surface); submerged (assimilation areas submerged in water column); amphiphytes (having the ability to produce terrestrial and aquatic growth forms, or aquatic and aerial leaves); and helophytes (anchored in the water-saturated sediment, with plant assimilation areas permanently in the air). For the purpose of correlation analyses and comparisons of average abundances, the ordinal values of the Kohler-scale were transformed into quantitative values (“quantities”) [40]. We equalized the transformed values as percentage cover-abundance values according to [41].

2.3. Environmental Parameters

The assessment of environmental conditions was performed in the sites as the survey of macrophytes. We also assessed parameters like land-use type beyond the riparian zone, characteristics of the riparian zone (width, completeness, and vegetation type), and morphology (bank structure) [42]. Each parameter includes four categories comprising quality gradient, coded numerically from 1 to 4:1 presented good, close to natural condition, while quality gradient values from 2 to 4 indicate worsening of environmental conditions. Results of the assessment of the land-use and the width of riparian zone are presented in Table 1. Apart from the mentioned environmental parameters, we also recorded the basic physical and chemical parameters (temperature of the water, pH, conductivity, concentration of dissolved O2, saturation with O2) with the multimeter (Eutech PCD-650, Singapore).

2.4. Statistical Analyses

Correlation analyses between species and parameters was calculated with PAST, version 2.17c [43]. Kendall tau correlation coefficients were calculated.
Detrended correspondence analysis (DCA) was performed in the first step of gradient analyses. This analysis also informed us whether the gradients in the matrix of plant species are linear or unimodal, and which direct gradient analysis to use in further analyses. When we performed DCA with the matrix of functional types/growth forms, the eigenvalue for the first axis was lower than 0.4 (0.08) and we selected Redundancy analysis (RDA), as suggested by ter Braak and Verdonschot [44]. These results provided the information about the relationships between environmental factors and the structure of macrophyte community and their growth forms, respectively.
We used forward selection of the variables (499 permutations were performed) to rank the relative importance of explanatory variables. Only the variables with significance p < 0.05 were considered in further analyses. All analyses were performed with CANOCO for Windows 4.5 program package [45].

3. Results

The entire list of macrophytes comprised of 73 plant taxa, while the number of macrophytes in specific waterbodies varied from 1 to 23 (Figure 2). Beside numerous native species, waterbodies also host two invasive alien species of Elodea, namely Elodea canadensis and E. nuttallii, present in 19 out of 32 sample sites (Figure 3), with E. nuttallii prevailing. The most abundant native species were Myriophyllum spicatum and M. verticillatum, Ceratophyllum demersum and Potamogeton natans, which were also present in various locations (Figure 4). Natant species Nuphar luteum was present at one site only.
E. nuttallii was the most abundant among all hydrophyte species, with more than 25% of the total abundance, followed by M. verticillatum, C. demersum, E. canadensis and M. spicatum (Figure 5).
The DCA analysis shows the similarity of surveyed sites in terms of the structure of macrophyte communities in the peak vegetation period. The closer sites are on the ordination plot, the more similar are the macrophyte communities. It is evident that the type of aquatic ecosystem does not dictate the macrophyte community structure (Figure 6).
Redundancy analysis revealed that the presence and abundance of Elodea affected the presence of native groups of macrophytes (Figure 7). When testing both species of Elodea separately, E. nuttallii explained 9% and E. canadensis 3%. However, when we tested sum of abundances of both species, this parameter explained 14% of macrophytes species parameters variability. Vectors representing the number and abundance of plant groups are in the opposite direction to Elodea vector. The distribution of the locations along this vector shows that the locations 10 and 17 are the most abundant with Elodea, as is also evident from Figure 3.
Correlation analyses revealed no significant negative effect of the alien Elodea species to the native flora of the studied water bodies (Table 2). We calculated positive correlation between the abundance of E. nuttallii and temperature of the water, and the share of arable land in the catchment areas of the studied wetlands.
The abundance of E. nuttallii was negatively correlated with the sum of abundances of floating-leaved macrophytes (Nymphaea alba and Spirodela polyrhiza).
Average values for specific types of the studied waterbodies are listed in Table 3. E. canadensis was absent in lentic ecosystems but relatively abundant in side-channels, while E. nuttallii was present in all types but was dominant in ponds, where its average cover-abundance value was 48%. Despite this fact the species richness and diversity of native flora was not lower, but even higher in ponds than in larger oxbow lakes.

4. Discussion

Small waterbodies are often intact and unpolluted, and as such they present a refuge for species which have disappeared from larger, more disturbed, water bodies [13]. In the case of the Drava river, the sections upstream the studied area are degraded and converted into the chain of reservoirs for HPPs. The surveyed ecosystems occur within the active floodplain, which remained relatively intact in terms of morphological alterations. However, in different river-fed wetlands, the flood regimes affect macrophytes community traits and thus the structure and function of the wetlands [46]. The entire set of the studied waterbodies hosted 73 macrophyte species, which is a rather high number in comparison to river habitats, where in over 1000 reaches of 33 Slovenian rivers 87 species were recorded [47]. In similar studies within the Danube river corridor, Schmidt-Mumm and Janauer [15] recorded 78 species in 49 transects sampled in oxbows and side-channels in Austria, while Gyosheva et al. [17] recorded 112 species within a much larger set of 144 samples from Bulgaria.
The study of macrophytes in subtropical ponds revealed that pond size was positively related to richness of emergent and floating species, and the isolation of the pond negatively affected the richness of amphibious species, which was a consequence of their dispersal strategies [48], but our results do not confirm such relations. Emergent species in the studied waterbodies presented a great share of species, namely 43. This high helophyte diversity may be a consequence of relative naturalness of the adjacent parts of their catchment areas within the floodplain and supported by rich seed banks as shown in a case of small ponds [7].
Diverse and abundant stands of helophytes provide a protection for hydrophytes in the water since they act as their buffer zones. Despite this protection, native species could be endangered by alien Elodea, as both species of Elodea found in surveyed water bodies usually exhibit high growth rates with a high tolerance to a wide range of environmental conditions, low vulnerability to grazing and other stress factors, high distribution and reproduction potential [49]. Our results revealed no influence from both Elodea species on the floristic composition of aquatic vegetation (Figure 2), which is stronger in the case of E. nuttalli since its abundance is responsible for 9% of variability of macrophyte stands. Besides, E. nuttallii is also documented to replace E. canadensis from several waterbodies where it has established before the invasion of E. nuttallii [50,51]. The ecophysiological differences between both species explain the invasion success of E. nuttallii over E. canadensis [52]. Szabó et al. [53] found out that under more eutrophic conditions, E. nuttallii grows quicker and reaches the water surface sooner in comparison to E. canadensis. In addition, intensive branching outcompetes all other plants, including E. canadensis.
In our case, no evident impact on the native plant diversity was confirmed, neither in case of single Elodea species, nor when both species were present (Table 2). One of the reasons is that the hydromorphological characteristics of the majority of studied waterbodies has not been modified, except the ponds that are of anthropogene origin. This also explains the highest abundance of E. nuttallii in the ponds (Table 3). Otahelová et al. [14] report that new man-modified aquatic habitats have been successfully invaded by E. nuttallii. Mazej-Grudnik and Germ [54] report that E. nuttallii can cause severe problems in water bodies that are heavily modified due to human activity. The reason for lower competitive ability of E. nuttallii over E. canadensis, as well as other submerged species, is connectivity of these waterbodies with the main course of the Drava river [55] that floods the entire floodplain during the extreme events. Vukov et al. [16] report that both species are characteristic for aquatic habitats with lower levels of connectivity with main channels. There is also a difference between these two species in their preference to the reaction of the water, according to Ellenberg indicator values (EIV) for reaction [56]. E. canadensis has a relatively high EIV = 7 (out of 9) for water pH, while E. nuttallii is indifferent to pH (x). Since the catchment area above the studied section of the Drava river is mostly in the Central Alps and built mainly by non-carboniferous rocks, the sediments forming the floodplain of the Drava river and the river itself contain relatively low contents of basic cations and provide habitats with relatively low pH. This might explain lower abundance values of E. canadensis in comparison to E. nuttallii in these ecosystems and its absence from lentic habitats (Table 3).
We obtained positive correlation between the abundance of E. nuttallii and temperature of the water, thus further increasing in temperatures of these small waterbodies may favour the spread of E. nuttalli. Mazej Grudnik et al. [57] report that one can expect a more invasive character of E. nuttallii in the years with higher temperatures in January and March.
On the other hand, the abundance of E. nuttallii was negatively correlated with the sum of abundances of floating macrophytes (e.g., Nymphaea alba and Spirodela polyrhiza). However, it is not a case for all floating species, since a study with Lemna revealed the opposite result, especially under low nutrient concentrations [58]. Elodea is effective in using nutrients as phosphorus and nitrogen, which results in nutrient deficiency for other primary producers [59]. In our case it seems that nutrients were not a problem, since the conductivity was relatively high; therefore, better position regarding light conditions in floating-leaved macrophytes in comparison to submerged Elodea deprived this species. We presume that the spreading of floating species may help to suppress the spread of these two IAS in the waterbodies. Netten et al. [60] found out that the free-floating Salvinia natans in mesocosms benefited from increased temperature and increased nutrient concentrations and lowered the potential of submerged E. nuttallii to take advantage of such conditions. Their results also indicate that with global warming, invasive free-floating plants might become more successful and cause decline of submerged plants. The environment below floating plants is poorer with light [61]. Deliberate introduction of the pleustophyte Spirodela polyrhiza, which is a native species and distributed in waterbodies in the studied region, would be easy to imply, but it may also affect other submerged species so the use of such a measure for mitigation of the spread of these invasive species should be studied in advance. The study in Slovenian watercourses revealed that the abundance of E. canadensis is negatively related to abundance of M. spicatum [62], which is also highly invasive in USA [63]. This effect was only partly confirmed in the present study. According to this knowledge, we strongly discourage the removal of the stands of M. spicatum as well as any other native macrophyte.

5. Conclusions

Surveyed water bodies along the river Drava harboured a high number of species. Against expectations, the presence of alien E. nuttallii and E. canadensis exerted no effect on presence and abundance of hydrophytes, possibly due to water level fluctuations in these water bodies. E. nuttallii reached the highest abundance in ponds, which are the only group of anthropogenic ecosystems. We can conclude that maintenance of good ecological status of waterbodies, including their morphology, is among the most important measures to prevent the spreading of invasive species.
Different hydrological dynamics, as one of the consequences of the climate changes, has led to increased frequency of the floods as well as droughts. Small water bodies and wetlands, respectively, found within the floodplains can mitigate both types of events since they enable substantially longer water retention than do regulated rivers. The maintenance and hydrological connectivity of these waterbodies in sufficient extent could not only contribute to higher species diversity but could also reduce the flood-waves and supply the water for the baseflow at lower water levels due to their retention capacity.

Author Contributions

Conceptualization, A.G. and M.G.; methodology, A.G. and M.G.; validation, M.G., A.G. and U.K.; formal analysis, A.G. and I.Z.; investigation, M.G., A.G. and U.K.; data curation, A.G., M.G. and I.Z.; writing—original draft preparation, A.G. and I.Z.; writing—review and editing, M.G., A.G. and I.Z.; visualization, A.G. and I.Z.; supervision, A.G.; funding acquisition, A.G. and I.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Slovenian Research Agency, within the core research funding Nr. P1-0212, ‘Biology of Plants’.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data can be provided upon reasonable request.

Acknowledgments

Authors thank Matej Holcar for the creation of Figure 1.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Hynes, H.B.N. The Ecology of Running Waters; University of Toronto Press: Toronto, ON, Canada, 1970. [Google Scholar]
  2. Zeiringer, B.; Seliger, C.; Greimel, F.; Schmutz, S. River Hydrology, Flow Alteration, and Environmental Flow. In Riverine Ecosystem Management; Springer: Cham, Switzerland, 2018; pp. 67–89. [Google Scholar]
  3. Tonkin, J.D.; Altermatt, F.; Finn, D.S.; Heino, J.; Olden, J.D.; Pauls, S.U.; Lytle, D.A. The Role of Dispersal in River Network Metacommunities: Patterns, Processes, and Pathways. Freshw. Biol. 2018, 63, 141–163. [Google Scholar] [CrossRef] [Green Version]
  4. Padial, A.A.; Ceschin, F.; Declerck, S.A.J.; de Meester, L.; Bonecker, C.C.; Lansac-Tôha, F.A.; Rodrigues, L.; Rodrigues, L.C.; Train, S.; Velho, L.F.M.; et al. Dispersal Ability Determines the Role of Environmental, Spatial and Temporal Drivers of Metacommunity Structure. PLoS ONE 2014, 9, e111227. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Molnár, Z. Types and Characteristics of the Oxbow-Lakes in Lower-Tisza-Valley—Classification from Landscape Planning Perspective. Landscape Environ. 2013, 7, 19–25. [Google Scholar]
  6. Williams, P.; Whitfield, M.; Biggs, J.; Bray, S.; Fox, G.; Nicolet, P.; Sear, D. Comparative Biodiversity of Rivers, Streams, Ditches and Ponds in an Agricultural Landscape in Southern England. Biol. Conserv. 2004, 115, 329–341. [Google Scholar] [CrossRef]
  7. Shutoh, K.; Yamanouchi, T.; Kato, S.; Yamagishi, H.; Ueno, Y.; Hiramatsu, S.; Nishihiro, J.; Shiga, T. The Aquatic Macrophyte Flora of a Small Pond Revealing High Species Richness in the Aomori Prefecture, Japan. J. Asia Pac. Biodivers. 2019, 12, 448–458. [Google Scholar] [CrossRef]
  8. Kubiak, A.P.; Krawczyk, R. Diversity of Macrophytes in Riverine Aquatic Habitats: Comparing Active River Channel and Its Cut-Offs. Ann. UMCS Biol. 2014, 69, 49–57. [Google Scholar] [CrossRef] [Green Version]
  9. Waldon-Rudzionek, B. Is the Flora of Oxbow Lakes Different from That of Fishponds? A Comparison of Two Types of Water Reservoirs in the Noteć River Valley and Bydgoszcz Canal Valley (NW Poland). Ecol. Quest. 2017, 25, 27. [Google Scholar] [CrossRef] [Green Version]
  10. Panzeca, P.; Troia, A.; Madonia, P. Aquatic Macrophytes Occurrence in Mediterranean Farm Ponds: Preliminary Investigations in North-Western Sicily (Italy). Plants 2021, 10, 1292. [Google Scholar] [CrossRef] [PubMed]
  11. Obolewski, K. Biodiversity of Macroinvertebrates in Oxbow-Lakes of Early Glacial River Basins in Northern Poland. In Ecosystems Biodiversity; InTech: Rijeka, Croatia, 2011. [Google Scholar]
  12. Schneiders, A.; Verheyen, R. A Concept of Integrated Water Management Illustrated for Flanders (Belgium). Ecosyst. Health 1998, 4, 256–263. [Google Scholar] [CrossRef]
  13. Biggs, J.; von Fumetti, S.; Kelly-Quinn, M. The Importance of Small Waterbodies for Biodiversity and Ecosystem Services: Implications for Policy Makers. Hydrobiologia 2017, 793, 3–39. [Google Scholar] [CrossRef]
  14. Oťaheľová, H.; Valachovič, M.; Hrivnák, R. The Impact of Environmental Factors on the Distribution Pattern of Aquatic Plants along the Danube River Corridor (Slovakia). Limnologica 2007, 37, 290–302. [Google Scholar] [CrossRef]
  15. Schmidt-Mumm, U.; Janauer, G.A. Macrophyte Assemblages in the Aquatic-Terrestrial Transitional Zone of Oxbow Lakes in the Danube Floodplain (Austria). Folia Geobot. 2016, 51, 251–266. [Google Scholar] [CrossRef]
  16. Vukov, D.; Ilić, M.; Ćuk, M.; Igić, R.; Janauer, G. The Relationship between Habitat Factors and Aquatic Macrophyte Assemblages in the Danube River in Serbia. Arch. Biol. Sci. 2017, 69, 427–437. [Google Scholar] [CrossRef] [Green Version]
  17. Gyosheva, B.; Kalchev, R.; Beshkova, M.; Valchev, V. Relationships between Macrophyte Species, Their Life Forms and Environmental Factors in Floodplain Water Bodies from the Bulgarian Danube River Basin. Ecohydrol. Hydrobiol. 2020, 20, 123–133. [Google Scholar] [CrossRef]
  18. Akasaka, M.; Higuchi, S.; Takamura, N. Landscape- and Local-Scale Actions Are Essential to Conserve Regional Macrophyte Biodiversity. Front. Plant Sci. 2018, 9, 599. [Google Scholar] [CrossRef] [PubMed]
  19. Bornette, G.; Puijalon, S. Macrophytes: Ecology of Aquatic Plants. In Encyclopedia of Life Sciences (ELS); Wiley: Chichester, UK, 2009. [Google Scholar] [CrossRef]
  20. Preiner, S.; Dai, Y.; Pucher, M.; Reitsema, R.E.; Schoelynck, J.; Meire, P.; Hein, T. Effects of Macrophytes on Ecosystem Metabolism and Net Nutrient Uptake in a Groundwater Fed Lowland River. Sci. Total Environ. 2020, 721, 137620. [Google Scholar] [CrossRef] [PubMed]
  21. Glińska-Lewczuk, K.; Burandt, P. Effect of River Straightening on the Hydrochemical Properties of Floodplain Lakes: Observations from the Łyna and Drwęca Rivers, N Poland. Ecol. Eng. 2011, 37, 786–795. [Google Scholar] [CrossRef]
  22. Ambrožič, Š.; Gaberščik, A.; Vrezec, A.; Germ, M. Hydrophyte Community Structure Affects the Presence and Abundance of the Water Beetle Family Dytiscidae in Water Bodies along the Drava River. Ecol. Eng. 2018, 120, 397–404. [Google Scholar] [CrossRef]
  23. Brysiewicz, A.; Czerniejewski, P.; Bonisławska, M. Effect of Diverse Abiotic Conditions on the Structure and Biodiversity of Ichthyofauna in Small, Natural Water Bodies Located on Agricultural Lands. Water 2020, 12, 2674. [Google Scholar] [CrossRef]
  24. Baattrup-Pedersen, A.; Riis, T. Macrophyte Diversity and Composition in Relation to Substratum Characteristics in Regulated and Unregulated Danish Streams. Freshw. Biol. 1999, 42, 375–385. [Google Scholar] [CrossRef]
  25. Hansen, J.P.; Wikström, S.A.; Axemar, H.; Kautsky, L. Distribution Differences and Active Habitat Choices of Invertebrates between Macrophytes of Different Morphological Complexity. Aquat. Ecol. 2011, 45, 11–22. [Google Scholar] [CrossRef]
  26. Haslam, S.M. River Plants of Western Europe: The Macrophytic Vegetation of Watercourses of the European Economic Community; Cambridge University Press: Cambridge, UK, 1987; ISBN 0-521-26427-8. [Google Scholar]
  27. Schneider, S.; Melzer, A. The Trophic Index of Macrophytes (TIM)—A New Tool for Indicating the Trophic State of Running Waters. Int. Rev. Hydrobiol. 2003, 88, 49–67. [Google Scholar] [CrossRef]
  28. Szpakowska, B.; Świerk, D.; Pajchrowska, M.; Gołdyn, R. Verifying the Usefulness of Macrophytes as an Indicator of the Status of Small Waterbodies. Sci. Total Environ. 2021, 798, 149279. [Google Scholar] [CrossRef]
  29. Kuhar, U.; Germ, M.; Gaberščik, A.; Urbanič, G. Development of a River Macrophyte Index (RMI) for Assessing River Ecological Status. Limnologica 2011, 41, 235–243. [Google Scholar] [CrossRef]
  30. van Geest, G.J.; Coops, H.; Roijackers, R.M.M.; Buijse, A.D.; Scheffer, M. Succession of Aquatic Vegetation Driven by Reduced Water-Level Fluctuations in Floodplain Lakes. J. Appl. Ecol. 2005, 42, 251–260. [Google Scholar] [CrossRef]
  31. Lu, J.; Bunn, S.E.; Burford, M.A. Nutrient Release and Uptake by Littoral Macrophytes during Water Level Fluctuations. Sci. Total Environ. 2018, 622–623, 29–40. [Google Scholar] [CrossRef] [PubMed]
  32. Bogut, I.; Vidaković, J.; Palijan, G.; Čerba, D. Benthic Macroinvertebrates Associated with Four Species of Macrophytes. Biologia 2007, 62, 600–606. [Google Scholar] [CrossRef]
  33. Pyšek, P.; Richardson, D.M. Invasive Species, Environmental Change and Management, and Health. Annu. Rev. Environ. Resour. 2010, 35, 25–55. [Google Scholar] [CrossRef] [Green Version]
  34. Janauer, G.; Exler, N.; Anačkov, G.; Barta, V.; Berczik, Á.; Boža, P.; Dinka, M.; Georgiev, V.; Germ, M.; Holcar, M.; et al. Distribution of the Macrophyte Communities in the Danube Reflects River Serial Discontinuity. Water 2021, 13, 918. [Google Scholar] [CrossRef]
  35. Ricciardi, A.; Hoopes, M.F.; Marchetti, M.P.; Lockwood, J.L. Progress toward Understanding the Ecological Impacts of Nonnative Species. Ecol. Monogr. 2013, 83, 263–282. [Google Scholar] [CrossRef]
  36. Katsanevakis, S.; Wallentinus, I.; Zenetos, A.; Leppäkoski, E.; Çinar, M.E.; Oztürk, B.; Grabowski, M.; Golani, D.; Cardoso, A.C. Impacts of Invasive Alien Marine Species on Ecosystem Services and Biodiversity: A Pan-European Review. Aquat. Invasions 2014, 9, 391–423. [Google Scholar] [CrossRef]
  37. Vimercati, G.; Probert, A.F.; Volery, L.; Bernardo-Madrid, R.; Bertolino, S.; Céspedes, V.; Essl, F.; Evans, T.; Gallardo, B.; Gallien, L.; et al. The EICAT+ Framework Enables Classification of Positive Impacts of Alien Taxa on Native Biodiversity. PLoS Biol. 2022, 20, e3001729. [Google Scholar] [CrossRef] [PubMed]
  38. Kohler, A.; Janauer, G.A. Zur Methodik Der Untersuchung von Aquatischen Makrophyten in Flie_gewassern. In Handbuch Angewandte Limnologie; Steinberg, C.H., Bernhardt, H., Klapper, H., Eds.; Ecomed: Landsberg am Lech, Germany, 1995; pp. 3–22. [Google Scholar]
  39. Euro+Med PlantBase—The Information Resource for Euro-Mediterranean Plant Diversity. Available online: http://ww2.bgbm.org/EuroPlusMed/ (accessed on 1 September 2022).
  40. Schaumburg, J.; Schranz, C.; Foerster, J.; Gutowski, A.; Hofmann, G.; Meilinger, P.; Schneider, S.; Schmedtje, U. Ecological Classification of Macrophytes and Phytobenthos for Rivers in Germany According to the Water Framework Directive. Limnologica 2004, 34, 283–301. [Google Scholar] [CrossRef] [Green Version]
  41. Braun-Blanquet, J. Pflanzensoziologie, Grundzüge Der Vegetationskunde, 3rd ed.; Springer: Berlin, Germany, 1964. [Google Scholar]
  42. Germ, M.; Janež, V.; Gaberščik, A.; Zelnik, I. Diversity of Macrophytes and Environmental Assessment of the Ljubljanica River (Slovenia). Diversity 2021, 13, 278. [Google Scholar] [CrossRef]
  43. Hammer, Ø.; Harper, D.A.T.; Ryan, P.D. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol. Electron. 2001, 4, 1–9. [Google Scholar]
  44. ter Braak, C.J.F.; Verdonschot, P.F.M. Canonical Correspondence Analysis and Related Multivariate Methods in Aquatic Ecology. Aquat. Sci. 1995, 57, 255–289. [Google Scholar] [CrossRef]
  45. ter Braak, C.J.F.; Smilauer, P. CANOCO Reference Manual and CanoDraw for Windows User’s Guide: Software for Canonical Community Ordination (Version 4.5); Canoco: Ithaca, NY, USA, 2002. [Google Scholar]
  46. Huang, Y.; Chen, X.-S.; Li, F.; Hou, Z.-Y.; Li, X.; Zeng, J.; Deng, Z.-M.; Zou, Y.-A.; Xie, Y.-H. Community Trait Responses of Three Dominant Macrophytes to Variations in Flooding During 2011–2019 in a Yangtze River-Connected Floodplain Wetland (Dongting Lake, China). Front. Plant Sci. 2021, 12, 604677. [Google Scholar] [CrossRef] [PubMed]
  47. Zelnik, I.; Kuhar, U.; Holcar, M.; Germ, M.; Gaberščik, A. Distribution of Vascular Plant Communities in Slovenian Watercourses. Water 2021, 13, 1071. [Google Scholar] [CrossRef]
  48. Pereira, K.M.; Hefler, S.M.; Trentin, G.; Rolon, A.S. Influences of Landscape and Climatic Factors on Aquatic Macrophyte Richness and Composition in Ponds. Flora 2021, 279, 151811. [Google Scholar] [CrossRef]
  49. Zehnsdorf, A.; Hussner, A.; Eismann, F.; Rönicke, H.; Melzer, A. Management Options of Invasive Elodea Nuttallii and Elodea Canadensis. Limnologica 2015, 51, 110–117. [Google Scholar] [CrossRef]
  50. Barrat-Segretain, M.-H. Invasive Species in the Rhône River Floodplain (France): Replacement of Elodea Canadensis Michaux by E. Nuttallii St. John in Two Former River Channels. Arch. Hydrobiol. 2001, 152, 237–251. [Google Scholar] [CrossRef]
  51. Barrat-Segretain, M.; Elger, A. Experiments on Growth Interactions between Two Invasive Macrophyte Species. J. Veg. Sci. 2004, 15, 109–114. [Google Scholar] [CrossRef]
  52. Szabó, S.; Peeters, E.T.H.M.; Borics, G.; Veres, S.; Nagy, P.T.; Lukács, B.A. The Ecophysiological Response of Two Invasive Submerged Plants to Light and Nitrogen. Front. Plant Sci. 2020, 10, 01747. [Google Scholar] [CrossRef] [Green Version]
  53. Szabó, S.; Peeters, E.T.H.M.; Várbíró, G.; Borics, G.; Lukács, B.A. Phenotypic Plasticity as a Clue for Invasion Success of the Submerged Aquatic Plant Elodea Nuttallii. Plant Biol. 2019, 21, 54–63. [Google Scholar] [CrossRef] [Green Version]
  54. Mazej Grudnik, Z.; Germ, M. Spatial Pattern of Native Species Myriophyllum Spicatum and Invasive Alien Species Elodea Nuttallii after Introduction of the Latter One into the Drava River (Slovenia). Biologia 2013, 68, 202–209. [Google Scholar] [CrossRef] [Green Version]
  55. Barrat-Segretain, M.-H.; Elger, A.; Sagnes, P.; Puijalon, S. Comparison of Three Life-History Traits of Invasive Elodea Canadensis Michx. and Elodea Nuttallii (Planch.) H. St. John. Aquat. Bot. 2002, 74, 299–313. [Google Scholar] [CrossRef]
  56. Ellenberg, H.; Weber, H.; Düll, R.; Wirth, V.; Werner, W.; Pauliβen, D. Zeigerwertevon Pflanzen in Mitteleuropa; Verlag Erich Goltze: Göttingen, Germany, 1992. [Google Scholar]
  57. Grudnik, Z.M.; Jelenko, I.; Germ, M. Influence of Abiotic Factors on Invasive Behaviour of Alien Species Elodea Nuttallii in the Drava River (Slovenia). Ann. Limnol. Int. J. Limnol. 2014, 50, 1–8. [Google Scholar] [CrossRef] [Green Version]
  58. Szabo, S.; Scheffer, M.; Roijackers, R.; Waluto, B.; Braun, M.; Nagy, P.T.; Borics, G.; Zambrano, L. Strong Growth Limitation of a Floating Plant (Lemna Gibba) by the Submerged Macrophyte (Elodea Nuttallii) under Laboratory Conditions. Freshw. Biol. 2010, 55, 681–690. [Google Scholar] [CrossRef]
  59. van Donk, E.; Gulati, R.D.; Iedema, A.; Meulemans, J.T. Macrophyte-Related Shifts in the Nitrogen and Phosphorus Contents of the Different Trophic Levels in a Biomanipulated Shallow Lake. In Nutrient Dynamics and Retention in Land/Water Ecotones of Lowland, Temperate Lakes and Rivers; Springer: Dordrecht, The Netherland, 1993; pp. 19–26. [Google Scholar] [CrossRef] [Green Version]
  60. Netten, J.J.C.A.; Nes, E.H.; Scheffer, M.; Roijackers, R.M.M. Effect of Temperature and Nutrients on the Competition between Free-Floating Salvinia Natans and Submerged Elodea Nuttallii in Mesocosms. Fundament. Appl. Limnol. 2010, 177, 125–132. [Google Scholar] [CrossRef]
  61. Klančnik, K.; Iskra, I.; Gradinjan, D.; Gaberščik, A. The Quality and Quantity of Light in the Water Column Are Altered by the Optical Properties of Natant Plant Species. Hydrobiologia 2018, 812, 203–212. [Google Scholar] [CrossRef]
  62. Kuhar, U.; Germ, M.; Gaberščik, A. Habitat Characteristics of an Alien Species Elodea Canadensis in Slovenian Watercourses. Hydrobiologia 2010, 656, 205–212. [Google Scholar] [CrossRef]
  63. Hoff, H.K.; Thum, R.A. Hybridization and Invasiveness in Eurasian Watermilfoil (Myriophyllum Spicatum): Is Prioritizing Hybrids in Management Justified? Invasive Plant Sci. Manag. 2022, 15, 3–8. [Google Scholar] [CrossRef]
Figure 1. Distribution of the studied waterbodies in the floodplain of the Drava river (Base map source: Surveying and Mapping Authority of the republic of Slovenia (2016).
Figure 1. Distribution of the studied waterbodies in the floodplain of the Drava river (Base map source: Surveying and Mapping Authority of the republic of Slovenia (2016).
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Figure 2. Total species number (green bars) and Shannon–Wiener (S–W) diversity index (black lines) in surveyed waterbodies.
Figure 2. Total species number (green bars) and Shannon–Wiener (S–W) diversity index (black lines) in surveyed waterbodies.
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Figure 3. Relative abundance of invasive alien species Elodea canadensis and E. nuttallii in surveyed waterbodies.
Figure 3. Relative abundance of invasive alien species Elodea canadensis and E. nuttallii in surveyed waterbodies.
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Figure 4. Relative abundance of native hydrophyte species with total abundance more than 2% present in surveyed waterbodies: Myr verMyriophyllum verticillatum, Cer demCeratophyllum demersum, Myr spiMyriophyllum spicatum, Pot natPotamogeton natans, Cha sp—Chara species, Nup lutNuphar luteum.
Figure 4. Relative abundance of native hydrophyte species with total abundance more than 2% present in surveyed waterbodies: Myr verMyriophyllum verticillatum, Cer demCeratophyllum demersum, Myr spiMyriophyllum spicatum, Pot natPotamogeton natans, Cha sp—Chara species, Nup lutNuphar luteum.
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Figure 5. Ratio of total relative abundance of hydrophyte species that presented more than 1% in surveyed waterbodies: Elo nut—Elodea nuttallii, Myr verMyriophyllum verticillatum, Cer demCeratophyllum demersum, Elo canElodea canadensis, Myr spiMyriophyllum spicatum, Pot natPotamogeton natans, Cha sp—Chara species, Nup lutNuphar luteum, Hip vulHippuris vulgaris, Pot berPotamogeton bertholdii, Tra nat—Trapa natans, Pot pecPotamogeton pectinatus, Lem triLemna trisulca, Ran cirRanunculus circinatus, Bra rutBrachythecium rutabulum, Nym albNymphaea alba, Pot perPotamogeton perfoliatus, others—the sum of abundances of species with less than 1%.
Figure 5. Ratio of total relative abundance of hydrophyte species that presented more than 1% in surveyed waterbodies: Elo nut—Elodea nuttallii, Myr verMyriophyllum verticillatum, Cer demCeratophyllum demersum, Elo canElodea canadensis, Myr spiMyriophyllum spicatum, Pot natPotamogeton natans, Cha sp—Chara species, Nup lutNuphar luteum, Hip vulHippuris vulgaris, Pot berPotamogeton bertholdii, Tra nat—Trapa natans, Pot pecPotamogeton pectinatus, Lem triLemna trisulca, Ran cirRanunculus circinatus, Bra rutBrachythecium rutabulum, Nym albNymphaea alba, Pot perPotamogeton perfoliatus, others—the sum of abundances of species with less than 1%.
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Figure 6. Detrended correspondence analysis ordination diagram showing the similarity of the macrophyte stands in different sites. Numbers from 1 to 32 indicate the location of the site with respect to the river Drava flow direction. Different symbols indicate different water bodies (white circles—ponds, light grey squares—oxbows, small dark grey right triangles—side channels, black right triangle—sample sites in the main channel of the river Drava.
Figure 6. Detrended correspondence analysis ordination diagram showing the similarity of the macrophyte stands in different sites. Numbers from 1 to 32 indicate the location of the site with respect to the river Drava flow direction. Different symbols indicate different water bodies (white circles—ponds, light grey squares—oxbows, small dark grey right triangles—side channels, black right triangle—sample sites in the main channel of the river Drava.
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Figure 7. Redundancy analysis plot showing the relationship between the number of different ecological groups of macrophytes and relative abundance of their growth forms and Elodea species abundance. Abundance of submerged plants is represented by two parameters, including and excluding Elodea (-Elodea). Different symbols indicate different water bodies (white circles—ponds, light grey squares—oxbows, small dark grey right triangles—side channels, black right triangle—sites in the main channel of the river Drava.
Figure 7. Redundancy analysis plot showing the relationship between the number of different ecological groups of macrophytes and relative abundance of their growth forms and Elodea species abundance. Abundance of submerged plants is represented by two parameters, including and excluding Elodea (-Elodea). Different symbols indicate different water bodies (white circles—ponds, light grey squares—oxbows, small dark grey right triangles—side channels, black right triangle—sites in the main channel of the river Drava.
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Table 1. Characteristics of the catchment area of specific waterbodies. Width of the riparian zone, where woody or herbaceous wetland vegetation is thriving and prevailing land-use behind the riparian zone is presented.
Table 1. Characteristics of the catchment area of specific waterbodies. Width of the riparian zone, where woody or herbaceous wetland vegetation is thriving and prevailing land-use behind the riparian zone is presented.
LocationWidth of Riparian ZoneLand-Use behind the Riparian ZoneType
11–5 marable land, grassland, housesriver
21–5 marable land, grassland, housespond
31–5 marable land, grassland, houseschannel
41–5 marable land, grassland, houseschannel
51–5 marable land, grassland, housesoxbow
6<1 mmainly arable land or urban areapond
71–5 mmainly arable land or urban areachannel
8<1 marable land, grassland, housesriver
9<1 mmainly arable land or urban areapond
101–5 mmainly arable land or urban areaoxbow
11<1 mmainly arable land or urban areapond
125–30 mgrassland, forest and/or wetland, some arable landpond
135–30 mgrassland, forest and/or wetland, some arable landchannel
141–5 mmainly arable land or urban areachannel
15<1 marable land, grassland, houseschannel
161–5 marable land, grassland, houseschannel
17<1 marable land, grassland, housesoxbow
18<1 mmainly arable land or urban areachannel
195–30 marable land, grassland, housespond
20<1 mmainly arable land or urban areaoxbow
211–5 marable land, grassland, houseschannel
221–5 marable land, grassland, houseschannel
23<1 marable land, grassland, housesoxbow
241–5 marable land, grassland, housesriver
25<1 marable land, grassland, houseschannel
26<1 mmainly arable land or urban areachannel
27<1 mmainly arable land or urban areachannel
285–30 marable land, grassland, housesriver
291–5 marable land, grassland, housespond
301–5 marable land, grassland, housespond
311–5 mgrassland, forest and/or wetland, some arable landchannel
321–5 mmainly arable land or urban areaoxbow
Table 2. Correlation coefficients (Kendall tau) between the abundance of Elodea canadensis, E. nuttallii and the sum of both species with diversity indices of native flora as well as with selected environmental parameters. Only significant (p < 0.05) correlations are shown. (* p = 0.05).
Table 2. Correlation coefficients (Kendall tau) between the abundance of Elodea canadensis, E. nuttallii and the sum of both species with diversity indices of native flora as well as with selected environmental parameters. Only significant (p < 0.05) correlations are shown. (* p = 0.05).
VariableE. canadensisE. nuttalliiE. canadensis and nuttallii
Number of native taxan.s.n.s.n.s.
Total abundance of plantsn.s.0.26790.2669
Shannon–Wiener diversity indexn.s.n.s.n.s.
Concentration of O2 [mg/L]n.s.0.2679n.s.
Temperature of the water [°C]n.s.0.2614 *n.s.
Cover of floating-leaved macrophytesn.s.−0.2782n.s.
Land-use in the catchmentn.s.0.29880.2805
Abundance of Nymphaea alban.s.−0.2617−0.3079
Abundance of Spirodela polyrhizan.s.−0.2886n.s.
Table 3. Average abundances (in %) of IAS Elodea canadensis and E. nuttallii in four types of waterbodies and average values of species-richness and diversity of native flora.
Table 3. Average abundances (in %) of IAS Elodea canadensis and E. nuttallii in four types of waterbodies and average values of species-richness and diversity of native flora.
OxbowsPondsSide-ChannelsRiver
E. canadensis0015.70.75
E. nuttallii14.54812.24.5
Nr. of native taxa810,511.49.5
S–W diversity index1.71.921.9
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Zelnik, I.; Germ, M.; Kuhar, U.; Gaberščik, A. Waterbodies in the Floodplain of the Drava River Host Species-Rich Macrophyte Communities despite Elodea Invasions. Diversity 2022, 14, 870. https://doi.org/10.3390/d14100870

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Zelnik I, Germ M, Kuhar U, Gaberščik A. Waterbodies in the Floodplain of the Drava River Host Species-Rich Macrophyte Communities despite Elodea Invasions. Diversity. 2022; 14(10):870. https://doi.org/10.3390/d14100870

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Zelnik, Igor, Mateja Germ, Urška Kuhar, and Alenka Gaberščik. 2022. "Waterbodies in the Floodplain of the Drava River Host Species-Rich Macrophyte Communities despite Elodea Invasions" Diversity 14, no. 10: 870. https://doi.org/10.3390/d14100870

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