Water Level Fluctuations and Air Temperatures Affect Common Reed Habitus and Productivity in an Intermittent Wetland Ecosystem

Lake Cerknica is an intermittent wetland ecosystem with extreme water level fluctuations. It hosts extensive reed stands that have colonized different habitat types. Two different stands were compared: a lake stand not directly influenced by the intermittent River Stržen and a riparian stand near River Stržen. Reed productivity (growth and assimilate allocation) was monitored for these reed stand types over 13 years (2007–2019), and this measurement was compared to monthly water levels and air temperatures. Reeds from the lake reed stand were significantly shorter with a lower shoot density, overall biomass production, and ratio of flowering plants. A correlation analysis revealed stronger and more numerous significant correlations between environmental and reed productivity parameters for the lake reed stand compared to the riparian reed stand. The variabilities of the growth and assimilate allocation parameters in the lake reed stand were both mostly explained by the combined water levels for June and July, which explained 47% and 52% of the variability, respectively. The most influential temperatures were in May, which explained 29% and 19% of the variability of growth and assimilate allocation parameters, respectively. For the riparian reed stand, water levels and temperatures out of the vegetation season appeared more important. Therefore, habitats with permanent water are more suitable for reeds than those with fluctuating water. However, fluctuating water conditions are expected to become more common due to climate change.


Introduction
Water level fluctuations directly affect ecosystems through their effects on the aquatic organisms, and they indirectly affect them by changing the physical and chemical conditions [1] that control different levels of the community structure [2]. The common reed (Phragmites australis (Cav.) Trin. and Steud) is a highly productive and cosmopolitan perennial helophyte that colonizes different wetland habitats [3]. It forms dense monospecific stands and is the dominant plant species in many ecosystems [4,5]. It shows high intraspecific diversity and phenotypic plasticity that enable its acclimation to adverse environmental conditions [6]. This is why the common reed is widely distributed across a variety of habitats [7].
One of the most important factors that significantly alters the habitat conditions of the common reed is the water level [1,5,8,9]. This defines the availability of water and nutrients [10], as well as the presence of oxygen in the root zone [11], and thus influences the structure of the reed stands. This is a collective result of different processes that include photosynthesis, respiration, mortality, and assimilate translocation between shoots and below-ground plant organs [12]. Li et al. [13] showed that water

Productivity Parameters.
The harvesting of the above-ground parts of the reed plants from 2007 to 2019 was performed during the fruiting phase at the end of the growing season, in September, following the work of Květ et al. [26] and Cronk and Fennessy [27]. Five 0.5 × 0.5 m plots were harvested from each location at

Productivity Parameters
The harvesting of the above-ground parts of the reed plants from 2007 to 2019 was performed during the fruiting phase at the end of the growing season, in September, following the work of Květ et al. [26] and Cronk and Fennessy [27]. Five 0.5 × 0.5 m plots were harvested from each location at each sampling. In addition to the plant above-ground biomass, the following parameters were determined: shoot density, flowering shoots, internodes and leaves per plant, shoot height, and shoot basal diameter.

Environmental Parameters
The water level data were obtained from the Stržen-Gorenje Jezero monitoring station of the Slovenian Environment Agency ( Figure 2) and the air temperatures from the nearest weather station (Postojna), as available from http://www.meteo.si/ (Figure 3).
Water 2020, 12, 2806 4 of 15 each sampling. In addition to the plant above-ground biomass, the following parameters were determined: shoot density, flowering shoots, internodes and leaves per plant, shoot height, and shoot basal diameter.

Environmental Parameters
The water level data were obtained from the Stržen-Gorenje Jezero monitoring station of the Slovenian Environment Agency ( Figure 2) and the air temperatures from the nearest weather station (Postojna), as available from http://www.meteo.si/ (Figure 3).

Statistical Analysis
Using the SPSS statistic software, version 22.0 (IBM Corp., Armonk, NY, USA), statistically significant differences between the lake and riparian reed stand productivities were evaluated using  each sampling. In addition to the plant above-ground biomass, the following parameters were determined: shoot density, flowering shoots, internodes and leaves per plant, shoot height, and shoot basal diameter.

Environmental Parameters
The water level data were obtained from the Stržen-Gorenje Jezero monitoring station of the Slovenian Environment Agency ( Figure 2) and the air temperatures from the nearest weather station (Postojna), as available from http://www.meteo.si/ (Figure 3).

Statistical Analysis
Using the SPSS statistic software, version 22.0 (IBM Corp., Armonk, NY, USA), statistically significant differences between the lake and riparian reed stand productivities were evaluated using Mann-Whitney non-parametric tests, and the relationships between different productivity and

Statistical Analysis
Using the SPSS statistic software, version 22.0 (IBM Corp., Armonk, NY, USA), statistically significant differences between the lake and riparian reed stand productivities were evaluated using Mann-Whitney non-parametric tests, and the relationships between different productivity and environmental parameters were calculated using Spearman's correlation analysis.
To examine the impact of water level and air temperature on reed plant productivity, we considered the data from the corresponding year (January to August) and from the end of the growing season from the year before (September to December), which might have affected the accumulation of reserves in the reed rhizomes.
A detrended correspondence analysis was used for the exploratory data analysis using the Canoco for Windows 4.5 program package (Microcomputer Power: Ithaca, NY, USA). Due to the obtained gradient lengths (<3 standard deviations) [28], a redundancy analysis (RDA) was used to determine whether the variations in the productivity parameters were related to monthly water levels and/or air temperatures. Productivity was determined as two groups: the growth parameters (i.e., shoot density, internodes, leaves per plant, shoot height, and stem basal diameter) and the assimilate allocation parameters (i.e., flowering shoots, biomass of leaves, stems, and flowers). The significance of the effects of the variables was determined using Monte Carlo tests with 999 permutations. The forward selection of the explanatory variables was used to avoid collinearity. All of the variables used in the analysis were standardized.

Results
Common reeds from the lake and riparian reed stands significantly differed for the productivity parameters (Table 1). Reeds from the lake reed stand were significantly shorter, with significantly lower shoot density, overall biomass production, and ratio of flowering plants. The habitus of single plants was similar regarding stem basal diameter and the number of internodes and leaves but not regarding height and biomass per plant (lake reed stand: 8.8 g per plant; riparian reed stand: 12.0 g per plant). The samples from the lake reed stand generally showed a higher variability in the measured parameters in comparison to the riparian reed stand samples. A correlation analysis revealed much stronger and more numerous significant correlations between the environmental and reed productivity parameters for the lake reed stand than for the riparian reed stand. For the lake stand, the reed productivity was mostly affected by the water levels at the end of the previous growing season, in October and November of the previous year, and the water levels at the beginning of the current season, in May and June. Almost all of these relations were negative (Table 2).
May and June were also the most important months regarding the air temperatures. However, the effects here were generally positive. In the riparian reed stand, the parameters most positively correlated to the water level were plant basal diameter and the height of the plants, while basal diameter was negatively correlated to air temperatures ( Table 3). The correlation analysis showed the importance of the winter months, especially December and January, when water level negatively correlated with the number of internodes. Table 3. Spearman's correlations between growth and biomass allocation parameters, as well as water levels and air temperatures, for the common reed plants from the riparian reed stand (Gorenje Jezero). A redundancy analysis was performed separately for the growth and assimilate allocation parameters, with different results shown. For the lake reed stand, the water levels in spring and summer appeared to be the most important parameter (Table 4 and Figures 4 and 5). The variability of the growth and assimilate allocation parameters was mostly explained by the combined water levels for June and July, which explained 47% of the variability for growth and 52% of the variability for assimilate allocation. The water levels in the other months were less important for the lake reed stand, although when combined, they explained an additional 18% and 24% of the variability of the growth and assimilate allocation parameters, respectively. High water levels in July and August negatively affected the number of leaves and internodes for the lake reed stand. The RDA plots revealed large differences across the study years (Figures 4 and 5).
For the air temperatures for the lake reed stand, the most influential month was May, which explained 29% of the variability of the growth parameters and 19% of the variability of the assimilate allocation parameters (Table 4). Air temperatures explained a total of 86% of the variability of the growth and a total of 76% of the variability of the assimilate allocation.    For the riparian reed stand, the water levels out of the vegetation season appeared to be the most important (Table 5 and Figures 6 and 7). The variability of the growth parameters was mostly explained by the combined water levels in February and December, which explained 34% of the variability. Meanwhile, the importance of the water levels in the other months was much lower, as only an additional 21% of sample variability was explained. The variability of the assimilate allocation parameters was mostly explained by the combined water levels in January and November, which explained 41% of the variability. Again, the importance of water levels in the other months was lower, with an additional 24% of the sample variability explained. The RDA plot again revealed large differences here across the study years.
For the air temperatures for the riparian reed stand, the most influential months were October and June, which explained 26% of the variability of the growth parameters, and July and February, which explained 28% of the variability of the assimilate allocation parameters (Table 5). Altogether, For the riparian reed stand, the water levels out of the vegetation season appeared to be the most important (Table 5 and Figures 6 and 7). The variability of the growth parameters was mostly explained by the combined water levels in February and December, which explained 34% of the variability. Meanwhile, the importance of the water levels in the other months was much lower, as only an additional 21% of sample variability was explained. The variability of the assimilate allocation parameters was mostly explained by the combined water levels in January and November, which explained 41% of the variability. Again, the importance of water levels in the other months was Water 2020, 12, 2806 9 of 15 lower, with an additional 24% of the sample variability explained. The RDA plot again revealed large differences here across the study years.     We also examined whether the reed productivity in the previous year affected the productivity parameters in the following (current) year. Here, the RDA revealed that the numbers of leaves, the number of internodes, the biomass of the leaves, and the biomass of the other parts in the previous year explained 8%, 4%, 4%, and 4%, respectively, of the productivity parameters in the following year. Therefore, these parameters combined explained 20% of the variability of the productivity parameters in the following year.

Discussion
The common reed is successful in habitats with stable or regular hydrology [29]. The higher variability in the measured parameters for samples from the lake reed stand in comparison to those from the riparian reed stand was a consequence of extreme water level fluctuations. For the lake location here, this could range from completely dry soil to 2 m depth of water, while the nearby River Stržen in the riparian reed stand maintains permanent high soil water table and floods up to 0.5 m. Hayball and Pearce [30] reported that in deep water, the common reed developed lower numbers of shoots, while a decrease in the water level increased the plant density and leaf numbers, which positively affected the leaf area index and consequently affected the productivity [15]. A high density of reed culms causes self-shading, which decreases the flowering rate and increases the leaf to stem mass ratio [29]. On the other hand, culm height and density significantly contribute to the competitive success of the common reed in terms of the shading out of other plant competitors in the habitat [31].
Plants that develop during moderate constant water levels grow faster than plants growing under fluctuating water levels [32,33]. This is also supported by the above-ground biomass measurements in the present study. The common reed is especially sensitive to rapid and extreme water level changes [34]. Extreme fluctuations affect reed fitness, partly due to the disturbed oxygenation of the rhizosphere [35] and possibly also due to negative effects on active mycorrhiza [36,37]. Such extreme changes are characteristic of the lake reed stand at Zadnji Kraj. In contrast, the For the air temperatures for the riparian reed stand, the most influential months were October and June, which explained 26% of the variability of the growth parameters, and July and February, which explained 28% of the variability of the assimilate allocation parameters (Table 5). Altogether, the air temperatures explained a total of 42% of the variability of the growth parameters and a total of 43% of the variability of the assimilate allocation parameters.
We also examined whether the reed productivity in the previous year affected the productivity parameters in the following (current) year. Here, the RDA revealed that the numbers of leaves, the number of internodes, the biomass of the leaves, and the biomass of the other parts in the previous year explained 8%, 4%, 4%, and 4%, respectively, of the productivity parameters in the following year. Therefore, these parameters combined explained 20% of the variability of the productivity parameters in the following year.

Discussion
The common reed is successful in habitats with stable or regular hydrology [29]. The higher variability in the measured parameters for samples from the lake reed stand in comparison to those from the riparian reed stand was a consequence of extreme water level fluctuations. For the lake location here, this could range from completely dry soil to 2 m depth of water, while the nearby River Stržen in the riparian reed stand maintains permanent high soil water table and floods up to 0.5 m. Hayball and Pearce [30] reported that in deep water, the common reed developed lower numbers of shoots, while a decrease in the water level increased the plant density and leaf numbers, which positively affected the leaf area index and consequently affected the productivity [15]. A high density of reed culms causes self-shading, which decreases the flowering rate and increases the leaf to stem mass ratio [29]. On the other hand, culm height and density significantly contribute to the competitive success of the common reed in terms of the shading out of other plant competitors in the habitat [31].
Plants that develop during moderate constant water levels grow faster than plants growing under fluctuating water levels [32,33]. This is also supported by the above-ground biomass measurements in the present study. The common reed is especially sensitive to rapid and extreme water level changes [34]. Extreme fluctuations affect reed fitness, partly due to the disturbed oxygenation of the rhizosphere [35] and possibly also due to negative effects on active mycorrhiza [36,37]. Such extreme changes are characteristic of the lake reed stand at Zadnji Kraj. In contrast, the more gradual changes that occur in the riparian reed stand at Gorenje Jezero appear to be less detrimental. In water fluctuation systems, the timing of the changes in water levels is also very important. For the lake reed stand at Zadnji Kraj, the variability of the growth and assimilate allocation parameters was explained by water levels in June and July (p < 0.001), which was the time of the vegetative development of plants, whereas temperatures seemed to be most important in May (p < 0.001). For the riparian reed stand at Gorenje Jezero, most of the variability of the growth and assimilate allocation parameters was explained by water levels out of the vegetation season and by temperatures at the end of the vegetation season, which may be related to the filling of reserves [5]. For the lake reed stand, there was positive correlation between leaf numbers and water levels in June (0.58; p < 0.01), and there were negative correlations with water levels in July (−0.31; p < 0.01) and from December to March (p < 0.05). On the other hand, no such significant correlations were found for the riparian reed stand, except for the negative correlation seen for December (−0.30; p < 0.05). Plant growth depends on the levels of available carbohydrates, which are strongly affected by environmental conditions [3]. A correlation analysis showed that in the lake reed stand, the plant height was negatively affected by the water levels in October of the previous year and in May and June of the current year, but it was positively related with air temperatures in May. In the riparian reed stand, the plant height was related to the water levels in December (−0.30; p < 0.05), July (0.36; p < 0.01), and August (0.46; p < 0.01). Autumnal rainfall can shorten the vegetation period and thus interrupt the filling of the reserves in the rhizomes, while high waters in late spring can prevent the development of reeds [5,32,38]. Previous studies have shown positive relationships between stem height and shoot density, which reflect productivity during the vegetation season [39]. However, no such correlation was obtained in the present study. The growth parameter that was most strongly correlated to the water level was basal diameter. For the lake reed stand, a strong negative correlation was obtained throughout the whole period of the vegetative development of reed, while for the riparian stand, this relation was strongly positive in April and June. This was possibly the consequence of the differences in maximal water levels between the two locations that might be unfavorable for lake but not for riparian stands. Thinner culms, which occurred in the years with deeper water, are more vulnerable to physical disturbances such as strong water movements and winds [40,41].
Irregular and strong water movements are usually the consequence of extreme water level fluctuations, like waves or currents, and may negatively affect the competitiveness of the common reed [29]. Water movement represents a physical force that can break reed culms and prevents the passive and humidity-induced aeration of the rhizome system at higher water levels, which also occurs via dead stems [16,42]. In water fluctuating systems, reed stands are frequently subjected to prolonged dry periods [21]. The common reed can withstand longer periods of water shortage through a reduction in leaf area and by an increased water-use efficiency [43]. Drought events are very common for the lake reed stand at Zadnji Kraj during the summer periods, with a positive correlation seen here between water levels and the numbers of leaves in June and July.
The negative effect on reed productivity may also be due to extreme temperatures, which may significantly increase the evapotranspiration rate in summer and may negatively affect reed rhizomes in winter. For example, Bodensteiner and Gabriel [44] attributed the reduction in reed stand area in the Upper Winnebago Pool Lakes in Wisconsin (USA) to the combined effects of extreme water levels and low temperatures in winter. We also obtained positive correlations with temperatures and some of the measured productivity parameters in the winter months at both locations.
In addition to differences in environmental factors like water levels, total radiation, and temperature, the fitness of plants during the previous season might also have a strong impact on plant height [3]. The present study showed little effect of the reed productivity parameters in the previous season, as these parameters explained only 20% of the variability of the productivity parameters in the current year.
This study showed that water depth represents the most important factor in common reed life. However, water depth is also an important predictor for the spread of common reed, which expands where the water levels are decreasing [45]. Water levels at the two locations affected different common reed parameters in different ways. In spite of that, water depth regulation may present a strong management tool [46], especially in human-made and human-managed aquatic systems. The increased extent of water level fluctuation in many aquatic systems may also be the consequence of different hydro-melioration measures in the landscape and thus the reduced capacity of the landscape to store water [47], as well as due to altered precipitation regimes due to global climate change. Renaturation measures to increase landscape water capacity may benefit every reed stand. Vital reed stands may increase the resilience of the landscape because by producing high biomass quantities, they provide various ecosystem services. They positively affect the local climate, purify water, present a source of biomass and a reservoir for water, and serve as a habitat and refuge for a variety of species [25,33,[48][49][50][51].

Conclusions
This study has shown that habitats with the permanent presence of water are more suitable habitats for the common reed in comparison to those with fluctuating water levels. This presents a problem in the light of global climate change, since water level fluctuations in different water bodies are expected to become more frequent. A favorable water regime in a landscape positively affects common reed production and its ecosystems services. Thus, measures to increase landscape water capacity, including assuring favorable conditions for reed stands, are needed to mitigate future extremes.