Outline
Comptes Rendus

Biodiversity/Biodiversité
Reed die-back in southern Europe? A case study from Central Italy
Comptes Rendus. Biologies, Volume 334 (2011) no. 4, pp. 327-336.

Abstract

Common reed die-back is a widely investigated phenomenon in Central Europe, not frequently recorded in S-European areas and almost unknown in the Mediterranean Basin. Symptoms of reed decline recently observed in the Italian Peninsula provided the starting point for a detailed investigation on a reed population in one of the largest freshwater ecosystems in Central Italy. The analyses were conducted over two vegetative seasons in 19 plots at seven locations. A set of 13 morphologic and phenologic reed traits were screened, monitored and statistically analysed. The data indicated the presence of the reed die-back syndrome in a wet Mediterranean ecosystem and enabled us to highlight a set of usable traits to detect the condition of decline. Among them, the stem height and diameter, the number of nodes, the relative growth rate and the lateral root diameter resulted the most significant factors highlighting the declining condition. Some environmental characteristics of the reed stands were also taken into account. The period of submersion and the presence of standing litter emerged as important features of the stands, strictly related to the degree of decline in the population. The results draw attention to the risk, in southern Europe too, of the loss of an ecosystem which plays an important role in biodiversity conservation.

Metadata
Received:
Accepted:
Published online:
DOI: 10.1016/j.crvi.2011.02.004
Keywords: Freshwater ecosystems, Lake Trasimeno, Phragmites australis, Plant traits, Decline, Shallow lakes

Daniela Gigante 1; Roberto Venanzoni 1; Vincenzo Zuccarello 2

1 Department of Applied Biology, University of Perugia, Borgo XX giugno, 74, 06121 Perugia, Italy
2 DiSTeBA, Ecotekne, University of Lecce, Via per Monteroni, 73100 Lecce, Italy
@article{CRBIOL_2011__334_4_327_0,
     author = {Daniela Gigante and Roberto Venanzoni and Vincenzo Zuccarello},
     title = {Reed die-back in southern {Europe?} {A} case study from {Central} {Italy}},
     journal = {Comptes Rendus. Biologies},
     pages = {327--336},
     publisher = {Elsevier},
     volume = {334},
     number = {4},
     year = {2011},
     doi = {10.1016/j.crvi.2011.02.004},
     language = {en},
}
TY  - JOUR
AU  - Daniela Gigante
AU  - Roberto Venanzoni
AU  - Vincenzo Zuccarello
TI  - Reed die-back in southern Europe? A case study from Central Italy
JO  - Comptes Rendus. Biologies
PY  - 2011
SP  - 327
EP  - 336
VL  - 334
IS  - 4
PB  - Elsevier
DO  - 10.1016/j.crvi.2011.02.004
LA  - en
ID  - CRBIOL_2011__334_4_327_0
ER  - 
%0 Journal Article
%A Daniela Gigante
%A Roberto Venanzoni
%A Vincenzo Zuccarello
%T Reed die-back in southern Europe? A case study from Central Italy
%J Comptes Rendus. Biologies
%D 2011
%P 327-336
%V 334
%N 4
%I Elsevier
%R 10.1016/j.crvi.2011.02.004
%G en
%F CRBIOL_2011__334_4_327_0
Daniela Gigante; Roberto Venanzoni; Vincenzo Zuccarello. Reed die-back in southern Europe? A case study from Central Italy. Comptes Rendus. Biologies, Volume 334 (2011) no. 4, pp. 327-336. doi : 10.1016/j.crvi.2011.02.004. https://comptes-rendus.academie-sciences.fr/biologies/articles/10.1016/j.crvi.2011.02.004/

Original version of the full text

1 Introduction

Phragmites australis [Cav.] Trin. ex Steud. is a Subcosmopolite clonal grass species, rather common all over the world; it is abundant in North America and Eurasia and widespread in Africa, Australia and South America [1]. Since the 1950s [2], a decline of reed beds has been detected in Central Europe (for a general overview: [3–6]). This phenomenon was defined as “a visible abnormal and non-reversible spontaneous retreat, disintegration or disappearance of a mature stand of common reed (Phragmites australis) within a period not longer than a decade” [5].

The proposed parameters to diagnose the reed die-back syndrome (RDBS hereafter) are manifold and refer to different plant traits. Some symptoms related with the reed decline are, for example, smaller than normal, weaker culms, high incidence of dead or decaying rhizomes, roots and buds, prematurely senesced culms, abnormal lignification and suberization within the adventitious root apices, presence of callus blocking the internal aeration of aerenchyma, clumping habit [4,7–11]. The clumped growth is a peculiar trait and seems to be a consequence of a blockage in the vascular tissue, resulting in the apical dominance breaking down [9,12]. The shoot density, shoot dry mass, leaf area index, time of flowering, number of flowering heads, structure of the root-system are further examples of biometric data indicating die-back conditions for P. australis from different sampling sites in northern Europe; the reed retreat from deep waters is also considered an indication of die-back [5].

Although reed is both directly and indirectly influenced by eutrophication [13], it has been noticed that the reed decline is not restricted to polluted lakes [4]. It is well known that P. australis can thrive without showing obvious signs of decline or damage in hypertrophic lakes [14–18] and can play a role in heavy metal accumulation [19]. The common reed behaves as a highly invasive species in some regions of the world, such as North America [20–28] and even parts of Europe [29]. Nevertheless, P. australis decline is a well-known phenomenon in Europe and it seems to affect the reed-beds regardless of their water quality.

So far, it has generally been suggested that the cause of the decline is due to a combination of factors. The situation is highly complicated since the same factors can be implicated in either decline or increase of reed populations. For most, the RDBS has been attributed to a combination of unnatural conditions, primarily including artificially stabilised water tables and increased eutrophication, but also exacerbated by sediment type, wave action, insect attack, low genetic diversity, grazing, algal mats and algal wash, and by introduction of alien grazers such as muskrat (Ondatra zibethicus L.) and coypus (Myocastor coypus Molina). There are large amounts of specialized literature available describing the patterns and tackling the causes of reed decline in most regions of Europe, but the (sub-)Mediterranean areas are a notable exception. Van Der Putten [5] reported that in the Mediterranean, characterized by hot and dry summers, P. australis shows a vigorous growth even in eutrophicated areas, with a tendency to expansion rather than retreat. Reed die-back in the Mediterranean has not actually been fully investigated yet. Lack of data is perhaps the main reason why the reed die-back is not believed to be an important issue in the Mediterranean and sub-Mediterranean regions of Europe. In the brackish waters of the Po Delta (NE Italy) Fogli et al. [30] reported on a decline of reed populations comparable to the RDBS. At Lake Trasimeno (central Itay), one of the largest freshwater ecosystems in Mediterranean Italy up to 50 years ago, during the last decades the reed bed has shown increasing signs of decline, suggesting the possible occurrence of die-back symptoms [31,32].

Reed beds are extremely important for biodiversity conservation in all the regions where Phragmites australis can be considered a native species, and particularly in Mediterranean areas, where the hydrologic balance of wetlands may be very fragile. In these areas, besides well known threats such as land reclamation, habitat fragmentation, water uptake, eutrophication, the climatic conditions may also play a role in damaging wetlands and their important functions, which are already suffering the effects of global warming. Although the reed beds do not show the highest biodiversity values when compared to other plant communities, the presence of tall aquatic macrophytes in shallow standing waters offers a specific environment for many other components of the ecosystems, from migrating birds to insects to rare planktonic communities [33,34]. Furthermore, they are highly vulnerable to invasions by alien species, which represent an alarming threat [35,36]. It appears therefore imperative to identify the patterns of change which are nowadays affecting these ecosystems and detect the processes underpinning these changes, in order to inform and support those involved in the biodiversity conservation of the most delicate habitats.

In this framework, the specific aim of this study was to use a set of life-history traits to ascertain whether the population changes observed in the reeds in Lake Trasimeno are an indication of RDBS. Further, we investigated the role of eco-hydrological conditions in the pattern-generation of trait syndromes.

2 Materials and methods

2.1 Study area

The study was performed at the Lake Trasimeno (Fig. 1), a shallow lake filling a wide basin in peninsular Central Italy at an average altitude of 257 m a.s.l.; the total area of the present basin, lake included, is 383.4 km2. The average surface of the lake is 121.5 km2 and the average water column depth is 4.2 m [37]. This lacustrine ecosystem is marred by several environmental problems. The water level is subject to great variation due to total dependence on rains and lack of notable tributaries. The anthropic impact is heavy, especially because of the intensive land use in the basin (agriculture and pig farms). The water level of Lake Trasimeno was increased at the end of the 1950s, by an artificially induced influx of water that totally submerged the flat shores [38]. It was an attempt to contrast the natural tendency of the lake to become swampy because of the constantly negative rainfall/evapotranspiration balance. Still nowadays, some intrinsic features of the lake tend towards a worsening of water quality, e.g. the long time, 24.4 years, for water replacement, and the high evaporation rate, 155 × 106 m2/year, due to the laminar shape of the lake [39,40].

Fig. 1

Study area at Lake Trasimeno, Central Italy (bathymetric equidistance on the map: 50 cm); in brackets the plot codes at each site.

Based on climatic data recorded in Monte del Lago climatic station (295 m a.s.l.; data from a period of 30 years), applying the bioclimatic indexes proposed by Rivas-Martínez et al. [41], processed according to Rivas-Martínez and Rivas-Saenz [42], the study area belongs to the Mediterranean pluviseasonal-oceanic bioclimate, upper mesomediterranean low subhumid belt [43]. The mean annual temperature is 13.6 °C, the mean annual precipitation is 747 mm, and the mean potential evapotranspiration is 761 mm.

During the last decades, the reed bed of Lake Trasimeno has been affected by a progressive decline, mostly evident from a notable retreat and certain abnormal traits, which have been recently accentuated [31,32,44,45]. In the last 50 years the surface occupied by the reeds along the lake's shore has decreased; a loss of about 66% of its total surface can be calculated only in the period between 1988 and 2005 (data in [46–48]). According to a diachronic analysis based on the comparison of aerial photographs from different periods during the last half century, a remarkable retreat of the reed bed has occurred in the SE quadrant of the lake's shore, in the area La Valle [49].

2.2 Sampling sites

The investigation was carried out in 19 plots (1 m2) located in seven different sites along the lake shore (Table 1, Fig. 1). The plots were located at different distance from the shore, in order to cover a water gradient from dry to permanently flooded habitats. The plots were located both in sites without any evident macroscopic sign of decay and in areas seemingly affected by retreat and/or decline (La Valle site), as indicated by Filipponi et al. [49].

Table 1

Names, codes and geographical coordinates of sites and plots.

Site Plot code Geographical coordinates
Oasi “La Valle” P01 N43° 05,699′ E12° 11,034′
P02 N43° 05,697′ E12° 11,036′
P03 N43° 05,694′ E12° 11,044′
P04 N43° 05,684′ E12° 10,925′
P05 N43° 05,681′ E12° 10,946′
P06 N43° 05,686′ E12° 10,983′
Poggio di Braccio P07 N43° 04,794′ E12° 07,580′
P08 N43° 04,762′ E12° 07,594′
Porto di Panicarola P09 N43° 05,020′ E12° 06,212′
P10 N43° 04,859′ E12° 06,518′
P11 N43° 04,848′ E12° 06,523′
Rio Pescia P12 N43° 06,752′ E12° 02,943′
P13 N43° 06,747′ E12° 02,933′
Castiglion del Lago P14 N43° 08,709′ E12° 01,952′
P15 N43° 08,254′ E12° 02,472′
Borghetto P16 N43° 11,071′ E12° 02,161′
P17 N43° 11,064′ E12° 02,154′
Passignano P18 N43° 11,412′ E12° 06,491′
P19 N43° 11,415′ E12° 06,495′

2.3 Trait measurements

In order to analyse and quantify the signs of decline, 13 parameters were selected from those documented in literature, and monitored. The list of selected traits is given in Table 2. In each plot, 15 stems of Phragmites australis were randomly chosen and measured. The traits were measured and monitored in the 19 plots for two years (vegetative seasons 2006 and 2007), from the beginning of April to the end of August.

Table 2

Selected plant traits and environmental factors used in the monitoring of Phragmites australis population at Lake Trasimeno.

Name of the plant trait Unit of measurement Sampling scale type
Number of nodes Number RM
Growth rate of the n. of nodes Direction coefficient, no/day RC, RM
Stem height cm RM
Growth rate of the stem height Direction coefficient, cm/day RC, RM
Stem diameter mm RM
Growth rate of the stem diameter Direction coefficient, mm/day RC, RM
Stem density no/m2 RC
Dead buds no/m2, % RC
Flowering rate no/m2, % RC
Clumping habit no/m2 RC
Rhizome diameter mm RM
Lateral root diameter mm RM
Lateral root amount Class: 1–5 IC
Environmental factor Unit of measurement Sampling scale type
 Water depth  cm  RM
 Standing litter  Class: 1 = scarce or absent, 2 = abundant  N

The number of nodes, stem height and stem diameter were measured fortnightly (n = 15 stems per plot). The growth rates of the three above-mentioned traits were calculated for each plot, considering the slope (direction coefficient) of the regression line of the three parameters. The stem density and clumping habit were measured at the end of the vegetative season (end of August). The flowering heads and prematurely dead buds were also measured fortnightly. The rhizomes and roots were measured at the end of August. The amount of lateral roots was estimated using a 5-class interval scale (1: very few, 2: few, 3: medium amount, 4: many, 5: very many).

The environmental factors investigated are also included in Table 2. The type of flooding and the presence/absence of standing litter in the sediment - both presumed to be important for driving vegetation dynamic processes in the reed beds - were reported. The water depth was measured at the start/end of the period of field activity (beginning of April-end of August) each of the two years, in order to show any flooding and its periodicity (permanent/temporary).

2.4 Data analysis

The data gathered were used to build a ‘13 × 19’ matrix (traits x plots) that was used for a cluster analysis. The following strategy was used in the data processing: reduction of the data dimensions by PCA and selection of the Principal Components, which can better explain the total variance; use of fuzzy clustering, fuzzy c-means [50], on the selected Principal Components; identification of the optimal partition by using the Dunn index [51]; identification of the Boolean partition of the plots, induced by the fuzzy partition. For the data analysis, the SYN-TAX 5.0 package [52] was used. The statistical significance of the measured data for the resulting groups was tested by ANOVA; the post hoc analysis was based on Fisher's Protected LSD test.

3 Results

The macro-morphologic and phenologic data differed widely among the 19 plots. Looking at the 13 positive eigenvalues resulting from the PCA, the first four can be seen to account for about 80% of the total variance (Table 3). The fuzzy c-means, applied to the first four principal components (with a fuzziness coefficient = 2), showed that the optimal partition is formed of four clusters. Table 4 shows the correlation coefficients among the first four principal components (PC) and the original variables.

Table 3

Eigen values resulting from the PCA; the first four account for about 80% of the total variance.

Eigenvalues 4.947 2.431 1.884 1.024 0.794 0.769 0.473 0.293 0.191 0.089 0.068 0.023 0.133
Eigenvalues (%) 38.05 18.70 14.49 7.88 6.11 5.92 3.64 2.26 1.47 0.68 0.52 0.18 0.10
Table 4

Correlation coefficients among the first four principal components (PC) and the original variables.

PC1 PC2 PC3 PC4
Number of nodes 0.894 0.199 0.021 −0.052
Growth rate of the number of nodes 0.869 0.024 −0.141 −0.086
Stem height 0.764 −0.344 −0.038 0.360
Growth rate of the stem height 0.248 0.595 −0.354 0.492
Stem diameter 0.494 −0.589 −0.197 −0.128
Growth rate of the stem diameter 0.221 0.941 0.041 0.185
Stem density 0.690 −0.424 −0.390 0.331
Flowering rate 0.790 −0.162 −0.214 −0.245
Prematurely dead buds −0.520 −0.447 0.281 0.626
Clumping habit −0.576 −0.140 −0.229 −0.141
Rhizome diameter 0.202 0.000 0.894 0.033
Lateral root diameter 0.481 −0.334 0.646 0.029
Lateral root amount −0.692 −0.387 −0.389 0.092

The Boolean partition induced by the fuzzy partition, according to the highest membership weight (Table 5), grouped the 19 plots in four clusters as follows:

  • • Cluster 1 (CL1): P01, P02, P03, P05, P06;
  • • Cluster 2 (CL2): P17, P18, P19, P12, P13, P09, P10;
  • • Cluster 3 (CL3): P16, P07, P08, P15, P04, P11;
  • • Cluster 4 (CL4): P14.

Table 5

Membership weights of the 19 plots per cluster, resulting from the Boolean partition; the highest values in each cluster are highlighted in bold: they point out the composition of the groups.

Cluster 1 Cluster 2 Cluster 3 Cluster 4
P01 0.8380 0.0285 0.1090 0.0245
P02 0.5729 0.0949 0.2884 0.0438
P03 0.8902 0.0177 0.0760 0.0161
P04 0.3489 0.1321 0.4712 0.0477
P05 0.5113 0.0853 0.3581 0.0453
P06 0.4526 0.1034 0.2142 0.2298
P07 0.2694 0.2289 0.3943 0.1075
P08 0.1889 0.0583 0.7343 0.0185
P09 0.1823 0.3429 0.3082 0.1666
P10 0.0956 0.4810 0.3904 0.0330
P11 0.1126 0.2933 0.5592 0.0349
P12 0.0351 0.8623 0.0853 0.0172
P13 0.0640 0.7516 0.1541 0.0302
P14 0.0089 0.0060 0.0081 0.9770
P15 0.2063 0.2340 0.4670 0.0927
P16 0.1004 0.0584 0.8301 0.0111
P17 0.2445 0.3288 0.2962 0.1306
P18 0.0147 0.9382 0.0394 0.0077
P19 0.0394 0.8332 0.1077 0.0197

For each cluster of plots, the median, average, maximum and minimum values, 1st and 3rd quartiles, mild and extreme outliers of the 13 plant traits were reported in box-and-whisker charts (Fig. 2). The statistical significance of the measured data (stem height, stem diameter, no of nodes and relative growth rates, the latter expressed respectively in cm/day, mm/day, no/day; lateral root amount and diameter, rhizome diameter, flowering rate, dead buds, clumping and stem density) is also reported in Fig. 2. The data analysis indicated different features for the resulting groups of stands of Phragmites australis. The considered parameters outline a very consistent pattern for the resulting clusters and are briefly described as follows.

Fig. 2

Box-and-whisker charts for the identified clusters of plots (Cluster 4 is not reported since it includes only one plot); median, average, maximum and minimum values, 1st and 3rd quartiles, mild and extreme outliers of the 13 indicated plant traits are reported. Different letters indicate statistically significant differences according to Fisher's protected LSD test; the significance level is indicated.

Cluster 1 (five plots) shows the lowest values for stem height, stem diameter, node number and growth rate of the last two traits. The rate of prematurely dead buds is the highest, the stem density and the flowering rate are the lowest. The lateral root diameter is low, especially when compared to Cluster 2, while the amount of lateral roots is the highest. Cluster 1 includes the only plots where the clumping habit was observed; the growth rate of the stem diameter is more prominently negative. As a whole, the reed stands of the Cluster 1 show a declining, non-vigorous condition together with some typical RDBS symptoms.

Cluster 2 (seven plots) shows, on the contrary, the highest values for stem height, stem diameter, node number and their growth rates; the diameters of lateral roots and rhizomes are also the highest in this group of plots, while the lateral roots are not extremely dense. The flowering rates are the highest, while the presence of dead buds is the lowest on average. The clumping habit was never detected in these plots. As a whole, Cluster 2 groups the plots where the reeds are in the most vigorous condition and are totally lacking in symptoms of decline.

Cluster 3 (six plots) shows in general intermediate values between Clusters 1 and 2. Only the growth rate of the stem height and the rhizome diameter reach the lowest values in these plots. The stem density is generally high. As a whole, the reed stands included in Cluster 3 appear to be in an intermediate condition; considering that prominent symptoms of RDBS are not present, their state can be described as sub-optimal.

Cluster 4 includes only one plot (P14) and thus it has not been included in the box-and-whisker charts; for this Cluster, the recorded values are the following: average stem height (n = 15): 2.073 m; av. stem diameter (n = 15): 6.7 mm; av. number of nodes (n = 15): 21.2; av. stem height growth rate: 1.419 cm/day (n = 15); av. stem diameter growth rate: 0.027 mm/day (n = 15); av. node number growth rate: 0.100 nodes/day (n = 15); stem density: 46.0 stems/m2; prematurely dead buds: 0.0; flowering rate: 66.7%; clumping habit: 0.0 clumps/m2; av. rhizome diameter: 13.70 mm (n = 5); av. lateral root diameter: 1.09 mm (n = 5); av. lateral root amount: 2.8 (interval scale, n = 5). The stem height and diameter are very low, although the latter shows a remarkable growth rate; the density is extremely low, however neither dead buds nor clumping habit are present. The other values are rather close to Cluster 1. Cluster 4 generally shows a non-vigorous, suffering condition, although not so prominent as in Cluster 1; for this reason it can be defined as sub-declining.

As a whole, the most significant parameters to emphasize the declining condition, according to the Fisher's Protected LSD test (ANOVA), are the stem height and diameter, the node number and its growth rate, the lateral root amount and diameter, the flowering rate and the presence of dead buds (p < 0.01), followed by the stem height growth rate and the stem diameter growth rate (p < 0.05).

The flowering rate at the end of the season (end of August) and the delay in the starting of flowering, expressed as number of days after the first plant begins to bloom, are reported in Fig. 3, as average values for each cluster. Lower values of flowering rate have been recorded in the plots where a remarkable delay in the start of the flowering was observed (especially Clusters 1 and 4).

Fig. 3

Flowering rate at the end of the season (end of August) and delay in the starting of flowering, expressed as number of days after the first plant begins to bloom; average values for each cluster.

Regarding the environmental features of the 19 plots, flooding is shown in Fig. 4: the median, average, maximum and minimum values, 1st and 3rd quartiles, mild and extreme outliers of the water depth at the end of August were reported in box-and-whisker charts for the three main clusters. Water is not present at the end of August in Cluster 4. The 19 plots relate to two basic types: temporarily or permanently flooded, the latter still being totally submerged at the end of August, the period when, due to climatic reasons, the water level reaches its minimum. All the plots from Cluster 1 are permanently flooded, while all the plots from Cluster 2 are flooded only in winter-early spring and are dry at the end of August. Cluster 3 includes plots of the two types, although the temporarily flooded type prevails; Cluster 4 is flooded only in winter.

Fig. 4

Box-and-whisker chart including median, average, maximum and minimum values, 1st and 3rd quartiles, mild and extreme outliers of the water depth at the end of August for the three main clusters of plots (Cluster 4 is not reported since it includes only one plot).

We calculated the number of plots for each cluster affected by presence of standing litter: all the plots (100%) from Cluster 1 are rich in organic deposits, mainly composed of autogenous reed litter. The same is true for Cluster 4. On the contrary, all the plots (100%) from Cluster 2 are lacking in litter. The plots from Cluster 3 are more variable; standing litter is present in 33% of the plots, but never in large amounts.

4 Discussion

4.1 Reed decline features and significant traits

On the basis of the above results, it was possible to detect a condition of strong decline for the plots of Cluster 1, all located in the S-Eastern sector of the lake (Fig. 1), highlighted by the anomalous values of several morphological attributes. Traits connected with the reed growth (stem height and diameter, node number and the relative growth rates), together with the clumping habit, reduced flowering rate, flowering delay and a relatively high incidence of dead buds, indicate a clear condition of decline for this subgroup of plots. These symptoms are indicative of RDBS as described by Van Der Putten [5], and allowed us to confirm that the syndrome is present in central Italy.

Furthermore, using the progression of the decline symptoms as a basis, the four clusters could be related to different degrees of decline, from suffering to healthy, which can be listed as follows: suffering condition with typical RDBS symptoms, corresponding to Cluster 1; suffering condition without typical RDBS symptoms, corresponding to Cluster 4; sub-optimal condition, corresponding to Cluster 3; optimal condition, corresponding to Cluster 2. This is the first time that this type of classification, based on a multivariate analysis of different symptoms regarding specific plant traits, has been done.

Remarkably, a negative growth rate of the stem diameter was observed in the most declining stands (Cluster 1); this peculiar datum derives from the fact that, during the vegetative season, the new shoots are smaller than the previous ones and the average value decreases in time, as suggested by Engloner [53]. Similar trends were also observed by other authors, who described a decrease in the shoot diameter or height during the vegetative period in declining populations of Phragmites australis [30,54–58].

A high number and surface of lateral roots are generally considered an indication of vigorous state [5]; however, Clevering [59] reports an increased percentage of aquatic roots in relation with an increasing amount of litter in the substrate in flooded conditions. Our results fit with Clevering's data. The extra amount of lateral roots might be a reaction of the plants to the general condition of stress on the root system, due to the permanent submersion and the high presence of litter and organic matter, both phenomena occurring in Cluster 1.

4.2 Ecological traits

When we consider the ecological conditions of the plots we can see in Fig. 4 that the most declining stands (Cluster 1) are characterized by a permanent pronounced submersion (more than 40 cm on average at the end of the dry season) and by constant presence of standing litter (data reported in the text). The area where the most declining stands are located is the La Valle site; at the end of the 1950s it was occupied by a very wide reed bed, larger than 2 km [49,60]. When the artificial rise of the water level occurred at the end of the 1950s [38], this area was affected by a permanent deep flooding that still occurs nowadays, because of its flat morphology. This is also the area where the most notable retreat of the reed bed has been reported [49].

It is known that the water-table fluctuations condition both the root aeration and the mineral availability in aquatic ecosystems [61,62]. It has been reported that the reed die-back generally affects aquatic stands [63,64]. In spite of the reed's well-developed mechanisms of flood tolerance [65], altered or artificially stabilised water tables have been cited as possible causes of the reed decline [66–71]. Ostendorp [4] includes the alterations in the lake levels among the possible causes of reed die-back; disturbance and decline of reed beds have been observed after extreme flooding [72].

Several Authors reported that reed beds tend to retreat from deep waters and to narrow along the banks [4,10,11,73]; this phenomenon might be related to a lack of carbohydrates [74,75]. It has been reported that the water depth where reed beds may occur is related to carbohydrate availability [76]; this suggests that the retreat from deep waters might derive from a shortage in the carbohydrate stock. It has been suggested that an increase in the water table might favour fermentation processes to provide energy [77,78], supporting the theory of exhaustion of carbohydrates as one of the causes of reed die-back and retreat [79].

High water level or prolonged flooding may also support the eutrophication processes, since these are slowed down by accelerated mineralization [80]. In this sense, water level fluctuations may play a positive role [11].

Permanent submergence (≥ 40 mm) of seedling shoots (20–30 mm) can have negative effects on growth and prevent shoot emergence, especially where the inundating waters are rich in algae [71]. Furthermore, according to Rea [67], stabilised water levels are contributing to reed decline due to a lack of vegetative and generative reproduction; eutrophic conditions exacerbate this situation.

It has also been reported that the excessive production and deposition of litter, especially when it completely derives from reed itself, might result in P. australis growth reduction or decline [59,74,75,81–85]. Cízková et al. [11,86] showed that the accumulation of organic matter is harmful to reed stands. It was suggested that reed's ability to maintain itself in deep water is undermined when the substrate contains standing litter; this has been indicated as one of the explanations for the retreat of reed from the water front of littoral zones [59]. Furthermore, it has been pointed out that when the rhizosphere is not oxygenated enough, it can lead to anoxia and production of phytotoxins [87,88]. According to Clevering [59] deep waters and litter-rich soils create unsuitable conditions for P. australis growth; this author suggests that an artificial decrease of the water level might be a successful way to restore declining reed populations.

According to Ostendorp [4], it should be considered that reeds may show a delayed response to changes in environmental conditions, since “Phragmites rhizomes can act as a buffer against unfavourable as well as against good conditions”. Thus, the reed bed retreat and decline observed in the La Valle area might represent a delayed reaction to the past artificial changes of the water table. These results match with other studies which show that the spatial dynamics of the reed beds are linked with water level fluctuations [89–91]. The analyzed data confirm the idea that a long-term accumulation of autogenous litter, combined with permanent flooding, may lead to a condition of reed decline. In dry or fluctuating water conditions, the same reed population shows vigorous condition and no (or few) symptoms of decline.

5 Conclusive remarks

It has been presumed that the reed die-back syndrome hardly occurs in southern Europe, since high average temperatures are typical in the Mediterranean areas, and the break-down of litter should proceed more rapidly [5]. Some studies confirm this hypothesis, e.g. in Portugal no signs of RDBS have been reported [92]. In the present study, however, abundant deposits of litter together with permanent, artificially induced flooding seem to create the conditions for the occurrence of RDBS even in a Mediterranean area. These findings highlight the close interaction existing between hydrological processes and biological systems.

The only Italian area where reed decline has already been observed, up to now, is located at the mouth of the Po river at Sacca di Goro [30]. This area is included, geographically, in the Mediterranean Basin; however, it cannot be called Mediterranean, neither from a bioclimatic nor from a biogeographic point of view [93,94]. Thus Lake Trasimeno is the first area with a Mediterranean climate where RDBS has been detected, indicating a larger diffusion than suggested by Van Der Putten [5].

By creating a gradient of decline, we wish to stress that even the situations currently in sub-optimal conditions already show some symptoms of decay. Reed decline has been considered the first link in a chain which may lead to a deterioration of the littoral biocoenosis [95]. One of the most important targets of the research projects dealing with reed decline in Europe was to individuate useful parameters which could indicate which reed stands are susceptible to dying back [5]. Thus, the identification of a set of significant traits providing indications of a declining trend in the populations might be useful in ecosystem monitoring. The sub-optimal reed stands should be treated with the proper care, in order to halt the decaying process before it reaches a point of no return. The intensity of the reed care should be gauged proportionally to the observed degree of decline, in order to preserve these delicate wet ecosystems.

Disclosure of interest

The authors have no actual or potential conflict of interest pertaining to this journal submission.

Acknowledgements

This study was funded by “Servizio Protezione Ambientale e Parchi”, Perugia's local environmental conservation body; the Authors wish to thank Director Dr. Roberta Burzigotti and Dr. F. Velatta. We also thank the keepers on the natural reserve “Oasi La Valle”, M. Muzzatti and M. Chiappini, for their cooperation.


References

[1] A.I. Engloner Structure, growth dynamics and biomass of reed (Phragmites australis)-A review, Flora - Morphology, Distribution, Functional Ecology of Plants, Volume 204 (2009) no. 5, pp. 331-346

[2] H. Hürlimann Lebensgeschichte des Schilfs an den Ufern der Schweizer Seen, Beitr Geobot Landesaufn Schweitz, Volume 30 (1951), pp. 1-232

[3] H. Brix The European research programme on reed die-back and progression (EUREED), Limnologica, Volume 29 (1999), pp. 5-10

[4] W. Ostendorp “Die-back” of reeds in Europe-a critical review of literature, Aquat Bot, Volume 35 (1989) no. 1, pp. 5-26

[5] W.H. van der Putten Die-back of Phragmites australis in European wetlands: an overview of the European Research Programme on reed die-back and progression (1993-1994), Aquat Bot, Volume 59 (1997), pp. 263-275

[6] C. Den Hartog; J. Kvet; H. Sukopp Reed. A common species in decline, Aquat Bot, Volume 35 (1989) no. 1, pp. 1-4

[7] J. Armstrong; E. Afreen-Zobayed; W. Armstrong Phragmites die-back: sulphide-and acetic acid-induced bud and root death, lignifications and blockages within aeration and vascular systems, New Phytol, Volume 134 (1996), pp. 601-614

[8] J. Armstrong; W. Armstrong; I.B. Armstrong; G. Pittaway Senescence and phytotoxin, insect, fungal and mechanical damage: factors reducing convective gas-flows in Phragmites australis, Aquat Bot, Volume 54 (1996), pp. 211-226

[9] J. Armstrong; W. Armstrong; W.H. van der Putten Phragmites die-back: bud and root death, blockages within the aeration and vascular systems and the possible role of phytotoxins, New Phytologist, Volume 133 (1996), pp. 399-414

[10] R.R. Boar; C.E. Crook; B. Moss Regression of Phragmites australis reedswamps and recent changes of water chemistry in the Norfolk Broadland, England, Aquat Bot, Volume 35 (1989), pp. 41-55

[11] H. Cízková; J. Strand; J. Lukavská Factors associated with reed decline in a eutrophic fishpond, Rozmberk (South Bohemia, Czech Republic), Folia Geobot Phytotax, Volume 31 (1996), pp. 73-84

[12] O.A. Clevering The effects of litter on growth and plasticity of Phragmites australis clones originating from infertile, fertile or eutrophicated habitats, Aquat Bot, Volume 64 (1999) no. 1, pp. 35-50

[13] de Nie H. W. The decrease in aquatic vegetation in Europe and its consequences for fish populations, EIFAC/CECPI Occasional paper N° 19, Food and Agriculture Organization of the United Nations, 1987, p. 52.

[14] E. Bittmann Das Schilf (Phragmites communis Trin.) und seine Verwendung im Wasserbau, Angew. Pflanzensoziol, Stolzenau (F.R.G.), Volume 7 (1953), pp. 1-41

[15] R. Neuhäusl Vegetation der Röhrichte und der sublitoralen Magnocariceten im Wittingauer Becken (R. Neuhäusl; J. Moravec; Z. Neuhäuslova-Novotna, eds.), Synökologische Studien über Rörichte, Wiesen und Auewälder, Vegetace, CSSR, A1, 1965, pp. 13-177

[16] H. Sukopp, W. Kunick, Veränderungen des Röhrichtbestandes der Berliner Havel 1962-1967, Berl. Naturschutzbl. 13/37 (1969) 303-313, 13/38 (1969) 332-344.

[17] F. Klötzli Biogenous influence on aquatic macrophytes especially Phragmites communis, Hidrobiologia, Volume 12 (1971), pp. 107-111

[18] T. Tscharntke Klärteiche-Feuchtgebiete in einer ausgeräumten Kulturlandschaft, Natur Landschaft, Volume 58 (1983), pp. 333-337

[19] C. Bragato; H. Brix; M. Malagoli Accumulation of nutrients and heavy metals in Phragmites australis (Cav.) Trin. ex Steudel and Bolboschoenus maritimus (L.) Palla in a constructed wetland of the Venice lagoon watershed, Environmental Pollution, Volume 144 (2006), pp. 967-975

[20] G.C. Tucker The genera of Arundioideae (Gramineae) in the southeastern United States, Journal of the Arnold Arboretum, Volume 71 (1990), pp. 145-177

[21] M. Marks; B. Lapin; J. Randall Phragmites australis (P. communis): threats, management and monitoring, Natural Areas Journal, Volume 14 (1994), pp. 285-294

[22] A.R. Bailey Detecting and monitoring Phragmites invasion of coastal wetlands: a comparison of remote sensing techniques, MS Thesis, University of Delaware, Newark, DE, USA, 1997

[23] R.M. Chambers; L.A. Meyerson; K. Saltonstall Expansion of Phragmites australis into tidal wetlands of North America, Aquat Bot, Volume 64 (1999), pp. 261-273

[24] L. Windham; R. Lathrop, Effects of Phragmites australis (Common Reed) invasion on aboveground biomass and soil properties in brackish tidal marsh of the Mullica River, 22, Estuaries, New Jersey, 1999 (p. 927-35)

[25] M.S. Ailstock; C. Norman; P. Bushmann Common Reed Phragmites australis: Control and Effects Upon Biodiversity in Freshwater Nontidal Wetlands, Restoration Ecology, Volume 9 (2001) no. 1, pp. 49-59

[26] T.S. Talley; L.A. Levin Modification of sediments and macrofauna by an invasive marsh plant, Biological invasions, Volume 3 (2001), pp. 51-68

[27] K. Saltonstall Cryptic invasion be a non-native genotype of the common reed, Phragmites australis, into North America, Proceedings of the National Academy of Sciences (PNAS), Volume 99 (2002), pp. 2445-2449

[28] L. Windham; L. Meyerson, Effects of Common Reed (Phragmites australis) expansions on nitrogen dynamics of tidal marshes of the Northeastern, 26, Estuaries, U.S, 2003 (p. 452-64)

[29] A. Brülisauer; F. Klötzli Habitat factors related to the invasion of reed (Phragmites australis) into wet meadows of the Swiss Midlands, Z Ökol Natursch, Volume 7 (1998), pp. 125-136

[30] S. Fogli; R. Marchesini; R. Gerdol Reed (Phragmites australis) decline in a brackish wetland in Italy, Marine Env Research, Volume 53 (2002), pp. 465-479

[31] D. Gigante; R. Venanzoni; V. Zuccarello Detection of reed-bed decline and die-back at the Lake Trasimeno (central Italy) (L. Mucina; J.M. Kalwij; V.R. Smith; M. Chytrý; P.S. White; S.S. Cillier; V.D. Pillar; M. Zobel; I.-F. Sun, eds.), Frontiers of Vegetation Science-An Evolutionary Angle,, K. Philips Images, Somerset West, SA, 2008, pp. 62-63

[32] D. Gigante, F. Ferranti, L. Reale, R. Venanzoni, V. Zuccarello, Nuovi dati sul declino della popolazione di Phragmites australis al Lago Trasimeno, in: Bottarin R., Schirpke U., Tappeiner U., Oggioni A., Bolpagni R. (Eds.), Macrofite & Ambiente, Atti XIX S. It.E. Congress, Bolzano, 15-18 settembre 2009, Vol. 3, 2010, pp. 23-41.

[33] I.M. Raspopov; L. Adamec; Š. Husák Influence of aquatic macrophytes on the littoral zone habitats of the Lake Ladoga, NW Russia, Preslia, Volume 74 (2002), pp. 315-321

[34] T. Tscharntke Fragmentation of Phragmites Habitats, Minimum Viable Population Size, Habitat Suitability, and Local Extinction of Moths, Midges, Flies, Aphids, and Birds, Conservation Biology, Volume 6 (1992), pp. 530-536

[35] M. Chytrý; P. Pyšek; L. Tichý; I. Knollová; J. Danihelka Invasions by alien plants in the Czech Republic: a quantitative assessment across habitats, Preslia, Volume 77 (2005), pp. 339-354

[36] M. Chytrý; J. Wild; P. Pyšek; L. Tichý; J. Danihelka; I. Knollová Maps of the level of invasion of the Czech Republic by alien plants, Preslia, Volume 81 (2009), pp. 187-207

[37] R. Burzigotti; W. Dragoni; C. Evangelisti; L. Gervasi The Role of Lake Trasimeno (central Italy) in the History of Hydrology and Water Management IWHA 3rd International Conference, Alexandria, Egypt, 2003

[38] E. Gambini Le oscillazioni di livello del lago Trasimeno, Quaderni del Museo della Pesca del Lago Trasimeno, N° 2, Grafiche Piemme, Perugia, 1995 (p. 139)

[39] P. Viotti, L. Galeotti, S. Sbaffoni, G. Sappa, M. Leccese, N. Stracqualursi, Analisi sperimentale dei flussi di fosforo dai sedimenti di un lago: il caso del Lago Trasimeno (Italia), VI Simpósio Ítalo Brasileiro de Engenharia Sanitária e Ambiental, 2002.

[40] A. De Bartolomeo; L. Poletti; G. Sanchini; B. Sebastiani; G. Morozzi Relationship among parameters of lake polluted sediments evaluated by multivariate statistical analysis, Chemosphere, Volume 55 (2004), pp. 1323-1329

[41] S. Rivas-Martínez; D. Sánchez Mata; M. Costa North American boreal and western temperate forest vegetation, It Geobot, Volume 12 (1999), pp. 5-316

[42] S. Rivas-Martínez, S. Rivas-Saenz, Worldwide Bioclimatic Classification System, 1996-2009, Phytosociological Research Center, Spain, available at: http://www.globalbioclimatics.org, 2009.

[43] D. Gigante; R. Venanzoni Some remarks about the annual subnitrophilous vegetation of the Thero-Brometalia order in Umbria (central Italy), Lazaroa, Volume 28 (2007), pp. 15-34

[44] M. Bresciani; C. Giardino; M. Musanti Il telerilevamento per lo studio dei canneti del Trasimeno, Micron, Volume 11 (2009), pp. 37-41

[45] M. Bresciani; D. Stroppiana; G. Fila; M. Montagna; C. Giardino Monitoring reed vegetation in environmentally sensitive areas in Italy, Rivista Italiana di Telerilevamento, Volume 41 (2009) no. 2, pp. 125-137

[46] M. Mearelli; M. Lorenzoni; L. Mantilacci Il Lago Trasimeno, Riv Idrobiol, Volume 29 (1990) no. 1, pp. 353-389

[47] R. Venanzoni; E. Rampiconi Utilizzo del GIS nella valutazione spazio-temporale della vegetazione palustre in un settore del Lago Trasimeno in relazione ai fattori antropici, Riv Idrobiol, Volume 40 (2001) no. 2-3, pp. 69-85

[48] A. Cecchetti, M. Ficola, G. Lazzerini, A. Pedini, F. Segantini, Vegetazione, habitat di interesse comunitario, uso del suolo del Parco del Lago Trasimeno, Ente Parco del Lago Trasimeno, Passignano sul Trasimeno, 2005.

[49] F. Filipponi, D. Gigante, R. Venanzoni, Analisi diacronica della frammentazione di un habitat palustre al Lago Trasimeno (Italia centrale), in: S. Assini, F. Bracco, P. Nola (Eds.), 46(S.I.S.V. Congress, Pavia, 17/19 febbraio 2010, Abstract Book, 2010, pp. 77-8.

[50] J.C. Bezdek Pattern Recognition with Fuzzy Objective Function Algorithms, Plenum Press, New York, 1981

[51] J.C. Dunn Well Separated Clusters and Optimal Fuzzy Partitions, J Cybernetics, Volume 4 (1974), pp. 95-104

[52] J. Podani SYN-TAX version 5.0 Computer Programs for Multivariate Data Analysis in Ecology and Systematics, Scientia Publishing, Budapest, 1993 (p. 104)

[53] A.I. Engloner Annual growth dynamics and morphological differences of reed (Phragmites australis [Cav.] Trin. ex Steudel) in relation to water supply, Flora, Volume 199 (2004), pp. 256-262

[54] H. Mochnacka-Lawacz Seasonal changes of Phragmites communis Trin. Part I. Growth, morphometrics, density and biomass, Pol Arch Hydrobiol, Volume 21 (1974), pp. 355-368

[55] M. Dinka The effect of mineral nutrient enrichment of Lake Balaton on the common reed (Phragmites australis), Folia Geobot Phytotax, Volume 21 (1986), pp. 65-84

[56] K. Hofmann Wachstumsverhalten von Schilf (Phragmites australis [Cav.] Trin. ex Steudel) in klärschlammbeschickten Filterbeeten, Arch Hydrobiol, Volume 107 (1986), pp. 385-409

[57] H. Rolletschek; A. Rolletschek; H. Kühl; J.-G. Kohl Clone specific differences in a Phragmites australis stand. II. Seasonal development of morphological and physiological characteristics at the natural site and after transplantation, Aquat Bot, Volume 64 (1999), pp. 247-260

[58] M. Hardej; T. Ozimek The effect of sewage sludge flooding on growth and morphometric parameters of Phragmites australis (Cav.) Trin. ex Steudel, Ecol Eng, Volume 18 (2002), pp. 343-350

[59] O.A. Clevering Effects of litter accumulation and water table on morphology and productivity of Phragmites australis, Wetlands Ecology and Management, Volume 5 (1998) no. 4, pp. 275-287

[60] B. Granetti La flora e la vegetazione del lago Trasimeno. Parte I: La vegetazione litoranea, Riv Idrobiol, Volume 4 (1965) no. 3, pp. 115-153

[61] H.A.P. Ingram Problems of hydrology and plant distribution in mires, J Ecol, Volume 55 (1967), pp. 711-724

[62] J. Navrátilová; J. Navrátil Vegetation gradients in fishpond mires in relation to seasonal fluctuations in environmental factors, Preslia, Volume 77 (2005), pp. 405-418

[63] S. Güsewell; F. Klötzli Assessment of aquatic and terrestrial reed (Phragmites australis) stands, Wetl Ecol Manag, Volume 8 (2000), pp. 367-373

[64] A. Rücker; S. Grosser; A. Melzer Geschichte und Ursachen des Röhrichtrückgangs am Ammersee (Deutschland), Limnologica, Volume 29 (1999) no. 1, pp. 11-20

[65] C. Gries; L. Kappen; R. Lösch Mechanism of flood tolerance in reed, Phragmites australis (Cav.) Trin. ex Steudel, New Phytol, Volume 114 (1990), pp. 589-593

[66] M. Dinka; P. Szeglet; I. Szabo Hungarian Group Report (W.H. van der Putten, ed.), Reed News (Reports of EC Project EUREED-EV5V-CT92-0083),, vol 3, Netherlands Institute of Ecology, Heteren, 1995, pp. 96-107

[67] N. Rea Water levels and Phragmites: decline from lack of regeneration or dieback from shoot death, Folia Geobot Phytotax, Volume 31 (1996), pp. 85-90

[68] S.E.B. Weisner; W. Granéli; B. Ekstam Influence of submergence on growth of seedlings of Scirpus lacustris and Phragmites australis, Freshwater Biol, Volume 29 (1993), pp. 371-375

[69] S.E.B. Weisner; J.A. Strand Rhizome architecture in Phragmites australis in relation to water depth: implications for within-plant oxygen transport distances, Folia Geobot Phytotax, Volume 31 (1996), pp. 91-97

[70] W. Armstrong; R. Brändle; M.B. Jackson Mechanisms of flood tolerance in plants, Acta Bot Neerl, Volume 43 (1994), pp. 307-358

[71] J. Armstrong; F. Afreen-Zobayed; S. Blyth; W. Armstrong Phragmites australis: effects of shoot submergence on seedling growth and survival and radial oxygen loss from roots, Aquat Bot, Volume 64 (1999), pp. 275-289

[72] W. Ostendorp; M. Dienst; K. Schmieder Disturbance and rehabilitation of lakeside Phragmites reeds following an extreme flood in Lake Constance (Germany), Hydrobiologia, Volume 506–509 (2003), pp. 687-695

[73] R.R. Boar; C.E. Crook Investigations into the causes of reed-swamp regression in the Norfolk Broads, Verh Internat Verein Limnol, Volume 22 (1985), pp. 2916-2919

[74] W.H. van der Putten The effects of litter on the growth of Phragmites australis (W. Ostendorp; R. Krumscheid-Plankert, eds.), Seeuferzerstörung and Seeuferrenaturierung in Mitteleuropa, Limnologie Aktuell 5, 1993, pp. 19-22

[75] W.H. van der Putten; B.A.M. Peters; M.S. van den Berg Effects of litter on substrate conditions and growth of emergent macrophytes, New Phytol, Volume 135 (1997), pp. 527-537

[76] S.E.B. Weisner Within-lake patterns in depth penetration of emergent vegetation, Freshw Biol, Volume 26 (1991), pp. 133-142

[77] A.M. Barclay; R.M.M. Crawford Plant growth and survival under strict anaerobiosis, J Exp Bot, Volume 134 (1982), pp. 541-549

[78] R. Brändle Kohlehydratgehalte und Vitalität isolierter Rhizome von Phragmites australis, Schoenoplectus lacustris and Typha latifolia nach mehrwöchigem Sauerstoffmangelstress, Flora, Volume 177 (1985), pp. 317-321

[79] W.H. van der Putten Assessing ecological change in European wetlands: how to know what parameters should be monitored to evaluate the die-back of common reed (Phragmites australis)? (G. Aubrecht; G. Dick; C. Prentice, eds.), Monitoring ecological change in wetlands of middle Europe, 31, 1994, pp. 61-68

[80] A. Gaberščik; O. Urbanc-Berčič; N. Kržič; G. Kosi; A. Brancelj The intermittent Lake Cerknica: Various faces of the same ecosystem, Lakes & Reservoirs: Research and Management, Volume 8 (2003), pp. 159-168

[81] W. Granéli Influence of standing litter on shoot production in reed, Phragmites australis (Cav.) Trin. ex Steudel, Aquat Bot, Volume 35 (1989) no. 1, pp. 99-109

[82] S.E.B. Weisner; W. Granéli Influence of substrate conditions on the growth of Phragmites australis after a reduction in oxygen transport to below-ground parts, Aquat Bot, Volume 35 (1989), pp. 71-80

[83] J. Armstrong; W. Armstrong; Z. Wu; F. Afreen-Zobayed A role for phytotoxins in the Phragmites die-back syndrome?, Folia Geobot Phytotax, Volume 31 (1996), pp. 127-142

[84] S.E.B. Weisner Effects of an organic sediment on performance of young Phragmites australis clones at different water depth treatments, Hydrobiology, Volume 330 (1996), pp. 189-194

[85] J. Graveland; H. Coops Decline of reed belts in the Netherlands: causes, consequences, and a strategy for reversing the trend, Landschap, Volume 14 (1997), pp. 67-86

[86] H. Cízková; H. Brix; J. Kopecky; J. Lukavska Organic acids in the sediments of wetlands dominated by Phragmites australis: Evidence of phytotoxic concentrations, Aquat Bot, Volume 64 (1999) no. 3–4, pp. 303-315

[87] F.N. Ponnamperuma Effects of flooding on soils (T.T. Kozlowski, ed.), Flooding and Plant Growth, Academic Press, Orlando, FL, 1984, pp. 10-46

[88] H.J. Laanbroek Bacterial cycling of minerals that affect plant growth in waterlogged soils: a review, Aquat Bot, Volume 38 (1990) no. 1, pp. 109-125

[89] D.A. Wilcox The role of wetlands as nearshore habitat in Lake Huron (M. Munawar; T. Edsall; J. Leach, eds.), The Lake Huron Ecosystem: Ecology, Fisheries and Management, Ecovision World Monograph Series III, SPB Academic Publishing, Amsterdam, 1995, pp. 223-245

[90] M. Zalewski; G.A. Janauer; G. Jolankai, Ecohydrology. A new paradigm for the sustainable use of aquatic resources. International Hydrological Programme UNESCO, 7, Technical Documents in Hydrology, Paris, 1997

[91] K. Schmieder; M. Dienst; W. Ostendorp; K. Jöhnk Effects of water level variations on the dynamics of the reed belts of lake Constance, Ecohydrology & Hydrobiology, Volume 4 (2004) no. 4, pp. 229-240

[92] J. Santos Oliveira; J. Almeida Femandes; C. Alves; J. Morais; P. Urbano Metals in sediment and water of three reed (Phragmites australis (Cav.) Trin. ex Stend.) stands, Hydrobiologia, Volume 415 (1999), pp. 41-45

[93] S. Rivas-Martínez; A. Penas; T.E. Díaz Bioclimatic Map of Europe-Bioclimates. Cartographic Service, University of León, Spain, 2004

[94] S. Rivas-Martínez; A. Penas; T.E. Díaz Biogeographic Map of Europe. Cartographic Service, University of León, Spain, 2004

[95] W. Ostendorp; C. Iseli; M. Krauss; P. Krumscheid-Plankert; J.-L. Moret; M. Rollier; F. Schanz Lake shore deterioration, reed management and bank restoration in some Central European lakes, Ecological Engineering, Volume 5 (1995), pp. 51-75


Comments - Policy