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Responses of ecotypes of Phragmites australis to increased seawater influence: a field study in the Danube Delta, Romania
Aquatic Botany 64 (1999) 351–358
Responses of ecotypes of Phragmites australis to increased seawater influence: a field study in the Danube Delta, Romania Jenica Hanganu a,∗ , Gridin Mihail a , Hugo Coops b a
b
Danube Delta Institute (DDI), 165 Babadag Str., Ro-8800 Tulcea, Romania Institute for Inland Water Management and Waste Water Treatment (RIZA), P.O. Box 17, 8200 AA Lelystad, The Netherlands
Abstract The effects of locally increased salinity in a complex of Fine and Giant reed (Phragmites australis) clones were investigated in the Tataru channel (Danube Delta, Romania). Following digging of the Tataru channel, the area closest to the sea became isolated from freshwater input, causing saline conditions to develop due to its proximity to the sea. The other side of the channel remained a freshwater area. The impact of increased salinity on the regression of reed was studied and related to a possible difference in susceptibility to high salt concentrations between different clones (Octoploid Giant reed versus Tetraploid Fine reed). Measurements were made in survey plots situated on both sides of the channel. In freshwater, Giant reed had higher and thicker shoots than Fine reed, but stem density was much smaller, resulting in a lower biomass per surface area of Giant reed. Growth of both Giant and Fine reed was severely reduced at the saline east side of the channel. A significant interaction was found between reed type and salinity. Giant reed density, height, stem diameter and biomass were more strongly affected by saline conditions than Fine reed. The salinization of the parts east of the channel might thus have affected Giant reed stands more strongly than Fine reed stands. The implications for reed succession under increased salinity in the delta are discussed. ©1999 Elsevier Science B.V. All rights reserved. Keywords: Aboveground biomass; Helophytes; Salinity; Phragmites australis
1. Introduction Anthropologically-induced changes in the environment have resulted in die-back of Reed (Phragmites australis (Cav.) Trin. ex Steudel) in various locations in central Europe, while ∗ Corresponding author. Tel.: +40-40-524-546; fax: +40-40-533-547 E-mail address: [email protected] (J. Hanganu)
0304-3770/99/$ – see front matter ©1999 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 3 7 7 0 ( 9 9 ) 0 0 0 6 2 - 5
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the regression is much less obvious in northern and southern Europe (Ostendorp, 1989; van der Putten, 1997). It has been hypothesized that eutrophication leads to a reduced number of genotypes, resulting in reed stands that are susceptible to die-back. An explanation for this phenomenon could be that monoclonal stands of reed are limited in their adaptive response to changing site conditions (Neuhaus et al., 1993). Characteristics of the Danube Delta is the occurrence of octoploid and hexaploid clones of reed, apart from the common tetraploid clones. These clonal types coincide with different morphologies, called ‘Giant reed’ and ‘Fine reed’, respectively. Rodewald-Rudescu (1974) distinguished several ecotypes occurring in the Danube Delta: those of floating reedbeds consist of Giant reed, whereas Fine reed ecotypes grow on firm soil. Giant reed might respond differently to environmental change (i.e., increased salinity) compared to Fine reed. Observations made in recent years suggest that reed stands in the Danube Delta are retreating, possibly affected by eutrophication which has occurred in recent times due to increased nutrient loads discharged by the Danube river. In addition, digging of artificial channels has resulted in altered hydrological conditions in many parts of the Delta. The effects of this may be observed particularly for the parts in the Delta closest to the sea, where the salinity has increased due to channel digging in recent times. In the present study, the effects of locally increased salinity in a complex of Fine and Giant reed clones were investigated. The following two questions were addressed: (1) Is there field evidence for the impact of increased salinity on the decreased performance of reed in the Danube Delta? and (2) is there a different degree of susceptibility to a high salt concentration between clones belonging to the Giant reed and the Fine reed ecotypes?
2. Materials and methods 2.1. Study area Reed stands in the Danube Delta close to the Black Sea coast were studied. The stands were located along the Tataru channel, which was created in 1992 by cutting through a number of parallel sand-dune ridges and depressions, and runs more or less parallel to the seashore (Fig. 1). Aerial photographs and satellite images show a uniform structure of the reed stands in 1990 (before channel construction) and a sharp transition across the channel on recent images (1995). The depressions are covered with extensive stands of Phragmites australis. Following channel digging, the area to the east (between the channel and the Black Sea) became isolated from freshwater input and more saline conditions developed due to its close distance to the sea (salinity of the seawater is ca. 5 g Cl− l−1 ). The parts west of the channel are supplied with fresh water from the Danube river. At five locations in a straight (ca. 1000 m) section of Tataru channel, survey plots were selected along five transects at both sides of the channel (from south to north, referred to as Tataru 1, 1B, 1A, 2, and 3, transects subdivided in to an East and a West part) (Fig. 1). The plots west of the channel were in fresh water, the eastern plots represented saline conditions. Since the channel was cut through existing reed vegetation, comparisons within
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Fig. 1. (a) Location of transects through the reed stands along the Tataru channel near the Black Sea coast. Dune ridges and depressions are shaded differently. The position along the transects of sampling plots is indicated. Inset: location of the study site in the Danube Delta (Romania).
intersected transects could be made. On the basis of plant habitus, the transects 1A, 1B and 2 were identified as the ‘Fine reed’ type, while transects 1 and 3 were predominantly of the ‘Giant reed’ type. Determination of ploidy levels confirmed that shoots assigned to Giant reed clones were all of the octoploid type (chromosome number 8n) (except one clone at Tataru 3-West, which was tetraploid), while most Fine reed was tetraploid (4n), with the exception of the dominant clone at Tataru 2-West, which was hexaploid (6n) (O.A. Clevering, unpublished data). Shoot samples consisted of different reed clones at each site. At some sites (e.g., Tataru 2-East (n = 17), 3-West (n = 11) and 1-West (n = 5)) one genotype was clearly dominant within the sampled shoots (by representing >75% of the sample), but only in the Tataru 1-West sample were all shoots of one genotype (H. Koppitz, unpublished data). 2.2. Soil and plant sampling Twice in 1996 (31 May and 28 August) and five times in 1997 (8 April, 8 May, 18 May, 30 July, and 4 September), water depth was measured and standing or intersitial water samples were collected at the sites. TDS (total salinity, g l−1 ) was measured using a portable conductivity meter (WTW-LS-196, Germany).
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Fig. 2. Total dissolved salts (mg l-1 ) and water depth (cm) in the west (freshwater) and east (saline) part of transect 1.
A soil survey of the transects was done in May 1996. Soils were sampled using a tubular PVC corer of 10.5 cm diameter; the top horizon was sampled for laboratory analysis of pH (water extract 1 : 2.5), organic matter content (% w/w, determined by loss-on-ignition at 450◦ C), total N (Kjeldahl method), total P (perchloric digestion) and total soluble salts (sum of cations Ca, Mg, Na, K, and anions Cl, SO4 , CO3 , HCO3 ; qantitatively measured from water extract 1 : 5). Measurements of the reed stands were made at the end of the growing season (late August 1996 and early September 1997. At each transect (Fig. 2) 1 to 4 plots of 1 m × 1 m (for all Giant reed and some Fine reed plots) or 0.5 m × 0.5 m (for the other Fine reed plots) were established in which the above-ground biomass was harvested. Live shoots were separated from dead shoots and counted. For each live shoot, basal diameter of the lowest green leafy sheath, total shoot length to the highest leaf tip and number of internodes were measured. Clear evidence of insect attack (e.g. top damaged, branched) was recorded. The biomass of live shoots with panicles was measured after drying to constant weight at 80◦ C. Data were standardised for plot size of 1 m2 . The effect of channel side and ecotype were tested using a two-way analysis of variance. Differences between treatments were tested using Least Significant Differences (P < 0.05).
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Table 1 Soil characteristics (average ± s.d.) of the saline (East) and the freshwater (West) side of the Tataru channel. Data from transects of Fine reed (1A, 1B and 2) and Giant reed (1 and 3) are pooled Saline
Porewater pH Organic matter (%) N-total (%) P-total (%) Soluble salts (%)
Freshwater
Fine reed n = 8
Giant reed n = 5
Fine reed n = 9
Giant reed n = 5
6.4 ± 0.9 63.5 ± 16.1 1.62 ± 0.46 0.07 ± 0.02 1.58 ± 0.31
6.4 ± 0.6 43.0 ± 5.5 1.55 ± 0.17 0.07 ± 0.01 1.59 ± 0.32
6.4 ± 0.7 68.8 ± 12.4 1.86 ± 0.42 0.08 ± 0.02 0.83 ± 0.18
7.3 ± 0.4 29.1 ± 9.5 1.09 ± 0.25 0.09 ± 0.03 0.48 ± 0.23
3. Results 3.1. Soil The depressions were permanently flooded; the soil is organic (Histosols) consisting of peat. The presence of marine shells in the layer below 50–70 cm suggests the sandy subsoil is of marine origin. The recently formed soil layers consist of fibric peat with live Phragmites roots and rhizomes. The samples from beneath Giant reed show a relatively low organic matter content (Table 1). Different levels of soil salinity were measured between the areas west and the areas east of the channel: the west side has a moderate salinity, in the east side the soil is strongly salinised. 3.2. Salinity and water level The channel clearly formed the division between freshwater and saline conditions; on the western side, average total salinity was 0.34 g l−1 (s.d. = 0.10, n = 16, min 0.0 g l−1 , max 0.5 g l−1 ), on the eastern side, it was 11.7 g l−1 (s.d. = 4.7, n = 36, min 4.9 g l−1 , max 22.0 g l−1 ). As expected, salinity and conductivity were highly correlated (R2 = 0.931, P < 0.01, n = 50). The water level in the reed stands alongside Tataru channel fluctuated by about 1 m. High water levels were observed in spring and early summer, while the water dropped in the late summer. The fluctuations in salt concentration at the eastern side were closely related to water level (Fig. 2), resulting from the relative amount of river water present. At high water levels there was a low salt concentration of the water due to dilution with river water, while at low levels seawater was less diluted and in combination with evaporation resulted in increased salinity. 3.3. Reed growth and morphology Giant reed had higher and thicker shoots than Fine reed at the west, freshwater side of the channel, but stem density was much smaller, resulting in an overall lower biomass per surface area of Giant reed (Table 2). Reed parameters of both Giant and Fine reed were strongly reduced at the saline, eastern side of the channel, with only the number of stems
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Table 2 Mean values (± s.d.) for reed parameters of Giant and Fine reed plots in the freshwater (West) and the saline (East) transectsa Giant reed Freshwater n = 6 m−2 )
Shoot density (# Shoot height (cm) Shoot basal diameter (mm) Number of internodes (# shoot−1 ) Shoot biomass (g dry wt m−2 ) a
11 ± 5C
349 ± 33A
14.4 ± 2.2A 24.8 ± 1.5A 981 ± 707AB
Fine reed Saline n = 7
Freshwater n = 20
53 ± 37B
142 ± 38A
5.0 ± 0.7C 16.4 ± 2.9B 619 ± 492B
6.6 ± 0.9B 19.4 ± 2.6B 1632 ± 508A
127 ± 28C
237 ± 21B
Saline n = 20 174 ± 59A 163 ± 38C 4.5 ± 1.1C 17.6 ± 1.9B 1074 ± 298B
Different symbols indicate significantly different (P < 0.05) values
Table 3 Results of two-way ANOVA (F-values) for shoot density, shoot height, shoot diameter, number of internodes, and aboveground biomass of reed. Main factors are reed form (Giant vs. Fine reed, df = 1) and channel side (west = freshwater vs. east = saline, df = 1)a Reed form Channel side Form × side a
Shoot density 75.22∗∗∗ 6.69∗∗ 0.12ns
Shoot height 14.84∗∗∗ 226.10∗∗∗ 57.16∗∗∗
Shoot diameter 127.33∗∗∗ 246.41∗∗∗ 98.46∗∗∗
Number of internodes 9.10∗∗ 49.83∗∗∗ 20.87∗∗∗
Biomass 13.90∗∗∗ 9.59∗∗ 0.44ns
Significance levels: ***: P < 0.001, **: P < 0.01, ns: not significant.
significantly higher in these plots. Interaction effects were found between reed form (Fine versus Giant reed) and channel side for shoot height, diameter and internode number (Table 3 ), indicating differences in shoot response to salinity between the Fine and Giant reed ecotypes. Average shoot height and diameter were reduced more under saline conditions in Giant reed (64 and 65%, respectively) than in Fine reed (31 and 32%, respectively). No such interaction was observed for the aboveground biomass. Despite the much taller individual shoots, the aboveground biomass formed by Giant reed stands was lower than the biomass of Fine reed stands on both sides of the channel, owing to lower shoot density. In Giant and Fine reed, the biomass was reduced by 37 and 34%, respectively, at the east side of the channel relative to the west side (Table 2). Die-back within reed stands was only observed among the Fine and Giant reed near the plots at the saline side of Transect 3, close to the sea. The salinity values measured at this location however, were not significantly higher than the other sites on the east side of the channel. Notably, the rate of insect attack was in the same range for Fine and Giant reed at freshwater and saline sites.
4. Discussion Phragmites australis is known to be a highly polymorphic species (Rodewald-Rudescu, 1974). Since large variation in morphological characters is largely present within single clones, it should at least be partially attributed to environmental differences. Several authors have shown the strong impact of water depth on reed morphology and biomass development (Haslam, 1972; Yamasaki and Tange, 1981; Coops et al., 1996); while others demonstrated
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the effects of high salinity on the development of reed stands (Hellings and Gallagher, 1992; Lissner and Schierup, 1997). Our results show a low aboveground biomass of the reed at the saline parts of the transects. Rodewald-Rudescu (1974) indicates a maximum chloride content of 8 g l−1 as the salinity level at which Phragmites growth is unaffected, which is similar to the average concentration of most saline transects in our study. However, since salinity fluctuates during the year, depending on the water level, reed growing in the depressions may experience much higher salt concentrations than the average value. The stands growing at the saline side of the channel showed some evidence of salt-stress, as we observed a general increase in the number of shoots and a decreased individual shoot size. Salt-stressed reed plants are reduced in height compared to normally growing plants (Sinicrope et al., 1990). Hellings and Gallagher (1992) showed that Phragmites consumes its rhizome reserves in periods of increased salinity. Unfortunately, no shoots of identical genotype were found on both sides of the channel, implying that part of the difference between reed growth on the east and west side of the channel could have been due to genetic variation. However, this was not likely given the relatively short period of existence of the channel. Various authors (Gr. Antipa, 1943; I. Prodan, 1939; C.Z. Pantu, 1935; C.S. Antonescu, 1951; cited in Rudescu et al., 1965) have distinguished varieties of reed previously described as P. a. var. stolonifera, P. a. var. rivularis, P. a. var. flavescens, and P. a.var. gigantissima in the Danube Delta. In our study area, the morphological distinction between two forms of reed was obvious; they are referred to as Giant reed and Fine reed, respectively. Giant reed was of the octoploid type (with the exception of one sample which was a tetraploid), whereas Fine reed was either tetraploid or hexaploid (14 samples from one clone). The ploidy level does not necessarily link to the morphology of the plants, although tall reed forms growing in the floating reed beds of the Danube Delta are frequently octoploid (Gorenflot et al., 1972). Likewise, the probability of Fine reed being tetraploid or hexaploid is high. Observations in the field indicate that Giant reed and Fine reed differ in their role in the succession of floating reed beds (J. Hanganu, unpublished results), Giant reed being the ecotype of floating mats expanding into open water. In the field, separate clones within each of the two ecotypes are usually hard to identify, although a patchy occurrence of tall and fine reed might indicate the coexistence of different clones. In the Danube Delta, tetraploid and octoploid (and infertile hexaploid) clones coexist. The characteristically tall growth of octoploid reed and the widespread occurrence of octoploid clones in the Danube Delta however suggest there could be a favourable factor for the proliferation of this type. In the study area, a change of the water level has resulted in floating reedbeds becoming fixed to firm soils, which may have started the decomposition process and local reed die-back. This may explain the low organic-matter content of the soil samples from Giant reed relative to Fine reed. In areas where brackish or saline conditions occur, selective mortality might result in ecotypes with an increased salt tolerance. Our results show a significant interaction between reed type and salinity, analogously to van der Toorn (1972) who found a higher salt tolerance of the riverine ecotype relative to the peat ecotype in the Netherlands. Giant reed density, height, stem diameter and biomass were more strongly affected by saline conditions than Fine reed. The salinisation of the areas east of the channel might thus have affected Giant
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reed stands stronger than it did Fine reed stands. Though the reduced performance of reed under salinised conditions does not directly imply die-back, the role of reed in the vegetation succession of the delta may be less pronounced under such conditions. Since the vegetation succession in the littoral zone of lakes in the delta starts with the expansion of Giant reed (Rodewald-Rudescu, 1974), salinisation of water bodies in the Delta may therefore retard the colonization of open water by floating reedbeds. In close vicinity to the sea, salinity impact is great. Regular flooding with fresh water from the river seems necessary for the reed stands to survive in this environment. The effects of isolation from a freshwater resource on reed stands due to channel digging were apparent even within four years. Based on the observed differences between the two ecotypes, we expect die-back of Giant reed to continue, ultimately resulting in disappearance of Phragmites from the depressions, while the more salt tolerant Fine reed-clones may become dominant east of the channel.
Acknowledgements Olga Clevering (NIOO, the Netherlands) and Heike Koppitz (Berlin University, Germany) kindly provided data on ploidy levels and clonal diversity. Linguistic corrections were made by Liesbeth Brouwer. The research was done within the framework of the EUREED-II project, which was supported by the Environment and Climate Programme of the Commission of the European Community (Contracts No. ENV4-CT95-0147 and IC20-CT-960020). References Coops, H., van den Brink, F.W.B., Van der Velde, G., 1996. Growth and morphological responses of four helophyte species in an experimental water-depth gradient. Aquat. Bot. 54, 11–24. Gorenflot, R., Raicu, P., Cartier, D., Ciobanu, I., Stoian, V., Staicu, S., 1972. Le complexe polyploide du Phragmites communis Trin. Comptes Rendus des Seances de l’Academie des Sciences, Paris, seance du 6 mars 1972, t.274, Serie D, pp. 1501–1504. Haslam, S.M., 1972. Phragmites communis Trin., biological flora of the British Isles. J. Ecol. 60, 565–610. Hellings, S.E., Gallagher, J.L., 1992. The effects of salinity and flooding on Phragmites australis. J. Appl. Ecol. 29, 41–49. Lissner, J., Schierup, H.-H., 1997. Effects of salinity on the growth of the common reed Phragmites australis (Cav.) Trin. ex Steudel. Aquat. Bot. 55, 247–260. Neuhaus, D., Kühl, H., Kohl, J.G., Dörfel, P., Börner, T., 1993. Investigation on the genetic diversity of Phragmites stands using genomic fingerprinting. Aquat. Bot. 45, 357–364. Ostendorp, W., 1989. ’Die-back’ of reeds in Europe – a critical review of literature. Aquat. Bot. 35, 5–26. Rodewald-Rudescu, L., 1974. Das Schilfrohr, Phragmites communis Trinius. Die Binnengewässer 27, 1–302. Rudescu, L., Niculescu, C., Chivu, I.P., 1965. Monografia stufului din Delta Dunarii. (Ed.). Academiei, RSR Sinicrope, T.L., Hine, P.G., Warren, R.S., Niering, W.A., 1990. Restoration of an impounded salt marsh in New England. Estuaries 13, 25–30. van der Putten, W.H., 1997. 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. 59, 263–275. van der Toorn, J. 1972. Variability of Phragmites australis (Cav.) Trin. ex Steudel in relation to the environment. Van Zee tot Land 48. Yamasaki, S., Tange, I., 1981. Growth responses of Zizania latifolia, Phragmites australis, Phragmites australis and Miscanthus sacchariflorus to varying inundation. Aquat. Bot. 10, 229–239.
Responses of ecotypes of Phragmites australis to increased seawater influence: a field study in the Danube Delta, Romania Jenica Hanganu a,∗ , Gridin Mihail a , Hugo Coops b a
b
Danube Delta Institute (DDI), 165 Babadag Str., Ro-8800 Tulcea, Romania Institute for Inland Water Management and Waste Water Treatment (RIZA), P.O. Box 17, 8200 AA Lelystad, The Netherlands
Abstract The effects of locally increased salinity in a complex of Fine and Giant reed (Phragmites australis) clones were investigated in the Tataru channel (Danube Delta, Romania). Following digging of the Tataru channel, the area closest to the sea became isolated from freshwater input, causing saline conditions to develop due to its proximity to the sea. The other side of the channel remained a freshwater area. The impact of increased salinity on the regression of reed was studied and related to a possible difference in susceptibility to high salt concentrations between different clones (Octoploid Giant reed versus Tetraploid Fine reed). Measurements were made in survey plots situated on both sides of the channel. In freshwater, Giant reed had higher and thicker shoots than Fine reed, but stem density was much smaller, resulting in a lower biomass per surface area of Giant reed. Growth of both Giant and Fine reed was severely reduced at the saline east side of the channel. A significant interaction was found between reed type and salinity. Giant reed density, height, stem diameter and biomass were more strongly affected by saline conditions than Fine reed. The salinization of the parts east of the channel might thus have affected Giant reed stands more strongly than Fine reed stands. The implications for reed succession under increased salinity in the delta are discussed. ©1999 Elsevier Science B.V. All rights reserved. Keywords: Aboveground biomass; Helophytes; Salinity; Phragmites australis
1. Introduction Anthropologically-induced changes in the environment have resulted in die-back of Reed (Phragmites australis (Cav.) Trin. ex Steudel) in various locations in central Europe, while ∗ Corresponding author. Tel.: +40-40-524-546; fax: +40-40-533-547 E-mail address: [email protected] (J. Hanganu)
0304-3770/99/$ – see front matter ©1999 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 3 7 7 0 ( 9 9 ) 0 0 0 6 2 - 5
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the regression is much less obvious in northern and southern Europe (Ostendorp, 1989; van der Putten, 1997). It has been hypothesized that eutrophication leads to a reduced number of genotypes, resulting in reed stands that are susceptible to die-back. An explanation for this phenomenon could be that monoclonal stands of reed are limited in their adaptive response to changing site conditions (Neuhaus et al., 1993). Characteristics of the Danube Delta is the occurrence of octoploid and hexaploid clones of reed, apart from the common tetraploid clones. These clonal types coincide with different morphologies, called ‘Giant reed’ and ‘Fine reed’, respectively. Rodewald-Rudescu (1974) distinguished several ecotypes occurring in the Danube Delta: those of floating reedbeds consist of Giant reed, whereas Fine reed ecotypes grow on firm soil. Giant reed might respond differently to environmental change (i.e., increased salinity) compared to Fine reed. Observations made in recent years suggest that reed stands in the Danube Delta are retreating, possibly affected by eutrophication which has occurred in recent times due to increased nutrient loads discharged by the Danube river. In addition, digging of artificial channels has resulted in altered hydrological conditions in many parts of the Delta. The effects of this may be observed particularly for the parts in the Delta closest to the sea, where the salinity has increased due to channel digging in recent times. In the present study, the effects of locally increased salinity in a complex of Fine and Giant reed clones were investigated. The following two questions were addressed: (1) Is there field evidence for the impact of increased salinity on the decreased performance of reed in the Danube Delta? and (2) is there a different degree of susceptibility to a high salt concentration between clones belonging to the Giant reed and the Fine reed ecotypes?
2. Materials and methods 2.1. Study area Reed stands in the Danube Delta close to the Black Sea coast were studied. The stands were located along the Tataru channel, which was created in 1992 by cutting through a number of parallel sand-dune ridges and depressions, and runs more or less parallel to the seashore (Fig. 1). Aerial photographs and satellite images show a uniform structure of the reed stands in 1990 (before channel construction) and a sharp transition across the channel on recent images (1995). The depressions are covered with extensive stands of Phragmites australis. Following channel digging, the area to the east (between the channel and the Black Sea) became isolated from freshwater input and more saline conditions developed due to its close distance to the sea (salinity of the seawater is ca. 5 g Cl− l−1 ). The parts west of the channel are supplied with fresh water from the Danube river. At five locations in a straight (ca. 1000 m) section of Tataru channel, survey plots were selected along five transects at both sides of the channel (from south to north, referred to as Tataru 1, 1B, 1A, 2, and 3, transects subdivided in to an East and a West part) (Fig. 1). The plots west of the channel were in fresh water, the eastern plots represented saline conditions. Since the channel was cut through existing reed vegetation, comparisons within
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Fig. 1. (a) Location of transects through the reed stands along the Tataru channel near the Black Sea coast. Dune ridges and depressions are shaded differently. The position along the transects of sampling plots is indicated. Inset: location of the study site in the Danube Delta (Romania).
intersected transects could be made. On the basis of plant habitus, the transects 1A, 1B and 2 were identified as the ‘Fine reed’ type, while transects 1 and 3 were predominantly of the ‘Giant reed’ type. Determination of ploidy levels confirmed that shoots assigned to Giant reed clones were all of the octoploid type (chromosome number 8n) (except one clone at Tataru 3-West, which was tetraploid), while most Fine reed was tetraploid (4n), with the exception of the dominant clone at Tataru 2-West, which was hexaploid (6n) (O.A. Clevering, unpublished data). Shoot samples consisted of different reed clones at each site. At some sites (e.g., Tataru 2-East (n = 17), 3-West (n = 11) and 1-West (n = 5)) one genotype was clearly dominant within the sampled shoots (by representing >75% of the sample), but only in the Tataru 1-West sample were all shoots of one genotype (H. Koppitz, unpublished data). 2.2. Soil and plant sampling Twice in 1996 (31 May and 28 August) and five times in 1997 (8 April, 8 May, 18 May, 30 July, and 4 September), water depth was measured and standing or intersitial water samples were collected at the sites. TDS (total salinity, g l−1 ) was measured using a portable conductivity meter (WTW-LS-196, Germany).
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Fig. 2. Total dissolved salts (mg l-1 ) and water depth (cm) in the west (freshwater) and east (saline) part of transect 1.
A soil survey of the transects was done in May 1996. Soils were sampled using a tubular PVC corer of 10.5 cm diameter; the top horizon was sampled for laboratory analysis of pH (water extract 1 : 2.5), organic matter content (% w/w, determined by loss-on-ignition at 450◦ C), total N (Kjeldahl method), total P (perchloric digestion) and total soluble salts (sum of cations Ca, Mg, Na, K, and anions Cl, SO4 , CO3 , HCO3 ; qantitatively measured from water extract 1 : 5). Measurements of the reed stands were made at the end of the growing season (late August 1996 and early September 1997. At each transect (Fig. 2) 1 to 4 plots of 1 m × 1 m (for all Giant reed and some Fine reed plots) or 0.5 m × 0.5 m (for the other Fine reed plots) were established in which the above-ground biomass was harvested. Live shoots were separated from dead shoots and counted. For each live shoot, basal diameter of the lowest green leafy sheath, total shoot length to the highest leaf tip and number of internodes were measured. Clear evidence of insect attack (e.g. top damaged, branched) was recorded. The biomass of live shoots with panicles was measured after drying to constant weight at 80◦ C. Data were standardised for plot size of 1 m2 . The effect of channel side and ecotype were tested using a two-way analysis of variance. Differences between treatments were tested using Least Significant Differences (P < 0.05).
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Table 1 Soil characteristics (average ± s.d.) of the saline (East) and the freshwater (West) side of the Tataru channel. Data from transects of Fine reed (1A, 1B and 2) and Giant reed (1 and 3) are pooled Saline
Porewater pH Organic matter (%) N-total (%) P-total (%) Soluble salts (%)
Freshwater
Fine reed n = 8
Giant reed n = 5
Fine reed n = 9
Giant reed n = 5
6.4 ± 0.9 63.5 ± 16.1 1.62 ± 0.46 0.07 ± 0.02 1.58 ± 0.31
6.4 ± 0.6 43.0 ± 5.5 1.55 ± 0.17 0.07 ± 0.01 1.59 ± 0.32
6.4 ± 0.7 68.8 ± 12.4 1.86 ± 0.42 0.08 ± 0.02 0.83 ± 0.18
7.3 ± 0.4 29.1 ± 9.5 1.09 ± 0.25 0.09 ± 0.03 0.48 ± 0.23
3. Results 3.1. Soil The depressions were permanently flooded; the soil is organic (Histosols) consisting of peat. The presence of marine shells in the layer below 50–70 cm suggests the sandy subsoil is of marine origin. The recently formed soil layers consist of fibric peat with live Phragmites roots and rhizomes. The samples from beneath Giant reed show a relatively low organic matter content (Table 1). Different levels of soil salinity were measured between the areas west and the areas east of the channel: the west side has a moderate salinity, in the east side the soil is strongly salinised. 3.2. Salinity and water level The channel clearly formed the division between freshwater and saline conditions; on the western side, average total salinity was 0.34 g l−1 (s.d. = 0.10, n = 16, min 0.0 g l−1 , max 0.5 g l−1 ), on the eastern side, it was 11.7 g l−1 (s.d. = 4.7, n = 36, min 4.9 g l−1 , max 22.0 g l−1 ). As expected, salinity and conductivity were highly correlated (R2 = 0.931, P < 0.01, n = 50). The water level in the reed stands alongside Tataru channel fluctuated by about 1 m. High water levels were observed in spring and early summer, while the water dropped in the late summer. The fluctuations in salt concentration at the eastern side were closely related to water level (Fig. 2), resulting from the relative amount of river water present. At high water levels there was a low salt concentration of the water due to dilution with river water, while at low levels seawater was less diluted and in combination with evaporation resulted in increased salinity. 3.3. Reed growth and morphology Giant reed had higher and thicker shoots than Fine reed at the west, freshwater side of the channel, but stem density was much smaller, resulting in an overall lower biomass per surface area of Giant reed (Table 2). Reed parameters of both Giant and Fine reed were strongly reduced at the saline, eastern side of the channel, with only the number of stems
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Table 2 Mean values (± s.d.) for reed parameters of Giant and Fine reed plots in the freshwater (West) and the saline (East) transectsa Giant reed Freshwater n = 6 m−2 )
Shoot density (# Shoot height (cm) Shoot basal diameter (mm) Number of internodes (# shoot−1 ) Shoot biomass (g dry wt m−2 ) a
11 ± 5C
349 ± 33A
14.4 ± 2.2A 24.8 ± 1.5A 981 ± 707AB
Fine reed Saline n = 7
Freshwater n = 20
53 ± 37B
142 ± 38A
5.0 ± 0.7C 16.4 ± 2.9B 619 ± 492B
6.6 ± 0.9B 19.4 ± 2.6B 1632 ± 508A
127 ± 28C
237 ± 21B
Saline n = 20 174 ± 59A 163 ± 38C 4.5 ± 1.1C 17.6 ± 1.9B 1074 ± 298B
Different symbols indicate significantly different (P < 0.05) values
Table 3 Results of two-way ANOVA (F-values) for shoot density, shoot height, shoot diameter, number of internodes, and aboveground biomass of reed. Main factors are reed form (Giant vs. Fine reed, df = 1) and channel side (west = freshwater vs. east = saline, df = 1)a Reed form Channel side Form × side a
Shoot density 75.22∗∗∗ 6.69∗∗ 0.12ns
Shoot height 14.84∗∗∗ 226.10∗∗∗ 57.16∗∗∗
Shoot diameter 127.33∗∗∗ 246.41∗∗∗ 98.46∗∗∗
Number of internodes 9.10∗∗ 49.83∗∗∗ 20.87∗∗∗
Biomass 13.90∗∗∗ 9.59∗∗ 0.44ns
Significance levels: ***: P < 0.001, **: P < 0.01, ns: not significant.
significantly higher in these plots. Interaction effects were found between reed form (Fine versus Giant reed) and channel side for shoot height, diameter and internode number (Table 3 ), indicating differences in shoot response to salinity between the Fine and Giant reed ecotypes. Average shoot height and diameter were reduced more under saline conditions in Giant reed (64 and 65%, respectively) than in Fine reed (31 and 32%, respectively). No such interaction was observed for the aboveground biomass. Despite the much taller individual shoots, the aboveground biomass formed by Giant reed stands was lower than the biomass of Fine reed stands on both sides of the channel, owing to lower shoot density. In Giant and Fine reed, the biomass was reduced by 37 and 34%, respectively, at the east side of the channel relative to the west side (Table 2). Die-back within reed stands was only observed among the Fine and Giant reed near the plots at the saline side of Transect 3, close to the sea. The salinity values measured at this location however, were not significantly higher than the other sites on the east side of the channel. Notably, the rate of insect attack was in the same range for Fine and Giant reed at freshwater and saline sites.
4. Discussion Phragmites australis is known to be a highly polymorphic species (Rodewald-Rudescu, 1974). Since large variation in morphological characters is largely present within single clones, it should at least be partially attributed to environmental differences. Several authors have shown the strong impact of water depth on reed morphology and biomass development (Haslam, 1972; Yamasaki and Tange, 1981; Coops et al., 1996); while others demonstrated
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the effects of high salinity on the development of reed stands (Hellings and Gallagher, 1992; Lissner and Schierup, 1997). Our results show a low aboveground biomass of the reed at the saline parts of the transects. Rodewald-Rudescu (1974) indicates a maximum chloride content of 8 g l−1 as the salinity level at which Phragmites growth is unaffected, which is similar to the average concentration of most saline transects in our study. However, since salinity fluctuates during the year, depending on the water level, reed growing in the depressions may experience much higher salt concentrations than the average value. The stands growing at the saline side of the channel showed some evidence of salt-stress, as we observed a general increase in the number of shoots and a decreased individual shoot size. Salt-stressed reed plants are reduced in height compared to normally growing plants (Sinicrope et al., 1990). Hellings and Gallagher (1992) showed that Phragmites consumes its rhizome reserves in periods of increased salinity. Unfortunately, no shoots of identical genotype were found on both sides of the channel, implying that part of the difference between reed growth on the east and west side of the channel could have been due to genetic variation. However, this was not likely given the relatively short period of existence of the channel. Various authors (Gr. Antipa, 1943; I. Prodan, 1939; C.Z. Pantu, 1935; C.S. Antonescu, 1951; cited in Rudescu et al., 1965) have distinguished varieties of reed previously described as P. a. var. stolonifera, P. a. var. rivularis, P. a. var. flavescens, and P. a.var. gigantissima in the Danube Delta. In our study area, the morphological distinction between two forms of reed was obvious; they are referred to as Giant reed and Fine reed, respectively. Giant reed was of the octoploid type (with the exception of one sample which was a tetraploid), whereas Fine reed was either tetraploid or hexaploid (14 samples from one clone). The ploidy level does not necessarily link to the morphology of the plants, although tall reed forms growing in the floating reed beds of the Danube Delta are frequently octoploid (Gorenflot et al., 1972). Likewise, the probability of Fine reed being tetraploid or hexaploid is high. Observations in the field indicate that Giant reed and Fine reed differ in their role in the succession of floating reed beds (J. Hanganu, unpublished results), Giant reed being the ecotype of floating mats expanding into open water. In the field, separate clones within each of the two ecotypes are usually hard to identify, although a patchy occurrence of tall and fine reed might indicate the coexistence of different clones. In the Danube Delta, tetraploid and octoploid (and infertile hexaploid) clones coexist. The characteristically tall growth of octoploid reed and the widespread occurrence of octoploid clones in the Danube Delta however suggest there could be a favourable factor for the proliferation of this type. In the study area, a change of the water level has resulted in floating reedbeds becoming fixed to firm soils, which may have started the decomposition process and local reed die-back. This may explain the low organic-matter content of the soil samples from Giant reed relative to Fine reed. In areas where brackish or saline conditions occur, selective mortality might result in ecotypes with an increased salt tolerance. Our results show a significant interaction between reed type and salinity, analogously to van der Toorn (1972) who found a higher salt tolerance of the riverine ecotype relative to the peat ecotype in the Netherlands. Giant reed density, height, stem diameter and biomass were more strongly affected by saline conditions than Fine reed. The salinisation of the areas east of the channel might thus have affected Giant
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reed stands stronger than it did Fine reed stands. Though the reduced performance of reed under salinised conditions does not directly imply die-back, the role of reed in the vegetation succession of the delta may be less pronounced under such conditions. Since the vegetation succession in the littoral zone of lakes in the delta starts with the expansion of Giant reed (Rodewald-Rudescu, 1974), salinisation of water bodies in the Delta may therefore retard the colonization of open water by floating reedbeds. In close vicinity to the sea, salinity impact is great. Regular flooding with fresh water from the river seems necessary for the reed stands to survive in this environment. The effects of isolation from a freshwater resource on reed stands due to channel digging were apparent even within four years. Based on the observed differences between the two ecotypes, we expect die-back of Giant reed to continue, ultimately resulting in disappearance of Phragmites from the depressions, while the more salt tolerant Fine reed-clones may become dominant east of the channel.
Acknowledgements Olga Clevering (NIOO, the Netherlands) and Heike Koppitz (Berlin University, Germany) kindly provided data on ploidy levels and clonal diversity. Linguistic corrections were made by Liesbeth Brouwer. The research was done within the framework of the EUREED-II project, which was supported by the Environment and Climate Programme of the Commission of the European Community (Contracts No. ENV4-CT95-0147 and IC20-CT-960020). References Coops, H., van den Brink, F.W.B., Van der Velde, G., 1996. Growth and morphological responses of four helophyte species in an experimental water-depth gradient. Aquat. Bot. 54, 11–24. Gorenflot, R., Raicu, P., Cartier, D., Ciobanu, I., Stoian, V., Staicu, S., 1972. Le complexe polyploide du Phragmites communis Trin. Comptes Rendus des Seances de l’Academie des Sciences, Paris, seance du 6 mars 1972, t.274, Serie D, pp. 1501–1504. Haslam, S.M., 1972. Phragmites communis Trin., biological flora of the British Isles. J. Ecol. 60, 565–610. Hellings, S.E., Gallagher, J.L., 1992. The effects of salinity and flooding on Phragmites australis. J. Appl. Ecol. 29, 41–49. Lissner, J., Schierup, H.-H., 1997. Effects of salinity on the growth of the common reed Phragmites australis (Cav.) Trin. ex Steudel. Aquat. Bot. 55, 247–260. Neuhaus, D., Kühl, H., Kohl, J.G., Dörfel, P., Börner, T., 1993. Investigation on the genetic diversity of Phragmites stands using genomic fingerprinting. Aquat. Bot. 45, 357–364. Ostendorp, W., 1989. ’Die-back’ of reeds in Europe – a critical review of literature. Aquat. Bot. 35, 5–26. Rodewald-Rudescu, L., 1974. Das Schilfrohr, Phragmites communis Trinius. Die Binnengewässer 27, 1–302. Rudescu, L., Niculescu, C., Chivu, I.P., 1965. Monografia stufului din Delta Dunarii. (Ed.). Academiei, RSR Sinicrope, T.L., Hine, P.G., Warren, R.S., Niering, W.A., 1990. Restoration of an impounded salt marsh in New England. Estuaries 13, 25–30. van der Putten, W.H., 1997. 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. 59, 263–275. van der Toorn, J. 1972. Variability of Phragmites australis (Cav.) Trin. ex Steudel in relation to the environment. Van Zee tot Land 48. Yamasaki, S., Tange, I., 1981. Growth responses of Zizania latifolia, Phragmites australis, Phragmites australis and Miscanthus sacchariflorus to varying inundation. Aquat. Bot. 10, 229–239.