Hydrobiologia 506–509: 625–634, 2003. © 2003 Kluwer Academic Publishers. Printed in the Netherlands.
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Long-term changes of submerged macrophytes in the Lower Danube Wetland System Sergiu Cristofor1 , Angheluta Vadineanu2 , Anca Sarbu3 , Carmen Postolache2 , Roxana Dobre2 & Mihai Adamescu2 1 Bucharest University,
Braila Ecological Research Station, Ciprian Porumbescu 4, RO-6100, Braila, Romania E-mail:
[email protected];
[email protected] 2 Bucharest University, Department of System Ecology, Spl. Independentei 91-95, RO-76201, Bucharest 5, Romania 3 Bucharest University, Department of Botany, Aleea Portocalelor 1-3, RO-77206, Bucharest 5, Romania Key words: biomass production, eutrophication, shallow lakes, space distribution, species richness, wetlands
Abstract Transition towards hypertrophy has affected biodiversity and productivity of most aquatic and wetland systems in the Lower Danube Wetland System (LDWS) over the last two decades. The aquatic macrophytes have been deeply involved in ecosystem reorganization in these circumstances. Representative shallow lakes and channels located in the river floodplain and delta were studied in this period in terms of space distribution, diversity, species composition, primary production and main hydrogeomorphic features (morphometrical and physico-chemical parameters). Changes in submerged vegetation dynamics along two successive decades after 1980 included diminishing areas of about 50% in the Danube Delta, restructuring primary producers by suppressing aquatic weed in some lakes or parts of lakes and decreasing species richness to few populations with upright and floating growth strategy. Biomass production showed different trends, from severe reduction in some lakes and periods to marked increase in other ones, provided by a changed and simplified species structure, generally dominated by Ceratophyllum demersum L. and Potamogeton species. It was concluded that the eutrophication effects are maintaining, modulated by diverse response mechanisms developed by submerged macrophytes. Finally, the main lessons to be learned for the management of aquatic macrophyte-dominated systems in the framework of redesigning the LDWS structures are emphasized on the basis of a large scale and long-term prospect of the Danube River and Black Sea Basins.
Introduction Aquatic and wetland ecosystems dominated by aquatic macrophytes are important components of the floodplain and delta landscapes in the Lower Danube Wetland System (LDWS): about 40% of the remaining natural floodplain and about 70% of the Danube Delta are water dominated surfaces. Structural and functional changes have occurred in the LDWS in the last decades, including drainage of about 80% of the former floodplain and of about 15% of the delta, decrease in sediment transport capacity to about 45% and of flood attenuation capacity of about 4.5 km3 as well as changes of water and sediment chemistry caused mainly by fast eutrophication and also by heavy metal and pesticide contamination. These changes have af-
fected not only the biodiversity and productivity of the aquatic and wetland systems themselves but also their role in maintaining the biodiversity and productivity of the entire LDWS (Rî¸snoveanu & Vˇadineau, 2003; Vadineanu et al., 1998). Different and often contradictory scenarios have been proposed in recent years to control and to recover the ecological state of specific aquatic systems of the LDWS, many of them directly or indirectly addressed to the macrophytes (Godeanu & Godeanu, 1998). Recent attempts to assess the functional role of the biodiversity of LDWS ecosystems emphasized the effects of declining wetland surface (from 60 to 33%) and of the aquatic plant biomass (48% to 17% from total herbaceous biomass) on river water quality and fish productivity (Vadineanu et al., 1992; Sarbu et al., 1996; Cristofor et al., 1997, 1998).
626 Based on an overview of the research programmes carried out in the last two decades, this paper presents from a long-term perspective the significance of the structural and functional changes in the aquatic vegetation dynamics for the trophic state of the LDWS as well as of the involved specific mechanisms for wetland management.
Description of sites studied The Lower Danube River System (LDRS) is 1080 km long on the Romanian territory and receives the water from the lower drainage area of 218 660 km2 , from which 90% cover the Romanian surface (Vadineanu et al., 1998). It includes the lower Danube floodplain, one of the largest and complex system of river margins in Europe (780 km length and 6–30 km width) and the Danube Delta, one of the most important wetland area (4152 km2 surface area). Three main large hydrogeomorphic units (HGMUs) form the floodplain: (1) upper floodplain between Calafat and Calarasi of 2220 km2; (2) middle floodplain or inner delta between Calarasi and Braila of 2413 km2 ; and (3) lower floodplain between Braila and Tulcea of 701 km2 . From the entire morphological floodplain surface of 6000 km2, 20% remained actually in natural regime: zone between river margins and digs (around 100–300 m width) and a series of more 47 alluvial isles. The most important remnant of the former inner delta is the Small Island of Braila (170 km2 ). The Danube Delta includes the following large HGMUs: (4) coastal delta between the three arms of 2570 km2 ; (5) Dranov floodplain of 876 km2 ; connecting the river with (6) a large complex of lagoon lakes, Razim-Sinoe, of 1015 km2 ; and (7) secondary Chilia Delta, of 732 km2 , under Ukrainian administration (Vadineanu & Cristofor, 1994; Vadineanu et al., 2001). The Danube Delta is a large protected area including also a part of the upstream river as well as the Black Sea littoral (totally 5800 km2 ) and has a triple legal status, of Biosphere Reserve, World Heritage Site and Ramsar Site. The Small Island of Braila is declared natural reserve and is also a Ramsar Site. Preserving still a high grade of natural systems, both sites are exceptionally important for a series of ecological values: species diversity (1688 plant species and 3800 animal species, including 300 bird species), landscape diversity (heterogeneous and dy-
namic complex of ecosystems of various types and in different succession stages as shallow lakes, channels, Phragmites and Typha wetlands, levees, sand dunes, oak, alder, willow and poplar forests, pastures). Other values refer to the productive potential (providing renewable resources like fish, reed, wood, livestock, etc.), buffer capacity, tourist potential, contribution to regional and global climate control as well as to hydrological and biogeochemical cycling, feeding, nesting and spawning habitats for migratory birds and fish and natural laboratory for science. Large surfaces of aquatic weed-dominated systems cover both areas. The mean values of the depths and the surface areas of these lakes are presented in the following list: L. Rosu: 2.61 m; 1445 ha; L. Puiu: 2.70 m; 865 ha; L. Matita: 2.39 m; 652 ha; L. Merhei: 1.67 m; 1057 ha; L. Isac: 2.00 m; L. Babina: 1.79 m; 432 ha; L. Bogdaproste: 1.43 m; 435 ha; L. Baclanesti: 1.39 m; 241 ha.
Materials and methods Two sets of selected data resulted from intensive and extensive research programmes developed and implemented in two large representative landscapes of the LDRS, the Danube Delta (1980–1988) and the Small Island Braila, were compared. The long term changes in dynamics of the aquatic vegetation from 11 shallow lakes and three channels located in these landscapes were assessed in terms of biomass production and species richness and diversity. Collection of data and samples was made in the framework of the large research programmes aimed at understanding the mechanisms of biological productivity of the Danube Delta and Floodplain, based on a joint sampling schedule for all pelagic and benthic compartments (phyto-, zoo-, and bacterio-plankton, zoobenthos, phytofilous fauna, etc.; see Rîcsnoveanu & Vˇadineanu, 2003). The specific sampling schedule for aquatic vegetation included monthly collection of 9–15 sampling units (3–5 replicates of 0.16 m2 ) in each lake as well as determinations of hydrogeomorphic features (depth, Secchi depth, light extinction coefficient, temperature, pH, nutrient concentration). Selected plant material was dried for 3 h at 105 ◦ C. Mean values of production per lakes were determined by the biomass increase method (Westlake, 1969). Species diagnosis is in accordance with the Romanian Flora (‘Flora RSR’).
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Figure 1. Dynamics of submerged vegetation areas in the Danube Delta between 1975 and 1994, in terms of: (a) Surface area (ha) and (b) Percentage of lake types: 1. dominated by submerged vegetation, 2. lakes in which primary production is based on both phytoplankton and aquatic weed and 3. lakes dominated by phytoplankton.
Results Space distribution Submerged vegetation was the dominant primary producer in most shallow lakes of the Danube Delta and Floodplain a long period before the 1980, mainly comprising populations of Chara fragilis Desv, Nitellopsis obtusa (Desv. In Lois) J. Gr., Najas marina L., Ceratophyllum demersum L., Potamogeton pectinatus L., P. trichoides L., P. crispus L., Vallisneria spiralis L. and Stratiotes aloides L. Their areas reduced gradually towards extinction in some lakes of the Danube Delta (Rosu, Puiu, Babina and Uzlina Lakes) in the period 1982–1989. After 1990, many of these lakes recovered their aquatic weed, but in a changed structural formula. A comparison of nine different representative lakes of the Danube Delta (Rosu, Puiu, Isac, Uzlina, Matita,
Merhei, Babina, Bogdaproste and Baclanesti Lakes) showed a reduction of aquatic vegetation areas from 6071 ha in 1980 to 3266 ha in 1982 and only 676 ha in 1987 (Fig. 1.). A relative tendency of repopulation after 1989 resulted in their area recovering to 2209 ha. A detailed mapping of aquatic vegetation was performed in three consecutive years (1980–1982) in the complex of lakes Matita–Merhei and in the lakes Bogdaproste and Baclanesti. In a very limited period, changes in space distribution were accompanied by restructuring of primary producers through replacing submerged macrophytes by phytoplankton. The algal blooms extended in time and space from the second part of the growing season of the year 1981. In 1982, the submerged macrophytes, very well developed in the previous years, were drastically suppressed. They completely disappeared in L. Matita and became represented by only three populations (Potamogeton pectinatus, Nitellopsis obtusa and Ceratophyllum demersum) on restricted/limited surfaces (towards the western end of L. Merhei) and periods (early summer) (Fig. 2). The lake Bogdaproste, generally totally covered by aquatic weed all the growth season, showed periodically marked differentiations in distribution of submerged macrophytes (Fig. 3). Only about half of the lake remained covered by submerged vegetation, the algal blooms suppressing them in the rest of the lake surface. The total disappearance of aquatic weed was recorded in summer 1994 in L. Baclanesti, a lake located in the Northern flowing water corridor entering the Danube Delta. In this season, the aquatic weed was missing in spite of light and nutrient regimes not being limited. The distribution of submerged vegetation in the water column showed also large dynamics. An example is presented also for the lake Bogdaproste, in which the presence of submerged macrophytes in deeper horizons or in the whole water column was associated with non-limiting light conditions (relative transparency coefficient over 40%, as it was defined by Botnariuc & Beldescu, 1961). The dominance of the plants with upright growth or floating strategy or their presence as floating individuals was associated with light conditions caused by algal blooms. Species diversity and structure The changes in space distribution of submerged macrophytes are associated with important changes in their
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Figure 2. Dynamics of space distribution of submerged macrophytes in Merhei Lake (the Danube Delta) between 1980 and 1982.
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Figure 3. Dynamics of space distribution of aquatic weed and algal blooms in Bogdaproste Lake (the Danube Delta) in selected periods during 1984–1988.
Figure 4. The main characteristics of the Danube Delta and Floodplain Lakes expressed in terms of productivity (g dw m−2 ), species richness, water depth (m) and the ratio of Secchi Depth: Depth between 1980 and 1994 (yearly mean values).
630 species structure (Fig. 4). The most important changes included: (i) replacement of the populations able to utilize the benthic or pelagic nutrient pools (i.e. Najas marina and Nitellopsis obtusa) by populations with vertical growth (Potamogeton sp., Ceratophyllum demersum, filamentous macro algae); (ii) increase of the species turnover resulting in high productive growth season (L. Bogdaproste and L. Baclanesti); (iii) reduction of species diversity from 40 species in 1970 (Flora RSR, 1952–1972) to 28 species (Ciocarlan, 1994).
demersum and Nitellopsis obtusa, 94% by C. demersum and filamentous algae in 1987 or 96% by C. demersum, Potamogeton sp. and filamentous algae in 1992. In 1993–1994, N. obtusa became again the dominant species, providing together with C. demersum and Potamogeton sp. 89–94% of the total production of 426–770 g dw m−2 .
Biomass production
Some remarks are useful to be underlined for the following discussions: (i) the important changes affecting the structure and functioning of these populations became obvious after 1980 as a result of a general accelerated eutrophication in the Lower Danube Wetland System; (ii) these changes occurred on the background of high biological productivity and diversity specific to a previous long period of natural meso-eutrophic state (1950–1970). The lakes of the floodplain zone differed from the lakes of the delta by both species richness and dominance (21 species in Delta, from which 11 species were dominant, and 18 species in floodplain, with only five dominant species), but similar dynamics trajectories could be distinguished (mainly from phytoplankton to macrophytes dominated lakes states). The recorded fluctuation domain of the biomass production, usually equivalent to about 100–3500 kcal m−2 , is similar to the values reported for the previous reference period by Andrei (1971), Botnariuc et al. (1968) and Botnariuc & Vadineanu (1982) for the Danube Delta and floodplain lakes as well as to the production reported by Gopal (1973) for the subtropical lakes, as the most productive lakes in the world. On the whole, three different trajectories could be distinguished in the dynamics of submerged macrophytes in the Danube Delta in the period 1980–1986 (Cristofor, 1986, 1987; Vadineanu et al., 1992): (i) qualitative (species turnover) and quantitative (species richness decline) changes of species structure associated with the maintenance or even increasing overall biomass production, (ii) decrease of species diversity and productivity on an extinction trajectory, and (iii) total loss of submerged macrophytes. The fact that in the following decade the submerged vegetation has been recovered in some lakes based on a changed structural formula does not support the hypothesis of a relative inhibition of the eutrophication symptoms as a result of reduction of
For the whole assemblage of studied lakes, the biomass production fluctuated from a few grams to over 790 g dw m−2 . Biomass dynamics was also very different (Fig. 5). For example, in L. Merhei the total yearly biomass production decreased from 281–493 g dw m−2 in the period 1980–1981 to 20–70 g dw m−2 in the following period. Similar dynamics were presented for the dominant population Potamogeton pectinatus in L. Isac, but its biomass production increased again to 130– 410 g dw m−2 after 1990. A different evolution of biomass production was shown by lakes Bogdaproste and Baclanesti, where this increased from 100–175 g dw m−2 in 1982 to 700–795 g dw m−2 in the following period. After a period of complete disappearance of submerged macrophytes in some lakes (i.e., L. Rosu during 1984–1990, L. Merhei and L. Babina during 1986–1990), a tendency of recovery of biomass production occurred, usually at low and moderate levels (20–50 g dw m−2 ) or even at higher levels (330 g dw m−2 in L. Merhei 1994). Few species contributed to the biomass production, one, two or three species producing more than 90% of the total production. For instance, in L. Merhei, 91% of the total production of 280 g dw m−2 was provided by three populations (Ceratophyllum demersum, Nitellopsis obtusa and filamentous algae) in 1980, and 92% of total production of 339 g dw m−2 were provided by only one population of Potamogeton pectinatus in 1993. In L. Isac, between 95 and 100% of total biomass were produced during 1991–1994 by Potamogeton sp. and filamentous algae. In L. Bogdaproste, the fluctuations of the biomass production were larger, with the total yearly production varying between 90 and 770 g dw m−2 . Between 80% and 95% of total biomass were produced during 1982–1985 by Ceratophyllum
Discussions
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Figure 5. Dynamics of species structure and biomass production (g dw m−2 ) of aquatic weed in three selected lakes of the Danube Delta between 1980 and 1994.
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Figure 6. Dynamics of submerged macrophytes standing crop (shadow area) and species richness (curve line) in selected lakes and channels of the Danube Delta and Floodplain (mean values/growth season for period 1991–1995).
nutrients entering the system after 1990. This is rather an alternative answer to a running eutrophication process, by which the submerged weeds contribute to ecosystem strategy for maximizing energy flow in the changed conditions of hypertrophic systems. In this case, the macrophyte productivity became higher by increasing dominance of a few populations able to access and to use efficiently the light energy on the background of deterioration of transparency, pH,
dissolved gases and toxicity conditions (Sarbu et al., 1999). The above-presented comparative study shows a non-linear long-term evolution of aquatic weeds, frequently changing their state transition and leading to differentiation in space and time of three macrophyte dynamics trajectories identified before (Vadineanu et al., 1992; Sarbu et al., 1996) between macrophytes and phytoplankton dominated states. These states coex-
633 ists in different lakes of the Danube Delta or alternate along the vegetation season in the lakes of the Small Island of Braila and some lakes of the Danube Delta on the background of a dominant transition towards the algal blooming states. The mechanisms by which the aquatic weeds have responded to the eutrophication process have been differently initiated in connection with the specific features of the lakes, especially with morphometry, river connectivity and permeability for external driving forces (mainly hydrologic and nutrients regime). The inter-specific competition played an important regulating role and included different forms: (i) the competition for light replaced gradually the competition for nutrients as the main regulating mechanism; in such circumstances, the populations with an upright and floating growth strategy (i.e. Potamogeton sp., Ceratophyllum demersum etc.), became dominant; (ii) competition for the respiratory gases and especially for the inorganic carbon became frequently involved in the aquatic weed answer to worsening pH and oxygen conditions; (iii) different tolerance for the toxic effect of high nutrient concentrations as well as of some metabolic products; (iv) allelopathic relationships extremely varying from self and hetero-inhibition to self and hetero-stimulation; (v) competition for colonization and efficiency of reproduction strategies.
Conclusions The main changes in the submerged vegetation dynamics along the successive two decades included changes in spatial distribution, mainly by diminishing areas as well as qualitative and quantitative changes of species richness, species dominance and biomass production. These changes induced important alteration of both the energy entering the aquatic system through the trophodynamic modules of primary producers and the phytophagous and detritophagous transfer of energy towards the successive trophodynamic modules. A general trend of deterioration of aquatic vegetation was recorded for most lakes of the Danube Delta during 1980–1989 in terms of space distribution, species richness and community structure as well as in biomass production. The relative tendency for aquatic vegetation to recover in some lakes was based on a changed structural formula and was not accompanied by recovery of water quality or suppression of blue-green algal blooms.
About 28% of the species identified in the 1980s were replaced by species of Potamogeton Submerged macrophyte transition trajectories are not linear they involve frequent reversible transitions modulated by the hydrological and nutrient regime of the river. On this very complex background, the maintenance of high trophic conditions could be confirmed for the recent period. A large and diverse range of response mechanisms of submerged macrophytes contributed to the transition of different shallow lakes (or even parts of them) through diverse domains of eutrophic or even hypertrophic states. Management alternatives have to be based on a proper knowledge of the significance of long-term dynamics in shallow lake ecosystems integrated in a large and complex water dominated landscape like LDWS. Submerged macrophytes are a major compartment to be considered in monitoring and research activities as well as to be addressed specifically by measures to control eutrophication at the large scale and long-term prospects of the Danube River and Black Sea catchments.
Acknowledgements We thank our colleagues for their direct or indirect contribution to this paper. Research support was provided the Romania National Council for the University Scientific Research in the framework of the World Bank co-financed research programme CNCSIS- C89/2000 “The Ecological Network for Lower Danube System”.
References Andrei, M., 1971. La production première de quelques aux associations de macrophytes aquatiques du complexe des lacs Crapina-Jijila (Dobroudja). Revue Roumaine de Biologie Série de Botanique 16: 335–339. Botnariuc, N., & S. Beldescu, 1961. Monograph of the lake complex Crapina–Jijila. I. Fiziografie. Hidrobiologia (Bucuresti) 11: 161– 242. Botnariuc, N., O. Boldor & R. Stanescu, 1968. Dependence of the variation of primary production in the Danube flood valley on floods and embankments. Hidrobiologia (Bucharest) 9: 63–74. Botnariuc, N. & A. Vadineanu, 1982. Ecologie (Ecology). Ed. did. si pedag., Bucharest: 440 pp. Ciocarlan, V., 1994. Flora Deltei Dunarii (Flora of the Danube Delta). Edited Ceres (Bucuresti): 115 pp. Cristofor, S., 1986. Tendencies in structure and production of submerged macrophyte communities of the Danube Delta, between 1980 and 1983. Hydrobiologia 19: 113–118.
634 Cristofor, S., 1987. L’évolution de l’état trophique des écosystèmes aquatiques caractéristiques du Delta du Danube. 6. Réponses de la végétation submerse en fonction de la réserve de nutriments et du régime hydrologique. Revue Roumaine de Biologie, Biologie de Animale (Bucarest) 32: 129–138. Cristofor, S., A. Sarbu, A. Vadineanu, G. Ignat, V. Iordache, C. Postolache, C. Dinu & C. Ciubuc, 1997. Effects of hydrological regimes on riparian vegetation in the Lower Danube Floodplain. Proc. 32. Konferenz der IAD, Wien, Osterreich: 233–236. Cristofor, S., A. Sarbu, A. Vadineanu, O. Ciolpan, G. Ignat & C. Ciubuc, 1998. Photosynthetic and respiratory answers of submerged macrophytes to eutrophication of the Danube Delta lakes. Proc. Danube Delta Research Institute, Tulcea: 279–288. Gopal, B., 1973. A survey of the Indian studies on ecology and production of wetland and shallow communities. Polish Archives of Hydrobiology (Warszawa) 20: 21–29. Godeanu, S. & M. Godeanu, 1998. Attempts at lake eutrophication control using competition between aquatic microphytes and macrophytes. In Farina, A., J. Kennedy & V. Bossu (eds), Proceedings of the INTECOL VII International Congress of Ecology. Florence, 19–25 July 1998/Italy: 161 pp. Rî¸snoveau, G. & A. Vˇadineanu, 2003. Long term functional changes within the oligochaeta communities within the Danube River Delta, Romania. Hydrobiologia 506–509: 399–405. Sarbu, A., S. Cristofor, A. Vadineanu & C. Dinu, 1996. Structure and dynamics of submerged vegetation in the Danube Delta between 1991–1995. Analele Sti. Inst. Delta Dunarii, Tulcea 5: 201–210.
Sarbu, A., A. Vadineanu & S. Cristofor, 1999. Invasive behavior of highly competitive submerged macrophytes in eutrophic conditions. Revue Roumaine de Biologie, Biologie de Végétale (Bucharest) 44: 117–127. Vadineanu, A., S. Cristofor & G. Ignat, 1992. Phytoplankton and submerged macrophytes in the aquatic ecosystems of the Danube Delta during the last decade. Hydrobiologia 243/244: 141–146. Vadineanu, A.& S. Cristofor, 1994. Basic requirements for assessment and management of large international water systems: Danube Delta/Black Sea. Proceedings International Workshop Monitoring Tailor-mads 20–23 Sept. 1994, Beekbergen, The Netherlands: 71–81. Vadineanu, A., S. Cristofor, A. Sarbu, G. Romanca, G. Ignat, N. Botnariuc & C. Ciubuc, 1998. Biodiversity changes along the Lower Danube River System. International Scientific publications, New Delhi. Int. J. Ecol. Environ. Sci. 24: 315–332. Vadineanu, A., S. Cristofor & V. Iordache, 2001. Biodiversity changes in the Lower Danube River System. In Gopal, B., W. J. Junk & J. A. Davis (eds), Biodiversity in Wetlands: Assessment, Function and Conservation, volume 2. Backhuys Publishers, Leiden, The Netherlands: 29–63. Westlake, D. F., 1969. 2.2. Macrophytes. In Vollenweider, R. A. (ed.), A Manual on Methods for Measuring Primary Production in Aquatic Environments, IBP Handbook. Blackwell Sci. Publ. Oxford. 12: 25–32.
