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Cent. Eur. J. Biol. • 4(2) • 2009 • 250–257 DOI: 10.2478/s11535-009-0013-5 Central European Journal of Biology Primary production dynamics of dominant hydrophytes in Lake Provala (Serbia) Research Article Ljiljana Nikolić1*, Slobodanka Pajević2, Branka Ljevnaić1 University of Novi Sad, Faculty of Agriculture, 21 000 Novi Sad, Serbia 1 University of Novi Sad, Faculty of Sciences and Mathematics, 21000 Novi Sad, Serbia 2 Received 12 November 2008; Accepted 11 February 2009 Abstract: The objective of this investigation was to analyze the primary production of the dominant hydrophytes by monitoring levels of organic matter and organic carbon and estimating photosynthetic potential via the total chlorophyll content. The survey was conducted in Lake Provala (Serbia) throughout the peak vegetation period of the year 2000. The contents of organic matter and organic carbon for Myriophyllum spicatum L. were 105.11 g m-2 and 73.66 g m-2, Nymphoides peltata (Gmel.) Kunt. were 95.51 g m-2 and 45.26 g m-2 and Ceratophyllum demersum L. were 52.17 g m-2 and 29.75 g m-2. Chlorophyll A (Chl a) and chlorophyll A+B (Chl a+b) pigments ranged from 1.54 mg g-1(Chl a) and 2.1 mg g-1(Chl a+b) in M. spicatum to 5.27 mg g-1(Chl a) and 7.53 mg g-1(Chl a+b) in C. demersum. At full leaf out, the latter aquatic plants exceeded 50% cover of the open water surface. All species achieved maximum growth in June, but significant differences in growth dynamics were observed. At the end of the vegetation period, these plants sink to the bottom and decompose Keywords: Aquatic macrophytes • Organic matter • Organic C • Chlorophyll © Versita Warsaw and Springer-Verlag Berlin Heidelberg. 1. Introduction Macrophytic type aquatic ecosystems are dominated by various aquatic vascular plant species which play an important role in the structure and function of these ecosystems [1]. Aquatic vascular macrophytes are adapted to living under certain aquatic conditions and their occurrence and distribution depend on an array of factors. These factors include water depth, transparency, regime, chemical composition, pH and salinity [2-11]. Sediment composition and properties are also important for the presence of certain macrophytic species in aquatic ecosystems [12-15]. The presence of macrophytes in aquatic biotopes have multiple impacts not only on the local biota but also on the properties of water and the underlying sediments [16,17]. In shallow lakes, environmental disturbances can change the distribution and abundance 250 of macrophytes [18]. Release of nutrients from decomposing macrophytes, their incorporation into lake sediments and their subsequent uptake by the growing macrophytes presents a considerable portion of nutrient cycling in a lake system [19]. Aquatic macrophytes have a high capacity for nutrient uptake from water, which affects the eutrophication process [20-24]. On the other hand, high productivity of aquatic macrophytes may create large problems, particularly at the time of decomposition of their biomass, which may accelerate the eutrophication process [25-27]. It is therefore important to monitor aquatic ecosystems for growth and development of macrophytes with high biomass production [28] thus protecting the ecological balance in these ecosystems. Shallow freshwater ecosystems are characterized by high productivity. Phytoplankton and emergent, floating and submerged macrophytes are principal * E-mail:[email protected] Unauthenticated Download Date | 6/16/17 5:09 PM L. Nikolić, S. Pajević, B. Ljevnaić primary producers [11,29]. Individual primary producers differ in productivity because they utilize different sources of carbon dioxide and nutrients and they differ in light energy utilization [29]. For example, the emergent species take up carbon dioxide from the air and are superior competitors for light. The position of the floating macrophytes is intermediate with respect to the terrestrial and emergent species. On the other side, the submerged species are similar to phytoplankton in that they use inorganic carbon and nutrients from water and they compete for light. On that account, phytoplankton and submerged macrophytes hold key positions regarding their contributions to the productivity of the water column. Their relationship is specific and related to their spatial distribution along water depth [30,31]. In general, it can be stated that macrophytes are dominant and principal primary producers in small, shallow and transparent aquatic ecosystems [11], while phytoplankton is the main link of the bioproduction chain in large, deep and poorly transparent aquatic ecosystems [32-34]. The objective of this investigation was to analyze the primary production dynamics of the dominant hydrophytes by monitoring their levels of organic matter and organic carbon and estimating their photosynthetic potential via the total chlorophyll content. These factors tend to accelerate the eutrophication process in a Danube floodplain lake. 1.1 Study area A man-made levee and a natural fluvial process had been essential for the formation of Lake Provala (the Vojvodina Province, Serbia). This lake was the result of the Danube flood water spilling through a broken levee in 1924, and the water rush formed a basin 19 m deep [35,36]. After the flood waters withdrew, a lake remained in the basin behind the levee. Its geographic position is 45o29’ North latitude and 18o86’ East longitude, at the altitude of 79 m. Presently, the Danube River flows 5.5 km west of the lake. At the average water level in the lake, its area is about 42,000 m2, and its volume, owing to the large depth (19 m max.), is 282,580 m3 (Figure 1). Water transparency in the deepest part of the lake is 150 cm [35]. The Vojvodina Province, a part of the Pannonian Plain, has a moderate continental climate. The location of Lake Provala has a mean annual temperature of 10.7oC and 17.5oC for the vegetation period. The amplitude difference of the mean monthly temperatures is 21.9oC, the temperatures ranging from -0.8oC in January to 21.1oC in July. The floristic composition of the lake and the riparian belt includes 65 plant species [37]. Emergent vegetation Figure 1. Isobathic map of Lake Provala. dominated by reed (Phragmites australis (Cav.) Trin. ex Steud) flourishes in the riparian area along the south banks of the lake. Lake waters are dominated by three hydrophytes, N. peltata., M. spicatum and C. demersum. 2. Experimental Procedures Floristic investigations and collection of macrophytic plant species for the analysis of primary production were conducted in the course of the 2000 vegetation period. Plant identification was performed according to Flora Europaea [38]. Organic matter, organic carbon and chlorophyll contents were measured according to standard methods [39]. Vascular aquatic macrophytes were collected from a boat, using a 0.5 m2 wooden frame and a 0.25 m2 Petite-Ponard dredge. Macrophytes were sampled in five replications, in previously labeled spots (the deepest part, medium deep and the shallowest part), throughout the growing season in one year. Whole plants were taken from sample areas of 0.5 m2 or 0.25 m2. Plant material was labeled and taken to laboratory where it was rinsed, wrung out and weighed. Samples were dried at 105oC for 30 hours i.e., until a constant weight was reached. Plant material was ground and burnt for as long as it emitted gasses. The residue was incinerated at 550oC for 6 hours. After cooling in a desiccator, the residue was weighed to calculate the 251 Unauthenticated Download Date | 6/16/17 5:09 PM Primary production dynamics of dominant hydrophytes in Lake Provala (Serbia) Plant Species Date (month/day) Biomass * 5/13 5/31 6/14 6/28 7/17 7/31 8/16 9/4 9/26 x S V I M. spicatum OM OC 163 76 194 90 258 120 208 97 84 39 43 20 - - - 158.33 73.66 96.56 44.91 56.91 56.93 455.18 211.66 N. peltata OM OC 50 23 71 33 180 84 244 114 132 62 60 28 78 36 103 48 28 13 105.11 49.00 65.79 31.35 68.88 69.27 247.21 114.95 C. demersum OM OC - 84 39 115 54 90 42 80 37 63 29 18 9 31 15 29 13 63.75 29.75 33.59 15.62 64.38 64.39 105.78 49.19 Table 1. Growing season changes in organic matter and organic carbon content for three aquatic plant species * OM - organic matter (g m-²); OC - organic carbon (g C m-2); x - arithmetic mean; S - standard deviation; V - variation coefficient; I - variation interval; N = 3 content of organic matter, which was expressed in g m-2. As most of the higher plants contain 46-48% of carbon in dry weight, organic carbon content was calculated using the factor 46.5% and expressed in g C m-2. Chlorophyll content (Chlorophyll A, Chl a and chlorophyll A+B, Chl a+b) was determined spectrophotometrically, in acetone extracts from fresh samples [40]. This analysis included three replications of five individual plants per species. Descriptive statistics were calculated for contents of organic matter and organic carbon (Table 1) using StatSoft Statistica 7.0 statistics software. Pigment content were made in triplicate and data were analyzed by Duncan’s multiple range test (P < 0.05). 3. Results During the investigated period, the hydrophytes N. peltata, M. spicatum and C. demersum were dominant in Lake Provala waters. In full vegetation, the three dominant aquatic plants flourished and overgrew one half of the open water surface, while the surface of the deepest part of the lake remains free of aquatic vegetation. M. spicatum, N. peltata and C. demersum were analyzed for organic matter, organic carbon and chlorophyll pigment contents, i.e., for indicators of biomass production in the investigated aquatic ecosystem. While individual M. spicatum developed at the depth of 6 m, the species grew in masses at the depth of 4 m and in a large part of the lake. During the investigation period, M. spicatum plants developed in late April, flowered in late May and ended its vegetation period already in August. The average annual contents of organic matter and organic carbon in M. spicatum plants were 158.33 g m-2 and 73.66 g m-2, respectively (Table 1). N. peltata occurred in the course of May. They reached maximum growth in summer and they persisted until late fall, when some plants were still in flower. N. peltata plants inhabited the shallower and narrower (southern) of the lake, growing at the depths between 2 and 4 m. The average annual contents of organic matter and organic carbon in N. peltata plants were 105.11 g m-2 and 49.00 g m-2, respectively (Table 1). In the investigation period, C. demersum occurred in late May. They occupied limited areas at the depths between 4 and 6 m located at the beginning of the southern elongation of the lake. The average annual contents of organic matter and organic carbon in C. demersum plants were 63.75 g m-2 and 29.75 g m-2, respectively (Table 1). The analyzed parameters (content of organic matter and content of organic C) showed relatively high coefficients and intervals of variation (Table 1). The average values of organic matter was about 80%, in agreement with the available literature [41,42]. The values of organic carbon we obtained for the analyzed species were slightly higher than those reported by Westlake [41], while other authors [11,32] recorded considerably higher average values. The average values of chlorophyll pigment content ranged from 1.54 mg g-1 (Chl a) and 2.15 mg g-1 (Chl a+b) in M. spicatum in the month of June to 5.27 mg g-1 (Chl a) and 7.53 mg g-1 (Chl a+b) in C. demersum also in June (Table 2). Our results show species specificity in the seasonal dynamics of pigment content (Table 2). The species M. spicatum showed no significant difference among the seasons, whereas N. peltata and C. demersum exhibited significant differences in chlorophyll content between the seasons in a single vegetation period. Seasonal variation in chlorophyll content may provide indirect indication of the dynamics of bioproduction by the analyzed plant species. The species N. peltata has 252 Unauthenticated Download Date | 6/16/17 5:09 PM L. Nikolić, S. Pajević, B. Ljevnaić M. spicatum Month Chlorophyll A C. demersum Chlorophyll A+B Chlorophyll A N. peltata Chlorophyll A+B Chlorophyll A Chlorophyll A+B May 1.86 a 2.49 a 4.23 b 5.76 b 3.27 b 4.28 b June 1.54 a 2.15 a 5.27 a 7.53 a 1.96 c 2.65 c July 1.79 a 2.40 a 1.88 d 2.58 e 3.04 b 3.81 b August - - 3.29 c 4.64 c 4.48 a 5.98 a September - - 2.87 c 3.71 d 4.64 a 5.84 a Table 2. Growing season changes in chlorophyll A and A+B for three aquatic plant species in Lake Provala (mg g-1). * Values with the same letter were not significantly different; N=5 the longest vegetation period and is distinguished for largest and longest photosynthetic activity, which results in the largest organic production and thus impact on the eutrophication process. We also show that the species differed significantly in chlorophyll content, especially N. peltata and C. demersum (Tables 2 and 3). The results of pigment content for the analyzed macrophyte species were in agreement with the available literature. these ecological factors affected the primary production in Lake Provala. The submerged, rooted species M. spicatum, thrived in the investigated aquatic ecosystem and was characterized by a long flowering period, from spring to fall, as reported by others [47]. At Lake Provala the peak flowering period occurred in May through August. Gopal and Goel describe M. spicatum as an adaptive, highly competitive species that tolerates low light intensity and low water temperature and possesses allelopathic substances that inhibit the growth and development of other aquatic species [48]. The last statement was confirmed in Lake Provala where M. spicatum formed predominantly pure stands. Compared with the other two hydrophytes, M. spicatum had higher average contents of organic matter and organic carbon, which agrees with other studies [32], but also a relatively high variation between the maximum and minimum values. 4. Discussion Numerous authors [11,21,32,43-46] have emphasized that there is a direct relationship between the primary production dynamics of macrophytes and light regime, temperature, water depth, sediment composition and the amount of available nutrients. Here we show that Plant species M. spicatum C. demersum N. peltata May June July August September Chlorophyll A 1.86 c 1.54 b 1.79 b - - Chlorophyll A+B 2.49 c 2.15 b 2.40 b - - Chlorophyll A 4.23 a 5.27 a 1.88 b 3.29 2.87 Chlorophyll A+B 5.76 a 7.53 a 2.58 b 4.64 3.71 Chlorophyll A 3.27 b 1.96 b 3.04 a 4.48 4.68 Chlorophyll A+B 4.28 b 2.65 b 3.81 a 5.98 5.84 Table 3. Chlorophyll A and A+B, average values of the three aquatic macrophytes (mg g.1 dry matter) * Values with the same letter were not significantly different; N = 3 253 Unauthenticated Download Date | 6/16/17 5:09 PM Primary production dynamics of dominant hydrophytes in Lake Provala (Serbia) On the other hand, Lillie reported somewhat higher average values, pointing out that the species produced maximum biomass when growing at the depths between 1.5 and 3 m [49]. The high variance in our study are undoubtedly associated with the adaptability of M. spicatum to changes in nutrient content, light intensity and water depth during growing period [9,50]. The floating, rooted, species N. peltata is characterized by a long flowering period and high biomass productivity [25,38,51]. In Lake Provala, it achieved maximum growth in summer and persisted till late fall, when individual plants could still be found in flower. The contents of organic matter (around 80% in relation to dry matter) and organic carbon (37% in relation to dry matter) in N. peltata were somewhat lower than those found in literature [32]. Still lower biomass values were registered for Nymphoides [52], who pointed out that water chemistry had an exceptionally high effect on macrophytic species and their bioproduction. On the other side, Brock et al. registered higher biomass values for N. peltata at the peak of the vegetation growth [53]. In addition to numerous abiotic factors, the biomass production dynamics is significantly affected by biotic factors such as the rate of colonization by epiphytic organisms [43,54], which is especially conspicuous in the case of species with large leaf area such as N. peltata. The submerged, unrooted species C. demersum, which occurs at all depths and in all regions and seasons [47], was found in Lake Provala on a limited area, near the bottom of this aquatic ecosystem, where it did not form large biomass. This might be due to Ceratophyllum and its high requirements for nitrogen and nitrogencontaining substances, which are moderately abundant in Lake Provala [27]. Also, Phillips et al. mention the negative allelopathic effects of Ceratophyllum on other aquatic plants [55]. Compared with the other two species, C. demersum had lower values of the analyzed parameters, which were somewhat lower than those found in literature [11]. The obtained data are a good illustration of the primary production dynamics of C. demersum in Lake Provala, and they also showed lowest variations. Overall C. demersum grew and produced biomass fairly uniformly through the vegetation period, with an exception in June when it reached a peak of the vegetation growth. The analysis of chlorophyll A and B in the three hydrophytes indicated the presence of species specificity as well as of seasonal dynamics of these pigments. According to Schagerl and Pichler [56], the content of chlorophyll A has a wide range of variation in aquatic plants, which speaks in favor of plant adaptation to different ecological conditions, in the first place light and temperature. In Lake Provala, the submerged species M. spicatum, which had the shortest vegetation period, showed no significant differences among the seasons [27], while the floating species N. peltata and the submerged species C. demersum exhibited significant differences in chlorophyll content among the dates of measurement throughout the vegetation period. The seasonal variation in pigment content was an indication of bioproduction dynamics with N. peltata having the longest period of bioproduction. Consequently, this species had the highest effect on the process of secondary pollution of the lake, due to the decay and decomposition of its biomass after the end of the vegetation period, which significantly bolster the eutrophication process [25,27,37]. It may be concluded from the above that the investigated aquatic ecosystem is dominated by macrophytes, one floating (N. peltata) and two submerged (M. spicatum and C. demersum). These plant species are characterized by uneven biomass growth during the vegetation period, which is brought about by the ambient climatic conditions and the trophic state of the investigated aquatic ecosystem. The enormous biomass which they form by the end of the vegetation period causes secondary pollution of the lake, which directly affects the trophic level of the ecosystem by accelerating the eutrophication process in this Danube floodplain lake. Additionally, the existent macrophytes achieve their maximum growth in June, during full tourist season, which is a further detriment for this small and relatively shallow lake. In spite of an important feature of macrophytes, that they take up large amounts of nutrients from lake water and benthic zone [22,23,25], it is necessary to monitor and control their growth and development [28,57] because their enormous bioproduction may negatively affect the ecological balance of small aquatic ecosystems and may accelerate the process of eutrophication in them. Because of the negative effects of the accelerated eutrophication process, certain measures are needed [25,28,57] to improve water quality and thus remediate the investigated aquatic ecosystem. Since Lake Provala is intended for tourism, sports and recreation, caution should be exercised when selecting methods for decelerating the eutrophication process. 254 Unauthenticated Download Date | 6/16/17 5:09 PM L. Nikolić, S. Pajević, B. 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