1 ROLE OF HYDROLOGY, NUTRIENTS AND FISH IN INTERACTION WITH GLOBAL CLIMATE CHANGE IN EFFECTING ECOLOGY OF SHALLOW LAKES IN TURKEY Meryem Beklioğlu Middle East Technical University, Biology Department 6531, Ankara ABSTRACT By 95% of the worl lakes are shallow. In effecting the primary production and associated species diversity, availability of nutrients [Nitrogen and Phosphorus] are critical. Extensive eesearch on eutrophicated the north temperate shallow lakes has shown deterioration of water clarity through increased phytoplankton biomass and suspended matter amount, and loss of ecological and conservation values through disappearance of submerged plants, predatory fish and waterfowl. Results of a longterm monitoring of Lakes Eymir and Mogan have shown that nutrient enrichment induced high phytoplankton biomass and plankti-bentivorous fish feeding induced turbid state resulted in loss of submerged plants. Furthermore, In Turkish shallow lakes located in a semi-arid to arid Mediterranean climate, where the hydrological changes are common phenomenones, are presumably very sensitive to water level fluctuations (WLF). Investigation on the relationships between WLF and submerged macrophyte development in five Turkish shallow lakes revaled that in all lakes, WLF emerged as a major factor determining submerged plant development. High submerged plant coverage was observed when the water level was low. Through global warming that lake levels are expected to go down. However, warmer water temperature, low dissolved oxygen availability associated with longer hydraulic residence stimulated salinity, internal phosphorus loading and suppression of denitrification. These processes are likely to increase nitrogen and phosphorus availability and in turn, increased turbid water condition through global warming. Unders such turbid conditions submerged plant development were supressed. Furthermore, warmer conditions stimulated anoxic water that led to major fish kill. On the otherhand, increased salinity is expected to lead to loss of freshwater species. Key words: carp, nitrogen, phoshorus, submerged plants, water level fluctutation
2 584 INTERNATIONAL CONGRESS ON RIVER BASIN MANAGEMENT INTRODUCTİON Freshwaters are crucial to the establishment of any human community and to the conservation of all land-based wild life. Most of the world s freshwaters area are shallow and made up of small individual lakes dominated by littoral [shallow plantdominated] communities that are more productive per unit area of water than deep ones and are more versatile in the uses to which they have been put [Moss, 1998]. These plant-dominated shallow waters are collectively called wetlands and include a huge range water courses from swamps to forests. Dominance by submerged plants is often closely related to increased ecological and conservation values owing to recovery in water quality and, with it, increased diversity and abundance of species, especially waterfowl [Hargeby et al. 1994, Noordhuıs et al., Van Gest et al. 5]. Consequently, the impact of water level fluctuations on the establishment of extensive and high diversity littoral zones in shallow lakes needs further investigation aimed to develop potential restoration tools [Coops & Hosper ]. The value of wetlands on a world scale is immense as shown by budgets made by Costanza et al.  for the value of natural goods and services provided by them. The value of wetlands proved to be greater than that of the drier systems, including forests and grasslands and amounted to trillions of dollars per year. The total value of the World s natural systems amounted to over thirty trillion US dollars per year, or three times the combined gross domestic products [GDP] of all the World s economies combined. The contribution of freshwater wetlands was over 1% and of wetlands as a whole, over a quarter. During the past century, increased urbanization and sewage disposal, regulation of wetlands and streams and more intensive crop and animal farming practices have increased the nutrient especially nitrogen and phosphorus [N and P, respectively] loading to many shallow lakes causing a world-wide problem of eutrophication [Jeppesen 1998]. Eutrophication of shallow lakes may result in deterioration of water clarity and loss of ecological and conservation values through disappearance of submerged plants, predatory fish and waterfowl [Scheffer et al. 1993, Moss et al. 1996, Jeppesen et al. 3]. The whole system and its integrity are very important in maintaining values for nature conservation and human exploitation. The results of eutrophication are high algal biomass often accompanied by massive summer blooming of cyanobacteria or green algae, few submerged macrophytes, dominance of planktibenthivorous fish and low water clarity [Moss, 1998]. Moreover, feeding of benthivorus fish like carp and bream deteriorate the ecological value and water quality of shallow lakes. During the past 1-3 years, several countries have made a great effort to improve the ecological quality of lakes by combating external loading [Sas, 1989], sometimes in combination with additional restoration measures such as biomanipulation [Hansson et al., 1998; Meijer et al., 1999; Beklioglu et al., 3]. To overcome biological resilience, plankti-benthivorous fish removal has been widely applied in
3 BASIN WATER MANAGEMENT 585 north temperate lakes with some success [Hansson et al. 1998, Mehner et al., Gulati & Van Donk ], whereas success of fish removal has been debatable in warm temperate and subtropical lakes [Scasso et al. 1, Beklioglu et al. 3, Jeppesen et al. 5]. However, trophic structure varies among warm lakes depending on whether they are located in dry or wet and low or high altitudes. Such as whole lake fish removal study was carried out in a semi-dry high altitude shallow Mediterranean lake and successfully initiated a clear-water state [Beklioglu et al. 3]. In semi-arid to arid regions, in addition to nutrient availability and associated trophic state, the functioning of lake ecosystems is controlled by the quantity and periodicity of the water. Shallow lakes are particularly sensitive to any rapid change in water level and input. Water level fluctuations may have an overriding effect on the water chemistry [ph, salinity, nutrients] and in turn, the ecology of shallow lakes, especially on the submerged plant development [Talling 1, Coops et al. 3, Beklioglu et al. 6, Tan and Beklioglu 6]. Understanding the role of water level change in ecosystem functioning is important, given the current concerns about global climate change. However, most research into climate change impacts has focused on high latitude or temperate lakes [Carvalho & Moss 1999, Jeppesen et al. 6], while less is known about low latitude lakes, especially in regions exhibiting an arid climate, such as the Mediterranean climatic region, which is particularly sensitive to global warming due to the predictions of a drier and hotter climate [Sánchez et al. 4]. Turkey is a rich country in freshwater resources with natural lakes, 75 dams, and 7 ponds [Kazanci et al, 1995]. The total surface area covered by these lakes is equal to 1, km. Also, most of the lakes of Turkey are shallow and have large surface areas [Lakes Beysehir, Marmara, Işıklı, Uluabat etc.]. These shallow lake wetlands that have rich aquatic vegetation community are also rich in biodiversity. Lakes in Turkey are subjected to nutrient [N & P] enrichment namely eutrophication and strong water level fluctuations induced through drought/wet conditions. The impact of the latter is predicted to be different according to trophic status or availability of nutrients. In addition to this feeding of benthivorus carp effect on ecology of shallow lakes. Here I aimed to evaluate the effects of hydrology, eutrophication, feeding of benthivorous fish, and biomanipulation as a restoration tool on the ecology of Turkish shallow lake wetlands. Further, the impacts of all these effects were discussed in the reflection of global climate change. Material and Methods Lakes, which are included in this study, are Lakes Beyşehir, Marmara, Uluabat, Mogan and Eymir vary in size and depth and are located in a zone ranging from southern to northern Anatolia, Turkey. Data related with water level fluctutations, fish, waterfowl and submerged plant development in Lakes Beyşehir, Marmara, Uluabat and Mogan were taken from
4 586 INTERNATIONAL CONGRESS ON RIVER BASIN MANAGEMENT Beklioglu et al. . Furthermore, the data on hydrology, major ions, nutrients and ecology of Lakes Eymir and Mogan were taken from Beklioglu et al. , Tan & Beklioglu , Karapınar , Ozen , Beklioglu & Tan [submitted]. Methodology on data collection and evaluations are thoroughly discussed in the literature cited above. Results and Discussion In shallow lake wetlands, dominance by submerged plants is often closely related to increased ecological and conservation values owing to recovery in water quality and, with it, increased diversity and abundance of species, especially waterfowl. A. Hydrology i. Water Level Fluctuations - Submerged Plant Development and Waterfowl Shallow lakes located in different geographic regions ranging from the north temperate zone to the Mediterranean, and in the southern hemisphere as well, respond to water level fluctuations, and their submerged plant coverage and density may thus vary widely regardless of top-down mechanisms [Blindow et al. 1997, Coops et al. 3, Havens et al. 4, Van Der Valk 5]. Large water level fluctuation results in a large amplitude change, which is a common phenomenon in semidry to dry Mediterranean climates due to high evaporative loss that is not balanced by an adequate water income, which occurs primarily during the rainy season in winter [Naselli-Flores 3]. In all of the study lakes, water level fluctuations emerged as the major factor affecting submerged plant coverage. Lakes Beyşehir, Uluabat, Marmara and Mogan had significantly higher vegetation cover during the low water level [LWL] period in comparison to the high water level [HWL] period (Figure 1). However, the duration and magnitude of the LWL period varied greatly from lake to lake. For example, in Lakes Beyşehir and Uluabat, throughout a year significant monthly approximately about m water level differences occurred between LWL and HWL periods and vegetation coverage expanded 3 % and 55 %, respectively. In Lake Marmara, however, the vegetation cover was high, while significant monthly differences (over m) occurred between LWL and HWL periods except for winter months (Oct.-Dec.). Similarly, in subtropical Lake Okeechobee submerged plants recovered when water level dropped by m alleviating stress of multiple years of high water [Havens et al. 4]. Also, an approximate 4-cm drop in water level occurring only in May in Lake Mogan was sufficient to expand the submerged plant coverage. This is similar to the results of Blindow et al. , who demonstrated that a 1-15 cm lower/higher water level than the spring average led to a catastrophic shift in the state of Swedish Lake Krankesjön. Consequently, LWL occurring only during the growing season, especially in spring and early summer
5 BASIN WATER MANAGEMENT 587 together with water clarity, can be critical for vegetation development and the magnitude of the water level decrease to allow submerged plants to recover can vary among lakes [Van Nes et al. ]. With an increase in submerged plants, waterfowl abundance, especially that of herbivorous coot, increased in all of the study lakes. Coot dominated the waterfowl community (75%), followed by diving ducks e.g. pochard and tufted duck. The increased waterfowl densities during the vegetated periods of Lake Beyşehir caused it to become an A-class wetland and Important Bird Area (IBA). Similarly, Lake Mogan acquired the status of a Specially Protected Area as well as an IBA during the high vegetation period. Finally, in Lake Uluabat, nearly half a million waterfowl were recorded during the vegetated state in 1996, which is the highest waterfowl density recorded in a Turkish wetland since 197. Based on this waterfowl census, the lake was designated a Ramsar site in 1997 [Yarar & Magnin 1997]. ii. Water Level Fluctutations and Water Residence Time and Major Ions Shallow lakes located in arid to semi-arid regions are particularly sensitive to water stock. As a result, sensitivity to hydrological conditions also has significant consequences for the in-lake concentration of major ions and nutrients, especially for determining the salinity and conductivity [Wetzel 1983, Talling 1]. The hydraulic residence time, which is estimated by dividing the lake volume (Vlake) by the volume of water flowing into the lake (Vin) per unit of time, is prone to hydrological alterations. Long term data from Lakes Eymir and Mogan revealed a significant increase in hydraulic residence time from around 1 yr -1 to nearly 7 yr -1 coinciding with the low water level periods (Figure a). The consequence of increased residence time was a several fold increase in the salinity. Lakes Eymir and Mogan with a salinity slightly above 1 can be classified as hard water lakes [Wetzel 1983]. The exceptionally dry conditions in 1, 4 and 5 resulting in the study s lowest lake level and highest retention time, caused an increase in salinity and conductivity to the highest values recorded during the study period [Figure b]. Hydrological extremes [floods and dry periods] are predicted to follow the global climatic changes. Semi-arid or arid Mediterranean lakes are predicted to receive lower input of water due to shorter precipitation seasons coupled with higher incidence of summer dry periods [Sánchez et al. 4]. Extrapolation of these results suggests that if such conditions occur, many freshwater lakes located in the Mediterranean region would turn saline in the future. Evidently, in Turkish lakes changes in salinity level in the past have frequently triggered shifts between saline and freshwater conditions [Karabiyikoglu et al. 1999]. A modelling study based on the worse climate change scenario, which assumed no reduction in the carbon dioxide emission to the atmosphere, with increases in air temperature ( C) and evaporation (1%), and decreases in precipitation (5%) and runoff water (3%) [Arnell, 3], predicted more than two fold in-
6 588 INTERNATIONAL CONGRESS ON RIVER BASIN MANAGEMENT crease in the salinity levels [Klepper, & Beklioglu, unpublished data]. Such an increase would likely to result in the loss of freshwater species diversity. B. Nutrients (N & P) & Fish. i. Eutrophication and Planti-benthivorous Fish Worldwide, lake eutrophication from excessive inputs of phosphorus and nitrogen, leads to water quality deterioration with significant losses of biodiversity, goods and services [Kristensen & Hansen, 1994; Dodson et al., ]. However, the earliest study from the pre-eutrophicated period on Lake Eymir revealed that the lake water was clear, with a summer Secchi disc transparency averaging >4 m, maximum value being 6 m [Geldiay 1949]. However, over 5 years of raw sewage effluent discharge shifted Lake Eymir from a state dominated by submerged plants to a turbid water state with high concentrations of TP, DIN, chlorophyll-a, and suspended solids, in addition to low Secchi depth [Beklioglu et al., 3]. Further, eutrophic conditions in the lake shifted the fish stock to a conditions of being being dominated by planktivorous carp and tench and the share of piscivorous pike became insignificant [Beklioglu et al., 3]. Several studies illustrate that, in shallow lakes, Benthivorous fish such as carp can be potentially destructive for aquatic plants, either directly through grazing and up-rooting or indirectly through increasing turbidity and nutrient release [Crivelli 1983, Breukelaar et al. 1994]. Beklioglu et al.  showed that in Lakes Marmara and Uluabat, sparse submerged plant development coincided with high carp biomass. Carp biomass and the binary index of submerged plant coverage also displayed a strong inverse correlation for these lakes (r:-.85 & r:-.7, respectively). For restoration of Lake Eymir, removal of about half of the tench and carp stocks, namely biomanipulation led to a.5-fold increase in annual Secchi disc transparency (to 6±15 cm from 11±43 cm), largely because of a 4.5-fold decrease in the inorganic suspended solids concentrations and, to some extent, decreased chlorophyll-a concentrations (9.4±6 mgl -1 and 11.4±.6 µg l -1, respectively) [Beklioglu et al. 3] (Figure 3). Fish removal triggered clear-water conditions resulting in a severalfold increase in especially spring Secchi depth during a five-year period. Rapid recolonisation of submerged plants, Potamogeton pectinatus L. and Ceratophyllum. demersum L., occurred, and the growth remained high for a consecutive period of four years, the cover ranging from 45 to 9% of the lake surface area. Biomanipulation of Lake Eymir is the only case from warm-temperate or semi-dry Mediterranean climatic region. The case showed that biomanipulation can be an effective restoration measure in arid climates for shifting a lake to the clear-water state with redevelopment of denser vegetation
7 BASIN WATER MANAGEMENT 589 a Lake Beysehir Water Level (m. a. s. l.) z-score WL z-sc b Lake Uluabat Water Level (m. a. s. l.) z-score WL z-sc c Lake Marmara Water Level (m. a. s. l.) z-score WL z-sc d Lake Mogan Water Level (m. a. s. l.) z-score WL z-sc Figure 1. Changes in water level [m.a.s.l] [WL] and the cumulative z-scores of water level for a] Lake Beyşehir, b] Lake Uluabat, c] Lake Marmara, d] and Lake Mogan, Lines on the second X-axis indicate the state of submerged plant development: thick dark line [ ] = high vegetation cover, thin dark line [ ] = low vegetation cover, and broken line [---] = lack of data.
8 59 INTERNATIONAL CONGRESS ON RIVER BASIN MANAGEMENT hydraulic residence time (t yr -1 ) a) = LakeEymir Lake Mogan Salinity (ppt) b) Lake Eymir Lake Mogan Figure. a) Hydraulic residence time and b) salinity values measured in Lakes Eymir & Mogan from 1998 to 5. ii. Eutrophication and climate change Low water level years in Lakes Eymir and Mogan, which are associated with longer hydraulic residence times, probably provide great opportunities for sedimentwater contact [Figure a] [Saunders & Kalff, 1]. Chl-a (µg/l) SS (mg/l) Bef. Bioman. Chl a SS Secchi-depth Dur. Bioman Secchi deptjh (cm) Figure 3. Mean concentrations of suspended solids, chlorophyll-a, and Secchi disk transperancy recorded before and during biomanipulation, and the consequent years in Lake Eymir. Thus, during drought periods the in-lake phosphorus concentrations in Lakes Eymir and Mogan increase several-fold and thus became more dependent on internal processes rather than external loading (Figure 4). Despite the fact that the external TP load was low, the in lake total phosphorus (TP) concentrations remained high (Figure 4). Further, in Lake Eymir, there has been a late increase in the ammonium concentration coinciding with decreased availability of dissolved oxygen (Figure 5). Anoxic conditions, which probably resulted from the increase in phytoplankton
9 BASIN WATER MANAGEMENT 591 production, interrupt the process of nitrification, leading to accumulation of ammonium and, in turn, reduced or completely stopped the process of denitrification. This is in aggrement with findings from the Parana wetland, Argentina, where ammonium and phosphorus increased along with an increase in anoxic conditions [O Farrell et al. 3, Izagurre et al. ]. However, the results of an investigation comprising of 1 European lakes demonstrated the occurrence of nitrogen depletion in these lakes within the past 15 years, which is partly attributed to enhanced temperatures [Weyhenmeier et al. submitted]. Thus, increased temperatures may result in different responses in nutrient concentrations, especially nitrogen, between cold and warm lakes due to variations in the denitrification processes in response to parameters such as the oxygen amount. Furthermore, it has recently been suggested that nitrogen may play a far more important role for the stability of submerged plants upon recovery, especially at relatively high phosphorus levels [Moss 1]. The late increase in ammonium concentrations may have contributed to the instability of clear-water conditions in Lake Eymir. Thus, in shallow warm lakes, the effects of global warming may require establishment of even lower thresholds not only for P but also for nitrogen loadings than those so far suggested to obtain a stable submerged plant dominated clearwater state [Romo et al. 4]. In Lake Eymir nutrient enrichment led to a several fold increase in the concentrations of chlorophyll-a associated with a significant decrease in the dissolved oxygen availability that result in occasional fish-kills in the summer occurred in 4 and 5 [Ozen & Beklioglu, unpublished data]. This may induce temporary unstable clear water conditions since the nutrient enrichment is high and the stability of induced clearwater conditions is expected to be short-lasting. TPlake TPload TPlake (kg) TPload (kg) Figure 4. Total phosphorus (TP) load from the catchments and in- lake TP amounts recorded between 1997 and 4 in Lake Eymir.
10 59 INTERNATIONAL CONGRESS ON RIVER BASIN MANAGEMENT Dissolved oxygen concentration (mg l -1 ) Bef. Bioman. Dur. Bioman. mean oxygen hypolimnetic oxygen 1 3 Figure 5. Mean and hypolimnetic dissolved oxygen concentration recorded in Lake Eymir during before and during biomanipulation, and the consequent years in Lake Eymir. In sum, ecology of Turkish shallow lakes and their associated species diversity are very sensitive to hydrological alterations, namely water level fluctuations and hydraulic residence time. In nutrient poor lakes, low water levels may enhance submerged plant development with obvious advancement of the littoral zone with associated species diversity. Eutrophication in Turkish shallow lakes may also lead to the loss of submerged plants with increased turbidity resulting from benthiplanktivorous fish feeding and increased phytoplankton production. Biomanipulation as a restoration measure can offer a help as removal of half of tench and carp populations led to the re-development of submerged plants with clearwater conditions. However, global climate warming appeared to complicate the lake processes through increasing salinity and in turn reducing the freshwater species diversity. Further the increase in salinity appears to be inevitable as shown by the predictive models. Furthermore, global warming may lead to further, enhancement of eutrophication through increasing bottom-up processes as a provider of nutrients. Therefore, it appears to be very critical to take control measures to prevent eutrophication of lakes and implement restoration methods along with better hydrological management. At present time, these are the biggest challenges of lake scientists, lake managers and state authorities. Acknowledgement. Several MSc and PhD students worked towards producing data that have been presented here, I am grateful to Arda Özen, Can Ozan Tan and Burcu Karapinar. Sara Banu Akkaş for linguistic help.
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2008 Impacts of Europe's changing climate ISSN 1830-2246 Introduction Global climate change is a reality. In Europe the most vulnerable regions are the Arctic, mountain areas, coastal zones and the Mediterranean.
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5.2.1 Recall the cell as the smallest unit of life and identify its major structures (including cell membrane, cytoplasm, nucleus, and vacuole). Taxonomy level: 1.1 and 1.2-A Remember Factual Knowledge
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