Recent habitat degradation in karstic Lake Uluabat, western Turkey: A coupled limnological–palaeolimnological approach

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Recent habitat degradation in karstic Lake Uluabat, western Turkey: A coupled limnological–palaeolimnological approach Jane M. Reeda,*, Melanie J. Lengb,c, Sandra Ryana,1, Stuart Blackd, Selc¸uk Altinsac¸lie,2, Huw I. Griffithsa,3 a

Department of Geography, University of Hull, Cottingham Road, Hull HU6 7RX, UK NERC Isotope Geosciences Laboratory, British Geological Survey, Keyworth, Nottingham NG12 5GG, UK c School of Geography, University of Nottingham, Nottingham NG7 2RD, UK d School of Human and Environmental Science, University of Reading, Whiteknights, P.O. Box 227, Reading RG6 6AB, UK e Department of Biology, University of Istanbul, Istanbul, Turkey b

A R T I C L E I N F O

A B S T R A C T

Article history:

The Ramsar site of Lake Uluabat, western Turkey, suffers from eutrophication, urban and

Received 13 November 2007

industrial pollution and water abstraction, and its water levels are managed artificially.

Received in revised form

Here we combine monitoring and palaeolimnological techniques to investigate spatial

1 August 2008

and temporal limnological variability and ecosystem impact, using an ostracod and mol-

Accepted 11 August 2008

lusc survey to strengthen interpretation of the fossil record. A combination of low inverte-

Available online 21 September 2008

brate Biological Monitoring Working Party scores (<10) and the dominance of eutrophic diatoms in the modern lake confirms its poor ecological status. Palaeolimnological analysis

Keywords:

of recent (last >200 yr) changes in organic and carbonate content, diatoms, stable isotopes,

Biomonitoring

ostracods and molluscs in a lake sediment core (UL20A) indicates a 20th century trend

Palaeolimnology

towards increased sediment accumulation rates and eutrophication which was probably

Diatoms

initiated by deforestation and agriculture. The most marked ecological shift occurs in the

Ostracods

early 1960s, however. A subtle rise in diatom-inferred total phosphorus and an inferred

Isotopes

reduction in submerged aquatic macrophyte cover accompanies a major increase in sedi-

Eutrophication

ment accumulation rate. An associated marked shift in ostracod stable isotope data indicative of reduced seasonality and a change in hydrological input suggests major impact from artificial water management practices, all of which appears to have culminated in the sustained loss of submerged macrophytes since 2000. The study indicates it is vital to take both land-use and water management practices into account in devising restoration strategies. In a wider context, the results have important implications for the conservation of shallow karstic lakes, the functioning of which is still poorly understood.  2008 Elsevier Ltd. All rights reserved.

* Corresponding author: Tel.: +44 1 482 466 061; fax: +44 1 482 466 340. E-mail addresses: [email protected] (J.M. Reed), [email protected] (M.J. Leng), [email protected] (S. Ryan), s.black@ reading.ac.uk (S. Black), [email protected] (S. Altinsac¸li). 1 Present address: Entec, 155 Aztec West, Park Avenue, Almondsbury, Bristol BS32 4UB, UK. 2 ¨ zdin Apartımanı No. 20, Daire 4, Istanbul, Turkey. Present address: Merdivenko¨y Mahallesi Ortabahar Sokak, O 3 Deceased. 0006-3207/$ - see front matter  2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2008.08.012

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1.

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Introduction

Concerns over the degradation of inland water quality and aquatic habitats have become key environmental issues. Over much of Europe, for example, the dictates of the EU Water Framework Directive (WFD; EU Directive 2000/60/EC) have led to the development of internationally coherent water chemistry and biomonitoring programmes. These are supported by a growing body of research into the pattern and process of biological response, aimed in part at predicting the ‘undisturbed’ reference state as a target for restoration of sustainable good ecological (e.g. Freshwater Biological Association, 2005). Turkish water resources have high economic and biodiversity value, but many lakes are suffering pollution impact (e.g. Green et al., 1996; Roberts and Reed, in press) and long-term monitoring programmes are not well developed. Given Turkey’s desire to become an EU member state, there is additional pressure to achieve good ecological and chemical status. Recent short-term studies of lakes, streams and groundwater indicate widespread problems of eutrophication (e.g. Akkoyunlu, 2003; Bekliog˘lu et al., 2003; Karakoc¸ et al., 2003; Karafistan and Arık-Colakog˘lu, 2005; Dalkıran et al., 2006; Dere et al., 2006; Duran, 2006; Aksoy and Scheytt, 2007; Duran and Suic¸mez, 2007), pesticide and heavy metal contamination (e.g. Arcak et al., 2000; Barlas et al., 2005; Kazancı et al., 2006; Demirel, 2007; Yılmaz, 2007), and hydrological impact (Magnin and Yarar, 1997; Lammens and van den Berg, 2001). A variety of potential causes can be identified, prominent amongst which are those associated with the expansion of agriculture, industry and urban populations. Restoration efforts include measures such as sewage diversion (e.g. Karakoc¸ et al., 2003), biomanipulation (e.g. Bekliog˘lu et al., 2003) ¨ zesmi and O ¨ zesmi, 2003). and socio-economic studies (e.g. O However, the definition of successful sustainable management or restoration plans is hindered by a lack of detailed understanding of the nature of environmental impact and ¨ zesmi and O ¨ zeecosystem response (Karakoc¸ et al., 2003; O smi, 2003). The potential of palaeolimnological research to reconstruct water pollution impact in lakes is well demonstrated (e.g. Battarbee, 1999; Smol, 2002). For countries such as Turkey, which lack large-scale monitoring programmes, palaeolimnology offers the only reliable means of establishing the timing and magnitude of ecosystem impact. Palaeolimnological data can be of particular value in contributing information on the reference state of a lake (e.g. Bennion et al., 2004; Leira et al., 2006; Bennion and Battarbee, 2007). Internationally, karstic tectonic systems have received less attention than the glacial lakes of northwestern Europe, and such studies should benefit environmental managers throughout the circum-Mediterranean. To date, palaeolimnological studies in Turkey have had focused on long-term palaeoclimate and vegetation history (Van Zeist and Bottema, 1982; Bottema and Woldring, 1984; Landmann et al., 1996; Eastwood et al., 1999, 2007; Leng et al., 1999; Reed et al., 1999; Roberts et al., 1999; Kashima, 2002; Jones et al., 2002, 2006, 2007). More recently, this has extended to recognising signatures of volcanic eruptions (Eastwood et al., 2002) and seismic activity (Leroy et al., 2002).

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Apart from a study of mineralogy, geochemistry and basic _ diatom and ostracod analysis in Lake Iznik, western Turkey (Franz et al., 2006), and of sediment accumulation rates in Lake Uluabat itself (Kazancı et al., 2004), conservation-based palaeolimnology is lacking. Here we combine a range of monitoring and palaeolimnological techniques to investigate spatial and temporal limnological variability and ecosystem change in an internationally important wetland in northwestern Turkey. In the modern environment, standard invertebrate biomonitoring techniques are used to assess current ecosystem health, and a survey of ostracod and mollusc distribution is used to strengthen palaeolimnological interpretation of fossil assemblages. In line with the approach taken in large-scale monitoring programmes (Bennion and Battarbee, 2007), our palaeolimnological study aims to establish the degree of recent (last ca. 200 yr) human impact on the physico-chemical and ecological character of the lake and to assess how far the ecosystem may have shifted from a former reference state. The focus on recent change assumes a degree of longterm stability, such that the 19th century character of the lake is taken as its ‘natural’ state prior to expansion of human activities, and marked change thereafter is likely to represent a deviation from the norm. We combine a well-tested range of proxy indicators (sediment organic and carbonate content, diatoms, ostracods and molluscs, authigenic and ostracod oxygen and carbon isotopes) to reconstruct the timing and magnitude of recent limnological change by analysis of a short sediment core, dated by 210Pb and 137Cs analysis of a parallel core at the same site.

2.

The study site

The Ramsar site, Lake Uluabat (or Lake Ulubat, Apolyont Go¨lu¨), is shallow (currently <2 m deep) and eutrophic. It is located south of the Sea of Marmara at 8 m a.s.l. in Bursa, northwestern Turkey (4010 0 N, 2835 0 E) (Fig. 1). The climate is Mediterranean-continental, with long hot summers and cold winters. Temperatures range from 16 to +40 C and mean annual precipitation is 668 mm. As with Lake Manyas (or Kusß) to the west, it is a karstic tectonic basin within Mesozoic limestones which was probably formed by the damming of a Holocene river channel (Kazancı et al., 2004). It is ca. 24 km long and 12 km wide, with an estimated catchment area of 10,555 km2 (Gu¨rlu¨k and Rehber, 2006). The lake is groundwater-fed, with additional inflow through the River Mustafakemalpasßa and minor drainage channels. The only outflow is the Kocac¸ay River in the north-west; during periods of drought its flow has been known to reverse, forming a temporarily closed hydrological system. The Uluabat catchment is in one of the most productive agricultural regions of Turkey, with approximately 16 urban settlements on the lake shores (Dalkıran et al., 2006), the largest of which are shown in Fig. 1. Most of the catchment is dedicated to arable farming and willow plantations, with some fruit plantations and stock breeding. During 1937– 1993, 148 km2 of natural floodplain was drained for agriculture, with the progressive construction along the western littoral and the lower reaches of the River Mastafakemalpasßa of artificial silt embankments (Magnin and Yarar, 1997).

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Fig. 1 – Map of Lake Uluabat, showing its location in western Turkey (inset), and modern land-use in the catchment.

Some remnant natural sand banks along the western littoral are populated by Tamarix scrub. Reed beds dominated by Phragmites australis and Typha spp. are extensive along the western and southern shores, and occur in patches to the north and east. Lake Uluabat has high economic and biodiversity value ¨ zesmi and O ¨ zesmi, 2003). The fisheries industry is of na(O tional importance, dominated by pike, Israeli carp (Tilapia) and smaller fish such as rudd and roach (Lammens and van den Berg, 2001). The lake once provided 30% of national Turkish crayfish production (Astacus leptodactylus) until they were almost extirpated by a disease in 1986. Until recently Lake Uluabat boasted the largest beds of the water lily (Nymphaea alba) in Turkey, with a diverse aquatic flora including Ceratophyllum demersum and Potamogeton crispus (Sec¸men and Leblebici, 1996), but plant macrophyte cover has declined seriously since 2001. In contrast, migratory bird populations have increased significantly, apparently linked to declining water quality in Lake Manyas (Magnin and Yarar, 1997). Lake Uluabat supports over 400,000 water birds, including the endangered Pelecanus crispus. As outlined below, Lake Uluabat is under pressure from eutrophication, industrial and urban pollution and water abstraction, and its naturally fluctuating water levels are now managed artificially. The lake was unprotected until its listing as a Ramsar site in 1998, and its biodiversity value is also reflected in its inclusion, in 2000, in the Living Lakes Network (http://www.livinglakes.org/partnership.htm). An eco¨ zesmi and system management plan has been set up (O ¨ zesmi, 2003; Salihog˘lu and Karaer, 2004; Gu¨rlu¨k and Rehber, O 2006), but management attempts are hampered by the need for additional limnological monitoring and deeper under-

standing of ecosystem functioning (Degirminci et al., 2005; Gu¨rlu¨k and Rehber, 2006).

3.

Current knowledge and uncertainties

Monitoring programmes have been of limited value in assessing temporal trends and specific impacts since the majority have generated a maximum of 1–2 yr data. Degirminci et al. (2005) noted that there was no system for monitoring external impacts. The lake is eutrophic; total phosphorus data are lacking, but maximum mean chlorophyll a (52.0 mg m3), nitrate (5.5 mg l1 N-NO3) and soluble reactive phosphorus (0.1 mg l1) values for 1998–1999 are high (Dalkıran et al., 2006). External impacts are poorly understood; diffuse agricultural pollution may be an important source of nutrient input (Magnin and Yarar, 1997) and, from a Holocene sediment chronology, Kazancı et al. (2004) suggest increased 20th century sediment accumulation rates are linked to deforestation and the expansion of agriculture. In contrast, other authors suggest that inflow from the R. Mustafakemalpasßa is the major source of both nutrients and accelerated siltation (Lam¨ zesmi and O ¨ zesmi, 2003; mens and van den Berg, 2001; O Barlas et al., 2005). Lammens and van den Berg (2001) report fluctuating nutrient levels linked to changing external river input and reduced internal plant macrophyte cover compared to a decade earlier. Other ecological studies are limited to phytoplankton surveys (Dalkıran, 2000; Karacaog˘lu et al., 2004), a survey of Ephemeroptera (Tanatmisß, 2002) and an analysis of littoral ostracod communities linked to the present study (Altınsac¸lı and Griffiths, 2001). Industrial activity includes extraction and mining of sand, lignite and heavy metals, which has been extensive

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historically along the R. Mustafakemalpasßa (Barlas et al., 2005). Mining activities have reportedly reduced since the 1960s and since 1999 are reported to mainly comprise sand extraction (Lammens and van den Berg, 2001). This is again at odds with a statement by Kazancı et al. (2006), that open cast mining and associated pollution are still intense. Urban population data are lacking. Water levels fluctuate naturally on an intra- and inter-annual basis. Historical data are fragmentary and contradictory. Most authors agree that a progressive reduction in lake volume has occurred over recent decades, possibly coupled with reduced seasonal fluctuation in water depth. Water abstraction is via four pumping stations on the shores (Fig. 1). Lammens and van den Berg (2001) suggest there has been a 1 m rise in minimum water-level since 1989 due to construction works on the outlet. In 1997, abstraction directly from the lake was for small-scale irrigation of 64 km2 of land, but the inflow was being reduced by river abstraction for irrigation of 203 km2 of land (Magnin and Yarar, 1997). Reported maximum depth has reduced from an estimated historic high of 10 m, to 6 m in 1997 (Magnin and Yarar, 1997) and recent estimates of 3.0–3.5 m in winter/spring and 1.0–1.5 m in summer (Lammens and van den Berg, 2001; Karacaog˘lu et al., 2004; Barlas et al., 2005, this study). From field observations in 2000, reduced water levels are evident in Go¨lyazı, where a bridge constructed in the 1970s straddles dry ground. Kazancı et al. (2004) estimate a ca. 7% reduction in surface-area from May 1987 to July 2000 based on Landsat images, although from our observations this contrast will have been due in part to seasonally low summer lake levels and to a drought in 2000. Siltation is thought to be an additional contributor to a rather larger estimate of a 12% reduction in lake area from 1984 to ¨ zsoy, 2002 cited in Dalkıran et al., 2006). 1993 (Aksoy and O The latter contradicts trends derived from basic State monitoring during 1982–2000 (Ryan, 2001; Bekliog˘lu et al., 2006; Dalkıran et al., 2006), which indicate a drop in mean water-level of ca. 3 m by 2000 from a peak in 1988, but also indicate water-level was only ca. 0.5 m above the 2000 level in 1982.

4.

Materials and methods

4.1.

Modern limnology

Due to their specific ecological preferences, ostracods and molluscs can provide valuable palaeolimnological proxy data on parameters such as habitat availability, dissolved oxygen content (DOC) and nutrient status, to complement inferences based on other proxies such as diatoms (Griffiths and Holmes, 2000; Griffiths et al., 2002). To strengthen interpretation of fossil assemblages based on their observed modern habitat preferences, a transect survey was carried out of species distribution in profundal habitats of the lake and in the open waters of the littoral zone. This complemented ostracod data from littoral habitats generated by Altınsac¸lı and Griffiths (2001) during 1995–1996, when the lake had extensive submerged macrophyte cover. Samples were collected along two 10-sample transects (Fig. 2) on 14 April, 2001, using a Garmin GPS to record the location. Transect A sampled the open waters at the centre of the lake basin, running towards the putative point-source of pollution, the R. Mustafakemalpasßa,

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and Transect B ran southwards from reed beds in the northeast. Conductivity, pH and DOC were measured with Whatman probes at 19 of the 20 sites. Water depth was measured with a hand-held echo sounder, and transparency with a Secchi disk. Samples were collected using an Ekman Grab, sieved in the field through a 63 lm sieve and preserved in 95% ethanol. In the laboratory samples were washed through a 180 lm sieve and hand picked while viewing at 10· on a Prior dissecting microscope. Standard counting techniques were used (Mouthon, 1986; Altinsac¸lı and Griffiths, 2001). Identification was made by reference to standard texts and local studies (Bronshtein, 1947; Meisch, 2000 for ostracods; Fitter and Manuel, 1986; Kubilay and Timur, 1995 for molluscs). Candonid ostracods were not identified to a lower level owing to difficulties in identifying congeneric juveniles; from Altınsac¸lı and Griffiths (2001), they may include benthic Candona angulata and Candona neglecta, or limnic Fabaeformiscandona caudata. The data were expressed as total number of individuals per Ekman grab sample (a volume of ca. 25 · 25 · 25 cm3). The same samples provided material for a simple invertebrate biomonitoring assessment of current water quality status, by calculation of Biological Monitoring Working Party (BMWP) scores to assess bulk organic pollution and/or eutrophication (Armitage et al., 1983). Samples were prepared as above and identified using standard texts (Croft, 1986; Williams and Feltmate, 1992). This biotic index was developed for running waters but is effective for lakes (e.g. Krno et al., 2006). Modified versions such as the Spanish BMWP (Alba Tercedor and Sa´nchez Ortega, 1988), may be more robust for diverse faunas of carbonate-rich waters of the circum-Mediterranean, but diversity was sufficiently low, and representativity of groups high, that the original system was deemed applicable. Rare occurrences of damsel flies (Odonata) were not identified to family level. Of the three relevant families in the scoring system, two (Platycnemidae and Coenagriidae) command a score of six and one (Lestidae) scores eight. An approximate score of six was adopted. Spatial variation in invertebrate distribution was explored using principal components analysis (PCA), which assumes a linear species response and is appropriate for small ecological data-sets (Jongman et al., 1995). In the absence of a larger environmental data-set, direct gradient analysis (redundancy analysis) was not appropriate. Since each sample represented organisms preserved in a ca. 25 cm-depth sediment sample, and some organisms (ostracods, molluscs, Chironomidae) preserve in sediment, whereas others (e.g. Odonata, Hemiptera) do not, the two groups are not equivalent numerically. Rather than transform species data to proportions, the analysis was performed on abundance data, transformed to Cornell format using C2 v. 1.4.2 (Juggins, unpublished), and PCA was performed using Canoco v. 3.14 (ter Braak, 1990). Results were displayed graphically using C2.

4.2.

Palaeolimnology

4.2.1.

Collection of sediment cores

A coring location was selected away from the immediate influence of the R. Mustafakemalpasßa, with the aims of (1) obtaining a sufficiently long chronological record with a short core

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Fig. 2 – Map showing the location of transect sites A and B. Inset A: location of sampling sites within Transect A. Inset B: location of sampling sites within Transect B, and location of the coring site for UL20A and UL20B.

(with the reported local siltation impact offshore from the delta), and (2) assessing lake-wide water quality status in an offshore location which was not reportedly subject to maximum impact (again, from the river). Co-ordinates of the sampling site were recorded using a Garmin GPS. Two cores, UL20A (32 cm) and UL20B (21 cm) were collected from within 1 m apart on 9 December 2000 (4011 0 0700 N, 2840 0 2000 E) in 2 m of water to the northeast of the lake basin, using a Glew gravity corer (Glew, 1991) (Fig. 2). Both cores retrieved an undisturbed sediment–water interface. Sediment cores were described and extruded in the field into sterile plastic bags, subsampling at 0.5 cm resolution for the top 1 cm, and 1 cm thereafter. In the laboratory sediment samples were stored at 4 C. The longer UL20A was selected as the master core and UL20B was retained for 210Pb and 137Cs dating.

4.2.2.

Basic sediment properties

Subsamples of ca. 1–2 g were taken at 1 cm intervals for measurement of percentage organic and carbonate content, by oven drying overnight at 50 C, and loss on ignition at 550 C

and 925 C, respectively, using standard techniques (Dean, 1974). Following calculation of organic and carbonate content, the additional parameter of carbonate-free organic carbon was calculated as the proportion of weight loss at 550 C, taking 100% as the sum of organic + final residue weight after ignition at 925 C.

4.2.3.

Diatom analysis

Subsamples of ca. 0.1 g were prepared using standard techniques (Battarbee, 1986) with hot H2O2 and HCl to oxidise organic matter and remove carbonates, respectively, and using Naphrax as a slide mountant. A resolution of 2 cm was applied initially, counting the upper sequence at 1 cm thereafter to improve interpretation of recent change. Where diatoms were well preserved, ca. 500 valves per slide were counted under oil immersion with phase contrast at a magnification of 1000·, on a Leica DMLB light microscope. Counts were reduced in some samples due to poor preservation. Taxonomy and nomenclature follows Krammer and Lange-Bertalot (1986, 1988, 1991a,b).

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Diatom-inferred total phosphorus (DI-TP) reconstruction was performed by classic weighted averaging regression and calibration, using C2, and based on the Combined European TP training set (Battarbee et al., 2000). The training set was collected largely from temperate Western Europe: shallow, hypereutrophic British and Scandinavian lakes (Anderson et al., 1993; Bennion, 1994; Bennion et al., 1996; Lotter et al., 1998), French crater lakes (Rioual, 2000) and central Alpine oligotrophic–mesotrophic lakes (Wunsam and Schmidt, 1995). There is not a more local TP training set. Results were displayed using Tilia, Tiliagraph and TGView (Grimm, 1991). Stratigraphic zone boundaries were defined using constrained incremental sum of squares, on square-root transformed data, using the program CONISS (Grimm, 1987).

4.2.4.

Ostracod and mollusc analysis

Sediment subsamples were taken at 1 cm intervals and prepared using standard techniques of drying and subsequent wet sieving at 180 and 63 lm (Griffiths and Holmes, 2000). Samples were hand picked while viewed at 10· on a Prior binocular microscope and mounted on micropalaeontological slides using gum tragacanth; larger gastropods were stored in glass tubes. Adult ostracods were identified and counted separately from juveniles. Abundance was expressed as individuals per 100 g dry sediment.

4.2.5.

Stable isotope analysis

Oxygen and carbon stable isotope ratios were measured on the authigenic (<80 lm fraction) carbonate fraction and on biogenic carbonate (ostracod valves). For authigenic carbonate, 1–2 g bulk sediment was subsampled at each level of UL20A and disaggregated in 5% sodium hypochlorite solution (10% chlorox) for 24 h to oxidise reactive organic material. Samples were then sieved at 80 lm to remove biogenic carbonates. The <80 lm fraction was washed with deionised water, dried at 40 C and ground in agate. The authigenic carbonate was reacted with anhydrous phosphoric acid in vacuo overnight at a constant 25 C. The CO2 liberated was separated from water vapour under vacuum and collected for isotope analysis. Measurements were made on a VG Optima dual inlet mass spectrometer. Overall analytical reproducibility was >0.1& for d13C and d18O (2r). Isotope values (d13C, d18O) are reported as permil (&) deviations of the isotopic ratios (13C/12C, 18O/16O) calculated to the VPDB scale using a within-run laboratory standard calibrated against NBS standards. To avoid within- and between-species variability, analysis of ostracod carbonate was based on up to 10 valves per sample of the dominant species, Physocypria kraepelini, cleaned with deionised water using a 0000 paintbrush. The species was present throughout the sequence, is relatively short lived, and is nektonic, that is, living in the water column; nektonic taxa should respond more directly to hydrologically mediated isotopic changes than bottom dwellers. Individuals comprising ca. 60 lg of ostracod carbonate were analysed using an automated common acid bath VG Isocarb + Optima dual inlet mass spectrometer. Where sufficient numbers of adults were preserved in a subsample, analysis was performed on several individuals to estimate the mean and standard deviation. Isotope values (d13C, d18O) are reported as

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permil (&) deviations of the isotopic ratios (13C/12C, 18O/16O) calculated to the VPDB scale using a within-run laboratory standard calibrated against NBS standards. Analytical reproducibility is typically <0.1& for both d13C and d18O (based on similarly sized laboratory standards).

4.2.6.

210

Pb and

137

Cs radiometric counting

Subsamples from UL20B were weighed and counted on a Harwell Instruments, Broad Energy (BE5030) high purity germanium coaxial photon detector. This detector has an ultra low background set up (detector and cryostat) with a 0.5 mm thick carbon-epoxy window and remote detector chamber. Detector specifications were full width at half maximum (‘FWHM’) @ 5.9 keV = 0.45 keV, FWHM @ 1.3 MeV = <1.2 keV. To keep self-absorption differences negligible, standard samples were used to calibrate the detectors using material of similar density and dimensions to the sediment analysed. The NIST standard reference material, SRM4357 was spiked with NIST SRM’s 3164 and 3159, which was configured into the same geometry. A secondary standard was also made in the form of a disc (80 mm diameter) from the same material to which the detectors had been calibrated previously. The 210Pb/226Ra activity ratio was determined from the activities at the 46.5 and 186.3 keV gamma-ray peaks, the latter following correction methods in De Corte et al. (2005). The activity of the 210Pb/214Pb, using the 46.5 keV/295 and 352 keV gamma-rays for 214Pb, and the 210Pb/214Bi ratios using the 46.5 keV/609 and 1764 keV gamma-rays for 214Bi, were also determined. All the ratios were then averaged. The 137Cs activity was determined using the 661 keV peak. Samples were counted for approximately 7–10 days each in order to reduce the uncertainties by accumulating a large number of counts in each analyte peak. Most analyte peaks were >10,000 net counts (i.e. <1% uncertainty). External reproducibility was checked using international standards (NIST-SRM 4357) and was found to be within 0.76%. Ages were obtained using the constant rate of supply (‘CRS’) model (Ivanovich and Harmon, 1992).

5.

Results

5.1.

Limnological survey

From the basic water chemistry and physical limnology (Table 1), pH values were high (>8), with only minor variation between samples. Transparency was relatively low (50– 115 cm), with minimum values in samples A1–2 and B1. The shallower-water samples A1–A5, closest to the R. Mustafakemalpasßa inflow (Fig. 2), had slightly lower dissolved oxygen content (DOC; range 5.6–8.2 mg l1; water depth 60– 110 cm), compared to DOC values of 8.0–10.8 mg l1 and water depth of 125–170 cm in A6–A10 and B1–10. The deepest waters were located close to the coring site at Go¨lyazı, but on water chemistry alone the two sampling zones showed marked similarities. Invertebrate results are given in Table 2 and results of PCA in Fig. 3. PCA Axes 1 and 2 together explain a relatively high percentage of total variance in the species data (49.5%). Fig. 3 shows clear separation of samples from the two tran-

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Table 1 – Table showing the site co-ordinates and basic limnological parameters of transect samples for the modern invertebrate, ostracod and mollusc survey Sample

Oxygen Secchi disc Water Water pH Conductivity Dissolved oxygen content (mg l1) saturation (%) depth (cm) depth (cm) temperature (C) (lS cm1)

Site location

A1 A2 A3 A4 A5 A6 A7 A8 A9 A10

4007 0 4700 N; 4007 0 5200 N; 4007 0 5700 N; 4007 0 6000 N; 4008 0 0300 N; 4008 0 0600 N; 4008 0 0900 N; 4008 0 1100 N; 4008 0 1600 N; 4008 0 1900 N;

2835 0 1800 E 2835 0 2200 E 2835 0 2600 E 2835 0 2900 E 2835 0 2600 E 2835 0 3500 E 2835 0 3300 E 2835 0 3300 E 2835 0 3900 E 2835 0 4400 E

60

21

8.2

533

5.6

61.0

50

100 110 110 125 130 150 140 150

23 26 24 23 25 25 24 24

8.3 8.3 8.4 8.4 8.4 8.4 8.5 8.5

561 544 546 540 527 553 548 533

7.5 6.6 8.2 7.8 9.8 8.7 10.8 9.5

91.1 80.2 95.6 91.3 111.7 105.0 119.3 110.8

60 90 100 100 120 140 100 115

B1 B2 B3 B4 B5 B6 B7 B8 B9 B10

4010 0 4900 N; 4010 0 4900 N; 4010 0 4200 N; 4010 0 3700 N; 4010 0 3100 N; 4010 0 2300 N; 4010 0 1800 N; 4010 0 1100 N; 4010 0 0500 N; 4010 0 0000 N;

2839 0 5800 E 2840 0 0100 E 2840 0 0600 E 2840 0 0700 E 2840 0 1000 E 2840 0 1300 E 2840 0 1500 E 2840 0 1700 E 2840 0 1800 E 2840 0 2100 E

140 140 150 160 170 170 160 170 170 170

22 22 22 22 22 22 22 22 22 22

8.6 8.7 8.7 8.7 8.6 8.6 8.6 8.6 8.6 8.7

550 553 535 530 528 526 528 529 523 522

9.6 9.2 10.4 9.3 8.7 8.5 8.3 7.9 9.0 9.0

104.0 101.0 121.0 109.2 96.6 91.4 96.6 90.8 105.6 104.4

60 80 80 90 80 85 80 100 100 110

Table 2 – Table showing invertebrate abundance (per Ekman grab sample; ca. 253 cm3) and BMWP scores for Transect A and B samples Sample A1

A2

A3

A4

A5

A6

A7

A8

A9

A10

B1

B2

B3

B4

B5

B6

B7

B8

B9

B10

Crustacea Ostracoda Physocypria kraepelini Darwinula stevensoni Ilyocypris gibba Candona spp. (adult) Candona spp. (juvenile)

0 0 0 0 0

15 2 7 0 0

12 1 3 1 2

25 14 5 0 0

10 5 0 0

41 3 9 0 3

22 16 3 0

35 40 5 0 1

40 23 8 0 2

125 91 21 0 13

519 1 1 0 77

279 0 0 0 75

554 0 0 0 105

222 1 0 0 41

168 1 3 0 38

102 5 2 0 61

113 46 26 0 53

36 0 10 1 50

38 0 7 0 74

36 11 19 0 102

Total Ostracoda

0

24

19

44

15

56

41

81

73

250

598

354

659

264

210

170

238

97

119

168

Copepoda Cladocera

0 0

32 40

83 16

54 18

7 15

243 61

46 4

92 1

21 0

152 8

3 6

11 1

14 25

3 0

1 0

4 3

3 0

9 0

2 0

21 0

Insecta Chironomidae Odonata (damsel fly larva) Hemiptera Notonecta ACARI

0 1 0 0 0

21 0 1 0 0

10 0 0 0 0

15 0 0 0 0

21 0 0 1 8

17 0 0 0 0

14 0 0 0 0

17 0 0 0 0

17 0 0 0 1

0 0 0 0 0

48 118 0 0 0

20 0 0 0 0

28 0 0 0 0

17 0 0 0 0

31 0 0 0 0

12 0 0 0 0

54 0 0 0 0

9 0 0 0 0

19 0 0 0 0

24 0 0 0 0

Gastropoda Bithynia spp. Valvata piscinalis Lymnaea peregra

0 0 0

0 0 0

0 0 0

0 0 0

0 0 0

0 0 0

0 0 0

0 0 0

0 0 0

0 0 0

2 2 1

0 0 0

0 0 0

0 0 0

0 0 0

0 0 0

0 0 0

0 0 0

0 0 0

0 0 0

Bivalvia Unio spp. Dreissena polymorpha

0 0

1 0

3 0

0 0

5 0

0 0

0 0

0 0

0 0

0 1

0 0

0 0

0 0

0 0

0 0

0 0

0 0

0 0

0 0

0 0

Oligochaeta Nematoda

27 12

49 101

22 36

36 21

9 16

302 32

30 66

35 114

31 122

4 268

15 156

14 204

101 130

1 404

2 141

26 309

520 312

0 123

12 233

173 128

BMWP score

7

9

9

3

14

3

3

3

3

1

15

3

3

3

3

3

3

3

3

3

2772

B I O L O G I C A L C O N S E RVAT I O N

2.0

1 4 1 ( 2 0 0 8 ) 2 7 6 5 –2 7 8 3

5.0 B7 Oligochaeta

4.0

1.0

3.0

Axis 2

Axis 2

A6

B 10

0.0

B6 A2 A8 B 9 A7 A10 A3 A9 A1

A4 B 8

B4

Nematoda

B3

1.0

B5

B2

Copepoda

0.0

B1

A5

-1.0 -1.0

2.0

Chironomidae Candona spp.

Physocypria kraepelini

Odonata

0.0

1.0

2.0

-1.0 -1.0

Axis 1

0.0

1.0

2.0

3.0

4.0

5.0

Axis 1

Fig. 3 – Scatter plots of Axis 2 against Axis 1 showing the distribution of (a) transect samples and (b) invertebrate taxa in principal components analysis (k1 = 0.28; k2 = 0.22; cumulative percentage variance of the species data for Axis 1 plus Axis 2 = 27.2%).

sects in the direction of Axis 1. This is driven by high abundance of ostracods (P. kraepelini and candonids) and nematode worms in Transect B, vs. higher abundance of zooplanktonic copepods in Transect A. Zooplanktonic cladocera were not abundant, but were also more common in Transect A. Rarer occurrences of other groups such as Odonata (damsel flies) and gastropods did not exert a significant influence on PCA results. It is noteworthy, however, that sample B1, which along with B3 has maximum scores on Axis 1, was the most

diverse assemblage of the data-set (Table 2); this was the only sample from reed beds. BMWP scores (Fig. 4) were low. Only two samples scored >10 (A5 and B1). The only common groups were the low scoring, pollution-tolerant Chironomidae and Oligochaeta. BMWP has the weakness that it does not take abundance into account. Apart from sample B1, the higher scores were due to the presence of sensitive taxa (e.g. Odonata) at very low abundance.

5.2.

Palaeolimnology

5.2.1.

Radiometric dating

16 14

BMWP score

12 10 8 6 4 2 0 A1

A2

A3

A4

A5

A6

A7

A8

A9

A10

Transect A 16

BMWP score

14 12 10

Results of 210Pb and 137Cs dating (Table 3 and Fig. 5) indicated that the sediment record extends back prior to at least the start of the 19th century. The estimated 210Pb age of 1964 ± 6 corresponds well with the peak in 137Cs values at 12.5 cm depth, indicative of the peak in weapons testing in 1963. Fig. 5a shows a clear discontinuity in 210Pb values between samples 15–16 cm and 14–15 cm. This reflects a major shift in sediment accumulation rate, to more rapid accumulation (0.26 kg m2 yr1) after the 1950s (Fig. 5b). Both sets of results indicated some reworking of sediments from the 1960s in the top 2 cm, with anomalously low 210Pb and high 137Cs values, respectively. Sediment disturbance was not observed during coring, and (see Diatom Analysis) the surface sediment of the master core was intact. Recent sediments may have been affected by the location of Lake Uluabat close to the epicentre _ of the 1999 Izmit earthquake (Homan and Eastwood, 2001).

8

5.2.2.

6 4 2 0 B1

B2

B3

B4

B5

B6

B7

B8

B9

B10

Transect B Fig. 4 – Graphs of invertebrate BMWP scores for Transect A and B samples.

Basic sediment properties

The two cores, UL20A and UL20B, were of homogeneous brown silty clay with no major lithostratigraphic boundaries. Both showed a trend towards less compaction in the upper sequence, with compact sediment from the core base to ca. 22 cm depth and soft, unconsolidated sediment above ca. 5 cm (ca. 1987). Loss-on-ignition results for UL20A (Fig. 6) show a clear trend towards increasing organic content from low values of

B I O L O G I C A L C O N S E RVAT I O N

Table 3 – Table showing the results of Depth (cm) Unsupported (Bq kg) 0.25 0.75 1.50 2.50 3.50 4.50 5.50 6.50 7.50 8.50 9.50 10.50 11.50 12.50 13.50 14.50 15.50 16.50 17.50 18.50 19.50 20.50

210

210

34.91 16.51 99.20 85.98 101.30 69.90 69.07 54.27 44.96 38.61 34.25 34.07 34.36 31.68 21.51 20.59 48.17 45.02 22.65 12.96 12.40 5.89

137

Pb and

Pb Unsupported (Bq kg)a

Cs radiometric analysis of UL20B

210

2.09 1.42 5.14 6.76 7.84 4.63 6.67 3.67 3.83 2.90 2.15 3.02 2.56 3.44 7.52 6.50 15.47 14.60 7.83 7.26 7.03 3.81

2773

1 4 1 ( 2 0 0 8 ) 2 7 6 5 –2 7 8 3

Pb

137 137 Cs Cs (Bq kg) (Bq kg)a

39.70 37.21 35.87 33.67 31.20 31.82 41.86 45.80 47.17 55.74 55.75 59.60 60.27 72.97 62.62 49.47 52.82 49.02 45.31 43.63 48.70 37.15

1.82 2.03 0.85 1.20 1.50 0.91 1.73 1.41 1.61 1.78 1.43 2.98 1.58 1.88 3.53 1.37 1.42 1.27 1.22 1.19 1.24 0.88

Estimated year Year of of deposition depositiona 1999.66 1999.42 1997.76 1995.57 1992.66 1989.33 1986.74 1983.55 1980.79 1978.27 1974.36 1973.30 1968.03 1964.09 1959.84 1955.60 1943.25 1927.18 1911.38 1892.07 1867.56 1692.02

5.91 4.06 9.96 9.27 10.06 8.36 8.31 7.37 6.71 6.21 5.85 5.84 5.86 5.63 7.64 8.54 9.94 14.71 13.76 23.60 33.52 92.43

ln Unsupported (Bq kg)

210

Pb

3.55 2.80 4.60 4.45 4.62 4.25 4.24 3.99 3.81 3.65 3.53 3.53 3.54 3.46 3.07 3.02 3.87 3.81 3.12 2.56 2.52 1.77

a Standard error.

8–10% from the core base to 13 cm depth (ca. 1962), and rising thereafter to a maximum of 17% at the sediment surface. The CaCO3-free organic curve gives a better representation of changes in the delivery of organic carbon to the sediment, exhibiting a minor rising trend from ca. 24 cm depth (pre19th century) to 17 cm depth (1920s), and a consistent rise thereafter from 12% to 29% at the sediment surface, which also exhibits an acceleration above ca. 13 cm depth. The carbonate curve almost paralleled these trends, with relatively stable values of ca. 15% from 32 to 21 cm, where compaction was greatest, rising to a peak of 29% at 4 cm depth.

5.0

Ln210Pb (Bq kg)

4.0 3.0

Middle = 0.26 kg m-2 a-1

2.0 Base = 0.07 kg m-2 a-1

1.0

5.2.3.

0.0 0

5

10

15

20

25

20

25

Depth (cm)

Estimated year of Deposition

2020 2000 1980 1960 1940 1920 1900 1880 1860 1840 1820 0

5

10

15

Depth (cm)

Fig. 5 – Graph of unsupported ln 210Pb against depth for core UL20B (a) and of estimated age against depth for (b), showing the location of the inferred change in sediment accumulation rate (dashed line).

Stable isotopes

Oxygen and carbon stable isotope values for bulk authigenic carbonate and ostracod calcite (Fig. 6) are highly dissimilar although this in part is a function of the different sampling regimes. Authigenic carbonate values are relatively stable and negative. d13Cauth varies in the range 4.0& to 6.6& and d18Oauth in the range 6.8& to 8.1&. The ostracod, P. kraepelini, was sufficiently well preserved for stable isotope analysis of 11 sample levels above 21 cm depth, but with a gap between 13 and 7 cm depth. At each level, 5–10 individual valves were analysed and the data are shown as the mean and range. In contrast to the relatively stable authigenic carbonate values, the ostracod data show a marked shift at ca. 13 cm depth (ca. 1962). Values from the base of the profile to ca. 13 cm depth are higher (d13Cost range of mean values 0.9& to 3.6&; d18Oost range of mean values 2.8& to 4.1&). There is a marked shift to more negative values above ca. 13 cm (d13Cost range of mean values 0.9& to 3.6&; d18Oost range of mean values 4.4& to 6.0&). The error bars are also much wider for both isotopes in the

2774

B I O L O G I C A L C O N S E RVAT I O N

1 4 1 ( 2 0 0 8 ) 2 7 6 5 –2 7 8 3

Stable isotopes (‰ vs. VPDB)

Loss on ignition (%) organic content 20

30

10

carbonate content 20

bulk authigenic carbonate

ostracod carbonate

δ 18Oauth δ13Cauth

30

-6.0

-8.0

δ 18Oost ( ) -6.0

-4.0

δ13Cost ( ) -2.0

0.0

0

5

10 Depth (cm)

Estimated date

10 2000 1998 1996 1993 1989 1987 1984 1981 1978 1974 1973 1968 1964 1960 1956 1943 1927 1911 1892 1868 1692

non-carb organic content

15

20

25

30

35

Fig. 6 – Diagram comparing organic and carbonate content, bulk authigenic and ostracod stable isotope data in the sediment core, UL20A. Organic content is expressed both as % loss on ignition (LOI) at 550 C, and as a percentage recalculated by exclusion of the % carbonate. % carbonate was calculated from LOI at 925 C. Subscript ‘auth’ denotes bulk authigenic carbonate; ‘ost’ denotes ostracod carbonate.

lower sequence, reflecting the greater variability of results for analysis of individual valves than in the upper sequence. Above ca. 13 cm depth, ostracod stable isotope values show weak covariance, but there is no relationship below 13 cm depth.

5.2.4.

Diatom analysis

One hundred and thirty-nine diatom taxa were identified, of which 95 were present in the training set for diatom-inferred total phosphorus (DI-TP) reconstruction, allowing reconstruction based on >80% of taxa in each sample. The summary diatom diagram (Fig. 7) shows lower total counts indicative of poor preservation in subsamples 11–12 cm, 14–15 cm, 20– 21 cm and 24–25 cm, below which diatoms were either absent or present as uncountable fragments. Three biostratigraphic zones could be recognised using CONISS. Diatom zone D1 (24.5–17.5 cm; pre-19th century to ca. 1911) was dominated by the common epiphytes (Germain, 1981), Epithemia sorex, Epithemia adnata, Rhoicosphenia abbreviata and Rhopalodia gibba, along with the cosmopolitan taxa, Cocconeis placentula and Amphora pediculus. The planktonic taxon, Aulacoseira granulata, was common in two of the four subsamples, a species characteristic of turbid, eutrophic waters. The transition to zone D2 (17.5–11.0 cm; ca. 1911– 1970) was marked by increased relative abundance of eutrophic planktonic species, A. granulata, Stephanodiscus hantzschii, Stephanodiscus medius, Cyclostephanos dubius and Cyclotella meneghiniana. These increases were at the expense of the epiphytic species. Zone D3 (11.0–0.0 cm; ca. 1970–2000) was marked by a further decline in relative abundance of Epithemia spp. and other epiphytes, with the consistent high relative abundance of the previous range of eutrophic planktonic

species, and a peak in DI-TP at 2.5 cm depth (ca. 1996). The relative abundance of A. pediculus also increased compared to zone D1; this species is often found in open-water, plankton-dominated samples (e.g. Roberts et al., 2001; Wilson et al., 2008), presumably exploiting floating algae or plants as a substrate, but is also a common coloniser (with C. placentula) on P. australis in neighbouring Lake Manyas under conditions of high turbidity and sediment load (Albay and Akc¸aalan, 2003). A range of more fragile taxa including small Navicula and Nitzschia spp. were also present consistently, some of which (Nitzschia palea, Nitzschia hungarica, Navicula cryptotenella) are known for their pollution tolerance. The more fragile of these taxa may have been under-represented in the lower sequence due to dissolution. The surface sediment sample was separated out in CONISS. This was probably because it contained a higher relative proportion of live frustules than sediment samples below, which in a well-mixed lake should integrate the diatom flora of the lake as a whole. The absence of E. adnata in particular indicates there was no reworking of sediment during coring, and the master core was undisturbed. The DI-TP reconstruction indicates that the lake has been eutrophic (>100 lg l1 TP) since prior to the 19th century. With the increase in relative abundance of eutrophic taxa, the subtle trend towards rising values towards the sediment surface, in Zone D1, provides evidence for anthropogenic eutrophication since the start of the 20th century.

5.2.5.

Ostracods

Ostracod results (Fig. 8) lacked evidence for major shifts in species assemblage composition. The most marked biostratigraphic transition occurred at 6 cm depth (ca. 1985). Spanning

B I O L O G I C A L C O N S E RVAT I O N

2775

1 4 1 ( 2 0 0 8 ) 2 7 6 5 –2 7 8 3

Planktonic

Benthic

ta ep

Pl an kt on ic Be nt hi c C ou nt D I-T P

va r.

ol i es a hi s t m a c ia m tum um a a tzs iu ius ian la la rev at la natunca aceea a s os at an ed u b hin el i u l ta b t a ita lla in a radntu mi tru oliv sol ibi ulu cer enta ola ta cen ab ba n u s h s m s d eg x t c a a a s h o a ib a pu io ito ce cu a a a p dic to yc pt ne tic lita lea ognpite n i a gr iscuiscu ano en ore l d p n g ln a d p a a m m r m e p y e n a c ira d d ph a m a s ia a is phe dia ia u a c ra ca pl ma ne ne pleua a a p a lea lib cr a v a fo a soa p a in a ca se anoanoste tell mi m one os alo lar lari ula ula ulasig phopho to chi or ell or ula or chi chi chi chi chi o e e h h o o i i c c c h b h c h c a c la ep ep cl cl ith pith occ hoi hoprag rag avi avi avi yro om om ym itzs mp ym mp avi mp itzs itzs itzs itzs itzs Au St St Cy Cy Ep E C R R F F N N N G G G C N A C A N A N N N N N 0

599 611 535 569 815 580 569 600

2 4 6 8 10

Depth (cm)

CONISS Coniss

573

D3

575 382 550

12 14

D2

311

16

562

18

440

20

272

22

D1

574

24

208 20

20

% % % % %

20

%

20

%

20

20

20 40 60 80 100

% % % % % % % % % % % % % % % % % % % % % % %

%

50 100 150 200

μg l-1

1.0

2.0 3.0

Total sum of squares

Fig. 7 – Summary diatom diagram for UL20A showing all taxa present at P2% relative abundance, the proportion of planktonic and benthic taxa, the diatom count per slide and diatom-inferred total phosphorus (DI-TP).

most of the sequence, Zone O1 (31.5–6.0 cm; pre-19th century to ca. 1985) was dominated by Candona spp., with lower abundance of P. kraepelini, Cypridopsis vidua and Ilyocypris gibba. The only identifiable adult Candona specimens were of C. angulata. Ostracods were present at very low abundance (<1 g1), rising slightly towards the upper zone boundary. The transition to Zone O2 (6.0–0.0 cm; ca. 1985–2000) was marked by an increase in the relative abundance of the limnic species, P. kraepelini, to >60% at the expense of benthic candonids, and the disappearance of I. gibba. Ostracod abundance rose to maximum values of ca. 100 g1 at 1–2 cm depth. Changes in abundance may be partly a function of higher preservation potential towards the sediment surface.

5.2.6.

Mollusca

Mollusc assemblages (Fig. 9) were dominated by gastropods; apart from at 1–2 cm depth, bivalves were absent or rare. All molluscs were rare in the compact sediments of Zone M1 (31.5–22.0 cm depth; pre-19th century), with occasional shells of the gastropods, Planorbis spp., Physa acuta and an indeterminate larval protoconch, and the bivalve genus, Pisidium. An increase in abundance and diversity occurred in Zone M2 (22.0–0.0 cm; pre-19th century to 2000), partly reflecting better preservation, and peaked at 237–238 inds. 100 g1 between 4 and 6 cm. Zone M2 exhibited co-dominance by the aquatic prosobranch (gill-breathing) Valvata piscinalis and pulmonate (air-breathing) Planorbis spp. Larval shells were abundant in the first half of the zone prior to the overall increase in

mollusc abundance above 10 cm depth. Mainly above this depth, other gastropods were present sporadically, including the pulmonates, Lymnaea peregra, Lymnaea truncatula, P. acuta and Physa fontanalis, and the prosobranchs Bithynia sp. and Bythinella sp.

6.

Discussion

6.1.

Current chemical and ecological status

The eutrophic status of Lake Uluabat is recognised from water chemistry monitoring (e.g. Dalkıran et al., 2006) and macrophyte surveys (Lammens and van den Berg, 2001), but ecological status at lower trophic levels had not been previously explored. The high pH values are typical of alkaline, karstic lakes, and the low water clarity is typical of shallow, turbid, eutrophic lakes. The general lack of between-sample variability in measured water chemistry parameters is consistent with full mixing in a shallow lake and suggests that, in spite of reported differences in residence time across the basin (Lammens and van den Berg, 2001), there is no strong evidence for local variability. The slightly lower DOC values in the shallower waters close to the Mustafakemalpasßa delta may just reflect water depth/temperature effects, since these samples do not also exhibit the lowest BMWP scores. Our invertebrate biomonitoring study had the limitation of being restricted to a single season (spring), but the combination of consistently low scores and the presence in the surface sediment of diatoms

2776

B I O L O G I C A L C O N S E RVAT I O N

)

)

ia

pr

pr

y oc

y oc

ys

ys

Ph

Ph

e

(J

ta la (J) u g p. gi is is an sp s s s i na na op op pr cy do ndo rid rid o n p p a lIy Ca C Cy Cy vi

k

)

(A

a du

vi

a bb

co d

k

)

a du

ra

p

e ra

e ra

O st

pe

in el

ab un da nc

i(J

i(A

lin

ia

1 4 1 ( 2 0 0 8 ) 2 7 6 5 –2 7 8 3

0 2

Zone O2 4 6 8 10

Depth (cm)

12 14 16 18

Zone O1 20 22 24 26 28 30 32

20

40

60

80

%

20

40

60

20

%

20

%

20

%

20

%

%

40

60

80

%

500

1000

1500

Inds./100g dry sed.

Fig. 8 – Diagram showing the relative and absolute abundance of ostracod taxa in UL20A. Counts are separated into adult (A) and juvenile (J) valves.

typical of eutrophic to hypereutrophic lakes, indicates poor ecological status at all levels of the ecosystem. The low BMWP scores (<10 in most samples) tends to indicate significant bulk organic or nutrient pollution (Abel, 1996). Although designed primarily to improve palaeolimnological interpretation, the homogeneity of ostracod transect samples also indicates low habitat diversity across the open waters. It is noteworthy that the highest BMWP scores (with abundant damsel flies and the only presence of gastropods) derived from sample B1, the only sample located in reed beds rather than the open water. This suggests low scores are partly a function of habitat availability, which must have been reduced with the loss of submerged aquatic macrophyte cover. Our study in 2001 was performed during a year which appeared to be unusual in the lack of development of extensive submerged macrophyte beds; less pollution-tolerant invertebrate groups tend to be more common within the plant-dominated habitat and it is likely that habitat degradation in addition to low water quality is a cause of low diversity. Since 2001 submerged aquatic plant cover has remained low and our study appears to have coincided with the start of a major decline in Lake Uluabat’s biodiversity. It is well demonstrated that a loss of plant cover could have important ramifications at all levels of the ecosystem, since plant habitats provide important refugia for invertebrates such as cladocera which

consume algae and can function to maintain a well-oxygenated, clear water state (Moss et al., 1996). Gastropods (V. piscinalis, L. peregra, Bithynia sp.) were also only present in the reed-bed sample, B1, and we would predict major changes to molluscan community structure if plant loss is prolonged. The results of a study of English ponds by Lodge and Kelly (1985) demonstrated that the loss of submerged macrophytes caused 99% of Lymnaea and ca. 35% of Valvata populations to die, with more rapid recolonisation with regrowth by Lymnaea, but Planorbis and Bithynia were not reduced. While some taxa such as Planorbis spp. can occupy both submerged and emergent macrophyte habitats, V. piscinalis is typically associated only with submerged vegetation, and was restricted to this habitat in eutrophic Radley Pond, UK (Lodge and Kelly, 1985). The Lake Uluabat gastropod community was not found in the open-water mud habitat; at best the gastropod fauna would be reduced to a lower diversity community restricted to shoreline emergent vegetation habitats should plant loss be sustained.

6.2.

Ostracods and molluscs as palaeolimnological proxies

The results of the ostracod and mollusc survey provide information on habitat distribution. The widespread occurrence and abundance of the ostracod, P. kraepelini, is consistent with

ce lv

m iu

es in M de ol t lu sc ab un d

(j) p. sp

id Ps

va

sp p.

s bi or n a Pl

an

et

a ul ra cat g re run pe a) t ) is x al di alb an t (ra a (g uta a n fo a ll ea ae ac a yni hine na mn ysa s t y th y m y Ph Bi B Ly L Ph

sp Pr p. ot oc on sp ch p. ia in d

0

ta lva Va

is al cin s pi

2777

1 4 1 ( 2 0 0 8 ) 2 7 6 5 –2 7 8 3

Bi

B I O L O G I C A L C O N S E RVAT I O N

2 4 6 8

Depth (cm)

10 Zone M2

12 14 16 18 20 22 24 26

Zone M1

28 30 32

20

40

60

80 100

%

20

40

60

80 100

%

20

%%

20

40

60

80 100

%

20

20

% %%

20

40

60

80 100

%

20

40

60

80 100

%

20

40

100

200 300

% Inds./100g dry sed.

Fig. 9 – Diagram showing the relative and absolute abundance of mollusc taxa in UL20A.

its nektonic (swimming) life habit in open waters, although, from its common occurrence close to reed beds in the littoral zone (Altınsac¸lı and Griffiths, 2001), it is not a good proxy indicator for water depth. The higher abundance of the shallow, limnic ostracod, Darwinula stevensoni, in Transect A is consistent with the conjecture of Altınsac¸lı and Griffiths (2001) that, based on its distribution in littoral reed beds, the taxon is common throughout the lake in all areas apart from the northeast. The distribution of I. gibba is more widespread than thought previously, being common in the waters of ca. 1 m depth in this study, rather than showing a preference for depths <0.5 m as suggested by Altınsac¸lı and Griffiths (2001). The marked preference of candonids for the habitats of Transect B may indicate the presence of the benthic species C. angulata, which Altınsac¸lı and Griffiths (2001) found to be particularly common in this part of the lake. In general, the data-set shows strong similarities to the faunal composition of the littoral zone described by Altınsac¸lı and Griffiths (2001), suggesting that in this lake it is not possible to distinguish definitively between open water and littoral zone habitats based on ostracod species composition alone. The exception is C. vidua, which is absent here but was common in the previous study. Since our samples are mainly from open-water habitats, it is possible its presence could be indicative of the proximity of reed beds, since it has a marked preference for well-vegetated zones (Bronshtein, 1947). The apparent habitat preferences of molluscs are discussed above; although rare, their clear, restricted distribution suggests these taxa are useful palaeolimnological indicators for the proximity of plant macrophytes.

6.3. Palaeolimnological evidence for changes in ecosystem status The palaeolimnogical data provide evidence for changes in the physical, chemical and biological environment of Lake Uluabat over time. The modern values for organic content are similar to other Mediterranean karstic eutrophic lakes such as Mikri Prespa, NW Greece (20%; Stevenson and Flower, 1991), and the pattern of increased organic content over time is a common function of eutrophication, with increased internal productivity. The high carbonate content is typical of karstic lakes, and the parallel rise over time may reflect a combination of increased productivity and/or input of minerogenic matter from the catchment. The negative bulk authigenic stable isotope values, and their lack of strong covariance, suggests an open lake with little evaporative concentration. Since there is little surface outflow, this indicates major groundwater aquifer throughput in the karstic system. The results are comparable to modern isotopic values from carbonate precipitating in the lake during 2001, of d13C 4.8&; d18O 7.6& (Leng, unpublished data). The large range in ostracod stable isotope values, which do not follow the same pattern of variation as the bulk authigenic values, reflects the fact that the ostracods capture a moment in time and the lake water is highly seasonal. The diatom data indicate that the lake has been eutrophic since prior to the 19th century and possibly as early as the 17th century, but a subtle diatom-inferred trend of increasing eutrophication correlates with the inferred increases in sediment accumulation rate and organic and carbonate content,

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and in combination provides clear evidence for 20th century nutrient enrichment which accelerated after ca. 1962 (ca. 13 cm depth). The inferred acceleration in nutrient status after ca. 1962 starts soon after the acceleration of sediment accumulation rates indicated by the 210Pb data at ca. 14– 15 cm depth; the apparent 1 cm offset may simply be a function of having used a second core for radiometric dating. In a previous study of sediment accumulation rates in Lake Uluabat, Kazancı et al. (2004) estimated an increasing trend from 0.2 cm yr1 prior to 2000 years BP, to >0.4 cm yr1 in the 20th century. The changes in diatom species assemblage composition are not as dramatic as in some studies of temperate lakes of northwestern Europe (e.g. Soppensee, Switzerland; Lotter, 2001), where recent eutrophication is marked by the first appearance and expansion of eutrophic taxa. In this lake, however, which has been eutrophic since at least the start of the 19th century and is known to lack a well-developed planktonic flora due to high turbidity (Karacaog˘lu et al., 2004), the gradual rise in eutrophic planktonic taxa does indicate accelerated eutrophication. Perhaps the most serious implication of the diatom data is that the rise of planktonic taxa occurs largely at the expense of epiphytic taxa. The decline in Epithemia spp. to <10% abundance above ca. 13 cm depth (ca. 1962) is likely to reflect a sustained reduction in submerged aquatic macrophyte cover. As noted, macrophyte cover is often the mainstay of ecosystem health in a eutrophic lake. From pre-2000 data, Bekliog˘lu et al. (2006) observed that plant growth in Lake Uluabat was most extensive in its shallow phases. The lake is currently in a shallow state, so the loss of plant cover, which has accelerated since 2000, indicates major ecological impact. Other palaeoecological data are provided by ostracods and molluscs, which do not exhibit a major transition in ca. 1962. The ostracod fauna is similar to that of the northeastern transect survey, being dominated by candonids, with increased abundance of the nektonic taxon, P. kraepelini, after ca. 1985. The increase in the latter would be consistent with the effects of reduced plant cover since 1985, but co-dominants are common in the reed beds of the modern littoral zone (Altınsac¸lı and Griffiths 2001). C. vidua, for example, is common above 26 cm depth. This may indicate on the one hand that until very recently the lake has been well vegetated; the weakness of P. kraepelini as a proxy for open water habitats was discussed above. On the other hand, C. vidua has a reported intolerance of very low oxygen availability (Meisch, 2000), and its presence is consistent with the directly measured water column parameters. From the foregoing, the co-dominance of V. piscinalis and Planorbis spp. in the molluscan fauna, with rare associated taxa which are common the modern lake, supports the inference of a well-vegetated lake throughout the recent past. As with the ostracod record, the similarity to the modern fauna (which is common in eutrophic ponds; Lodge and Kelly, 1985), and the abundance of pulmonate taxa which can tolerate relatively low oxygen conditions, again suggests that the lake has been eutrophic throughout. The transition in ca. 1962 also correlates, as far as ostracod preservation permits the definition of the transition, with the major shift in d18Oost values, from more positive, fluctuating

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values in the lower record to more negative, stable values in the upper record. This we suggest is due a greater seasonality in the lower record. The weak covariance between d13Cost and d18Oost above ca. 13 cm depth, and lack of covariance below, may indicate the lake became more hydrologically ‘closed’, or endorheic, after ca. 1962. In a hydrologically stable lake, a shift to more negative oxygen stable isotope values would indicate reduced rather than enhanced evaporative concentration. Here, it is more likely to indicate a seasonal shift in the provenance (spring vs. river water) and isotopic composition of inflowing water, since it is not reflected in an associated shift in bulk stable isotope values. Equally, since both oxygen and carbon isotope values change (rather than carbon alone), it is unlikely to have been driven by ecosystem shifts such as changes in the trophic structure. The diatom planktonic:benthic ratio may also be influenced by changing lake level, with increases in the proportion of plankton at the coring site with rising lake level. In this study, however, it is impossible to infer lake-level change with confidence. Although the results of water-level and surfacearea monitoring data are so contradictory, the consensus is that, if anything, the lake has shallowed over the last decades. The increase in diatom plankton in the upper sequence is consistent both with higher productivity and higher water levels, but can only be interpreted logically in terms of the former.

6.4.

External impacts

In the light of the fragmentary and contradictory record of changing land-use practices, industrial and urban activity, and water management practices outlined above, all of which lack clear chronological detail, it is impossible to determine precisely the relative impacts of these multiple stressors, but some useful conclusions may be drawn. Our results confirm (as in the Holocene study of Kazancı et al., 2004), that a pattern of increased sediment accumulation rates was initiated in the early 20th century, and suggest that eutrophication has been driven at least in part by nutrient input from sediment supply. The most likely cause, as suggested by Kazancı et al. (2004), is deforestation and the expansion of agriculture in the catchment. High estimated sediment accumulation rates in the early mid-20th century in karstic _ Lake Iznik, western Turkey (Franz et al., 2006) also correlated well with inferred mineralogical evidence for deforestation, although accumulation rates appeared to decrease subsequently with recent nutrient enrichment. An alternate explanation is changing river discharge and siltation from the R. Mustafakemalpasßa. Lammens and van den Berg (2001) suggest discharge has reduced rather than increased since the 1960s, however. They link this with reduced mining activity, although water abstraction (Magnin and Yarar, 1997) must also have had an influence. In either case, this general pattern does not match the inferred trend of accelerated sediment accumulation rate and eutrophication since ca. 1960 in our record. Urban sources may also be significant; Green et al. (1996) noted that phosphorus stripping in sewage treatment plants was deemed too expensive by the State to reduce urban pollution in Lake Burdur, central Turkey. The 1960s are commonly a time of intensification of both agricultural and

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urban pollution across Europe but in the absence of relevant information we cannot ascertain this. The trend from ca. 1960 towards plant loss with accelerated sediment accumulation rate does correlate with ostracod stable isotope evidence for reduced seasonal fluctuation and a shift in the hydrological regime. This suggests that accelerated ecological impact is at least in part a function of water management practices. The wide variation in the lower ostracod stable isotope record is consistent with the summer reproductive biology of P. kraepelini (Meisch, 2000) and probably reflects a greater degree of summer seasonal fluctuation prior to embankment of the lake, which started in 1937, and the subsequent management of the outflow during the 1980–1990s (Lammens and van den Berg, 2001). The reduction in variability in the upper record is consistent with more stable lake levels from the 1980s; we lack ostracod data for ca. 1960–1980 to define these trends in more detail. With artificial management of the River Mustafakemalpasßa, it is possible that with reduced inflow the hydrological input from springs is more significant than previously, although the lack of a response in the bulk authigenic data suggests a more seasonal and/or local change in hydrological regime.

6.5.

Implications for lake management

From this study, the most serious impact on the physicochemical and ecological status of Lake Uluabat appears to have been during the 1960s, against a trend of rising nutrient levels since the start of the 20th century. The most important outcome of the palaeolimnological study is that there is clear evidence for the impact of both catchment land-use activities and water management practices, and that the most rapid and marked change in ecological status appears to be associated more with the latter. Since the 1960s, an additional source of pressure from nutrient enrichment must also derive from the reported recent switch of bird migration routes from Lake Manyas to Lake Uluabat as water quality deteriorated in the former (cf. Noordhuis et al., 2002). The loss of aquatic macrophyte communities since 2000 has also been observed, and the poor ecological status of the modern lake at lower levels of the trophic web. Without intervention, it seems likely that the endpoint for Lake Uluabat will be to become as degraded as Lake Manyas. In the context of the WFD approach to conservation and restoration of lakes, it has been ascertained that there is no ecologically distinct ‘natural baseline’ to define as a restoration target. A clear target would be to restore the lake to its pre-1960s state, however. Our study confirms the suggestion of Lammens and van den Berg (2001) that a reduction in nutrient loading alone would be insufficient, and that natural water-level fluctuations must also be restored. An obvious restoration strategy in addition to reducing external nutrient input, would be to encourage regrowth of littoral reed beds, which were formerly more extensive, to act as a buffer zone for nutrient input (Moss et al., 1996). The restoration of natural fluctuations again becomes significant, since Lammens and van den Berg (2001) predicted the loss of reed beds over time under the current regime. A key to improving ecological status is to encourage submerged plant regrowth. In Lake Uluabat, a reduction in exter-

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nal nutrient input alone would be unlikely to be sufficient. In lake restoration, plant regrowth is often hampered by a variety of factors including grazing and/or bioturbation by birds (e.g. Noordhuis et al., 2002; Irfanullah and Moss, 2004), or fish (e.g. Korner, 2001; Matsuzaki et al., 2007). While fish stocks including the turbidity-inducing carp have declined (Lammens and van den Berg, 2001), reported pressure from bird grazing is extreme. Our results also indicate that the reduction in aquatic macrophytes is linked to changes in water management practices. A similar phenomenon was observed by van Geest et al. (2005), who demonstrated the negative impact of reduced water-level fluctuations on aquatic vegetation succession in floodplain lakes of the Lower Rhine. In Lake Uluabat, which appears to have undergone a long-term trend towards reduction in submerged macrophyte cover driven by multiple ecosystem impacts, it is unlikely that ecosystem ‘stability’ could be restored without recourse to biomanipulation (cf. Bootsma et al., 1999). Again, an obvious strategy which has proved successful in other lakes would be to encourage recolonisation by exclusion of bird and fish populations in artificial embayments. In the longer term, however, short of culling, the only viable solution to the increased pressure from migratory birds would be to carry out a major restoration project on neighbouring Lake Manyas.

6.6.

Wider implications: the conservation of karstic lakes

Even in research focused specifically on the EU WFD, there has been a marked bias in conservation-based palaeolimnology towards temperate glacial lakes of northwestern Europe (e.g. Jeppesen et al., 2002; Battarbee et al., 2005; McGowan et al., 2005; Bradshaw et al., 2006; Leira et al., 2006), and there is a dearth of palaeolimnological impact studies across the circum-Mediterranean. In shallow, productive lakes, much of the research, as here, has exploited the value of diatoms as sensitive environmental indicators of trophic status, while strengthening interpretation of ecosystem status by employing a multi-proxy approach (Bennion and Battarbee, 2007). The problem is not simply one of a lack of relevant diatombased training sets (cf. Reed, 2007) and of sufficient knowledge of pre-impact reference states. Many lakes across the circum-Mediterranean are karstic, groundwater-fed systems in tectonically active areas and the assumption that the ‘temperate-lake’ approach to evaluation of ecological status is valid has not been tested. The results of this study are important in demonstrating the response of a karstic lake ecosystem to external and internal stresses. Here, the results of diatom analysis showed a relatively subtle eutrophication response. In a palaeolimnological study of shallow Lake Mikri Prespa (Greece), Stevenson and Flower (1991) also demonstrated little diatom response in spite of accelerated sediment and nutrient input and water abstraction (Stevenson and Flower, 1991; Hollis and Stevenson, 1997). Similarly, in shallow Lake Dojran (Greece-Former Yugoslav Republic of Macedonia), Griffiths et al. (2002) interpreted a subtle diatom-inferred trend towards eutrophication, and a stable ostracod fauna, as indicative that in spite of high nutrient loading and excessive water abstraction, the ecological status of the lake had not been seriously affected.

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Several authors (e.g. Hollis and Stevenson, 1997 for Mikri Prespa; Bertahas et al., 2006 for Lake Trichonis, Greece; de Vicente et al., 2006 for Laguna Nueva, Spain) have argued that high groundwater discharge in karstic lakes buffers them from the effects of accelerated nutrient input. In a temperate lake, a subtle diatom response may indeed be indicative of minimal impact, with little cause for concern. We have suggested previously (Griffiths et al., 2002), however, that karstic lakes may exhibit a stable phase of apparent buffering by groundwaters, but that this may be followed by an ecological threshold of major ecosystem impact. In Lake Uluabat, this pattern is suggested by the rapid loss of aquatic macrophytes since 2000. In Mikri Prespa, the eutrophic diatom A. granulata is now abundant (G. Wilson, personal communication), while Lake Dojran has all but disappeared and is highly eutrophic (S. Krstic¸, personal communication). Although rather anecdotal, all these case studies support the contention that signs of apparently minor ecological change should be taken more seriously in karstic, groundwater-fed lakes than in glacial lakes. The study also demonstrated the significant impact of changed water management practices on the ecological status of Lake Uluabat. Water abstraction is not a major issue in humid regions, and glacial lakes do not exhibit the same degree of natural lake-level fluctuation as karstic lakes such as Lake Uluabat and many other fresh lakes across the circum-Mediterranean. For obvious reasons, the larger monitoring projects in northwestern Europe do not have a focus on hydrological impact. As cited here, individual studies have been carried out, but the results of this study demonstrate clearly the need for larger-scale monitoring and palaeolimnological research into the additional impacts of water management practices on ecology.

Acknowledgements We would like to offer our sincere thanks to the various organisations who provided support for this project, comprising the Royal Society (RSRG 22163 to J.M.R.), the British Council Britain–Turkey Partnerships Programme (H.I.G., S.A., J.M.R.), and the Rotary Club of Turkey (S.R.). The project was carried out during the tenure of a Leverhulme Special Research Fellowship to J.M.R. (SRF/66). Thanks are also due to John Garner and Keith Scurr for help with the map, to Songul Altınsac¸lı for help in the field, and to two anonymous referees for their constructive comments on the manuscript. We dedicate this paper to the memory of Huw and his undying enthusiasm.

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