Cite this paper:
ZHANG Xiaosen, XU Xinyu, Jane M. REED. Sedimentary diatom and pigment-inferred recent anthropogenic accelerated eutrophication of a Mediterranean lake (Lake Dojran, Republic of North Macedonia/Greece)[J]. Journal of Oceanology and Limnology, 2020, 38(6): 1787-1798

Sedimentary diatom and pigment-inferred recent anthropogenic accelerated eutrophication of a Mediterranean lake (Lake Dojran, Republic of North Macedonia/Greece)
ZHANG Xiaosen1,2, XU Xinyu1, Jane M. REED2
1 Institute of Loess Plateau, Shanxi University, Taiyuan 030006, China;
2 Department of Geography, Geology and Environment, University of Hull, Hull HU6 7RX, UK
Abstract:
Lake eutrophication is recognised as a serious global challenge, and many regional legislative programmes are being made to attempt to relieve nutrient pollution and restore deteriorated lake ecological state. However, it is of primary importance to understand the degradation processes and reference conditions. The palaeolimnological approach allows us to use ecological evidences preserved in lake sediments to track the changes of lake trophic status under human impact. Diatoms, a proxy for ecological and limnological change, and pigments, a proxy for algal production and composition, were analysed on a short sediment sequence from Lake Dojran (Republic of North Macedonia and Greece), and their preservation qualities were evaluated before environmental interpretation. Good diatom preservation is inferred mainly from the consistent co-occurrence of robust, highly-silicified taxa and small taxa throughout the sequence. Pigment evaluation of the comparison between wet sediment samples in dark and cold storage and their corresponding dry sediment samples lyophilized immediately after the recovery reveals that sediment restoration conditions are critical for the accuracy of analysis. We show that the increased chlorophyll and xanthophyll pigment concentrations, particularly the siliceous-algae pigment fucoxanthin and diatoxanthin, together with the distinct increase in diatom concentration, indicate accelerated lake eutrophication and a major ecological shift linked to intensified water abstraction practice and agricultural expansion in the late 18th to early 19th century. Evidence of diatom assemblage composition is muted probably by the dominance of widely-tolerant small fragilaroid species in diatom composition and the better competitive ability of cyanobacteria and chlorophytes than diatoms for low light under eutrophic and turbid conditions. This study improves our understanding of recent human-induced environmental change and current ecological restoration target in this lake.
Key words:    diatom, pigment|Lake Dojran|Mediterranean|lake eutrophication|palaeolimnology   
Received: 2019-12-25   Revised: 2020-02-17
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References:
Athanasiadis N, Tonkov S, Atanassova J, Bozilova E. 2000. Palynological study of Holocene sediments from Lake Doirani in northern Greece. Journal of Paleolimnology, 24(3):331-342, https://doi.org/10.1023/A:1008161819212.
Battarbee R W, Jones V J, Flower R J, Cameron N G, Bennion H, Carvalho L, Juggins S. 2001. Diatoms. In:Smol J P, Birks H J B, Last W M eds. Tracking Environmental Change using Lake Sediments. Volume 3:Terrestrial, Algal, and Siliceous Indicators. Kluwer Academic Publishers, Dordrecht. p.155-202.
Bennion H, Battarbee R W, Sayer C D, Simpson G L, Davidson T A. 2011. Defining reference conditions and restoration targets for lake ecosystems using palaeolimnology:a synthesis. Journal of Paleolimnology, 45(4):533-544, https://doi.org/10.1007/s10933-010-9419-3.
Bennion H, Battarbee R. 2007. The European Union Water Framework Directive:opportunities for palaeolimnology. Journal of Paleolimnology, 38(2):285-295, https://doi.org/10.1007/s10933-007-9108-z.
Bennion H, Carvalho L, Sayer C D, Simpson G L, Wischnewski J. 2012. Identifying from recent sediment records the effects of nutrients and climate on diatom dynamics in Loch Leven. Freshwater Biology, 57(10):2 015-2 029, https://doi.org/10.1111/j.1365-2427.2011.02651.x.
Bennion H, Sayer C D, Tibby J, Carrick H J. 2010. Diatoms as indicators of environmental change in shallow lakes. In:Smol J P, Stoermer E F eds. The Diatoms:Applications for the Environmental and Earth Sciences. 2nd edn.Cambridge University Press, Cambridge. p.152-173.
Bennion H, Simpson G L, Goldsmith B J. 2015. Assessing degradation and recovery pathways in lakes impacted by eutrophication using the sediment record. Frontiers in Ecology and Evolution, 3:94, https://doi.org/10.3389/fevo.2015.00094.
Bronk Ramsey C. 2009. Bayesian analysis of radiocarbon dates. Radiocarbon, 51(1):337-360, https://doi.org/10.1017/S0033822200033865.
Conley D J, Paerl H W, Howarth R W, Boesch D F, Seitzinger S P, Havens K E, Lancelot C, Likens G E. 2009. Controlling eutrophication:nitrogen and phosphorus. Science, 323(5917):1 014-1 015, https://doi.org/10.1126/science.1167755.
Cruces F, Rivera P, Urrutia R. 2010. Observations and comments on the diatom Stephanodiscus minutulus(Kützing) Cleve & Möller (Bacillariophyceae) found for the first time in Chile from bottom sediments collected in Lake Laja. Gayana Botánica, 67(1):12-18. http://doi.org/10.4067/S0717-66432010000100002.
Egeland E S, Garrido J L, Clementson L, Andresen K, Thomas C S, Zapata M, Airs R, Llewellyn C A, Newman G L, Rodríguez F, Roy S. 2011. Data sheets aiding identification of phytoplankton carotenoids and chlorophylls. In:Roy S, Llewellyn C A, Egeland E S, Johnsen G eds. Phytoplankton Pigments:Characterization, Chemotaxonomy and Applications in Oceanography. Cambridge University Press, Cambridge. p.675-822.
Elser J, Bennett E. 2011. A broken biogeochemical cycle. Nature,478(7367):29-31, https://doi.org/10.1038/478029a.
Fourtanier E, Kociolek J P. 2011. Catalogue of Diatom Names, On-line Version, updated 19 Sep. 2011. http://researcharchive.calacademy.org/research/diatoms/names/index.asp.
Francke A, Wagner B, Leng M J, Rethemeyer J. 2013. A Late Glacial to Holocene record of environmental change from Lake Dojran (Macedonia, Greece). Climate of the Past, 9(1):481-498, https://doi.org/10.5194/cp-9-481-2013.
Griffiths H I, Reed J M, Leng M J, Ryan S, Petkovski S. 2002. The recent palaeoecology and conservation status of Balkan Lake Dojran. Biological Conservation, 104(1):35-49, https://doi.org/10.1016/S0006-3207(01)00152-5.
Guilizzoni P, Lami A. 2002. Paleolimnology:use of algal pigments as indicators. In:Bitton G ed. Encyclopedia of Environmental Microbiology. John Wiley & Sons, New York. p.2 306-2 317.
Guiry M D, Guiry G M. 2019. AlgaeBase. World-Wide Electronic Publication, National University of Ireland. http://www.algaebase.org.
Hall R I, Smol J P. 2010. Diatoms as indicators of lake eutrophication. In:Smol J P, Stoermer E F eds. The Diatoms:Applications for the Environmental and Earth Sciences. 2nd edn. Cambridge University Press, Cambridge. p.122-151.
Hobbs W O, Fritz S C, Stone J R, Donovan J J, Grimm E C, Almendinger J E. 2011. Environmental history of a closed-basin lake in the US Great Plains:diatom response to variations in groundwater flow regimes over the last 8500 cal. yr BP. Holocene, 21(8):1 203-1 216, https://doi.org/10.1177/0959683611405242.
Houk V, Klee R, Tanaka H. 2010. Atlas of freshwater centric diatoms with a brief key and descriptions. Part III. Stephanodiscaceae A:Cyclotella, Tertiarius, Discostella. Fottea, 10(Supplement):1-498.
Houk V, Klee R, Tanaka H. 2014. Atlas of freshwater centric diatoms with a brief key and descriptions. Part IV. Stephanodiscaceae B:Stephanodiscus, Cyclostephanos, Pliocaenicus, Hemistephanos, Stephanocostis, Mesodictyon & Spicaticribra. Fottea, 14(Supplement):1-530.
IPCC. 2013. Climate Change 2013:The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge and New York. 1 535p.
Jeffrey S W, Mantoura R F C, Bjørnland T. 1997. Data for the identification of 47 key phytoplankton pigments. In:Jeffrey S W, Mantoura R F C, Wright S W eds. Phytoplankton Pigments in Oceanography:Guidelines to Modern Methods. UNESCO Publishing, Paris. p.447-560.
Krammer K, Lange-Bertalot H. 1986. Süsswasserflora von Mitteleuropa. Band 2/1:Bacillariophyceae. Teil 1:Naviculaceae. Gustav Fischer Verlag, Stuttgart. 876p.
Krammer K, Lange-Bertalot H. 1988. Süsswasserflora von Mitteleuropa. Band 2/2:Bacillariophyceae. Teil 2:Epithemiaceae, Bacillariaceae, Surirellaceae. Gustav Fischer Verlag, Stuttgart. 596p.
Krammer K, Lange-Bertalot H. 1991a. Süsswasserflora von Mitteleuropa. Band 2/3:Bacillariophyceae. Teil 3:Centrales, Fragilariaceae, Eunotiaceae. Gustav Fischer Verlag, Stuttgart. 576p.
Krammer K, Lange-Bertalot H. 1991b. Süsswasserflora von Mitteleuropa. Band 2/4:Bacillariophyceae. Teil 4:Achnanthaceae. Gustav Fischer Verlag, Stuttgart. 437p.
Krammer K. 2002. Diatoms of Europe:Diatoms of the European Inland Waters and Comparable Habitats. Volume 3:Cymbella. Gantner Verlag, Ruggell. 584p.
Lami A N, Guilizzoni P, Marchetto A. 2000. High resolution analysis of fossil pigments, carbon, nitrogen and sulphur in the sediment of eight European Alpine lakes:the MOLAR project. Journal of Limnology, 59(S1):15-28, https://doi.org/10.4081/jlimnol.2000.s1.15.
Lange-Bertalot H. 2001. Diatoms of Europe:Diatoms of the European Inland Waters and Comparable Habitats. Volume 2:Navicula Sensu Stricto, 10 Genera Separated from Navicula Sensu Lato, Frustulia. Gantner Verlag, Ruggell. 526p.
Leavitt P R, Hodgson D A. 2001. Sedimentary pigments. In:Smol J P, Birks H J B, Last W M eds. Tracking Environmental Change using Lake Sediments. Volume 3:Terrestrial, Algal, and Siliceous Indicators. Kluwer Academic Publishers, Dordrecht. p.295-325.
Lešoski J, Zdraveski N, Kristić S. 2010. Preliminary results on cyanobacterial survey on Dojran Lake-the beginning of revealing of the ultimate truth about the lake's water quality. In:Conference on Balkan Water Observation and Information System for Decision Support (BALWOIS). Ohrid.
Levkov Z, Krstic S, Metzeltin D, Nakov T. 2007. Iconographia Diatomologica. Volume 16:Diatoms of Lakes Prespa and Ohrid. Gantner Verlag, Ruggell. 613p.
Levkov Z, Stojanovski P. 2000-2001. Changes in Doiran Lake's diatom flora, a 13 years study. Godisen zbornik Biologija, 53-54:22-38.
Levkov Z. 2009. Diatoms of Europe:Diatoms of the European Inland Waters and Comparable Habitats. Volume 5:Amphora Sensu Lato. Gantner Verlag, Ruggell. 842p.
Lionello P. 2012. The Climate of the Mediterranean Region:From the Past to the Future. Elsevier, Amsterdam. 592p.
Lokoska L, Jordanoski M, Veljanoska-Sarafiloska E, Tasevska O. 2006. Water quality of Lake Dojran from biological and physical-chemical aspects. In:Conference on Balkan Water Observation and Information System for Decision Support (BALWOIS). Ohrid.
Masi A, Francke A, Pepe C, Thienemann M, Wagner B, Sadori L. 2018. Vegetation history and paleoclimate at Lake Dojran (FYROM/Greece) during the Late Glacial and Holocene. Climate of the Past, 14(3):351-367, https://doi.org/10.5194/cp-14-351-2018.
McGowan S, Barker P, Haworth E Y, Leavitt P R, Maberly S C, Pates J. 2012. Humans and climate as drivers of algal community change in Windermere since 1850. Freshwater Biology, 57(2):260-277, https://doi.org/10.1111/j.1365-2427.2011.02689.x.
McGowan S. 2013. Palaeolimnology:pigment studies. In:Elias S A, Mock C J eds. Encyclopedia of Quaternary Science. 2nd edn. Elsevier, Amsterdam. p.326-338.
Paerl H W, Scott J T, McCarthy M J, Newell S E, Gardner W S, Havens K E, Hoffman D K, Wilhelm S W, Wurtsbaugh W A. 2016. It takes two to tango:when and where dual nutrient (N & P) reductions are needed to protect lakes and downstream ecosystems. Environmental Science & Technology, 50(20):10 805-10 813, https://doi.org/10.1021/acs.est.6b02575.
Popovska C, Bonacci O. 2008. Ecohydrology of Dojran Lake. In:Hlavinek P, Bonacci O, Marsalek J, Mahrikova I, eds. Dangerous Pollutants (Xenobiotics) in Urban Water Cycle. Springer, Dordrecht. p.151-160.
Popovska C, Gesovska V, Ivanoski D. 2005. Ecological and hydrological state of Dojran Lake. Vodoprivreda, 37(216-218):175-180.
Reimer P J, Bard E, Bayliss A, Beck J W, Blackwell P G, Ramsey C B, Buck C E, Cheng H, Edwards R L, Friedrich M, Grootes P M, Guilderson T P, Haflidason H, Hajdas I, Hatté C, Heaton T J, Hoffmann D L, Hogg A G, Hughen K A, Kaiser K F, Kromer B, Manning S W, Niu M, Reimer R W, Richards D A, Scott E M, Southon J R, Staff R A, Turney C S M, van der Plicht J. 2013. IntCal13 and Marine13 radiocarbon age calibration curves 0-50,000 years cal BP. Radiocarbon, 55(4):1 869-1 887, https://doi.org/10.2458/azu_js_rc.55.16947.
Reuss N, Conley D J. 2005. Effects of sediment storage conditions on pigment analyses. Limnology and Oceanography:Methods, 3(10):477-487, https://doi.org/10.4319/lom.2005.3.477.
Rimet F, Druart J C, Anneville O. 2009. Exploring the dynamics of plankton diatom communities in Lake Geneva using emergent self-organizing maps (1974-2007). Ecological Informatics, 4(2):99-110, https://doi.org/10.1016/j.ecoinf.2009.01.006.
Roberts N, Reed J M. 2009. Lakes, wetlands, and Holocene environmental change. In:Woodward J C ed. The Physical Geography of the Mediterranean. Oxford University Press, Oxford. p.255-286.
Rockström J, Steffen W, Noone K, Persson Å, Chapin F S, Lambin E F, Lenton T M, Scheffer M, Folke C, Schellnhuber H J, Nykvist B, de Wit C A, Hughes T, van der Leeuw S, Rodhe H, Sörlin S, Snyder P K, Costanza R, Svedin U, Falkenmark M, Karlberg L, Corell R W, Fabry V J, Hansen J, Walker B, Liverman D, Richardson K, Crutzen P, Foley J A. 2009. A safe operating space for humanity. Nature, 461(7263):472-475, https://doi.org/10.1038/461472a.
Ryves D B, Juggins S, Fritz S C, Battarbee R W. 2001. Experimental diatom dissolution and the quantification of microfossil preservation in sediments. Palaeogeography, Palaeoclimatology, Palaeoecology, 172(1-2):99-113, https://doi.org/10.1016/S0031-0182(01)00273-5.
Sayer C D. 2001. Problems with the application of diatomtotal phosphorus transfer functions:examples from a shallow English lake. Freshwater Biology, 46(6):743-757, https://doi.org/10.1046/j.1365-2427.2001.00714.x.
Scheffler W, Morabito G. 2003. Topical observations on centric diatoms (Bacillariophyceae, Centrales) of Lake Como (N. Italy). Journal of Limnology, 62(1):47-60, https://doi.org/10.4081/jlimnol.2003.47.
Smol J P, Stoermer E F. 2010. The Diatoms:Applications for the Environmental and Earth Sciences. 2nd edn. Cambridge University Press, Cambridge. 686p.
Smol J P. 2019. Under the radar:long-term perspectives on ecological changes in lakes. Proceedings of the Royal Society B:Biological Sciences, 286:20190834, https://doi.org/10.1098/rspb.2019.0834.
Sotiria K, Petkovski S. 2004. Lake Dojran-An overview of the current situation. Greek Biotope/Wetland Centre(EKBY) and Society for the Investigation and Conservation of Biodiversity and the Sustainable Development of Natural Ecosystems (BIOECO), Thermi. 117p.
Steffen W, Richardson K, Rockström J, Cornell S E, Fetzer I, Bennett E M, Biggs R, Carpenter S R, de Vries W, de Wit C A, Folke C, Gerten D, Heinke J, Mace G M, Persson L M, Ramanathan V, Reyers B, Sorlin S. 2015. Planetary boundaries:guiding human development on a changing planet. Science, 347(6223):1259855, https://doi.org/10.1126/science.1259855.
Stojov V. 2012. Hydrological state of Dojran Lake related to tectonic, climatic and human impacts. In:Conference on Balkan Water Observation and Information System for Decision Support (BALWOIS). Ohrid.
Sutton M A, Oenema O, Erisman J W, Leip A, van Grinsven H, Winiwarter W. 2011. Too much of a good thing. Nature, 472(7342):159-161, https://doi.org/10.1038/472159a.
Tasevska O, Kostoski G, Guseska D. 2010. Rotifers based assessment of the Lake Dojran water quality. In:Conference on Balkan Water Observation and Information System for Decision Support (BALWOIS). Ohrid.
Temponeras M, Kristiansen J, Moustaka-Gouni M. 2000. Seasonal variation in phytoplankton composition and physical-chemical features of the shallow Lake Doïrani, Macedonia, Greece. Hydrobiologia, 424(1):109-122, https://doi.org/10.1023/A:1003909229980.
Tilman D, Kiesling R, Sterner R, Kilham S S, Johnson F A. 1986. Green, bluegreen and diatom algae:taxonomic differences in competitive ability for phosphorus, silicon and nitrogen. Archiv für Hydrobiologie, 106(4):473-485.
Verdonschot P F M, Spears B M, Feld C K, Brucet S, Keizer-Vlek H, Borja A, Elliott M, Kernan M, Johnson R K. 2013. A comparative review of recovery processes in rivers, lakes, estuarine and coastal waters. Hydrobiologia, 704(1):453-474, https://doi.org/10.1007/s10750-012-1294-7.
Veuger B, van Oevelen D. 2011. Long-term pigment dynamics and diatom survival in dark sediment. Limnology and Oceanography, 56(3):1 065-1 074, https://doi.org/10.4319/lo.2011.56.3.1065.
Wan L L, Chen X Y, Deng Q H, Yang L, Li X W, Zhang J Y, Song C L, Zhou Y Y, Cao X Y. 2019. Phosphorus strategy in bloom-forming cyanobacteria (Dolichospermum and Microcystis) and its role in their succession. Harmful Algae, 84:46-55, https://doi.org/10.1016/j.hal.2019.02.007.
Wang S Y, Xiao J, Wan L L, Zhou Z J, Wang Z C, Song C L, Zhou Y Y, Cao X Y. 2018. Mutual dependence of nitrogen and phosphorus as key nutrient elements:one facilitates Dolichospermum flos-aquae to overcome the limitations of the other. Environmental Science & Technology, 52(10):5 653-5 661, https://doi.org/10.1021/acs.est.7b04992.
Zhang X S, Reed J M, Wagner B, Francke A, Levkov Z. 2014. Lateglacial and Holocene climate and environmental change in the northeastern Mediterranean region:diatom evidence from Lake Dojran (Republic of Macedonia/Greece). Quaternary Science Reviews, 103:51-66, https://doi.org/10.1016/j.quascirev.2014.09.004.
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