Abstract
Lake nutrient budgets and hydrology are being altered by human activities and climate change, yet little is known of how fertilization and hydrologic mechanisms interact to structure assemblages of primary producers. Here, we present sediment records from a large shallow lake in Southwest China to separate the relative importance of nutrients and hydrological fluctuation in regulating the abundance and composition of primary producers during the twentieth century, with a focus on their differential effects on diatoms and cyanobacteria. Shifts in sedimentary particle-size distribution were consistent with the documented events of hydrological regulation during ~ 1953–1971 and subsequent changes in water level associated with severe droughts. Nutrient enrichment since ~ 1965 resulted in a significant increase in the abundance of total phototrophs (pheophytin a, β-carotene) as inferred from pigment analyses, with stronger responses of cyanobacteria (echinenone, zeaxanthin) over siliceous algae (diatoxanthin). Fossil diatom assemblages revealed a pronounced replacement of benthic taxa by eutrophic and planktonic species (e.g., Fragilaria crotonensis) since ~ 1973, but we observed a significant increase of small benthic Fragilaria sensu lato taxa following ~ 2005, which generally corresponded with a moderate increase in fossil pigments. Although eutrophication was the paramount predictor of changes in phototrophs during the last century, variation in lake hydrology due to climate and water management also modulated phototroph abundances and, more recently, diatom assemblages. Specifically, our sediment evidence suggests that hydrological fluctuation has overridden fertilization by nutrients in structuring diatom composition, leading to a heterogeneous response of cyanobacteria and diatoms to external forcing of this shallow lake.
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References
Adrian R, O’Reilly CM, Zagarese H, Baines SB, Hessen DO, Keller W, Livingstone DM, Sommaruga R, Straile D, Donk EV, Weyhenmeyer GA, Winder M (2009) Lakes as sentinels of climate change. Limnol Oceanogr 54:2283–2297
Anderson JN (2000) Miniview: diatoms, temperature and climatic change. Eur J Phycol 35:307–314
Appleby PG (2001) Chronostratigraphic techniques in recent sediments. In: Smol JP, Birks HJB, Last WM (eds) Tracking environmental change using lake sediments. Volume 1: Basin analysis, coring and chronological techniques, vol 1. Kluwer Academic Publishers, Dordrecht, pp 171–203
Barica J, Kling HJ, Gibson J (1980) Experimental manipulation of algal bloom composition by nitrogen addition. Can J Fish Aquat Sci 37:1175–1183
Battarbee RW (2010) Aquatic ecosystem variability and climate change – a palaeoecological perspective climate change impacts on freshwater ecosystems. In: Kernan M, Battarbee RW, Moss B (eds) Climate change impacts on freshwater ecosystems. Wiley, Chichester, pp 15–37
Battarbee RW, Jones VJ, Flower RJ, Cameron NG, Bennion H (2001) Diatoms. In: Smol JP, Birks HJB, Last WM (eds) Tracking environmental change using lake sediments. Volume 3: terrestrial, algal, and siliceous indicators, vol 3. Kluwer Academic Publishers, Dordrecht, pp 155–201
Beaulieu M, Pick F, Palmer M, Watson S, Winter J, Zurawell R, Gregory-Eaves I, Prairie Y (2014) Comparing predictive cyanobacterial models from temperate regions. Can J Fish Aquat Sci 71:1830–1839
Bennion H, Fluin J, Simpson GL (2004) Assessing eutrophication and reference conditions for Scottish freshwater lochs using subfossil diatoms. J Appl Ecol 41:124–138
Berthon V, Alric B, Rimet F, Perga M-E (2014) Sensitivity and responses of diatoms to climate warming in lakes heavily influenced by humans. Freshw Biol 59:1755–1767
Brugam RB, McKeever K, Kolesa L (1998) A diatom-inferred water depth reconstruction for an Upper Peninsula, Michigan, lake. J Paleolimnol 20:267–276
Bunting L, Leavitt PR, Gibson CE, McGee EJ (2007) Degradation of water quality in Lough Neagh, Northern Ireland, by diffuse nitrogen flux from a phosphorus-rich catchment. Limnol Oceanogr 52:354–369
Byllaardt JV, Cyr H (2011) Does a warmer lake mean smaller benthic algae? Evidence against the importance of temperature-size relationships in natural systems. Oikos 120:162–169
Carvalho L, Kirika A (2003) Changes in shallow lake functioning: response to climate change and nutrient reduction. Hydrobiologia 506–509:789–796
Chen X, Yang X, Dong X, Liu Q (2011) Nutrient dynamics linked to hydrological condition and anthropogenic nutrient loading in Chaohu Lake (southeast China). Hydrobiologia 661:223–234
Chen X, Yang X, Dong X, Liu E (2013) Environmental changes in Chaohu Lake (southeast, China) since the mid 20th century: the interactive impacts of nutrients, hydrology and climate. Limnologica 43:10–17
Chen C, Zhao L, Zhu C, Wang J, Jiang J, Yang S (2014a) Response of diatom community in Lugu Lake (Yunnan–Guizhou Plateau, China) to climate change over the past century. J Paleolimnol 51:357–373
Chen G, Selbie DT, Griffiths K, Sweetman JN, Botrel M, Taranu ZE, Knops S, Bondy J, Michelutti N, Smol JP, Gregory-Eaves I (2014b) Proximity to ice fields and lake depth as modulators of paleoclimate records: a regional study from southwest Yukon, Canada. J Paleolimnol 52:185–200
Chou G, Xia F (1998) Enhancing environmental management promotes water quality in Yilong Lake. Yunnan Environ Sci 17:54–56
Cuddington K, Leavitt PR (1999) An individual-based model of pigment flux in lakes: implications for organic biogeochemistry and paleoecology. Can J Fish Aquat Sci 56:1964–1977
Cui B, Zhai H (2006) Characteristics of wetland functional degradation and its ecological water requirement for restoration in Yilong Lake of Yunnan Plateau. Chin Sci Bull 51:127–135
Dai A (2011) Drought under global warming: a review. Wiley Interdiscip Rev Clim Change 2:45–65
Deng J, Qin B, Sarvala J, Salmaso N, Zhu G, Ventelä A-M, Zhang Y, Gao G, Nurminen L, Kirkkala T, Tarvainen M, Vuorio K (2016) Phytoplankton assemblages respond differently to climate warming and eutrophication: a case study from Pyhäjärvi and Taihu. J Great Lakes Res 42:386–396
Digerfeldt G, Olsson S, Sandgren P (2000) Reconstruction of lake-level changes in lake Xinias, central Greece, during the last 40,000 years. Palaeogeogr Palaeoclimatol Palaeoecol 158:65–82
Editorial Committee of Shiping County Annals (ECSCA) (2005) Shiping county annals. Yunnan People’s Press, Kunming (in Chinese)
Finkel ZV, Vaillancourt CJ, Irwin AJ, Reavie ED, Smol JP (2009) Environmental control of diatom community size structure varies across aquatic ecosystems. Proc R Soc B 276:1627–1634
Hall RI, Leavitt PR (1999) Effects of agriculture, urbanization, and climate on water quality in the northern Great Plains. Limnol Oceanogr 44:739–756
Hambright KD, Zohary T, Eckert W, Schwartz SS, Schelske CL, Laird KR, Leavitt PR (2008) Exploitation and destabilization of a warm, freshwater ecosystem through engineered hydrological change. Ecol Appl 18:1591–1603
Hayes NM, Patoine A, Haig HA, Simpson GL, Swarbrick VJ, Wiik E, Leavitt PR (2019) Spatial and temporal variation in nitrogen fixation and its importance to phytoplankton in phosphorus-rich lakes. Freshw Biol 64:269–283
Heiri O, Lotter F, Lemcke G (2001) Loss on ignition as a method for estimating organic and carbonate content in sediments: reproducibility and comparability of results. J Paleolimnol 25:101–110
Hu Z, Li Y, Li S (2012) Spatial and temporal distributions of diatom communities and their relationships with environmental factors in Lake Erhai. J Lake Sci 24:400–408
Huisman J, Matthijs HCP, Visser PM (2005) Harmful cyanobacteria, Springer, Dordrecht, pp 243
IPCC (2013) Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva
Jarvis IAN, Gale AS, Jenkyns HC, Pearce MA (2006) Secular variation in Late Cretaceous carbon isotopes: a new δ13C carbonate reference curve for the Cenomanian-Campanian (99.6–70.6 Ma). Geol Mag 143:561–608
Jeppesen E, Søndergaard M, Jensen JP, Havens KE, Anneville O, Carvalho L, Coveney M, Deneke R, Dokulil MT, Foy B, Gerdeaux D, Hampton SE, Hilt S, Kangur K, Köhler J, Lammens E, Lauridsen TL, Manca M, Miracle M, Moss B, Nõges P, Persson G, Phillips G, Portielje R, Romo S, Schelske CL, Straile D, Tatrai I, Willén E, Winder M (2005) Lake responses to reduced nutrient loading-an analysis of contemporary long-term data from 35 case studies. Freshw Biol 50:1747–1771
Jin XC (1995) China lake environment, Vol 3. Haiyang Publishers, China, pp 263–273
Jöhnk KD, Huisman JEF, Sharples J, Sommeijer BEN, Visser PM, Stroom JM (2008) Summer heatwaves promote blooms of harmful cyanobacteria. Global Change Biol 14:495–512
Kang W, Chen G, Wang J, Huang L, Wang L, Li R, Hu K, Liu Y, Tao J, Blais JM, Smol JP (2019) Assessing the impact of long-term changes in climate and atmospheric deposition on a shallow alpine lake from southeast Tibet. Sci Total Environ 650:713–724
Krammer K, Lange-Bertalot H (1986–1991) Bacillariophyceae 1–4. In: Ettl H, Gerloff J, Heynig H, Mollenhauer D (eds) Susswasserflora von Mitteleuropa, Band 1–4. Gustav Fischer Verlag, Jena
Lake PS (2011) Drought and aquatic ecosystems: effects and responses. Wiley, Oxford, pp 400
Leavitt PR, Hodgson DA (2001) Sedimentary pigments. In: Smol JP, Birks HJB, Last WM (eds) Tracking environmental change using lake sediments. Volume 3: terrestrial, algal, and siliceous indicators, vol 3. Kluwer Academic Publishers, Dordrecht, pp 295–325
Leavitt PR, Brock CS, Ebel C, Patoine A (2006) Landscape-scale effects of urban nitrogen on a chain of freshwater lakes in central North America. Limnol Oceanogr 51:2262–2277
Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge
Ley S, Yu M, Li K, Tseng C, Chen C, Kao P, Huang F (1963) Limnological survey of the lakes of Yunnan Plateau. Oceanol ET Limnol Sinica 5:87–114
Li Y, Liu Y, Zhao L, Hastings A, Guo H (2015) Exploring change of internal nutrients cycling in a shallow lake: a dynamic nutrient driven phytoplankton model. Ecol Model 313:137–148
Liu Y, Chen G, Hu K, Shi H, Huang L, Chen X, Lu H, Zhao S, Chen L (2017) Biological responses to recent eutrophication and hydrologic changes in Xingyun Lake, southwest China. J Paleolimnol 57:343–360
Maavara T, Parsons CT, Ridenour C, Stojanovic S, Durr HH, Powley HR, Van Cappellen P (2015) Global phosphorus retention by river damming. Proc Natl Acad Sci USA 112:15603–15608
Marc B, Falcão D, Marinho M, Pagano M, Moura A (2000) Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought. Aquat Microbial Ecol 23:13–27
McGowan S, Leavitt PR, Hall RI, Anderson NJ, Jeppesen E, Odgaard BV (2005) Controls of algal abundance and community composition during ecosystem state change. Ecology 86:2200–2211
Menking KM (1997) Climate signals in clay mineralogy and grain-size variations in Owens Lake core OI-92, eastern California. Spec Paper Geol. Soc Am 317:25–36
Meyer TJ (2001) Sediment organic matter. In: Smol JP, Birks HJB, Last WM (eds) Tracking environmental change using lake sediments. Volume 2: physical and geochemical methods, vol 3. Kluwer Academic Publishers, Dordrecht, pp 239–269
Meyers PA, Ishiwatari R (1993) Lacustrine organic geochemistry - an overview of indicators of organic matter sources and diagenesis in lake sediments. Org Geochem 20:867–900
Moorhouse HL, McGowan S, Jones MD, Barker P, Leavitt PR, Brayshaw SA, Haworth EY (2014) Contrasting effects of nutrients and climate on algal communities in two lakes in the Windermere catchment since the late 19th century. Freshw Biol 59:2605–2620
Paerl H, Huisman J (2008) Blooms like it hot. Science 320:57–58
Peršić V, Horvatić J, Has-Schön E, Bogut I (2007) Changes in N and P limitation induced by water level fluctuations in Nature Park Kopački Rit (Croatia): nutrient enrichment bioassay. Aquat Ecol 43:27–36
Posch T, Köster O, Salcher MM, Pernthaler J (2012) Harmful filamentous cyanobacteria favoured by reduced water turnover with lake warming. Nat Clim Change 2:809–813
Reynolds CS (1987) The response of phytoplankton communities to changing lake environments. Swiss J Hydrol 49:220–236
Reynolds CS (2006) Ecology of Phytoplankton (ecology, biodiversity and conservation). Cambridge University Press, Cambridge
Romo S, Soria JM, Campo FFD, Benkaddour YO, Barón-Sola Á (2013) Water residence time and the dynamics of toxic cyanobacteria. Freshw Biol 58:513–522
Round F, Crawford R, Man D (2007) The diatoms biology and morphology of the genera. Cambridge University Press, Cambridge
Rühland K, Paterson AM, Smol JP (2008) Hemispheric-scale patterns of climate-related shifts in planktonic diatoms from North American and European lakes. Glob Change Biol 14:2740–2754
Rühland KM, Paterson AM, Smol JP (2015) Lake diatom responses to warming: reviewing the evidence. J Paleolimnol 54:1–35
Saulnier-Talbot É, Gregory-Eaves I, Simpson KG, Efitre J, Nowlan TE, Taranu ZE, Chapman LJ (2014) Small changes in climate can profoundly alter the dynamics and ecosystem services of tropical crater lakes. Plos One 9:e86561
Scheffer M (1998) Ecology of shallow lakes. Chapman and Hall, London
Schindler DW (2006) Recent advances in the understanding and management of eutrophication. Limnol Oceanogr 51:356–363
Serruya C, Pollingher U (1977) Lowering of water level and algal biomassin Lake Kinneret. Hydrobiologia 54:73–80
Shi L, Sun Q (2005) Brief talk on effect of aquatic plant purifying water body of Yilong Lake. Yunnan Environ Sci 24:40–42
Smol JP (2010) The power of the past: using sediments to track the effects of multiple stressors on lake ecosystems. Freshwater Biol 55:43–59
Smol JP, Wolfe AP, Birks HJ, Douglas MS, Jones VJ, Korhola A, Pienitz R, Ruhland K, Sorvari S, Antoniades D, Brooks SJ, Fallu MA, Hughes M, Keatley BE, Laing TE, Michelutti N, Nazarova L, Nyman M, Paterson AM, Perren B, Quinlan R, Rautio M, Saulnier-Talbot E, Siitonen S, Solovieva N, Weckstrom J (2005) Climate-driven regime shifts in the biological communities of arctic lakes. Proc Natl Acad Sci USA 102:4397–4402
Sommerfield C, Nittrouer C (1999) Modern accumulation rates and a sediment budget for the Eel shelf: a flood-dominated depositional environment. Mar Geol 154:227–241
Søndergaard M, Jensen JP, Jeppesen E (2003) Role of sediment and internal loading of phosphorus in shallow lakes. Hydrobiologia 506:135–145
Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton, pp 439
Stoermer EF, Smol JP (2001) The diatoms: applications for the environmental and earth science. Cambridge University Press, Cambridge
Taranu ZE, Zurawell RW, Pick F, Gregory-Eaves I (2012) Predicting cyanobacterial dynamics in the face of global change: the importance of scale and environmental context. Glob Change Biol 18:3477–3490
Taranu ZE, Gregory-Eaves I, Leavitt PR, Bunting L, Buchaca T, Catalan J, Domaizon I, Guilizzoni P, Lami A, McGowan S, Moorhouse H, Morabito G, Pick FR, Stevenson MA, Thompson PL, Vinebrooke RD (2015) Acceleration of cyanobacterial dominance in north temperate-subarctic lakes during the Anthropocene. Ecol Lett 18:375–384
ter Braak CJF, Prentice IC (1988) A theory of gradient analysis. Adv Ecol Res 18:271–313
ter Braak CJF, Šmilauer P (2002) CANOCO reference manual and CanoDraw for windows user’s guide: software for canonical community ordination [version 4.5]. Microcomputer Power, Ithaca
Tilman D (1987) Resource competition and community structure. Monogr Popul Biol 17:1–296 (Princeton University Press)
Vadeboncoeur Y, Jeppesen E, Zanden MJV, Schierup HH, Christoffersen K, Lodge DM (2003) From Greenland to green lakes: Cultural eutrophication and the loss of benthic pathways in lakes. Limnol Oceanogr 48:1408–1441
Vogt RJ, Sharma S, Leavitt PR (2018) Direct and interactive effects of climate, meteorology, river hydrology, and lake characteristics on water quality in productive lakes of the Canadian Prairies. Can J Fish Aquat Sci 75:47–59
Wagner C, Adrian R (2009) Cyanobacteria dominance: quantifying the effects of climate chang. Limnol Oceanogr 54:2460–2468
Wang Z (1997) Survey of zooplankton and fish productivity in Yilong Lake, Yunnan J Fish China 402–407
Wang W, Wang L (2008) Current situation of agricultural non-point source pollution and Control Countermeasures in Yilong lake. Yunnan Agric Sci Technol 3:139–141
Wang H, Yang Z, Wang L, Liu Y, Song Y, Gao J (2014) The application of TVDI in drought monitoring over Yunnan province during 2009 to 2010. J Yunnan Univ Sci 36:59–65
Wang J, Chen G, Kang W, Hu K, Wang L (2019) Impoundment intensity determines temporal patterns of hydrological fluctuation, carbon cycling and algal succession in a dammed lake of Southwest China. Water Res 148:162–175
Whitmore TJ, Brenner M, Jiang Z, Curtis JH, Moore AM, Engstrom DR, Wu Y (1997) Water quality and sediment geochemistry in lakes of Yunnan Province, southern China. Environ Geol 32:45–55
Wieland E, Santschi P, Höhener P, Sturm M (1993) Scavenging of Chernobyl 137Cs and natural 210Pb in Lake Sempach, Switzerland. Geochimica Et Cosmochimica Acta 57:2959–2979
Winder M, Hunter DA (2008) Temporal organization of phytoplankton communities linked to physical forcing. Oecologia 156:179–192
Wu J, Jiang X, Xia W, Pan H, Yin Y (2002) Climate and primary productivity over the last 500 years of the Chenghai Lake,Yunnan. Mar Geol Quat Geol 22:95–98
Wu F, Zheng M, Hu G (2016) The estimation of vegetation coverage of Yanshan County in Yunnan by remote sensing based on OLI data. Environ Sci Survey 36:5–7
Xie L, Xie P, Li S, Tang H, Liu H (2003) The low TN:TP ratio, a cause or a result of Microcystis blooms?. Water Res 37:2073–2080
Xu M, Chang CP, Fu CB, Qi Y, Robock A, Robinson D, Zhang HM (2006) Steady decline of east Asian monsoon winds, 1969–2000: evidence from direct ground measurements of wind speed. J Geophy Res 111:1–8
Xu H, Paerl H, Qin B, Zhu G, Gao G (2010) Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic lake Taihu, China. Limnol Oceanogr 55:420–432
Xu J, Wen Z, Ke Z, Zhang M, Zhang M, Guo N, Hansson LA, Xie P (2014) Contrasting energy pathways at the community level as a consequence of regime shifts. Oecologia 175:231–241
Yang L, Li H (2010) Wetlands of Yunnan. China Forestry Publishing House, Beijing, pp 94–101
Yang X, Lu X (2014) Drastic change in China’s lakes and reservoirs over the past decades. Sci Rep 4:6041
Zhang Y, zhang E, Liu M (2009) Spectral absorption properties of chromophoric dissolved organic matter and particulate matter in Yunnan Plateau lakes. J Lake Sci 21:255–263
Zhang J, Wang Z, Song Z, Xie Z, Li L, Song L (2012) Bioaccumulation of microcystins in two freshwater gastropods from a cyanobacteria-bloom plateau lake, Lake Dianchi. Environ Pollut 164:227–234
Zhao L (2013) The regime shifts and inversion of catastrophic driving factors in the ecosystems of Yilong Lake, Yunnan. Dissertation, University of Chinese Academy of Science
Zhao L, Li Y, Zou R, He B, Zhu X, Liu Y, Wang J, Zhu Y (2013) A three-dimensional water quality modeling approach for exploring the eutrophication responses to load reduction scenarios in Lake Yilong (China). Environ Pollut 177:13–21
Acknowledgements
This work was supported by the National Key Research and Development Program of China [Grant number 2017YFA0605202], National Natural Science Foundation of China [Grant number 41171048, U1133601], and Ministry of Education of China [grant number 213034A]. PRL and IGE were supported by the Canada Research Chair program. We are grateful to Huibin Lu and Haibin Shi for their field work assistance, as well as Jiaoyuan Wang, Jianshuang Tao and Wengang Kang for their constructive comments. Constructive comments provided by two anonymous reviewers and editor are appreciated.
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Hu, K., Chen, G., Gregory-Eaves, I. et al. Hydrological fluctuations modulate phototrophic responses to nutrient fertilization in a large and shallow lake of Southwest China. Aquat Sci 81, 37 (2019). https://doi.org/10.1007/s00027-019-0633-4
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DOI: https://doi.org/10.1007/s00027-019-0633-4