Abstract
Autochthonous and allochthonous organic carbon (OC) are important carbon sources for zooplankton in lakes, and changes in the abundance and proportions of those sources may affect zooplankton community composition and lake ecosystem function. Nevertheless, long-term changes in assimilation of autochthonous and allochthonous carbon by zooplankton and associated climate- and environment-related forcing mechanisms have rarely been studied. We used a sediment record of cladoceran remains and geochemical variables from Lake Jirentso on the Tibetan Plateau to track long-term changes in sources of carbon for cladocera over the past ~ 950 years. High cladoceran:diatom accumulation rate ratios during the cold Little Ice Age indicated that cladocerans assimilated more allochthonous OC that was released from glaciers and frozen soils to replenish their food supply, a consequence of low primary production in the lake. In contrast, low cladoceran:diatom accumulation rate ratios during the Current Warm Period indicated that cladocerans utilized more autochthonous OC. Less autochthonous OC was available for cladocerans during the Medieval Warm Period than during the Current Warm Period. The total accumulation rate of cladocerans was significantly correlated with the annual mean air temperature, total phosphorus, and the organic carbon to nitrogen ratio in the sediment core. Recent warming and sharply increased nutrient inputs affected the cladoceran and diatom assemblages, further inducing a shift in the diet of zooplankton towards more recently produced OC. The sediment record from Lake Jirentso, which represents the last ~ 950 years of deposition, spanned an ideal time window for assessing historical changes related to the impacts of climate and nutrients on zooplankton carbon sources.
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References
Alric B, Jenny JP, Berthon V, Arnaud F, Pignol C, Reyss JL, Sabatier P, Perga ME (2013) Local forcings affect lake zooplankton vulnerability and response to climate warming. Ecology 94:2767–2780
Appleby PG (2001) Chronostratigraphic techniques in recent sediments. In: Last WM, Smol JP (eds) Tracking environmental change using lake sediments: basin analysis, coring, and chronological techniques, vol 1. Kluwer Academic Publishers, Dordrecht, pp 171–203
Battarbee RW, Jones VJ, Flower RJ, Cameron NG, Bennion H, Carvalho L, Juggins S (2001) Diatoms. In: Last WM, Smol JP (eds) Tracking environmental change using lake sediments Terrestrial algal and siliceous indicators, vol 3. Kluwer Academic Publishers, Dordrecht, pp 155–202
Bellamy AR, Bauer JE, Grottoli AG (2017) Influence of land use and lithology on sources and ages of nutritional subsidies to stream macroinvertebrates: a multi-isotopic approach. Aquat Sci 79:925–939
Biskaborn BK, Smith SL, Noetzli J, Matthes H, Vieira G, Streletskiy DA et al (2019) Permafrost is warming at a global scale. Nat Commun 10:264
Bjerring R, Becares E, Declerck S, Gross EM, Hansson LA, Kairesalo T, Nykänen M, Halkiewicz A, Kornijów R, Conde-Porcuna JM, Seferlis M, Nõges T, Moss B, Amsinck SL, Odgaard BV, Jeppesen E (2009) Subfossil Cladocera in relation to contemporary environmental variables in 54 Pan-European lakes. Freshw Biol 54:2401–2417
Blaauw M, Christen JA (2011) Flexible paleoclimate age-depth models using an autoregressive gamma process. Baye Anal 6:457–474
Boschker HTS, Kromkamp JC, Middelburg JJ (2005) Biomarker and carbon isotopic constraints on bacterial and algal community structure and functioning in a turbid, tidal estuary. Limnol Oceanogr 50:70–80
Cameron KA, Stibal M, Hawkings JR, Mikkelsen AB, Telling J, Kohler TJ, Gözdereliler E, Zarsky JD, Wadham JL, Jacobsen CS (2017) Meltwater export of prokaryotic cells from the Greenland ice sheet. Environ Microbiol 19:524–534
Carpenter SR, Cole JJ, Pace ML, Van de Bogert M, Bade DL, Bastviken D, Gille CM, Hodgson JR, Kitchell JF, Kritzberg ES (2005) Ecosystem subsidies: terrestrial support of aquatic food webs from 13C addition to contrasting lakes. Ecology 86:2737–2750
Catalan J, Pla-Rabés S, Wolfe AP, Smol JP, Rühland KM, Anderson NJ, Kopáček J, Stuchlík E, Schmidt R, Koinig KA, Camarero L, Flower RJ, Heiri O, Kamenik C, Korhola A, Leavitt PR, Psenner R, Renberg I (2013) Global change revealed by palaeolimnological records from remote lakes: a review. J Palaeolimnol 49:513–535
Chang J, Zhang E, Liu E, Sun W, Langdon PG, Shulmeister J (2018) A 2500-year climate and environmental record inferred from subfossil chironomids from Lugu Lake, southwestern China. Hydrobiologia 811:1–14
Cheng H, Edwards RL, Sinha A, Spötl C, Yi L, Chen S, Kelly M, Kathayat G, Wang XF, Li XL, Kong XG, Wang YJ, Ning YF, Zhang HW (2016) The Asian monsoon over the past 640,000 years and ice age terminations. Nature 534:640–646
Cook GT, Bonsall C, Hedges REM, McSweeney K, Boronean V, Pettitt PB (2001) A freshwater diet-derived C-14 reservoir effect at the stone age sites in the iron gates gorge. Radiocarbon 43:453–460
Dickson L, Bull ID, Gates PJ, Evershed RP (2009) A simple modification of a silicic acid lipid fractionation protocol to eliminate free fatty acids from glycolipid and phospholipid fractions. J Microbiol Methods 78:249–254
Fellman JB, Hood E, Raymond PA, Hudson J, Bozeman M, Arimitsu M (2015) Evidence for the assimilation of ancient glacier organic carbon in a proglacial stream food web. Limnol Oceanogr 60:1118–1128
Ge Q, Zheng J, Hao Z, Liu H (2013) General characteristics of climate changes during the past 2000 years in China. Sci China Earth Sci 56:321–329
Guo LD, Ping CL, Macdonald RW (2007) Mobilization pathways of organic carbon from permafrost to arctic rivers in a changing climate. Geophys Res Lett 34:L13603
Hågvar S, Ohlson M (2013) Ancient carbon from a melting glacier gives high 14C age in living pioneer invertebrates. Sci Rep 3:2820
Holtvoeth J, Rushworth D, Imeri A, Cara M, Vogel H, Wagner T, Wolff GA (2016) Improved end–member characterization of modern organic matter pools in the Ohrid Basin (Albania, Macedonia) and evaluation of new palaeoenvironmental proxies. Biogeosciences 13:795–816
Hood E, Battin TJ, Fellman JB, O’Neel S, Spencer RGM (2015) Storage and release of organic carbon from glaciers and ice sheets. Nat Geosci 8:91–96
Hu Z, Anderson NJ, Yang X, McGowan S (2014) Catchment-mediated atmospheric nitrogen deposition drives ecological change in two alpine lakes in SE Tibet. Glob Change Biol 20:1614–1628
Jeppesen E, Jensen JP, Skovgaard H, Hvidt CB (2001) Changes in the abundance of planktivorous fish in Lake Skanderborg during the past two centuries-a palaeoecological approach. Palaeogeogr Palaeoclimatol Palaeoecol 172:143–152
Jeppesen E, Nõges P, Davidson TA, Haberman J, Nõges T, Blank K, Lauridsen TL, Søndergaard M, Sayer C, Laugaste R, Johansson LS, Bjerring R, Amsinck SL (2011) Zooplankton as indicators in lakes-a plea for including zooplankton in the ecological quality assessment of lakes according to the European Water Framework Directive (WFD)-Hydrobiologia 676: 270–297
Jeziorski A, Paterson AM, Smol JP (2012) Changes since the onset of acid deposition among calcium-sensitive cladoceran taxa within soft water lakes of Ontario, Canada. J Paleolimnol 48:323–327
Jiang XZ, Du NS (1979) Fauna Sinica, crustacean: freshwater Cladocera. Science Press, Beijing
Kendrick MR, Huryn AD, Bowden WB, Deegan LA, Findlay RH, Hershey AE, Peterson BJ, Beneš JP, Schuett EB (2018) Linking permafrost thaw to shifting biogeochemistry and food web resources in an arctic river. Glob Change Biol 24:5738–5750
Kong LY (2015) Study on the response of cladoceran in alpine lakes to environment change during the past 200 years in Western Sichuan Plateau. Dissertation. Nanjing Institute of Geography and Limnology
Kong LY, Yang XD, Kattel G, Anderson NJ, Hu Z (2017) The response of Cladocerans to recent environmental forcing in an Alpine Lake on the SE Tibetan Plateau. Hydrobiologia 784:171–185
Kuang XY, Liu J, Wang HL, Wang SM (2008) Interhemispheric comparison of climate change in the last millennium based on the ECHO-G simulation. Chin Sci Bull 53:2692–2700
Legutke S, Voss R (1999) The Hamburg Atmosphere-Ocean Coupled Circulation Model ECHO-G. Technical Report No.18. Hamburg: German Climate Computer Center (DKRZ)
Li ZG (2014) Glacier and Lake Changes across the Tibetan Plateau during the Past 50 years of climate change. J Resour Ecol 5:123–131
Liu GM, Chen FZ, Liu ZW (2008) Preliminary study on cladoceran microfossils in the sediments of Lake Taihu. J Lake Sci 20:470–476
Lotter AF, Birks HJB, Hofmann W, Marchetto A (1998) Modern diatom, cladocera, chironomid, and chrysophytecyst assemblages as quantitative indicators for the reconstruction of past environmental conditions in the Alps II. Nutrients J Paleolimnol 19:443–463
Mahowald N, Jickells TD, Baker AR, Artaxo P, Benitez-Nelson CR, Bergametti G, Bond TC, Chen Y, Cohen DD, Herut B (2008) Global distribution of atmospheric phosphorus sources, concentrations and deposition rates, and anthropogenic impacts. Glob Biogeochem Cycles 22:37–42
Manca M, Comoli P (2004) Reconstructing long-term changes in Daphnia’s body size from subfossil remains in sediments of a small lake in the Himalayas. J Paleolimnol 32:95–107
Mayorga E, Aufdenkampe AK, Masiello CA, Krusche AV, Hedges JI, Quay PD (2005) Young organic matter as a source of carbon dioxide outgassing from Amazonian rivers. Nature 436:538–541
Meyers PA, Teranes JL (2001) Sediment organic matter. In: Last WM, Smol JP (eds) Tracking environmental change using lake sediments Terrestrial algal and siliceous indicators, vol 3. Kluwer Academic Publishers, Dordrecht, pp 239–270
Middelburg JJ (2014) Stable isotopes dissect aquatic food webs from the top to the bottom. Biogeosciences 11:2357–2371
Mladenov N, Sommaruga R, Morales-Baquero R, Laurion I, Camarero L, Diéguez MC, Camacho A, Delgado A, Torres O, Chen Z, Felip M, Reche I (2011) Dust inputs and bacteria influence dissolved organic matter in clear alpine lakes. Nat Commun 2:405
Nova CC, Bozelli RL, Spitzy A, Müller-Navarra D (2019) Living in a browning environment: effects on Daphnia’s growth and fatty acid pattern. Limnol Oceanogr 64:18–31
Orland IJ, Edwards RL, Cheng H, Kozdon R, Cross M, Valley JW (2015) Direct measurements of deglacial monsoon strength in a Chinese stalagmite. Geology 43:555–558
Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269
Qiu J (2010) Measuring the meltdown. Nature 468:141–142
Reimer PJ, Baillie MGL, Bard E, Bayliss A, Beck JW, Blackwell PG, Buck CE, Burr GS, Edwards RL (2013) IntCal13 and Marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon 55:1869–1887
Saros JE, Anderson NJ (2015) The ecology of the planktonic diatom Cyclotella and its implications for global environmental change studies. Biol Rev Camb Philos Soc 90:522–541
Sichuan Statistical Yearbook (2005) Area ploughed by tractors and lrrigated, consumption of chemical fertilizers, number of hydropower stations and electricity consumption in rural areas. Sichuan Provincial Bureau of Statistics
Smol JP (2008) Pollution of lakes and rivers: a paleoenvironmental perspective. Blackwell Publishing, Oxford
Søndergaard M, Liboriussen L, Asger R, Jeppesen E (2008) Lake restoration by fish removal: short- and long-term effects in 36 Danish lakes. Ecosystems 11:1291–1305
Stibal M, Tranter M, Benning LG, Rehak J (2008) Microbial primary production on an Arctic glacier is insignificant in comparison with allochthonous organic carbon input. Environ Microbiol 10:2172–2178
Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (2013) IPCC climate change 2013: the physical science basis. Cambridge University Press, Cambridge
Sun HL (1996) Formation and evolution of Qinghai-Xizang Plateau. Shanghai Science Technology Press, Shanghai
Szeroczyńska K, Sarmaja-Korjonen K (2007) Atlas of Subfossil Cladoceran from Central and Northern Europe. Friends of the Lower Vistula Society, Świecie, pp 10–11
Taipale SJ, Brett MT, Hahn HW, Martin-Creuzburg D, Yeung S, Hiltunen M, Strandberg U, Kankaala P (2014) Differing Daphnia magna assimilation efficiencies for terrestrial, bacterial, and algal carbon and fatty acids. Ecology 95:563–576
Tan LC, Cai Y, Cheng H, Edwards LR, Lan J, Zhang H, Dong L, Le M, Zhao P, Gao Y (2018) High resolution monsoon precipitation changes on southeastern Tibetan Plateau over the past 2300 years. Quat Sci Rev 195:122–132
Thompson LG, Yao T, Mosley-Thompson E, Davis ME, Henderson KA, Lin PN (2000) A high-resolution millennial record of the South Asian monsoon from Himalayan ice cores. Science 289:1916–1919
Vadeboncoeur Y, Jeppesen E, Zanden VMJ, Schierup HH, Christoffersen K, Lodge D (2003) From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways. Limnol Oceanogr 48:1408–1418
Wang Q, Anderson NJ, Yang X, Xu M (2020) Interactions between climate change and early agriculture in SW China and their effect on lake ecosystem functioning at centennial timescales over the last 2000 years. Quat Sci Rev 233:106238
Wang R, Balkanski Y, Boucher O, Ciais P, Peñuelas J, Tao S (2015) Significant contribution of combustion-related emissions to the atmospheric phosphorus budget. Nat Geosci 8:48–54
Wolff JO, Maier-Reimer E, Legutke S (1997) The Hamburg Ocean Primitive Equation Model. German Climate Computer Center (DKRZ) Technical Report No. 13, 98
Xiao XY, Haberle SG, Shen J, Yang XD, Han Y, Zhang EL, Wang SM (2014) Latest Pleistocene and Holocene vegetation and climate history inferred from an alpine lacustrine record, northwestern Yunnan Province, southwestern China. Quat Sci Rev 86:35–48
Yao TD, Wu GJ, Pu JC, Jiao KQ, Huang CL (2004) Relationship between calcium and atmospheric dust recorded in Guliya ice core. Sci Bull 49:706–710
Zhang Y, Song L, Liu XJ, Li WQ, Lu SH, Zheng LX, Bai ZC, Cai GY, Zhang FS (2012) Atmospheric organic nitrogen deposition in China. Atmos Environ 46:195–204
Zheng X, Fu C, Xu X, Yan X, Huang Y, Han S, Hu F, Chen G (2002) The Asian nitrogesn cycle case study. AMBIO A J Hum Environ 31:79–87
Zigah PK, Minor EC, McNichol AP, Xu L, Werne JP (2017) Constraining the sources and cycling of dissolved organic carbon in a large oligotrophic lake using radiocarbon analyses. Geochim Cosmochim Acta 208:102–108
Zigah PK, Minor EC, Werne JP (2012) Radiocarbon and stable-isotope geochemistry of organic and inorganic carbon in Lake Superior. Global Biogeochem Cycles 26:1–20
Zigah PK, Minor EC, Werne JP, McCallister SL (2011) Radiocarbon and stable carbon isotopic insights into provenance and cycling of carbon in Lake Superior. Limnol Oceanogr 56:867–886
Acknowledgements
We acknowledge XD Yang, Y Chen, and L Liu for field assistance, LY Kong and S Min for assistance in ECHO-G modeling, and LC Tan for sharing data on oxygen isotopes. The “Pioneer” and “Leading Goose” R&D Program of Zhejiang (2022C02038), National Science Foundation of China (31971475, 31930074, and 31770509), and the China-Netherlands Joint Programme (JSTP) (GJHZ05) supported this publication. JJM was supported by the Netherlands Earth System Science Center. EJ was supported by the Tübitak outstanding researchers program, BIDEB 2232 (project 118C250).
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Su, Y., Li, K., Zhang, Y. et al. Effects of climate change and nutrient concentrations on carbon sources for zooplankton in a Tibetan Plateau lake over the past millennium. J Paleolimnol 68, 249–263 (2022). https://doi.org/10.1007/s10933-022-00245-w
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DOI: https://doi.org/10.1007/s10933-022-00245-w