Abstract
Understanding how biological communities respond to climate change is a major challenge in ecology. The response of ectotherms to changes in temperature depends not only on their species-specific thermal tolerances but also on temperature-mediated interactions across different trophic levels. Warming is predicted to reinforce trophic cascades in linear aquatic food chains, but little is known about how warming might affect the lower trophic levels of food webs involving extensive fish omnivory, a common scenario in subtropical and tropical waterbodies. In this study, a mesocosm warming experiment was conducted involving a pelagic food chain (fish–zooplankton–phytoplankton) topped by the omnivorous bighead carp [Aristichthys nobilis (Richardson)]. We found that temperature elevation significantly enhanced the growth of fish and suppressed zooplankton, including both metazooplankton and ciliates, while abundances of phytoplankton, despite disruption of temporal dynamics, did not increase correspondingly—likely due to fish predation. Our results suggest that trophic cascades are less unlikely to be reinforced by warming in food chains involving significant omnivory. Moreover, we found that warming advanced the spring abundance peak of phytoplankton abundance and that of the parthenogenetic rotifer Brachionus quadridentatus; whereas, it had no effect on the only sexually reproducing copepod, Mesocyclops leuckarti, presumably due to its prolonged life history. Our study also confirmed that warming may lead to a phenological mismatch between some predators and their prey because of the distinct life histories among taxa, with potentially severe consequences for resource flow in the food chain, at least in the short term.
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References
Adrian R, Wilhelm S, Gerten D (2006) Life-history traits of lake plankton species may govern their phenological response to climate warming. Glob Change Biol 12:652–661. https://doi.org/10.1111/j.1365-2486.2006.01125.x
Afzal M, Rab A, Akhtar N, Ahmed I, Khan MF, Qayyum M (2008) Growth performance of bighead carp Aristichthys nobilis (Richardson) in monoculture system with and without supplementary feeding. Pak Vet J 28:57–62
Barton BT, Schmitz OJ (2009) Experimental warming transforms multiple predator effects in a grassland food web. Ecol Lett 12:1317–1325. https://doi.org/10.1111/j.1461-0248.2009.01386.x
Bascompte J, Melian CJ, Sala E (2005) Interaction strength combinations and the overfishing of a marine food web. Proc Natl Acad Sci USA 102:5443–5447. https://doi.org/10.1073/pnas.0501562102
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Behrens MD, Lafferty KD (2007) Temperature and diet effects on omnivorous fish performance: implications for the latitudinal diversity gradient in herbivorous fishes. Can J Fish Aquat Sci 64:867–873. https://doi.org/10.1139/f07-063
Beisner BE, McCauley E, Wrona FJ (1997) The influence of temperature and food chain length on plankton predator–prey dynamics. Can J Fish Aquat Sci 54:586–595. https://doi.org/10.1139/f96-312
Bottrell H (1976) A review of some problems in zooplankton production studies. Norw J Zool 24:419–456
Brandl Z (2005) Freshwater copepods and rotifers: predators and their prey. Hydrobiologia 546:475–489. https://doi.org/10.1007/s10750-005-4290-3
Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789. https://doi.org/10.1890/03-9000
Brucet S, Boix D, Quintana XD, Jensen E, Nathansen LW, Trochine C, Meerhoff M, Gascón S, Jeppesen E (2010) Factors influencing zooplankton size structure at contrasting temperatures in coastal shallow lakes: implications for effects of climate change. Limnol Oceanogr 55:1697–1711. https://doi.org/10.4319/lo.2010.55.4.1697
Burgis MJ (1970) The effect of temperature on the development time of eggs of Thermocyclops sp., a tropical cyclopoid from Lake George, Uganda. Limnol Oceanogr 15:742–747. https://doi.org/10.4319/lo.1970.15.5.0742
Chen F, Gulati RD, Li J, Liu ZW (2011) A comparison of the size distribution of the filamentous green alga Ulothrix in Daphnia guts and lake water from Lake Taihu, China. J Plankton Res 33:1274–1283. https://doi.org/10.1093/plankt/fbr029
Chiang SC, Du NS (1979) Fauna Sinica. Science Press, Beijing
Corliss JO (1979) The ciliated protozoa: characterization, classification, and guide to the literature, 2nd edn. Pergamom, Oxford
Cremer MC, Smitherman RO (1980) Food habits and growth of silver and bighead carp in cages and ponds. Aquaculture 20:57–64. https://doi.org/10.1016/0044-8486(80)90061-7
Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv Mar Biol 26:249–293. https://doi.org/10.1016/S0065-2881(08)60202-3
Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci USA 106:12788–12793. https://doi.org/10.1073/pnas.0902080106
De Senerpont Domis LN, Mooij WM, Hülsmann S, Van Nes EH, Scheffer M (2007) Can overwintering versus diapausing strategy in Daphnia determine match-mismatch events in zooplankton-algae interactions? Oecologia 150:682–698. https://doi.org/10.1007/s00442-006-0549-2
Deng J, Qin B, Paerl HW, Zhang Y, Ma J, Chen Y (2014) Earlier and warmer springs increase cyanobacterial (Microcystis spp.) blooms in subtropical Lake Taihu, China. Freshw Biol 59:1076–1085. https://doi.org/10.1111/fwb.12330
Dickman EM, Newell JM, González MJ, Vanni MJ (2008) Light, nutrients, and food-chain length constrain planktonic energy transfer efficiency across multiple trophic levels. Proc Natl Acad Sci USA 105:18408–18412. https://doi.org/10.1073/pnas.0805566105
Duan H, Ma R, Xu X, Kong F, Zhang S, Kong W, Hao J, Shang L (2009) Two-decade reconstruction of algal blooms in China’s Lake Taihu. Environ Sci Technol 43:3522–3528. https://doi.org/10.1021/es8031852
Edwards M, Richardson AJ (2003) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 4030:881–884. https://doi.org/10.1038/nature02808
Feuchtmayr H, Moss B, Harvey I, Moran R, Hatton K, Connor L, Atkinson D (2010) Differential effects of warming and nutrient loading on the timing and size of the spring zooplankton peak: an experimental approach with hypertrophic freshwater mesocosms. J Plankton Res 32:1715–1725. https://doi.org/10.1093/plankt/fbq087
Finke DL, Denno RF (2005) Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades. Ecol Lett 8:1299–1306. https://doi.org/10.1111/j.1461-0248.2005.00832.x
Foissner W, Berger H (1996) A user-friendly guide to the ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes, and waste waters, with notes on their ecology. Freshw Biol 35:375–482
Foissner W, Berger H, Schaumburg J (1999) Identification and ecology of limnetic plankton ciliates. Informationsberichte des Bayer. Landesamtes für Wasserwirtschaft, Heft, vol 3/99, pp 1–793
Frenken T, Velthuis M, de Senerpont Domis LN, Stephan S, Aben R, Kosten S, Van Donk E, Van de Waal DB (2016) Warming accelerates termination of a phytoplankton spring bloom by fungal parasites. Glob Change Biol 22:299–309. https://doi.org/10.1111/gcb.13095
Gerten D, Adrian R (2000) Climate-driven changes in spring plankton dynamics and the sensitivity of shallow polymictic lakes to the North Atlantic Oscillation. Limnol Oceanogr 45:1058–1066. https://doi.org/10.4319/lo.2000.45.5.1058
Gerten G, Adrian R (2002) Species-specific changes in the phenology and peak abundance of freshwater copepods in response to warm summers. Freshw Biol 47:2163–2173. https://doi.org/10.1046/j.1365-2427.2002.00970.x
González-Bergonzoni I, Meerhoff M, Davidson TA, Teixeira-de Mello F, Baattrup-Pedersen A, Jeppesen E (2012) Meta-analysis shows a consistent and strong latitudinal pattern in fish omnivory across ecosystems. Ecosystems 15:492–503. https://doi.org/10.1007/s10021-012-9524-4
Gophen M (1976) Temperature effect on lifespan, metabolism, and development time of Mesocyclops leuckarti (Claus)*. Oecologia 277:271–277. https://doi.org/10.1007/BF00345104
Gudasz C, Bastviken D, Steger K, Premke K, Sobek S, Tranvik LJ (2010) Temperature- controlled organic carbon mineralization in lake sediments. Nature 466:478–481
Gyllström M, Hansson LA (2004) Dormancy in freshwater zooplankton: Induction, termination and the importance of benthic-pelagic coupling. Aquat Sci 66:274–295. https://doi.org/10.1007/s00027-004-0712-y
Hansen AM, Santer B (1995) The influence of food resources on the development, survival and reproduction of the two cyclopoid copepods: Cyclops vicinus and Mesocyclops leuckarti. J Plankton Res 17:631–646. https://doi.org/10.1093/plankt/17.3.631
Hansson LA, Nicolle A, Granéli W, Hallgren P, Kritzberg E, Persson A, Björk J, Nilsson PA, Bronmark C (2013) Food-chain length alters community responses to global change in aquatic systems. Nat Clim Change 3:228–233. https://doi.org/10.1038/nclimate1689
He H, Jin H, Jeppesen E, Li K, Liu Z, Zhang Y (2018) Fish-mediated plankton responses to increased temperature in subtropical aquatic mesocosm ecosystems: implications for lake management. Water Res 144:304–311. https://doi.org/10.1016/j.watres.2018.07.055
Hoekman D (2010) Turning up the heat: temperature influences the relative importance of top-down and bottom-up effects. Ecology 91:2819–2825. https://doi.org/10.1890/10-0260.1
Hu HJ, Wei YX (2006) The freshwater algae of China: systematics, taxonomy and ecology. Science Press, Beijing
Jeppesen E, Jensen JP, Jensen C, Faafeng B, Hessen DO, Søndergaard M, Lauridsen T, Brettum P, Christoffersen K (2003) The impact of nutrient state and lake depth on top-down control in the pelagic zone of lakes: a study of 466 lakes from the temperate zone to the arctic. Ecosystems 6(4):313–325. https://doi.org/10.1007/PL00021503
Jeppesen E, Meerhoff M, Holmgren K, González-Bergonzoni I, Teixeira-de Mello F, Declerck SAJ, Meester LD, Søndergaard M, Lauridsen TL, Bjerring R, Conde-Porcuna JM, Mazzeo N, Iglesias C, Reizenstein M, Malmquist HJ, Liu ZW, Balayla D, Lazzaro X (2010) Impacts of climate warming on lake fish community structure and potential effects on ecosystem function. Hydrobiologia 646:73–90. https://doi.org/10.1007/s10750-010-0171-5
Jeppesen E, Nõges P, Davidson TA, Haberman J, Nõges T, Blank K, Lauridsen TL, Søndergaard M, Sayer C, Laugaste R, Johansson LS, Bjerring R, Amisinck 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. https://doi.org/10.1007/s10750-011-0831-0
Jin XC, Tu QY (1990) The standard methods for observation and analysis in lake eutrophication, 2nd edn. Environmental Science Press, Beijing
Knisely K, Geller W (1986) Selective feeding of four zooplankton species on natural lake phytoplankton. Oecologia 69:86–94. https://doi.org/10.1007/BF00399042
Kratina P, Greig HS, Thompson PL, Carvalho-Pereira TSA, Shurin JB (2012) Warming modifies trophic cascades and eutrophication in experimental freshwater communities. Ecology 93:1421–1430. https://doi.org/10.1890/11-1595.1
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw. https://doi.org/10.18637/jss.v082.i13
Lacerot G (2010) Effects of climate on size structure and functioning of aquatic food webs. Ph.D. Thesis. Wageningen University
Lampert W, Fleckner W, Rai H, Taylor BE (1986) Phytoplankton control by grazing zooplankton: a study on the spring clear-water phase. Limnol Oceanogr 31:478–490. https://doi.org/10.4319/lo.1986.31.3.0478
Lewandowska AM, Boyce DG, Hofmann M, Matthiessen B, Sommer U, Worm B (2014) Effects of sea surface warming on marine plankton. Ecol Lett 17:614–623. https://doi.org/10.1111/ele.12265
Li J, Chen FZ, Liu ZW, Xu KD, Zhao BY (2013) Compositional differences among planktonic ciliate communities in four eutrophic subtropical lakes in China. Limnology 14:105–116
Liu Z, Hu J, Zhong P, Zhang X, Ning J, Larsen SE, Chen D, Gao Y, He Hu, Jeppesen E (2018) Successful restoration of a tropical shallow eutrophic lake: strong bottom-up but weak top-down effects recorded. Water Res 146:88–97
Lynn DH (2008) The ciliated protozoa: characterization, classification, and guide to the literature, 3rd edn. Springer, Berlin, pp 1–605
McCauley E (1984) The estimation of the abundance and biomass of zooplankton in samples. A Man Methods Assess Second Product Fresh Waters 17:228–265
Meerhoff M, Clemente JM, de Mello FT, Iglesias C, Pedersen AR, Jeppesen E (2007) Can warm climate-related structure of littoral predator assemblies weaken the clear water state in shallow lakes? Glob Change Biol 13:1888–1897. https://doi.org/10.1111/j.1365-2486.2007.01408.x
Meerhoff M, Teixeira-de Mello F, Kruk C, Alonso C, González-Bergonzoni I, Pacheco JP, Lacerot G, Arim M, Beklioğlu M, Brucet S, Goyenola G, Iglesias C, Mazzeo N, Kosten S, Jeppesen E (2012) Environmental warming in shallow lakes: a review of effects on community structure as evidenced from space-for-time substitution approaches. Adv Ecol Res 46:259–350. https://doi.org/10.1016/B978-0-12-396992-7.00004-6
Paerl HW, Xu H, McCarthy MJ, Zhu G, Qin B, Li Y, Gardner WS (2011) Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N and P) management strategy. Water Res 45:1973–1983. https://doi.org/10.1016/j.watres.2010.09.018
Peeters F, Straile D, Lorke A, Livingstone DM (2007) Earlier onset of the spring phytoplankton bloom in lakes of the temperate zone in a warmer climate. Glob Change Biol 13:1898–1909. https://doi.org/10.1111/j.1365-2486.2007.01412.x
Pimm SL, Lawton JH (1978) On feeding on more than one trophic level. Nature 275:542–544. https://doi.org/10.1038/275542a0
Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2013) nlme: Linear and nonlinear mixed effects models. R Package Version 3:1–96
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Radke RJ, Kahl U (2002) Effects of a filter-feeding fish [silver carp, Hypophthalmichthys molitrix (Val.)] on phyto- and zooplankton in a mesotrophic reservoir: results from an enclosure experiment. Freshw Biol 47:2337–2344. https://doi.org/10.1046/j.1365-2427.2002.00993.x
Rolinski S, Horn H, Petzoldt T, Paul L (2007) Identifying cardinal dates in phytoplankton time series to enable the analysis of long-term trends. Oecologia 153:997–1008. https://doi.org/10.1007/s00442-007-0783-2
Satterthwaite FE (1946) An approximate distribution of estimates of variance components. Biom Bull 2(6):110–114. https://doi.org/10.2307/3002019
Schaus MH, Vanni MJ, Wissing TE, Bremigan MT, Garvey JE, Stein RA (1997) Nitrogen and phosphorus excretion by detritivorous gizzard shad in a reservoir ecosystem. Limnol Oceanogr 42:1386–1397
Sentis A, Hemptinne JL, Brodeur J (2014) Towards a mechanistic understanding of temperature and enrichment effects on species interaction strength, omnivory and food-web structure. Ecol Lett 17:785–793. https://doi.org/10.1111/ele.12281
SEPA (2002) Analytical methods for water and wastewater monitor, 4th edn. Chinese Environmental Science Press, Beijing
Shen JR, Du NS (1979) Fauna sinica, crustacea, freshwater copepoda. Science Press, Beijing
Shi K, Zhang Y, Zhang Y, Li N, Qin B, Zhu G, Zhou Y (2019) Phenology of phytoplankton blooms in a trophic lake observed from long-term MODIS data. Environ Sci Technol 53:2324–2331. https://doi.org/10.1021/acs.est.8b06887
Shurin JB, Clasen JL, Greig HS, Kratina P, Thompson PL (2012) Warming shifts top-down and bottom-up control of pond food web structure and function. Philos Trans R Soc B 367:3008–3017. https://doi.org/10.1098/rstb.2012.0243
Sommer U, Lewandowska A (2011) Climate change and the phytoplankton spring bloom: warming and overwintering zooplankton have similar effects on phytoplankton. Glob Change Biol 17:154–162. https://doi.org/10.1111/j.1365-2486.2010.02182.x
Šorf M, Davidson TA, Brucet S, Menezes RF, Søndergaard M, Lauridsen TL, Landkuldehus F, Liboriussen L, Jeppesen E (2015) Zooplankton response to climate warming: a mesocosm experiment at contrasting temperatures and nutrient levels. Hydrobiologia 742:185–203. https://doi.org/10.1007/s10750-014-1985-3
Svensson F, Karlsson E, Gårdmark A, Olsson J, Adill A, Zie J, Snoeijs P, Eklöf JS (2017) In situ warming strengthens trophic cascades in a coastal food web. Oikos 126:1150–1161. https://doi.org/10.1111/oik.03773
Tackx ML, De Pauw N, Van Mieghem R, Azémar F, Hannouti A, Van Damme S, Fiers F, Daro N, Meire P (2004) Zooplankton in the Scheide estuary, Belgium and the Netherlands. Spatial and temporal patterns. J Plankton Res 26:133–141. https://doi.org/10.1093/plankt/fbh016
Talling JF (2003) Phytoplankton-zooplankton seasonal timing and the “clear-water phase” in some English lakes. Freshw Biol 48:39–52. https://doi.org/10.1046/j.1365-2427.2003.00968.x
Tanabe K, Namba T (2005) Omnivory creates chaos in simple food web models. Ecology 86:3411–3414. https://doi.org/10.1890/05-0720
Teixeira-De Mello F, Meerhoff M, Pekcan-Hekim Z, Jeppesen E (2009) Substantial differences in littoral fish community structure and dynamics in subtropical and temperate shallow lakes. Freshw Biol 54:1202–1215. https://doi.org/10.1111/j.1365-2427.2009.02167.x
Thompson RM, Hemberg M, Starzomski BM, Shurin JB (2007) Trophic levels and trophic tangles: the prevalence of omnivory in real food webs. Ecology 88:612–617. https://doi.org/10.1890/05-1454
Usui T, Butchart SHM, Phillimore AB (2017) Temporal shifts and temperature sensitivity of avian spring migratory phenology : a phylogenetic meta-analysis. J Anim Ecol 86:250–261. https://doi.org/10.1111/1365-2656.12612
Velthuis M, De Senerpont Domis LN, Frenken T, Stephan S, Kazanjian G, Aben R, Hilt S, Kosten S, Van Donk E, Van de Waal DB (2017) Warming advances top-down control and reduces producer biomass in a freshwater plankton community. Ecosphere 8:e01651. https://doi.org/10.1002/ecs2.1651
Wang HJ, Liang XM, Jiang PH, Wang J, Wu SK, Wang HZ (2008) TN: TP ratio and planktivorous fish do not affect nutrient-chlorophyll relationships in shallow lakes. Freshw Biol 53:935–944. https://doi.org/10.1111/j.1365-2427.2007.01950.x
Watson NHF, Smallman BN (1971) The role of photoperiod and temperature in the induction and termination of an arrested development in two species of freshwater cyclopia copepods. Can J Zool 49:855–862. https://doi.org/10.1139/z71-128
Winder M, Schindler DE (2004) Climatic effects on the phenology of lake processes. Glob Change Biol 10:1844–1856. https://doi.org/10.1111/j.1365-2486.2004.00849.x
Winder M, Schindler DE, Essington TE, Litt AH (2009) Disrupted seasonal clockwork in the population dynamics of a freshwater copepod by climate warming. Limnol Oceanogr 54:2493–2505. https://doi.org/10.4319/lo.2009.54.6_part_2.2493
Wootton KL (2017) Omnivory and stability in freshwater habitats: does theory match reality? Freshw Biol 62:821–832. https://doi.org/10.1111/fwb.12908
Yang G, Qin B, Tang X, Gong Z, Zhong C, Zou H, Wang X (2012) Contrasting zooplankton communities of two bays of the large, shallow, eutrophic Lake Taihu, China: their relationship to environmental factors. J Great Lakes Res 38:299–308. https://doi.org/10.1016/j.jglr.2012.03.011
Yu J, Liu ZW, He H, Zhen W, Guan BH, Chen FZ, Li KY, Zhong P, Teixeira-de Mello F, Jeppesen E (2016) Submerged macrophytes facilitate dominance of omnivorous fish in a subtropical shallow lake: implications for lake restoration. Hydrobiologia 775:97–107. https://doi.org/10.1007/s10750-016-2717-7
Yvon-Durocher G, Allen AP, Cellamare M, Dossena M, Gaston KJ, Leitao M, Trimmer M (2015) Five years of experimental warming increases the biodiversity and productivity of phytoplankton. PLoS Biol 13(12):e1002324. https://doi.org/10.1371/journal.pbio.1002324
Zhang ZS, Huang XF (1991) Methods in freshwater plankton study (Book in Chinese). Science Press, Beijing
Zhang M, Duan H, Shi X, Yu Y, Kong F (2012) Contributions of meteorology to the phenology of cyanobacterial blooms: implications for future climate change. Water Res 46:442–452. https://doi.org/10.1016/j.watres.2011.11.013
Zhang J, Xie P, Tao M, Guo L, Chen J, Li L, Zhang L (2013) The impact of fish predation and cyanobacteria on zooplankton size structure in 96 subtropical lakes. PloS One 8(10):e76378. https://doi.org/10.1371/journal.pone.0076378
Zhang H, Ekvall MK, Xu J, Hansson LA (2015) Counteracting effects of recruitment and predation shape establishment of rotifer communities under climate change. Limnol Oceanogr 60:1577–1587. https://doi.org/10.1002/lno.10122
Zhang H, Urrutia-Cordero P, He L, Geng H, Chaguaceda F, Xu J, Hansson LA (2018) Life-history traits buffer against heat wave effects on predator–prey dynamics in zooplankton. Glob Change Biol 24:4747–4757. https://doi.org/10.1111/gcb.14371
Zingel P, Paaver T, Karus K, Agasild H, Noges T (2012) Ciliates as the crucial food source of larval fish in a shallow eutrophic lake. Limnol Oceanogr 57(4):1049–1056. https://doi.org/10.4319/lo.2012.57.4.1049
Acknowledgements
We express our gratitude to Xiaoxia Chen, Kai Peng, and Ruijie Shen for their help in the field and the laboratory work and Anne-Mette Poulsen for linguistic assistance. This study was supported by National Science Foundation of China (31930074; 31971473), Chinese National Key Research and Development Project (2017YFA0605201), and NIGLAS 135 Project (NIGLAS2017GH01, NIGLAS2018GH04). HH was supported by China Scholarship Council for a 1-year research stay in Denmark. EJ was supported by AQUACOSM (Network of Leading European AQUAtic MesoCOSM Facilities Connecting Mountains to Oceans from the Arctic to the Mediterranean), AnaEE Denmark (anaee.dk), and the Tübitak program BIDEB 2232.
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HH, KL, and ZL planned and designed this research. HH, JL, QL, and YH performed sampling and laboratory analysis work. HH, JL, YC, WL, JY, EJ, and ZL wrote the manuscript. All authors analyzed the data, commented on, and approved the manuscript and agreed upon the submission.
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He, H., Li, Q., Li, J. et al. Turning up the heat: warming influences plankton biomass and spring phenology in subtropical waters characterized by extensive fish omnivory. Oecologia 194, 251–265 (2020). https://doi.org/10.1007/s00442-020-04758-x
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DOI: https://doi.org/10.1007/s00442-020-04758-x