Advertisement

Aquatic Sciences

, 80:34 | Cite as

Responses of primary producers in shallow lakes to elevated temperature: a mesocosm experiment during the growing season of Potamogeton crispus

  • Beibei Hao
  • Anna Fabrin Roejkjaer
  • Haoping Wu
  • Yu Cao
  • Erik Jeppesen
  • Wei Li
Research Article

Abstract

Climate warming may influence the relationship among macrophyte–periphyton–phytoplankton and change the producer community structure in shallow lakes, as elevated temperature has been suggested to promote the dominance of phytoplankton. We performed a 5-month experiment (starting in winter, December) to elucidate the responses of three phototrophic communities (macrophyte—Potamogeton crispus, periphyton, phytoplankton) and their interactions to elevated temperature (4.5 °C) under eutrophic, subtropical conditions. The biomass and composition of periphyton were not significantly affected by increased temperature, while the biomass of phytoplankton increased with a shift in phytoplankton composition towards higher dominance of chlorophytes and cyanobacteria. Warming also reduced the survival of P. crispus and accelerated the decline of P. crispus. At both ambient and heated temperatures, a shift occurred at the end of the experiment from a clear-state dominated by P. crispus to a clear-state dominated by filamentous algae and warming facilitated this shift. Our results thus indicated that, when submerged macrophytes diminished or disappeared, filamentous algae exhibited functional compensation that maintained low phytoplankton development, primarily at elevated temperatures.

Keywords

Climate warming Periphyton Phytoplankton Filamentous algae Primary producers 

Notes

Acknowledgements

This work was supported by the National Key Research and Development Program of China (2016YFA0601000), the National Natural Science Foundation of China (31500296, 31670368) and by the UCAS Joint PhD Training Program. EJ was supported by the MARS project (Managing Aquatic ecosystems and water Resources under multiple Stress) funded under the 7th EU Framework Programme, Theme 6 (Environment including Climate Change), Contract No.: 603378 (http://www.mars-project.eu). We thank Wenmin Huang, Hui Shao and Zhi Li for their assistance with the experiment. We thank Dr. Anne Mette Poulsen for English editing.

References

  1. Alsterberg C, Sundbäck K, Hulth S (2012) Functioning of a shallow-water sediment system during experimental warming and nutrient enrichment. PLoS One 7:e51503CrossRefGoogle Scholar
  2. APHA (1989) Standard methods for the examination of water and wastewater, 17th edn. American Public Health Association, Washington, DCGoogle Scholar
  3. Azcón-Bieto J, Osmond CB (1983) Relationship between photosynthesis and respiration the effect of carbohydrate status on the rate of COCO2 production by respiration in darkened and illuminated wheat leaves. Plant Physiol 71:574–581CrossRefGoogle Scholar
  4. Bolduan BR, Van Eeckhout GC, Quade HW, Gannon JE (1994) Potamogeton crispus—the other invader. Lake Reserv Manag 10:113–125CrossRefGoogle Scholar
  5. Cao Y, Li W, Jeppesen E (2014) The response of two submerged macrophytes and periphyton to elevated temperatures in the presence and absence of snails: a microcosm approach. Hydrobiologia 738:49–59CrossRefGoogle Scholar
  6. Carignan R, Kalff J (1982) Phosphorus release by submerged macrophytes: significance to epiphyton and phytoplankton. Limnol Oceanogr 27:419–427CrossRefGoogle Scholar
  7. Catling P, Dobson I (1985) The biology of Canadian weeds. 69. Potamogeton crispus L. Can J Plant Sci 65:655–668CrossRefGoogle Scholar
  8. Clarke KR, Gorley RN (2006) PRIMER V6: user manual-tutorial. Plymouth Marine Laboratory, PlymouthGoogle Scholar
  9. Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci 106:12788–12793CrossRefGoogle Scholar
  10. De Senerpont Domis LN, Van de Waal DB, Helmsing NR, Van Donk E, Mooij WM (2014) Community stoichiometry in a changing world: combined effects of warming and eutrophication on phytoplankton dynamics. Ecology 95:1485–1495CrossRefGoogle Scholar
  11. Ding Y, Ren G, Zhao Z, Xu Y, Luo Y, Li Q, Zhang J (2007) Detection, causes and projection of climate change over China: an overview of recent progress. Adv Atmos Sci 24:954–971CrossRefGoogle Scholar
  12. 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 45:1058–1066CrossRefGoogle Scholar
  13. Gerten D, Adrian R (2002) Effects of climate warming, North Atlantic Oscillation, and El Niño-Southern Oscillation on thermal conditions and plankton dynamics in Northern Hemispheric lakes. Sci World J 2:586–606CrossRefGoogle Scholar
  14. Gran G (1952) Determination of the equivalence point in potentiometric titrations. Part II Analyst. Acta Chem Scand 77:661–671Google Scholar
  15. Gulen H, Eris A (2003) Some physiological changes in strawberry (Fragaria × ananassa ‘Camarosa’) plants under heat stress. J Hortic Sci Biotechnol 78:894–898CrossRefGoogle Scholar
  16. Häder D-P, Villafane VE, Helbling EW (2014) Productivity of aquatic primary producers under global climate change. Photochem Photobiol Sci 13:1370–1392CrossRefGoogle Scholar
  17. Hao B, Wu H, Cao Y, Xing W, Jeppesen E, Li W (2017) Comparison of periphyton communities on natural and artificial macrophytes with contrasting morphological structures. Freshw Biol 62:1783–1793CrossRefGoogle Scholar
  18. He H, Zhu X, Song X, Jeppesen E, Liu Z (2015) Phytoplankton response to winter warming modified by large-bodied zooplankton: an experimental microcosm study. J Limnol 74:618–622Google Scholar
  19. Hongda C (1985) Life history, biomass and cut-branch propagation of Potamogeton. crispus. Acta Hydrobiol Sin 1:003Google Scholar
  20. Howard-Williams C (1981) Studies on the ability of a Potamogeton pectinatus community to remove dissolved nitrogen and phosphorus compounds from lake water. J Appl Ecol 18:619–637CrossRefGoogle Scholar
  21. IPCC (2007) Climate change 2007: the physical science basis. In: Working group I Contribution to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  22. IPCC (2013) Climate change 2013: the physical science basis. In: Working group I Contribution to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  23. Jeppesen E, Kronvang B, Meerhoff M, Søndergaard M, Hansen KM, Andersen HE, Lauridsen TL, Liboriussen L, Beklioglu M, Özen A (2009) Climate change effects on runoff, catchment phosphorus loading and lake ecological state, and potential adaptations. J Environ Qual 38:1930–1941CrossRefGoogle Scholar
  24. Jian Y, Li B, Wang J, Chen J (2003) Control of turion germination in Potamogeton crispus. Aquat Bot 75:59–69CrossRefGoogle Scholar
  25. Jupp B, Spence D (1977) Limitations on macrophytes in a eutrophic lake, Loch Leven: I. Effects of phytoplankton. J Ecol 65:175–186Google Scholar
  26. Kosten S, Jeppesen E, Huszar VLM, Mazzeo N, Van N, Egbert T, Peeters ET, Scheffer M (2011) Ambiguous climate impacts on competition between submerged macrophytes and phytoplankton in shallow lakes. Freshw Biol 56:1540–1553CrossRefGoogle Scholar
  27. Kunii H (1982) Life-cycle and growth of Potamogeton crispus L. in a Shallow Pond, Ojaga-Ike. Bot Mag Tokyo 95:109–124CrossRefGoogle Scholar
  28. Li H, Sun Q, Zhao S, Zhang W (2004) Plant physiology biochemistry principle and experimental technique. Higher Education Press, BeijingGoogle Scholar
  29. Li Z, He L, Zhang H, Urrutia-Cordero P, Ekvall MK, Hollander J, Hansson LA (2017) Climate warming and heat waves affect reproductive strategies and interactions between submerged macrophytes. Glob Change Biol 23:108–116CrossRefGoogle Scholar
  30. Liikanen A, Murtoniemi T, Tanskanen H, Väisänen T, Martikainen PJ (2002) Effects of temperature and oxygenavailability on greenhouse gas and nutrient dynamics in sediment of a eutrophic mid-boreal lake. Biogeochemistry 59:269–286CrossRefGoogle Scholar
  31. Lurling M, Eshetu F, Faassen EJ, Kosten S, Huszar VL (2013) Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshw Biol 58:552–559CrossRefGoogle Scholar
  32. Mahdy A, Hilt S, Filiz N, Beklioğlu M, Hejzlar J, Özkundakci D, Papastergiadou E, Scharfenberger U, Šorf M, Stefanidis K (2015) Effects of water temperature on summer periphyton biomass in shallow lakes: a pan-European mesocosm experiment. Aquat Sci 77:499–510CrossRefGoogle Scholar
  33. Mckee D, Hatton K, Eaton JW, Atkinson D, Atherton A, Harvey I, Moss B (2002) Effects of simulated climate warming on macrophytes in freshwater microcosm communities. Aquat Bot 74:71–83CrossRefGoogle Scholar
  34. Mooij WM, Hülsmann S, Domis LNDS, Nolet BA, Bodelier PL, Boers PC, Pires LMD, Gons HJ, Ibelings BW, Noordhuis R (2005) The impact of climate change on lakes in the Netherlands: a review. Aquat Ecol 39:381–400CrossRefGoogle Scholar
  35. Morán XAG, López-Urrutia Á, Calvo-Díaz A, Li WK (2010) Increasing importance of small phytoplankton in a warmer ocean. Glob Change Biol 16:1137–1144CrossRefGoogle Scholar
  36. Moss B (1990) Engineering and biological approaches to the restoration from eutrophication of shallow lakes in which aquatic plant communities are important components, Biomanipulation Tool for Water Management. Springer, pp. 367–377Google Scholar
  37. Moss B (2005) A filamentous green algae-dominated temperate shallow lake: Variations on the theme of clear-water stable states? Archiv für Hydrobiologie 163:25–47CrossRefGoogle Scholar
  38. Mujere N, Moyce W (2017) Climate Change Impacts on Surface Water Quality, Environmental Sustainability and Climate Change Adaptation Strategies. IGI Global, pp. 322–340Google Scholar
  39. O’Reilly CM, Alin SR, Plisnier P-D, Cohen AS, McKee BA (2003) Climate change decreases aquatic ecosystem productivity of Lake Tanganyika. Africa Nature 424:766–768CrossRefGoogle Scholar
  40. Olsen S, Chan F, Li W, Zhao S, Søndergaard M, Jeppesen E (2015) Strong impact of nitrogen loading on submerged macrophytes and algae: a long-term mesocosm experiment in a shallow Chinese lake. Freshwater biology 60:1525–1536CrossRefGoogle Scholar
  41. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669CrossRefGoogle Scholar
  42. Patrick DA, Boudreau N, Bozic Z, Carpenter GS, Langdon DM, LeMay SR, Martin SM, Mourse RM, Prince SL, Quinn KM (2012) Effects of climate change on late-season growth and survival of native and non-native species of watermilfoil (Myriophyllum spp.): implications for invasive potential and ecosystem change. Aquatic botany 103:83–88CrossRefGoogle Scholar
  43. Phillips G, Eminson D, Moss B (1978) A mechanism to account for macrophyte decline in progressively eutrophicated freshwaters. Aquat Bot 4:103–126CrossRefGoogle Scholar
  44. Rasband W (1997) ImageJ. US national institutes of health, bethesda, Maryland. AvailableGoogle Scholar
  45. Rasconi S, Gall A, Winter K, Kainz MJ (2015) Increasing water temperature triggers dominance of small freshwater plankton. PloS one 10:e0140449CrossRefGoogle Scholar
  46. Rasconi S, Winter K, Kainz MJ (2017) Temperature increase and fluctuation induce phytoplankton biodiversity loss–Evidence from a multi-seasonal mesocosm experiment. Ecology evolution 7:2936–2946CrossRefGoogle Scholar
  47. Rogers K, Breen C (1980) Growth and reproduction of Potamogeton crispus in a South African lake. J Ecol 68:561–571CrossRefGoogle Scholar
  48. Rooney N, Kalff J (2000) Inter-annual variation in submerged macrophyte community biomass and distribution: the influence of temperature and lake morphometry. Aquat Bot 68:321–335CrossRefGoogle Scholar
  49. Sand-Jensen K, Borum J (1991) Interactions among phytoplankton, periphyton, and macrophytes in temperate freshwaters and estuaries. Aquat Bot 41:137–175CrossRefGoogle Scholar
  50. Sastroutomo SS (1980) Environmental control of turion formation in curly pondweed (Potamogeton crispus). Physiol Plant 49:261–264CrossRefGoogle Scholar
  51. Scheffer M, Hosper S, Meijer M, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8:275–279CrossRefGoogle Scholar
  52. Short FT, Neckles HA (1999) The effects of global climate change on seagrasses. Aquat Bot 63:169–196CrossRefGoogle Scholar
  53. 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 Lond B Biol Sci 367:3008–3017CrossRefGoogle Scholar
  54. Straile D, Adrian R (2000) The North Atlantic Oscillation and plankton dynamics in two European lakes—two variations on a general theme. Glob Change Biol 6:663–670CrossRefGoogle Scholar
  55. Tarkowska-Kukuryk M, Mieczan T (2012) Effect of substrate on periphyton communities and relationships among food web components in shallow hypertrophic lake. J Limnol 71:30CrossRefGoogle Scholar
  56. Tjoelker M, Reich P, Oleksyn J (1999) Changes in leaf nitrogen and carbohydrates underlie temperature and CO2 acclimation of dark respiration in five boreal tree species. Plant Cell Environ 22:767–778CrossRefGoogle Scholar
  57. Tobiessen P, Snow PD (1984) Temperature and light effects on the growth of Potamogeton crispus in Collins Lake, New York State. Can J Bot 62:2822–2826CrossRefGoogle Scholar
  58. Trochine C, Guerrieri M, Liboriussen L, Meerhoff M, Lauridsen TL, Søndergaard M, Jeppesen E (2011) Filamentous green algae inhibit phytoplankton with enhanced effects when lakes get warmer. Freshw Biol 56:541–553CrossRefGoogle Scholar
  59. Wahid A, Close T (2007) Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biol Plant 51:104–109CrossRefGoogle Scholar
  60. Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJ, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefGoogle Scholar
  61. Wang H, Wang H, Liang X, Wu S (2014) Total phosphorus thresholds for regime shifts are nearly equal in subtropical and temperate shallow lakes with moderate depths and areas. Freshw Biol 59(8):1659–1671CrossRefGoogle Scholar
  62. Wang J, Song Y, Wang G (2016) Causes of large Potamogeton crispus L. population increase in Xuanwu Lake. Environ Sci Pollut Res 24:1–8CrossRefGoogle Scholar
  63. Wei L (2006) Method for monitoring and analysis water and waste water. China Environmental Science Press, BeijingGoogle Scholar
  64. Winder M, Hunter DA (2008) Temporal organization of phytoplankton communities linked to physical forcing. Oecologia 156:179–192CrossRefGoogle Scholar
  65. Wu J, Cheng S, Liang W, He F, Wu Z (2009) Effects of sediment anoxia and light on turion germination and early growth of Potamogeton crispus. Hydrobiologia 628:111–119CrossRefGoogle Scholar
  66. Zhang X, Odgaard R, Olesen B, Lauridsen L, Liboriussen T, Søndergaard L, Liu M, Jeppesen Z, E (2015) Warming shows differential effects on late-season growth and competitive capacity of Elodea canadensis and Potamogeton crispus in shallow lakes. Inland Waters 5:421–432CrossRefGoogle Scholar
  67. Zhang P, Bakker ES, Zhang M, Xu J (2016) Effects of warming on Potamogeton crispus growth and tissue stoichiometry in the growing season. Aquat Bot 128:13–17CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical GardenChinese Academy of SciencesWuhanChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Department of BioscienceAarhus UniversitySilkeborgDenmark
  4. 4.Sino-Danish Centre for Education and Research (SDC)University of Chinese Academy of SciencesBeijingChina
  5. 5.Hubei Key Laboratory of Wetland Evolution and Ecological Restoration, Wuhan Botanical GardenChinese Academy of SciencesWuhanChina

Personalised recommendations