Abstract
Global warming can affect biomass accumulation and the dynamics of periphytic communities, potentially altering their role in aquatic ecosystem functioning. We conducted a 38-day mesocosm experiment to investigate the effects of an increase in winter temperature on periphyton biomass accumulation under eutrophic conditions. We evaluated the warming effect on colonization phases, identifying the most affected phase. The experiment had two treatments (control: current winter temperature of 23.5 ℃, warming: + 5.7 ℃ under IPCC scenario). It was carried out in growth chambers under controlled temperature, light, and humidity. Periphyton and water samplings were performed on days 3, 6, 9, 13, 17, 21, 27, and 38. The increase in temperature did not affect the organic matter accrual rate of the periphyton. However, it negatively affected the net and gross accrual rate of the algal biomass. Ash-free dry mass and chlorophyll-a ratio in the periphyton increased at higher temperatures, indicating a decrease in autotrophic components in the periphyton in the warming treatment. We detected losses in algal biomass during the intermediate and advanced colonization phases. Our results showed a decrease in periphytic algal biomass with an increase in average temperature in winter. In conclusion, a warming scenario can negatively influence periphyton biomass in eutrophic ecosystems, where algal growth in the community is generally unfavorable.
Similar content being viewed by others
Availability of data and materials
The datasets generated and analyzed during the present study are available from the corresponding author on reasonable request.
References
Amaral LM, de Almeida Castilho MC, Henry R, Ferragut C (2020) Epipelon, phytoplankton and zooplankton responses to the experimental oligotrophication in a eutrophic shallow reservoir. Environ Pollut 263:114603
APHA American Public Health Association (2012) Standard methods for the examination of water and wastewater. American Public Health Association, Washington
Beck WS, Markman DW, Oleksy IA, Lafferty MH, Poff NL (2019) Seasonal shifts in the importance of bottom–up and top–down factors on stream periphyton community structure. Oikos 128:680–691
Bicudo DC, Fonseca BM, Bini LM, Crossetti LO, Bicudo CEM, Araújo-Jesus T (2007) Undesirable side-effects of water hyacinth control in a shallow tropical reservoir. Freshw Biol 52:1120–1133
Biggs BJF (1996) Patterns in benthic algal of streams. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal ecology: freshwater benthic ecosystems. Academic Press, New York, pp 31–56
Bondar-Kunze E, Kasper V, Hein T (2021) Responses of periphyton communities to abrupt changes in water temperature and velocity, and the relevance of morphology: a mesocosm approach. Sci Total Environ 768:145200
Borduqui M, Ferragut C (2012) Factors determining periphytic algae succession in a tropical hypereutrophic reservoir. Hydrobiologia 683:109–122
Casartelli MR, Lavagnolli GJ, Ferragut C (2016) Periphyton biomass accrual rate changes over the colonization process in a shallow mesotrophic reservoir. Acta Limnol Bras. https://doi.org/10.1590/S2179-975X0116
Crossetti LO, Bicudo DC, Bini LM, Dala-Corte RB, Ferragut C, Bicudo CEM (2019) Phytoplankton species interactions and invasion by Ceratium furcoides are influenced by extreme drought and water-hyacinth removal in a shallow tropical reservoir. Hydrobiologia 831:71–85
Cunha DGF, Calijuri MDC, Lamparelli MC (2013) A trophic state index for tropical/ subtropical reservoirs (TSItsr). Ecol Eng 60:126–134
De Nicola DM (1996) Periphyton responses to temperature at different ecological levels. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal ecology: freshwater benthic ecosystems. Academic Press, San Diego, pp 149–181
De Nicola DM, Kelly M (2014) Role of periphyton in ecological assessment of lakes. Freshw Sci 33:619–638
Dodds WK (2003) The role periphyton in phosphorus retention in shallow freshwater aquatic systems. J Phycol 39:840–849
Domis LNS, 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 95:1485–1495
Dunck B, Rodrigues L, Bicudo DC (2015) Functional diversity and functional traits of periphytic algae during a short-term successional process in a Neotropical floodplain lake. Braz J Biol 75:587–597
Dunck B, Algarte VM, Cianciaruso MV, Rodrigues L (2016) Functional diversity and trait–environment relationships of periphytic algae in subtropical floodplain lakes. Ecol Ind 67:257–266
Enberg S, Piiparinen J, Majaneva M, Vähätalo AV, Autio R, Rintala JM (2015) Solar PAR and UVR modify the community composition and photosynthetic activity of sea ice algae. FEMS Microbiol Ecol. 91:fiv102
Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633
Gomes AMDA, Marinho MM, Berjante Mesquita MC, Prestes ACC, Lürling M, Azevedo SM (2020) Warming and eutrophication effects on the phytoplankton communities of two tropical water systems of different trophic states: an experimental approach. Lake Reserv Manag 25:275–282
Hao B, Wu H, Zhen W, Jo H, Cai Y, Jeppesen E, Li W (2020) Warming effects on periphyton community and abundance in different seasons are influenced by nutrient state and plant type: a shallow lake mesocosm study. Front Plant Sci. https://doi.org/10.3389/fpls.2020.00404
Hansson LA, Nicolle A, Granéli W, Hallgren P, Kritzberg E, Persson A, Bjork J, Nilsson A, Brönmark C (2013) Food-chain length alters community responses to global change in aquatic systems. Nat Clim Change 3:228–233
Hansson LA, Ekvall MK, He L, Li Z, Svensson M, Urrutia-Cordero P et al (2020) Different climate scenarios alter dominance patterns among aquatic primary producers in temperate systems. Limnol Oceanogr 65:2328–2336
Havens KE, East TL, Meeker RH, Davis WP, Steinman AD (1996) Phytoplankton and periphyton responses to in situ experimental nutrient enrichment in a shallow subtropical lake. J Plankton Res 18:551–566
Huysman MJJ, Vyverman W, De Veylder L (2014) Molecular regulation of the diatom cell cycle. J Exp Bot 65:2573–2584
IPCC Intergovernmental Panel on Climate Change. Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva: IPCC, 2021. Available via https://www.ipcc.ch/report/ar6/wg1/. Cited 12 Jun 2023
Jeppesen E, Søndergaard M, Meerhoff M, Lauridsen TL, Jensen JP (2007) Shallow lake restoration by nutrient loading reduction some recent findings and challenges ahead. Hydrobiologia 584:239–252
Jeppesen E, Kronvang B, Meerhoff M, Søndergaard M, Hansen KM, Andersen HE, Olesen JE (2009) Climate change effects on runoff, catchment phosphorus loading and lake ecological state, and potential adaptations. J Environ Qual 38:1930–1941
Kazanjian G, Velthuis M, Aben R, Stephan S, Peeters ETHM, Frenken T, Touwen J, Xue F, Kosten S, Van de Waal DB, de Senerpont Domis LN, van Donk E, Hilt S (2018) Impacts of warming on top-down and bottom-up controls of periphyton production. Sci Rep 8:9901
Lambert AS, Dabrin A, Morin S, Gahou J, Foulquier A, Coquery M, Pesce S (2016) Temperature modulates phototrophic periphyton response to chronic copper exposure. Environ Pollut 208:821–829
Lan B, Li H, Xiang X, Lin J, Yin J, Yang S (2018) Spatial-temporal characteristics of epilithic algae succession on artificial substrata in relation to water quality in Erhai Lake, Yunnan Province, China. Biologia 73:821–830
Mahdy A, Hilt S, Filiz N, Beklioğlu M, Hejzlar J, Özkundakci D, Adrian R (2015) Effects of water temperature on summer periphyton biomass in shallow lakes: a pan-European mesocosm experiment. Pan-Am J Aquat Sci 77:499–510
Meerhoff M, Teixeira-de Mello F, Kruk C, Alonso C, Gonzalez-Bergonzoni I, Pacheco JP, Jeppesen E (2012) Environmental warming in shallow lakes: a review of potential changes in community structure as evidenced from space-for-time substitution approaches. Adv Ecol Res 46:259–349
McCormick PV (1996) Resource competition and species coexistence in freshwater benthic algal assemblages. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal ecology: freshwater benthic ecosystems. Academic Press, USA, pp 229–252
MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria 1. J Phycol 38:17–38
Moss B, Kosten S, Meerhoff M, Battarbee RW, Jeppesen E, Mazzeo N, Havens K, Lacerot G, Liu Z, de Meester L, Paerl H, Scheffer M (2011) Allied attack: climate change and eutrophication. Inland Waters 1:101–105
Pacheco JP, Aznarez C, Meerhoff M, Liu Y, Li W, Baattrup-Pedersen A, Cao Y, Jeppesen E (2021) Small-sized omnivorous fish induce stronger effects on food webs than warming and eutrophication in experimental shallow lakes. Sci Total Environ 797:148998
Puts IC, Ask J, Myrstener M, Bergström AK (2023) Contrasting impacts of warming and browning on periphyton. Limnol Oceanogr Lett 8:1–11
Richardson K, Beardall J, Raven JA (1983) Adaptation of unicellular algae to irradiance: an analysis of strategies. New Phytol 93:157–191
Rühland KM, Paterson AM, Smol JP (2015) Lake diatom responses to warming: reviewing the evidence. J Paleolimnol 54:1–35
Salk KR, Venkiteswaran JJ, Couture RM, Higgins SN, Paterson MJ, Schiff SL (2021) Warming combined with experimental eutrophication intensifies lake phytoplankton blooms. Limnol Oceanogr 67:147–158
Santos TR, Castilho MC, Henry R, Ferragut C (2020) Relationship between epipelon, epiphyton and phytoplankton in two limnological phases in a shallow tropical reservoir with high Nymphaea coverage. Hydrobiologia 847:1121–1137
Sartory DP, Grobbelaar JU (1984) Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiologia 114:177–187
Silva SFM, Torgan LC, Schneck F (2019) Temperature and surface runoff affect the community of periphytic diatoms and have distinct effects on functional groups: evidence of a mesocosms experiment. Hydrobiologia 839:37–50
Stevenson RJ (1996) An introduction to algal ecology in freshwater benthic habitats. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal ecology: freshwater benthic ecosystems. Academic Press, San Diego, pp 3–30
Urrutia-Cordero P, Ekvall MK, Ratcovich J, Soares M, Wilken S, Zhang H, Hansson LA (2017) Phytoplankton diversity loss along a gradient of future warming and brownification in freshwater mesocosms. Freshw Biol 62:1869–1878
Vadeboncoeur Y, Steinman AD (2002) Periphyton function in lake ecosystems. T Sci World J 2:1–20
Vadeboncoeur Y, Lodge DM, Carpenter SR (2001) Whole-lake fertilization effects on distribution of primary production between benthic and pelagic habitats. Ecology 82:1065–1077
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 48:1408–1418
Vadeboncoeur Y, Moore MV, Stewart SD, Chandra S, Atkins KS, Baron JS, Bouma-Gregson K, Brothers S, Francoeur SN, Genzoli L, Higgins SN, Hilt S, Katona LR, Kelly D, Oleksy IA, Ozersky T, Power ME, Roberts D, Smits AP, Timoshkin O, Tromboni F, Zanden MJV, Volkova EA, Waters S, Wood SA, Yamamuro M (2021) Blue waters, green bottoms: benthic filamentous algal blooms are an emerging threat to clear lakes worldwide. Bioscience 71:1011–1027
Vasconcelos FR, Diehl S, Rodríguez P, Hedström P, Karlsson J, Byström P (2016) Asymmetrical competition between aquatic primary producers in a warmer and browner world. Ecology 97:2580–2592
Zhang X, Mei X, Gulati RD, Liu Z (2015) Effects of N and P enrichment on competition between phytoplankton and benthic algae in shallow lakes: a mesocosm study. Environ Sci Pollut Res 22:4418–4424
Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223
Weather Station of the Institute of Astronomy, Geophysics and Atmospheric Sciences of the University of São Paulo (IAG). Weather Bulletin 2022 (In Portuguese). Available via http://www.estacao.iag.usp.br/boletim.php. Cited in June/12/2023
Wong WH, Rabalais NN, Turner RE (2016) Size-dependent top-down control on phytoplankton growth by microzooplankton in eutrophic lakes. Hydrobiologia 763:97–108
Wu Y, Xia L, Yu Z, Shabbir S, Kerr PG (2014) In situ bioremediation of surface waters by periphyton. Bioresour Technol 151:367–372
Acknowledgements
The authors are grateful for the financial support of the Fundação de Amparo à Pesquisa do Estado de São Paulo for the development of the project (FAPESP 2017/50341-0). LDS is grateful for the scientific initiation scholarship granted by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2022/08479-2) and ROC is grateful for the master’s scholarship granted by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and FAPESP (2022/16879-0). All authors would like to thank the technicians and graduate students for their support in collections and laboratory analyses.
Funding
The authors declare that there are no competing financial interests.
Author information
Authors and Affiliations
Contributions
L.D. Sapucaia, R.O. Carneiro, and C. Ferragut: conceptualized experimental sampling, wrote, and edited the original draft; L.D. Sapucaia generated the biotic data; all authors generated the abiotic results. All authors revised and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Ethical approval
Not applicable/not required.
Consent to participate
All the authors consent to participate in this manuscript.
Consent for publication
All the authors consent the publication of this manuscript.
Additional information
Handling Editor: Simon Belle.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sapucaia, L.D., Carneiro, R.O. & Ferragut, C. Effect of increasing temperature on periphyton accrual under controlled environmental conditions. Limnology (2024). https://doi.org/10.1007/s10201-024-00749-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10201-024-00749-6