Original Articles Open access

A multi-stressor environment impairs the photosynthetic performance of Virescentia viride-brasiliensis (Batrachospermales, Rhodophyta)

Authors

Published
4 September 2025
Section
Original Articles
DOI
10.4081/jlimnol.2025.2219

Abstract

Red algae belonging to Batrachospermales are important contributors to the energy input of lotic ecosystems. Given the importance of these algae for the lotic food web, we tested the photosynthetic performance of a relatively widespread and sensitive species (Virescentia viride-brasiliensis) in multi-stressor scenarios. Experiments were performed by exposing algal samples to three nominal concentrations (0.05 mg/L, 0.6 mg/L, and 1.2 mg/L) of tebuthiuron, a commonly used pesticide in Brazil, combined with three projected temperatures due to climate change (21.6ºC, 23.9ºC, and 26ºC). We observed a decrease in photosynthetic yield (Y(II)), regulated energy dissipation (Y(NPQ)), net photosynthetic rate (NPR), and dark respiration rate (DRR), while an increase in non-regulated energy dissipation (Y(NO)) was recorded, all of which indicate stress responses. Furthermore, we observed a dose-dependence relationship in which the negative effects increased with increasing tebuthiuron concentrations and in the scenario with a more severe temperature increase (26ºC). The high sensitivity of V. viride-brasiliensis to tebuthiuron highlights its potential bioindicator status because the tebuthiuron concentration accepted as safe for drinking water (0.05 mg/L) was sufficient to decrease its photosynthetic yield. Ultimately, these results show the importance of managing pesticide usage, especially considering the simultaneous occurrence of global warming.

Keywords

Edited by

Andras Abonyi, MTA Centre for Ecological Research, Institute of Ecology and Botany, Vácrátót, Hungary

References

  1. Belle S, Musazzi S, Tõnno I, Poska A, Leys B, Lami A, 2018. Long-term effects of climate change on carbon flows through benthic secondary production in small lakes. Freshwater Biol 63:530-538. DOI: https://doi.org/10.1111/fwb.13090
  2. Branco CCZ, Necchi Júnior O, Peres CK, 2010. Effects of artificial substratum types and exposure time on macroalgal colonization in a tropical stream. Fundam Appl Limnol 178:17–27. DOI: https://doi.org/10.1127/1863-9135/2010/0178-0017
  3. Branco CCZ, Riolfi TA, Crulhas BP, Tonetto AF, Bautista AIN, Necchi Júnior O, 2017. Tropical lotic primary producers: Who has the most efficient photosynthesis in low-order stream ecosystems? Freshwater Biol 62:1623-1636. DOI: https://doi.org/10.1111/fwb.12974
  4. Collins M, Knutti R, Arblaster J, Dufresne J-L, Fichefet T, Friedlingstein P, et al. 2013. Long-term Climate Change: Projections, Commitments and Irreversibility, p. 1029-1136. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, et al. (eds.), Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, New York. DOI: https://doi.org/10.1017/CBO9781107415324.024
  5. Cosgrove J, Borowitzka MA, 2011. Chlorophyll fluorescence terminology: An introduction, p. 1-17. In: Suggett DJ, Prásil O, Borowitzka MA (eds.), Chlorophyll a fluorescence in aquatic sciences: methods and applications. Dordrecht, Springer. DOI: https://doi.org/10.1007/978-90-481-9268-7_1
  6. Downes BJ, Lake PS, Schreiber ESG, Glaister A, 2000. Habitat structure, resources and diversity: the separate effects of surface roughness and macroalgae on stream invertebrates. Oecologia 123:569-581. DOI: https://doi.org/10.1007/PL00008862
  7. European Chemicals Agency, 2021. Tebuthiuron - Substance Infocard. Helsinki. [Searched on 30 November 2021]. Available from: https://echa.europa.eu/substance-information/-/substanceinfo/100.047.070
  8. Ferreira DF, 2011. Sisvar: a computer statistical analysis system. Cienc Agrotec 35:1039-1042. DOI: https://doi.org/10.1590/S1413-70542011000600001
  9. Heartsill-Scalley T, Aide TM, 2003. Riparian vegetation and stream condition in a tropical agriculture–secondary forest mosaic. Ecol Appl 13:225-234. DOI: https://doi.org/10.1890/1051-0761(2003)013[0225:RVASCI]2.0.CO;2
  10. Klughammer C, Schreiber U, 2008. Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. PAM Appl Notes 1:27-35.
  11. Krieger-Liszkay A, 2005. Singlet oxygen production in photosynthesis. J Exp Bot 56:337-346. DOI: https://doi.org/10.1093/jxb/erh237
  12. Littler MM, Arnold KE, 1985. Electrodes and chemicals, p. 349-375. In: Littler MM, Littler DS (eds.), Handbook of phycological methods. Ecological field methods: macroalgae. New York, Cambridge University Press.
  13. Liu J, 2010. Phenylurea Herbicides, p. 1725-1731. In: Krieger R (ed.), Hayes' handbook of pesticide toxicology. Academic Press, Cambridge. DOI: https://doi.org/10.1016/B978-0-12-374367-1.00080-X
  14. Lu Y, Li S, Sha M, Wang B, Cheng G, Guo Y, Zhu J, 2020. Cascading effects caused by fenoxycarb in freshwater systems dominated by Daphnia carinata and Dolerocypris sinensis. Ecotoxicol Environ Saf 203:111022. DOI: https://doi.org/10.1016/j.ecoenv.2020.111022
  15. Madeira CL, Acayaba RD, Santos VS, Villa JEL, Jacinto-Hernández C, Azevedo JAT, et al. 2023. Uncovering the impact of agricultural activities and urbanization on rivers from the Piracicaba, Capivari, and Jundiai basin in São Paulo, Brazil: A survey of pesticides, hormones, pharmaceuticals, industrial chemicals, and PFAS. Chemosphere 341:139954. DOI: https://doi.org/10.1016/j.chemosphere.2023.139954
  16. Marotzke J, Jakob C, Bony S, Dirmeyer PA, O’Gorman PA, Hawkins E, et al. 2017. Climate research must sharpen its view. Nat Clim Change 7:89-91. DOI: https://doi.org/10.1038/nclimate3206
  17. Martinuzzi S, Januchowski-Hartley SR, Pracheil BM, McIntyre PB, Plantinga AJ, Lewis DJ, Radeloff VC, 2014. Threats and opportunities for freshwater conservation under future land use change scenarios in the United States. Glob Chang Biol 20:113-124. DOI: https://doi.org/10.1111/gcb.12383
  18. Necchi Júnior O, 2016. An overview of river algae, p. 1-4. In: Necchi Júnior O (ed)., River algae. Springer, New York. DOI: https://doi.org/10.1007/978-3-319-31984-1_1
  19. Neres-Lima V, Machado-Silva F, Baptista DF, Oliveira RBS, Andrade PM, Oliveira AF, et al. 2017. Allochthonous and autochthonous carbon flows in food webs of tropical forest streams. Freshwater Biol 62:1012-1023. DOI: https://doi.org/10.1111/fwb.12921
  20. Nickus U, Bishop K, Erlandsson M, Evans CD, Forsius M, Laudon H, et al. 2010. Direct impacts of climate change on freshwater ecosystems, p. 38-64. In: Kernan M, Battarbee RW, Moss B (eds.), Climate Change Impacts on Freshwater Ecosystems. Wiley-Blackwell, Hoboken. DOI: https://doi.org/10.1002/9781444327397.ch3
  21. Oliveira AAS, Vieira LC, Dreossi SC, Dorta DJ, Gravato C, Ferreira MES, Oliveira, DP, 2023. Integrating morphological, biochemical, behavioural, and molecular approaches to investigate developmental toxicity triggered by tebuthiuron in zebrafish (Danio rerio). Chemosphere 340:139894. DOI: https://doi.org/10.1016/j.chemosphere.2023.139894
  22. Oliveira RC, Vilas Boas LK, Branco CCZ, 2016. Assessment of the potential toxicity of glyphosate-based herbicides on the photosynthesis of Nitella microcarpa var. wrightii (Charophyceae). Phycologia 55:577-584. DOI: https://doi.org/10.2216/16-12.1
  23. Oliveira RC, Vilas Boas LK, Branco CCZ, 2021. Effect of herbicides based on glyphosate on the photosynthesis of green macroalgae in tropical lotic environments. Fund Appl Limnol 195:85-93 DOI: https://doi.org/10.1127/fal/2021/1365
  24. Pereira JL, Antunes SC, Castro BB, Marques CR, Gonçalves AMM, Gonçalves F, Pereira R, 2009. Toxicity evaluation of three pesticides on non-target aquatic and soil organisms: commercial formulation versus active ingredient. Ecotoxicology 18:455-463. DOI: https://doi.org/10.1007/s10646-009-0300-y
  25. Qian Y, Matsumoto H, Liu X, Li S, Liang X, Liu Y, et al. 2017. Dissipation, occurrence and risk assessment of a phenylurea herbicide tebuthiuron in sugarcane and aquatic ecosystems in South China. Environm Pollut 227:389-396. DOI: https://doi.org/10.1016/j.envpol.2017.04.082
  26. Scanlon BR, Jolly I, Sophocleous M, Zhang L, 2007. Global impacts of conversions from natural to agricultural ecosystems on water resources: Quantity versus quality. Water Resour Res 43:W03437. DOI: https://doi.org/10.1029/2006WR005486
  27. Schreiber U, Bilger W, Neubauer C, 1995. Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis, p. 49-70. In: Schulze E-D, Caldwell MM (eds), Ecophysiology of photosynthesis. Springer, Berlin. DOI: https://doi.org/10.1007/978-3-642-79354-7_3
  28. Scott AJ, Knott M, 1974. A cluster analysis method for grouping means in the analysis of variance. Biometrics 30:507-512. DOI: https://doi.org/10.2307/2529204
  29. Sheath RG, Cole KM, 1992. Biogeography of stream macroalgae in North America. J Phycol 28:448-460. DOI: https://doi.org/10.1111/j.0022-3646.1992.00448.x
  30. Stancheva R, Sheath RG, 2016. Benthic soft-bodied algae as bioindicators of stream water quality. Knowl Manag Aquat Ecosyst 417:15. DOI: https://doi.org/10.1051/kmae/2016002
  31. Szöcs E, Brinke M, Karaoglan B, Schäfer RB, 2017. Large scale risks from agricultural pesticides in small streams. Environ Sci Technol 51:7378-7385. DOI: https://doi.org/10.1021/acs.est.7b00933
  32. Thomas MLH, 1988. Photosynthesis and respiration of aquatic macro-flora using the light and dark bottle oxygen method and dissolved oxygen analyzer, p. 64-77. In: Lobban CS, Chapman DJ, Kremer BP (eds.), Experimental Phycology: A laboratory manual. Cambridge University Press, Cambridge.
  33. Thomas MC, Flores F, Kaserzon S, Reeks TA, Negri AP, 2020. Toxicity of the herbicides diuron, propazine, tebuthiuron, and haloxyfop to the diatom Chaetoceros muelleri. Sci Rep 10:19592. DOI: https://doi.org/10.1038/s41598-020-76363-0
  34. Tilman D, Fargione J, Wolff B, D'antonio C, Dobson A, Howarth R, et al. 2001. Forecasting agriculturally driven global environmental change. Science 292: 281-284. DOI: https://doi.org/10.1126/science.1057544
  35. U.S. Environmental Protection Agency, 1988. Tebuthiuron, p. 1-16. Health Advisory. U.S. Environmental Protection Agency, Washington.
  36. Vilas Boas LK, Oliveira RC, Necchi Júnior O, Branco CCZ, 2019. Temperature effects on photosynthesis in gametophytic and sporophytic stages of the freshwater red alga Sirodotia delicatula (Rhodophyta, Batrachospermales) under a global warming perspective. Phycol Res 67:39-44. DOI: https://doi.org/10.1111/pre.12345
  37. Vilas Boas LK, Branco CCZ, 2022. Effect of tebuthiuron and temperature increase related to climate change on the photosynthesis of Nitella microcarpa var. wrightii (Charophyceae). J Appl Phycol 34:1721-1729. DOI: https://doi.org/10.1007/s10811-022-02750-x
  38. Vilas Boas LK, Branco CCZ, 2024. The herbicide tebuthiuron and temperature increase related to climate change can impair the photosynthesis of Oedogonium sp. (Chlorophyta). Acta Bot Bras 38:e20230091. DOI: https://doi.org/10.1590/1677-941x-abb-2023-0091
  39. Watanabe M, 2005. Freshwater culture media, p. 13-20. In: Andersen R (ed.), Algal culturing techniques. Elsevier Academic Press, London. DOI: https://doi.org/10.1016/B978-012088426-1/50003-2
  40. Woodward G, Perkins DM, Brown LE, 2010. Climate change and freshwater ecosystems: impacts across multiple levels of organization. Philos T Roy Soc B 365:2093-2106. DOI: https://doi.org/10.1098/rstb.2010.0055
  41. Yadav A, Pandey LK, 2023. In situ effects of arsenic, aluminnium and chromium stresses on algal periphyton of the river Ganga at Varanasi, India. J Limnol 82:2112. DOI: https://doi.org/10.4081/jlimnol.2023.2112

Metrics

Citations and online attention from Dimensions, Altmetric and PlumX.

PlumX Metrics

License

Copyright (c) 2025 The Author(s)

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.