Marine Ecology Progress Series
MEPS is a leading hybrid research journal on all aspects of marine, coastal and estuarine ecology. Priority is given to outstanding research that advances our ecological understanding.
DOI: https://doi.org/10.3354/meps14867
copiedAdditive effects of climate change-related stress factors in Fucus serratus and Fucus vesiculosus
- Morten Foldager Pedersen
- Živilė Buivydaitė
- Nicolaj Stelzner Grønvall
- Mille Anna Lilja
- Florin Krijom
- Jacob Nepper-Davidsen
ABSTRACT:
Here we investigated the effects of elevated temperature and low salinity on 2 important tidal foundation species, Fucus serratus and Fucus vesiculosus, to determine how these stressors interact. We conducted a 2-factorial experiment, exposing F. serratus and F. vesiculosus to 15 and 25°C combined with 5 and 25 PSU salinity over a period of 5 wk. The measured endpoints were survival, growth rate, chlorophyll a fluorescence (max. quantum yield and electron transport rate), photosynthetic performance, antioxidant capacity evaluated through superoxide dismutase enzyme activity, and oxidative damages assessed through lipid peroxidation products. Our results showed that exposure to high temperature and low salinity separately had negative effects on both species, but strongest for F. serratus. The combined effects of heat and low salinity were generally stronger than the isolated effects of each stressor, and were additive in most cases, suggesting that the effects of elevated temperature and low salinity can be predicted from single factor experiments. Our study provides valuable insights into the interaction effects of elevated temperature and reduced salinity on 2 important foundation species and highlights the vulnerability of these Fucus species to climate change-induced changes in abiotic factors.
KEYWORDS
Bäck S, Ruuskanen A (2000) Distribution and maximum growth depth of Fucus vesiculosus along the Gulf of Finland. Mar Biol 136:303-307 Crossref
Bäck S, Collins JC, Russell G (1992) Effects of salinity on growth of Baltic and Atlantic Fucus vesiculosus. Br Phycol J 27:39-47 Crossref
Bass A, Wernberg T, Thomsen M, Smale D (2021) Another decade of marine climate change experiments: trends, progress and knowledge gaps. Front Mar Sci 8:714462 Crossref
Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in Hedera canariensis. Photosynth Res 25:173-185 Crossref PubMed
Bird NL, Chen LCM, McLachlan J (1979) Effects of temperature, light and salinity on growth in culture of Chondrus crispus, Furcellaria lumbricalis, Gracilaria tikvahiae (Gigartinales, Rhodophyta), and Fucus serratus (Fucales, Phaeophyta). Bot Mar 22:521-527 Crossref
Bollen M, Pilditch CA, Battershill CN, Bischof K (2016) Salinity and temperature tolerance of the invasive alga Undaria pinnatifida and native New Zealand kelps: implications for competition. Mar Biol 163:194 Crossref
Boyd PW, Lennartz ST, Glover DM, Doney SC (2015) Biological ramifications of climate-change-mediated oceanic multi-stressors. Nat Clim Chang 5:71-79 Crossref
Burrows EM (1964) Ecological experiments with species of Fucus. In: de Virville AD, Feldmann J (eds) Proc Fourth Intl Seaweed Symp. Pergamon Press, Oxford, p 166-170
Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of human stressors in marine systems. Ecol Lett 11:1304-1315 Crossref PubMed
Darling ES, Côté IM (2008) Quantifying the evidence for ecological synergies. Ecol Lett 11:1278-1286 Crossref PubMed
Davison IR (1991) Environmental effects on algal photosynthesis: temperature. J Phycol 27:2-8 Crossref
Davison IR, Pearson GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197-211 Crossref
Diez I, Muguerza N, Santolaria A, Ganzedo U, Gorostiaga JM (2012) Seaweed assemblage changes in the eastern Cantabrian Sea and their potential relationship to climate change. Estuar Coast Shelf Sci 99:108-120 Crossref
Filbee-Dexter K, Wernberg T, Grace SP, Thormar J and others (2020) Marine heatwaves and the collapse of marginal North Atlantic kelp forests. Sci Rep 10:13388 Crossref PubMed
Fortes MD, Lüning K (1980) Growth rates of North Sea macroalgae in relation to temperature, irradiance and photoperiod. Helgol Meeresunters 34:15-29 Crossref
Fox J, Weisberg S (2019) An R companion to applied regression, 3rd edn. Sage, Thousand Oaks, CA. socialsciences.mcmaster.ca/jfox/Books/Companion/ Link
Fryer MJ, Andrews JR, Oxborough K, Blowers DA, Baker NR (1998) Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature. Plant Physiol 116:571-580 Crossref PubMed
Genty B, Briantais JM, Baker NR (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87-92 Crossref
Graiff A, Liesnera D, Karsten U, Bartsch I (2015) Temperature tolerance of western Baltic Sea Fucus vesiculosus— growth, photosynthesis and survival. J Exp Mar Biol Ecol 471:8-16 Crossref
Gunderson AR, Armstrong EJ, Stillman JH (2016) Multiple stressors in a changing world: the need for an improved perspective on physiological responses to the dynamic marine environment. Annu Rev Mar Sci 8:357-378 Crossref PubMed
Harley CDG, Anderson KM, Demes KW, Jorve JP, Kordas RL, Coyle TA, Graham MH (2012) Effects of climate change on global seaweed communities. J Phycol 48:1064-1078 Crossref PubMed
Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643-9684 Crossref PubMed
Haupt-Herting S, Fock HP (2002) Oxygen exchange in relation to carbon assimilation in water-stressed leaves during photosynthesis. Ann Bot 89:851-859 Crossref PubMed
Heinrich S, Valentin K, Frickenhaus S, John U, Wiencke C (2012) Transcriptomic analysis of acclimation to temperature and light stress in Saccharina latissima (Phaeophyceae). PLOS ONE 7:e44342 Crossref PubMed
Hobday AJ, Alexander LV, Perkins SE, Smale DA and others (2016) A hierarchical approach to defining marine heatwaves. Prog Oceanogr 141:227-238 Crossref
Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed ecology and physiology, 2nd edn. Cambridge University Press, Cambridge Crossref
IPCC (2013) Climate change 2013: the physical science basis. In: Stocker TF, Qin D, Plattner GK, Tignor M and others (eds) Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, and New York, NY
Jueterbock A, Tyberghein L, Verbruggen H, Coyer JA, Olsen JL, Hoarau G (2013) Climate change impact on seaweed meadow distribution in the North Atlantic rocky intertidal. Ecol Evol 3:1356-1373 Crossref PubMed
Jueterbock A, Kollias S, Smolina I, Fernandes JMO, Coyer JA, Olsen JL, Hoarau G (2014) Thermal stress resistance of the brown alga Fucus serratus along the North-Atlantic coast: acclimatization potential to climate change. Mar Genomics 13:27-36 Crossref PubMed
Kessler A, Goris N, Lauvset SK (2022) Observation-based Sea surface temperature trends in Atlantic large marine ecosystems. Prog Oceanogr 208:102902 Crossref
Kirst CO (1990) Salinity tolerance of eukaryotic marine algae. Annu Rev Plant Biol 41:21-53 Crossref
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209-218 Crossref PubMed
Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253-278 Crossref PubMed
Lindenthal A, Hinrichs C, Jandt-Scheelke S, Kruschke T and others (2024) Baltic Sea surface temperature analysis 2022: a study of marine heatwaves and overall high seasonal temperatures. State Planet 4-osr8:16 Crossref
Lovelock CE, Winter K (1996) Oxygen-dependent electron transport and protection from photoinhibition in leaves of tropical tree species. Planta 198:580-587 Crossref PubMed
Lüning K (1990) Seaweeds: their environment, biogeography, and ecophysiology. John Wiley & Sons, Hoboken, NJ
Malm T, Kautsky L, Engkvist R (2001) Reproduction, recruitment and geographical distribution of Fucus serratus L. in the Baltic Sea. Bot Mar 44:101-108 Crossref
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence— a practical guide. J Exp Bot 51:659-668 Crossref PubMed
Meier HEM (2006) Baltic Sea climate in the late twenty-first century: a dynamical downscaling approach using two global models and two emission scenarios. Clim Dyn 27:39-68 Crossref
Moreno-Marín F, Brun FG, Pedersen MF (2018) Additive response to multiple environmental stressors in the seagrass Zostera marina L. Limnol Oceanogr 63:1528-1544 Crossref
Müller R, Laepple T, Bartsch I, Wiencke C (2009) Impact of oceanic warming on the distribution of seaweeds in polar and cold-temperate waters. Bot Mar 52:617-638 Crossref
Myers N (1995) Environmental unknowns. Science 269:358-360 Crossref PubMed
Nejrup LB, Pedersen MF (2012) The effect of temporal variability in salinity on the invasive red alga Gracilaria vermiculophylla. Eur J Phycol 47:254-263 Crossref
Nepper-Davidsen J, Andersen DT, Pedersen MF (2019) Exposure to simulated heatwave scenarios causes long-term reductions in performance in Saccharina latissima. Mar Ecol Prog Ser 630:25-39 Crossref
Nielsen HD, Nielsen SL (2008) Evaluation of imaging and conventional PAM as a measure of photosynthesis in thin- and thick-leaved marine macroalgae. Aquat Biol 3:121-131 Crossref
Nygård CA, Dring MJ (2008) Influence of salinity, temperature, dissolved inorganic carbon and nutrient concentration on the photosynthesis and growth of Fucus vesiculosus from the Baltic and Irish Seas. Eur J Phycol 43:253-262 Crossref
Olsson J, Dyrrdal AV, Médus E, Södling J and others (2022) Sub-daily rainfall extremes in the Nordic-Baltic region. Hydrol Res 53:807-824 Crossref
Paine RT, Tegner MJ, Johnson EA (1998) Compounded perturbations yield ecological surprises. Ecosystems 1:535-545 Crossref
Parkhill J, Maillet G, Cullen JJ (2001) Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J Phycol 37:517-529 Crossref
Payne MR (2018) Overview and status of Marine Heatwaves in waters around Denmark. RPubs: rpubs.com/markpayne Link
Pearson GA, Hoarau G, Lago-Leston A, Coyer JA and others (2010) An expressed sequence tag analysis of the intertidal brown seaweeds Fucus serratus (L.) and F. vesiculosus (L.) (Heterokontophyta, Phaeophyceae) in response to abiotic stressors. Mar Biotechnol (NY) 12:195-213 Crossref PubMed
Pedersen MF, Borum J, Fotel FL (2010) Phosphorus dynamics and limitation of fast- and slow-growing temperate seaweeds in Oslofjord, Norway. Mar Ecol Prog Ser 399:103-115 Crossref
Pica ML, Vitale E, Donadio R, Costanzo G and others (2024) Functional ecological traits in young and adult thalli of canopy-forming brown macroalga Gongolaria barbata (Phaeophyta) from a transitional water system. PeerJ 12:e17959 Crossref PubMed
Przeslawski R, Byrne M, Mellin C (2015) A review and meta-analysis of the effects of multiple abiotic stressors on marine embryos and larvae. Glob Change Biol 21:2122-2140 Crossref PubMed
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge Crossref
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Sala E, Knowlton N (2006) Global marine biodiversity trends. Annu Rev Environ Resour 31:93-122 Crossref
Salo T, Pedersen MF (2014) Synergistic effects of altered salinity and temperature on estuarine eelgrass (Zostera marina) seedlings and clonal shoots. J Exp Mar Biol Ecol 457:143-150 Crossref
Salvucci ME, Crafts-Brandner SJ (2004) Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco Activase in plants from contrasting thermal environments. Plant Physiol 134:1460-1470 Crossref PubMed
Sokolova IM (2013) Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr Comp Biol 53:597-608 Crossref PubMed
Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic vertebrates. Mar Environ Res 79:1-15 Crossref PubMed
Strain EMA, Thomson RJ, Micheli F, Mancuso FP, Airoldi L (2014) Identifying the interaction roles of stressors in driving the global loss of canopy-forming to mat-forming algae in marine ecosystems. Glob Change Biol 20:3300-3312 Crossref PubMed
Takolander A, Leskinen E, Cabeza M (2017) Synergistic effects of extreme temperature and low salinity on foundational macroalga Fucus vesiculosus in the northern Baltic Sea. J Exp Mar Biol Ecol 495:110-118 Crossref
Thomsen MS, Stæhr PAU, South PM (2024) Fabulous but forgotten fucoid forests. Ecol Evol 14:e70491 Crossref PubMed
Thonig A, Knott KE, Kesäniemi JE, Hansen BW, Banta GT (2016) Population and reproductive dynamics of the polychaete Pygospio elegans in a boreal estuary complex. Invertebr Biol 135:370-384 Crossref
Todgham AE, Stillman JH (2013) Physiological responses to shifts in multiple environmental stressors: relevance in a changing world. Integr Comp Biol 53:539-544 Crossref PubMed
Trenberth KE (2011) Changes in precipitation with climate change. Clim Res 47:123-138 Crossref
Wernberg T, Russell BD, Thomsen MS, Gurgel CFD, Bradshaw CJA, Poloczanska ES, Connell SD (2011) Seaweed communities in retreat from Ocean warming. Curr Biol 21:1828-1832 Crossref PubMed
Wernberg T, Smale DA, Thomsen MS (2012) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob Change Biol 18:1491-1498 Crossref
York PH, Gruber RK, Hill R, Ralph PJ, Booth DJ, Macreadie PI (2013) Physiological and morphological responses of the temperate seagrass Zostera muelleri to multiple stressors: investigating the interactive effects of light and temperature. PLOS ONE 8:e76377 Crossref PubMed
Morten Pedersen (Corresponding Author)
- Department of Science and Environment, Roskilde University, 4000 Roskilde, Denmark
Živilė Buivydaitė (Co-author)
- Department of Science and Environment, Roskilde University, 4000 Roskilde, Denmark
Nicolaj Grønvall (Co-author)
- Department of Science and Environment, Roskilde University, 4000 Roskilde, Denmark
Mille Lilja (Co-author)
- Department of Science and Environment, Roskilde University, 4000 Roskilde, Denmark
Florin Krijom (Co-author)
- Department of Science and Environment, Roskilde University, 4000 Roskilde, Denmark
Jacob Nepper-Davidsen (Co-author)
- Department of Science and Environment, Roskilde University, 4000 Roskilde, Denmark
Handling Editor:
Simonetta Fraschetti, Naples, Italy
Reviewers:
3 anonymous referees
Acknowledgements:
This work was funded by Roskilde University while M.F.P. was partly funded by the GecoKelp project (grant no NFR 335371 from the Norwegian Research Council). Part of this study represents results originating from a Bachelor thesis conducted by co-authors Ž.B., N.S.G., M.A.L., and F.K. under supervision of M.F.P. We thank technicians Rikke Guttesen and Torben B. Knudsen from Roskilde University for valuable assistance with some of the laboratory analyses and 3 anonymous referees for providing constructive critiques and valuable suggestions which helped to improve the quality of our manuscript.