Abstract
Marine heatwaves (MHWs) caused by anthropogenic climate change are becoming a key driver of change at the ecosystem level. Thermal conditions experienced by marine organisms across their distribution, particularly towards the equator, are likely to approach their physiological limits, resulting in extensive mortality and subsequent changes at the population level. Populations at the margins of their species’ distribution are thought to be more sensitive to climate-induced environmental pressures than central populations, but our understanding of variability in fitness-related physiological traits in trailing versus leading-edge populations is limited. In a laboratory simulation study, we tested whether two leading (Iceland) and two trailing (Spain) peripheral populations of the intertidal macroalga Corallina officinalis display different levels of maximum potential quantum efficiency (Fv/Fm) resilience to current and future winter MHWs scenarios. Our study revealed that ongoing and future local winter MHWs will not negatively affect leading-edge populations of C. officinalis, which exhibited stable photosynthetic efficiency throughout the study. Trailing edge populations showed a positive though non-significant trend in photosynthetic efficiency throughout winter MHWs exposure. Poleward and equatorward populations did not produce significantly different results, with winter MHWs having no negative affect on Fv/Fm of either population. Additionally, we found no long-term regional or population-level influence of a winter MHWs on this species’ photosynthetic efficiency. Thus, we found no statistically significant difference in thermal stress responses between leading and trailing populations. Nonetheless, C. officinalis showed a trend towards higher stress responses in southern than northern populations. Because responses rest on a variety of local population traits, they are difficult to predict based solely on thermal pressures.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Araújo R, Serrão E A, Sousa-Pinto I, et al. 2014. Spatial and temporal dynamics of fucoid populations (Ascophyllum nodosum and Fucus serratus): a comparison between central and range edge populations. PloS One, 9(3): 92177, doi: https://doi.org/10.1371/journal.pone.0092177
Atkinson J, King N G, Wilmes S B, et al. 2020. Summer and winter marine heatwaves favor an invasive over native seaweeds. Journal of Phycology, 56(6): 1591–1600, doi: https://doi.org/10.1111/jpy.13051
Badger M R, Björkman O, Armond P A. 1982. An analysis of photo-synthetic response and adaptation to temperature in higher plants: temperature acclimation in the desert evergreen Nerium oleander L. Plant, Cell and Environment, 5: 85–99
Bates D, Maechler M, Bolker B, et al. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1): 1–48
Bennett S, Wernberg T, Arackal Joy B, et al. 2015. Central and rear-edge populations can be equally vulnerable to warming. Nature Communications, 6: 10280, doi: https://doi.org/10.1038/ncomms10280
Berkelmans R, Willis B L. 1999. Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore Central Great Barrier Reef. Coral Reefs, 18: 219–28, doi: https://doi.org/10.1007/s003380050186
Bertocci I, Araújo R, Vaselli S, et al. 2011. Marginal populations under pressure: spatial and temporal heterogeneity of Ascophyllum nodosum and associated assemblages affected by human trampling in Portugal. Marine Ecology Progress Series, 439: 73–82, doi: https://doi.org/10.3354/meps09328
Bolker B M, Brooks M E, Clark C J, et al. 2009. Generalize linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution, 24(3): 127–135, doi: https://doi.org/10.1016/j.tree.2008.10.008
Bridle J R, Vines T H. 2007. Limits to evolution at range margins: when and why does adaptation fail?. Trends in Ecology and Evolution, 22(3): 140–147
Brody H M. 2004. Phenotypic Plasticity: Functional and Conceptual Approaches. Oxford: Oxford University Press
Brown J H. 1984. On the relationship between abundance and distribution of species. The American Naturalist, 124(2): 255–279, doi: https://doi.org/10.1086/284267
Brussard P F. 1984. Geographic patterns and environmental gradients: the central-marginal models in Drosophila revisited. Annual Review of Ecology Systematics, 15: 25–64, doi: https://doi.org/10.1146/annurev.es.15.110184.000325
Bulger AJ, Tremaine S C. 1985. Magnitude of seasonal effects on heat tolerance in Fundulus heteroclitus. Physiological Zoology, 58: 197–204, doi: https://doi.org/10.1086/physzool.58.2.30158567
Chapple J P, Smerdon G R, Berry R J, et al. 1998. Seasonal changes in stress-70 protein levels reflect thermal tolerance in the marine bivalve Mytilus edulis L. Journal of Experimental Marine Biology and Ecology, 229: 53–68, doi: https://doi.org/10.1016/S0022-0981(98)00040-9
Charpy-Roubaud C, Sournia A. 1990. The comparative estimation of phytoplanktonic, microphytobenthic and microphytobenthic primary production in the oceans. Marine Microbial Food Webs, 4: 31–57
Crawley M J. 2012. The R Book. Chichester, West Sussex, United Kingdom: Wiley
Crafts-Brandner S J, Salvucci M E. 2002. Sensitivity of photosynthesis in a C4 plant, maize, to heat stress. Plant physiology, 129(4): 1773–1780, doi: https://doi.org/10.1104/pp.002170
Davison I R. 1987. Adaptation of photosynthesis in Laminaria saccharina (Phaeophyta) to changes in growth temperature. Journal of Phycology, 23: 273–83, doi: https://doi.org/10.1111/j.1529-8817.1987.tb04135.x
Dudgeon S R, Davison I R, Vadas R L. 1990. Freezing tolerance in the intertidal red algae Chondrus crispus and Mastocarpus stellatus: relative importance of acclimation and adaptation. Marine Biology, 106: 36–427, doi: https://doi.org/10.1007/BF01344323
Eckert C G, Samis K E, Lougheed S C. 2008. Genetic variation across species’ geographical ranges: The central-marginal hypothesis and beyond. Molecular Ecology, 17: 1170–1188, doi: https://doi.org/10.1111/j.1365-294X.2007.03659.x
Egilsdottir H, Noisette F, Noel L M-L J, et al. 2013. Effects of pCO2 on physiology and skeletal mineralogy in a tidal pool coralline alga Corallina elongata. Marine Biology, 160: 2103–2112.
Foster M S. 2001. Rhodoliths: between rocks and soft places. Journal of Phycology, 37: 659–667, doi: https://doi.org/10.1046/j.1529-8817.2001.00195.x
Fredriksen S. 2003. Food web studies in a Norwegian kelp forest based on stable isotope (δ13C and δ15N) analysis. Marine Ecology Progress Series, 260: 71–81, doi: https://doi.org/10.3354/meps260071
Guo Q. 2014. Central-marginal population dynamics in species invasions. Frontiers in Ecology and Evolution, 2: 23.
Hampe A, Petit R J. 2005. Conserving biodiversity under climate change: the rear edge matters. Ecology letters, 8(5): 461–467, doi: https://doi.org/10.1111/j.1461-0248.2005.00739.x
Helmuth B, Harley C D, Halpin P M, et al. 2002. Climate change and latitudinal patterns of intertidal thermal stress. Science, 298(5595): 1015–1017, doi: https://doi.org/10.1126/science.1076814
Hind K R, Gabrielson P W, Lindstrom S C, et al. 2014. Misleading morphologies and the importance of sequencing type specimens for resolving coralline taxonomy (Corallinales, Rhodophyta): Pachyarthron cretaceum is Corallina officinalis. Journal of Phycology, 50(4): 760–764, doi: https://doi.org/10.1111/jpy.12205
Hobday A J, Alexander L, Perkins S, et al. 2016. A hierarchical approach to defining marine heatwaves. Progress in Oceanography, 141: 227–238, doi: https://doi.org/10.1016/j.pocean.2015.12.014
Hu X P, Appel A G. 2004. Seasonal variation of critical thermal limits and temperature tolerance in Formosan and Eastern subterranean termites (Isoptera: Rhinotermitidae). Environmental Entomology, 33: 197–205, doi: https://doi.org/10.1603/0046-225X-33.2.197
IPCC, 2014. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, R. K. Pachauri, L. A. Meyer (eds.)]. pp. Geneva, Switzerland, IPCC: 151
IPCC, 2021. Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change [Masson-Delmotte V, Zhai P, Pirani A, et al. (eds.)]. Cambridge University Press.
IPCC, 2022. Summary for Policymakers [Pörtner H-O, Roberts D C, Poloczanska E S, et al. (eds.)]. In: Climate Change 2022: Impacts, Adaptation, and Vulnerability. Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press.
Jones S J, Lima F P, Wethey D S. 2010. Rising environmental temperatures and biogeography: Poleward range contraction of the blue mussel, Mytilus edulis L., in the western Atlantic. Journal of Biogeography, 37: 2243–2259
Kassambara A. 2021. Pipe-friendly framework for basic statistical tests (Version 0.7). https://www.cran.r-project.org/web/packages/rstatix/index.html[2021-06-13/2022-09-27]
Kim J H, Min J, Kang E J, et al. 2018. Elevated temperature and changed carbonate chemistry: effects on calcification, photosynthesis, and growth of Corallina officinalis (Corallinales, Rhodophyta). Phycologia, 57(3): 280–286, doi: https://doi.org/10.2216/17-71.1
King N G, McKeown N J, Smale D A, et al. 2019. Evidence for different thermal ecotypes in range centre and trailing edge kelp populations. Journal of Experimental Marine Biology and Ecology, 514: 10–17
Kolzenburg R, 2022. The direct influence of climate change on marginal populations: a review. Aquatic Sciences, 84(2): 1–20
Kolzenburg R, Coaten D J, Ragazzola F. 2022. Physiological characterisation of the calcified alga Corallina officinalis (Rhodophyta) from the leading to trailing edge in the Northeast Atlantic. European Journal of Phycology, 58(1): 83–98
Kolzenburg R, Nicastro K R, McCoy S J, et al. 2019. Understanding the margin squeeze: Differentiation in fitness-related traits between central and trailing edge populations of Corallina officinalis. Ecology and Evolution, 9(10): 5787–5801, doi: https://doi.org/10.1002/ece3.5162
Kübler J E, Davison I R. 1993. High-temperature tolerance of photosynthesis in the red alga Chondrus crispus. Marine Biology, 117: 327–35, doi: https://doi.org/10.1007/BF00345678
Laufkötter C, Zscheischler J, Frölicher T L. 2020. High-impact marine heatwaves attributable to human-induced global warming. Science, 369(6511): 1621–1625, doi: https://doi.org/10.1126/science.aba0690
Layne J R Jr, Claussen D L, Manis M L. 1987. Effects of acclimation temperature, season, and time of day on the critical thermal maxima and minima of the crayfish Orconectes rusticus. Journal of Thermal Biology, 12: 183–7, doi: https://doi.org/10.1016/0306-4565(87)90001-5
Lima F P, Ribeiro P A, Queiroz N, et al. 2007. Do distributional shifts of northern and southern species of algae match the warming pattern?. Global Change Biology, 13(12): 2592–2604.
Lüning K. 1984. Temperature tolerance and biogeography of seaweeds: the marine algal flora of Helgoland (North Sea) as an example. Helgoläander Meeresuntersuchungen, 38: 305–17.
Magill C L, Maggs C A, Johnson M P, et al. 2019. Sustainable Harvesting of the Ecosystem Engineer Corallina officinalis for Biomaterials. Frontiers in Marine Science, 6: 285, doi: https://doi.org/10.3389/fmars.2019.00285
Meteo. 2021. Ministry of the Environment, Territory and Infrastructures - Xunta de Galicia, accessed 30 March 2021, http://www2.meteogalicia.gal/galego/observacion/plataformas/platHistorico.asp?Nest=15100&red=102
Mineur F, Arenas F, Assis J, et al. 2015. European seaweeds under pressure: Consequences for communities and ecosystem functioning. Journal of Sea Research, 98: 91–108, doi: https://doi.org/10.1016/j.seares.2014.11.004
Mota C F, Engelen A H, Serrao E A, et al. 2018. Differentiation in fitness-related traits in response to elevated temperatures between leading and trailing edge populations of marine macrophytes. PloS One, 13(9): 0203666
Ntuli N N, Nicastro K R, Zardi G I, et al. 2020. Rejection of the genetic implications of the “Abundant Centre Hypothesis” in marine mussels. Scientific Reports, 10: 604, doi: https://doi.org/10.1038/s41598-020-57474-0
Oliver E C, Donat M G, Burrows M T, et al. 2018. Longer and more frequent marine heatwaves over the past century. Nature Communications, 9(1): 1324, doi: https://doi.org/10.1038/s41467-018-03732-9
Padilla-Gamino J L, Carpenter R C. 2007. Seasonal acclimatization of Asparagopsis taxiformis (Rhodophyta) from different biogeographic regions. Limnology and Oceanography, 52: 833–42, doi: https://doi.org/10.4319/lo.2007.52.2.0833
Ragazzola F, Foster L C, Form A U, et al. 2013. Phenotypic plasticity of coralline algae in a high CO2 world. Ecology and Evolution, 3(10): 3436–3446, doi: https://doi.org/10.1002/ece3.723
Rendina F, Bouchet P J, Appolloni L, et al. 2019. Physiological response of the coralline alga Corallina officinalis L. to both predicted long-term increases in temperature and short-term heatwave events. Marine Environmental Research, 150: 104764, doi: https://doi.org/10.1016/j.marenvres.2019.104764
Saada G, Nicastro K R, Jacinto R, et al. 2016. Taking the heat: distinct vulnerability to thermal stress of central and threatened peripheral lineages of a marine macroalga. Diversity and Distributions, 22(10): 1060–1068, doi: https://doi.org/10.1111/ddi.12474
Sagarin R D, Gaines S D. 2002. The ‘abundant centre’ distribution: to what extent is it a biogeographical rule?. Ecology Letters, 5(1): 137–147
Sexton J P, McIntyre P J, Angert A L, et al. 2009. Evolution and ecology of species range limits. Annual Review of Ecology, Evolution and Systematics, 40: 415–436
Smale D A, Wernberg T, Oliver E C J, et al. 2019. Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Nature Climate Change, 9(4): 306–312, doi: https://doi.org/10.1038/s41558-019-0412-1
Steller D L, Riosmena-Rodríguez R, Foster M S, et al. 2003. Rhodolith bed diversity in the Gulf of California: the importance of rhodolith structure and consequences of disturbance. Aquatic conservation: Marine and Freshwater Ecosystems, 13(S1): S5–S20, doi: https://doi.org/10.1002/aqc.564
Straub S C, Wernberg T, Thomsen M S, et al. 2019. Resistance, extinction, and everything in between—The diverse responses of seaweeds to marine heatwaves. Frontiers in Marine Science, 6: 763, doi: https://doi.org/10.3389/fmars.2019.00763
Tavares A I, Nicastro K R, Kolzenburg R, et al. 2018. Isolation and characterization of nine microsatellite markers for the red alga Corallina officinalis. Molecular Biology Reports, 45(6): 2791–2794
Underwood A J. 1997. Experiments in Ecology. Their Logical Design and Interpretation Using Analysis of Variance. Cambridge University Press: Cambridge
Whittaker R H. 1956. Vegetation of the Great Smoky Mountains. Ecological Monographs, 26: 2–80
Williamson C J, Brodie J, Goss B, et al. 2014. Corallina and Ellisolandia (Corallinales, Rhodophyta) photophysiology over daylight tidal emersion: interactions with irradiance, temperature and carbonate chemistry. Marine Biology, 161: 2051–2068, doi: https://doi.org/10.1007/s00227-014-2485-8
Williamson C J, Perkins R, Yallop M L, et al. 2018. Photoacclimation and photoregulation strategies of Corallina (Corallinales, Rhodophyta) across the NE Atlantic. European Journal of Phycology, 53(3): 290–306, doi: https://doi.org/10.1080/09670262.2018.1442586
Yang A, Dick C W, Yao X, et al. 2016. Impacts of biogeographic history and marginal population genetics on species range limits: a case study of Liriodendron chinense. Scientific Reports, 6(1): 25632, doi: https://doi.org/10.1038/srep25632
Zardi G I, Nicastro K R, Serrão E A, et al. 2015. Closer to the rear edge: Ecology and genetic diversity down the core-edge gradient of a marine macroalga. Ecosphere, 6(2): 1–25
Zuur A F, Ieno E N, Smith G M. 2007. Analysing Ecological Data. Vol 680. New York: Springer
Acknowledgements
All the authors would like to thank the technical staff (Marc Martin, Jenny Mackellar and Dr Graham Malyon) of the Institute of Marine Science (University of Portsmouth) for their extraordinary support during the COVID-19 lockdowns. Without them, we would not have been able to run the experiment.
Author information
Authors and Affiliations
Corresponding author
Additional information
Foundation item: The Fundação para a Ciência e Tecnologia (FCT-MEC, Portugal) under contract No. UIDB/04326/2020 awarded to Gerardo Zardi; the South African Research Chairs Initiative (SARChI) of the Department of Science and Technology and the National Research Foundation of South Africa under contract No. 64801 awarded to Christopher McQuaid; the Fund of European Unions’ Horizon 2020 Research and Innovation Programme under the Marie Skłodowska-Curie contract No. 101034329; the WINNINGNormandy Program supported by the Normandy Region for Gerardo Zardi.
Electronic supplementary material
13131_2023_2275_MOESM1_ESM.pdf
Photosynthetic response to a winter heatwave in leading and trailing edge populations of the intertidal red alga Corallina officinalis (Rhodophyta)
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Kolzenburg, R., Ragazzola, F., Tamburello, L. et al. Photosynthetic response to a winter heatwave in leading and trailing edge populations of the intertidal red alga Corallina officinalis (Rhodophyta). Acta Oceanol. Sin. (2024). https://doi.org/10.1007/s13131-023-2275-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13131-023-2275-6