The effects of warming on the ecophysiology of two co-existing kelp species with contrasting distributions
- 570 Downloads
The northeast Atlantic has warmed significantly since the early 1980s, leading to shifts in species distributions and changes in the structure and functioning of communities and ecosystems. This study investigated the effects of increased temperature on two co-existing habitat-forming kelps: Laminaria digitata, a northern boreal species, and Laminaria ochroleuca, a southern Lusitanian species, to shed light on mechanisms underpinning responses of trailing and leading edge populations to warming. Kelp sporophytes collected from southwest United Kingdom were maintained under 3 treatments: ambient temperature (12 °C), +3 °C (15 °C) and +6 °C (18 °C) for 16 days. At higher temperatures, L. digitata showed a decline in growth rates and Fv/Fm, an increase in chemical defence production and a decrease in palatability. In contrast, L. ochroleuca demonstrated superior growth and photosynthesis at temperatures higher than current ambient levels, and was more heavily grazed. Whilst the observed decreased palatability of L. digitata held at higher temperatures could reduce top-down pressure on marginal populations, field observations of grazer densities suggest that this may be unimportant within the study system. Overall, our study suggests that shifts in trailing edge populations will be primarily driven by ecophysiological responses to high temperatures experienced during current and predicted thermal maxima, and although compensatory mechanisms may reduce top-down pressure on marginal populations, this is unlikely to be important within the current biogeographical context. Better understanding of the mechanisms underpinning climate-driven range shifts is important for habitat-forming species like kelps, which provide organic matter, create biogenic structure and alter environmental conditions for associated communities.
KeywordsOcean warming Macroalgae Chemical defence Thermal tolerance Range shifts
We thank Richard Billington for assistance with biochemical analyses and Esther Hughes (DASSH, MBA) for assistance with Fig. 1. D.A.S. was funded by the Natural Environmental Research Council (UK) Independent Research Fellowship (NE/K008439/1).
Author contribution statement
All authors conceived and designed the experiments. MH performed the experiments. MH and AF analysed the data. AP provided and analysed field-based survey data. MH and DS wrote the manuscript; AF and AP provided editorial advice.
- Bates AE, Pecl GT, Frusher S, Hobday AJ, Wernberg T, Smale DA, Sunday JM, Hill NA, Dulvy NK, Colwell RK, Holbrook NJ, Fulton EA, Slawinski D, Feng M, Edgar GJ, Radford BT, Thompson PA, Watson RA (2014) Defining and observing stages of climate-mediated range shifts in marine systems. Glob Environ Change 26:27–38. doi: 10.1016/j.gloenvcha.2014.03.009 CrossRefGoogle Scholar
- Beaugrand G, McQuatters-Gollop A, Edwards M, Goberville E (2013) Long-term responses of North Atlantic calcifying plankton to climate change. Nat Clim Change 3:263–267. http://www.nature.com/nclimate/journal/v3/n3/abs/nclimate1753.html#supplementary-information
- Bigger DS, Marvier MA (1998) How different would a world without herbivory be?: a search for generality in ecology. Integr Biol 1:60–67. doi: 10.1002/(SICI)1520-6602(1998)1:2<60:AID-INBI4>3.0.CO;2-Z CrossRefGoogle Scholar
- Brodie J, Williamson CJ, Smale DA, Kamenos NA, Mieszkowska N, Santos R, Cunliffe M, Steinke M, Yesson C, Anderson KM, Asnaghi V, Brownlee C, Burdett HL, Burrows MT, Collins S, Donohue PJC, Harvey B, Foggo A, Noisette F, Nunes J, Ragazzola F, Raven JA, Schmidt DN, Suggett D, Teichberg M, Hall-Spencer JM (2014) The future of the northeast Atlantic benthic flora in a high CO2 world. Ecol Evol 4:2787–2798. doi: 10.1002/ece3.1105 CrossRefPubMedPubMedCentralGoogle Scholar
- De Wreede RE, Klinger T (1988) Reproductive strategies in algae. In: Douest JL, Douest LL (eds) Plant reproductive ecology: patterns and strategies. Oxford University Press, Melbourne, pp 267–284Google Scholar
- Hughes SL, Holliday NP, Kennedy J, Berry DI, Kent EC, Sherwin T, Dye S, Inall M, Shammon T, Smyth T (2010) Temperature (air and sea). MCCIP Annual Report Card 2010–2011, MCCIP Science Review, pp 16Google Scholar
- IPCC (2013) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds). Cambridge University Press, Cambridge, UK and New York, NY, USA, pp 1535Google Scholar
- Johnson CR, Mann KH (1986) The importance of plant defence abilities to the structure of subtidal seaweed communities: the kelp Laminaria longicruris de la Pylaie survives grazing by the snail Lacuna vincta (Montagu) at high population densities. J Exp Mar Biol Ecol 97:231–267. doi: 10.1016/0022-0981(86)90244-3 CrossRefGoogle Scholar
- Ladah L, Zertuche-González J (2007) Survival of microscopic stages of a perennial kelp (Macrocystis pyrifera) from the center and the southern extreme of its range in the Northern Hemisphere after exposure to simulated El Niño stress. Mar Biol 152:677–686. doi: 10.1007/s00227-007-0723-z CrossRefGoogle Scholar
- Müller R, Laepple T, Bartsch I, Wiencke C (2009) Impact of ocean warming on the distribution of seaweeds in polar and cold-temperate waters. Bot Mar 52:617–638Google Scholar
- Pereira TR, Engelen AH, Pearson GA, Serrao EA, Destombe C, Valero M (2011) Temperature effects on the microscopic haploid stage development of Laminaria ochroleuca and Sacchoriza polyschides, kelps with contrasting life histories. Cah Biol Mar 52:1–10Google Scholar
- Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte CM, Halpern BS, Holding J, Kappel CV, O’Connor MI, Pandolfi JM, Parmesan C, Schwing F, Thompson SA, Richardson AJ (2013) Global imprint of climate change on marine life. Nat Clim Change 3:919–925. doi: 10.1038/nclimate1958. CrossRefGoogle Scholar
- Smale DA, Moore PJ (2017) Variability in kelp forest structure along a latitudinal gradient in ocean temperature. J Exp Mar Biol Ecol 486:255–264Google Scholar
- Sunday JM, Pecl GT, Frusher S, Hobday AJ, Hill NA, Holbrook NJ, Edgar GJ, Stuart-Smith RD, Barrett NS, Wernberg T, Watson RA, Smale DA, Fulton EA, Slawinski D, Feng M, Radford BT, Bates AE (2015) Species traits and climate velocity explain geographic range shifts in an ocean warming hotspot. Ecol Lett 18:944–953CrossRefPubMedGoogle Scholar
- Valladares F, Matesanz S, Guilhaumon F, Araújo MB, Balaguer L, Benito-Garzón M, Cornwell W, Gianoli E, van Kleunen M, Naya DE, Nicotra AB, Poorter H, Zavala MA (2014) The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol Lett 17:1351–1364. doi: 10.1111/ele.12348 CrossRefPubMedGoogle Scholar
- Vergés A, Steinberg PD, Hay ME, Poore AGB, Campbell AH, Ballesteros E, Heck KL, Booth DJ, Coleman MA, Feary DA, Figueira W, Langlois T, Marzinelli EM, Mizerek T, Mumby PJ, Nakamura Y, Roughan M, van Sebille E, Gupta AS, Smale DA, Tomas F, Wernberg T, Wilson SK (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 281:20140846. doi: 10.1098/rspb.2014.0846 CrossRefPubMedPubMedCentralGoogle Scholar
- Wernberg T, Bennett S, Babcock RC, de Bettignies T, Cure K, Depczynski M, Dufois F, Fromont J, Fulton CJ, Hovey RK, Harvey ES, Holmes TH, Kendrick GA, Radford B, Santana-Garcon J, Saunders BJ, Smale DA, Thomsen MS, Tuckett CA, Tuya F, Vanderklift MA, Wilson SK (2016) Climate driven regime shift of a temperate marine ecosystem. Science 353:169–172CrossRefPubMedGoogle Scholar