The endemic kelp Lessonia corrugata is being pushed above its thermal limits in an ocean warming hotspot.

kelp multiple drivers nitrate nutrients ocean warming thermal optimum thermal performance curves

Journal

Journal of phycology
ISSN: 1529-8817
Titre abrégé: J Phycol
Pays: United States
ID NLM: 9882935

Informations de publication

Date de publication:
01 Mar 2024
Historique:
revised: 22 01 2024
received: 29 09 2023
accepted: 28 01 2024
medline: 1 3 2024
pubmed: 1 3 2024
entrez: 1 3 2024
Statut: aheadofprint

Résumé

Kelps are in global decline due to climate change, which includes ocean warming. To identify vulnerable species, we need to identify their tolerances to increasing temperatures and determine whether tolerances are altered by co-occurring drivers such as inorganic nutrient levels. This is particularly important for those species with restricted distributions, which may already be experiencing thermal stress. To identify thermal tolerance of the range-restricted kelp Lessonia corrugata, we conducted a laboratory experiment on juvenile sporophytes to measure performance (growth, photosynthesis) across its thermal range (4-22°C). We determined the upper thermal limit for growth and photosynthesis to be ~22-23°C, with a thermal optimum of ~16°C. To determine if elevated inorganic nitrogen availability could enhance thermal tolerance, we compared the performance of juveniles under low (4.5 μmol · d

Identifiants

pubmed: 38426571
doi: 10.1111/jpy.13434
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Department of Natural Resources and Environment - Abalone Industry Reinvestment Fund
ID : AIRF Project 2020/47

Informations de copyright

© 2024 The Authors. Journal of Phycology published by Wiley Periodicals LLC on behalf of Phycological Society of America.

Références

Adams, M. P., Collier, C. J., Uthicke, S., Ow, Y. X., Langlois, L., & O'Brien, K. R. (2017). Model fit versus biological relevance: Evaluating photosynthesis-temperature models for three tropical seagrass species. Scientific Reports, 7(1), 39930.
Angilletta, M. J. (2006). Estimating and comparing thermal performance curves. Journal of Thermal Biology, 31(7), 541-545. https://doi.org/10.1016/j.jtherbio.2006.06.002
Banzon, V., Smith, T. M., Chin, T. M., Liu, C., & Hankins, W. (2016). A long-term record of blended satellite and in situ sea-surface temperature for climate monitoring, modeling and environmental studies. Earth System Science Data, 8(1), 165-176.
Bartsch, I., Vogt, J., Pehlke, C., & Hanelt, D. (2013). Prevailing sea surface temperatures inhibit summer reproduction of the kelp Laminaria digitata at Helgoland (North Sea). Journal of Phycology, 49(6), 1061-1073.
Bonaviri, C., Graham, M., Gianguzza, P., & Shears, N. T. (2017). Warmer temperatures reduce the influence of an important keystone predator. Journal of Animal Ecology, 86(3), 490-500.
Box, G. E., & Cox, D. R. (1964). An analysis of transformations. Journal of the Royal Statistical Society, Series B: Statistical Methodology, 26(2), 211-243.
Boyd, P. W., Collins, S., Dupont, S., Fabricius, K., Gattuso, J. P., Havenhand, J., Hutchins, D. A., Riebesell, U., Rintoul, M. S., & Vichi, M. (2018). Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change-A review. Global Change Biology, 24(6), 2239-2261.
Bristow, L. A., Mohr, W., Ahmerkamp, S., & Kuypers, M. M. (2017). Nutrients that limit growth in the ocean. Current Biology, 27(11), R474-R478.
Britton, D., Layton, C., Mundy, C., Brewer, E., Gaitan-Espitia, J., Beardall, J., Raven, J., & Hurd, C. (2024). Cool-edge populations of the kelp Ecklonia radiata under global ocean change scenarios: Strong sensitivity to warming but little effect of ocean acidification. Proceedings of the Royal Society B: Biological Sciences, 291(2015), 20232253.
Britton, D., Schmid, M., Noisette, F., Havenhand, J. N., Paine, E. R., McGraw, C. M., Revill, A. T., Virtue, P., Nichols, P. D., & Mundy, C. N. (2020). Adjustments in fatty acid composition is a mechanism that can explain resilience to marine heatwaves and future ocean conditions in the habitat-forming seaweed Phyllospora comosa (Labillardière) C. Agardh. Global Change Biology, 26(6), 3512-3524.
Butler, C. L., Lucieer, V. L., Wotherspoon, S. J., & Johnson, C. R. (2020). Multi-decadal decline in cover of giant kelp Macrocystis pyrifera at the southern limit of its Australian range. Marine Ecology Progress Series, 653, 1-18.
Campbell, A. H., Harder, T., Nielsen, S., Kjelleberg, S., & Steinberg, P. D. (2011). Climate change and disease: Bleaching of a chemically defended seaweed. Global Change Biology, 17(9), 2958-2970.
Case, R. J., Longford, S. R., Campbell, A. H., Low, A., Tujula, N., Steinberg, P. D., & Kjelleberg, S. (2011). Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga. Environmental Microbiology, 13(2), 529-537.
Collén, J., Guisle-Marsollier, I., Léger, J. J., & Boyen, C. (2007). Response of the transcriptome of the intertidal red seaweed Chondrus crispus to controlled and natural stresses. New Phytologist, 176(1), 45-55.
Collins, S., Whittaker, H., & Thomas, M. K. (2022). The need for unrealistic experiments in global change biology. Current Opinion in Microbiology, 68, 102151.
Colvard, N., & Helmuth, B. (2017). Nutrients influence the thermal ecophysiology of an intertidal macroalga: multiple stressors or multiple drivers? Ecological Applications, 27(2), 669-681. https://doi.org/10.1002/eap.1475
Doney, S. C., Ruckelshaus, M., Emmett Duffy, J., Barry, J. P., Chan, F., English, C. A., Galindo, H. M., Grebmeier, J. M., Hollowed, A. B., & Knowlton, N. (2012). Climate change impacts on marine ecosystems. Annual Review of Marine Science, 4, 11-37.
Eggert, A. (2012). Seaweed responses to temperature. In C. Wiencke & B. Bischof (Eds.), Seaweed biology: Novel insights into ecophysiology, ecology and utilization (pp. 47-66). Springer.
Endo, H., Suehiro, K., Gao, X., & Agatsuma, Y. (2017). Interactive effects of elevated summer temperature, nutrient availability, and irradiance on growth and chemical compositions of juvenile kelp, Eisenia bicyclis. Phycological Research, 65(2), 118-126.
Fairhead, V., & Cheshire, A. (2004). Rates of primary productivity and growth in Ecklonia radiata measured at different depths, over an annual cycle, at West Island, South Australia. Marine Biology, 145, 41-50.
Fernández, P. A., Gaitán-Espitia, J. D., Leal, P. P., Schmid, M., Revill, A. T., & Hurd, C. L. (2020). Nitrogen sufficiency enhances thermal tolerance in habitat-forming kelp: Implications for acclimation under thermal stress. Scientific Reports, 10(1), 3186.
Flukes, E. B., Wright, J. T., & Johnson, C. R. (2015). Phenotypic plasticity and biogeographic variation in physiology of habitat-forming seaweed: Response to temperature and nitrate. Journal of Phycology, 51(5), 896-909.
Fox, J., & Weisberg, S. (2019). Using car functions in other functions. CRAN R.
Frusher, S. D., Hobday, A. J., Jennings, S. M., Creighton, C., D'Silva, D., Haward, M., Holbrook, N. J., Nursey-Bray, M., Pecl, G. T., & van Putten, E. I. (2014). The short history of research in a marine climate change hotspot: From anecdote to adaptation in south-east Australia. Reviews in Fish Biology and Fisheries, 24, 593-611.
Gerard, V. A. (1998). The role of nitrogen nutrition in high-temperature tolerance of the kelp, Laminaria saccharina (Chromophyta). Oceanographic Literature Review, 2(45), 351.
Hammann, M., Wang, G., Boo, S. M., Aguilar-Rosas, L. E., & Weinberger, F. (2016). Selection of heat-shock resistance traits during the invasion of the seaweed Gracilaria vermiculophylla. Marine Biology, 163, 1-11.
Hobday, A. J., & Pecl, G. T. (2014). Identification of global marine hotspots: Sentinels for change and vanguards for adaptation action. Reviews in Fish Biology and Fisheries, 24, 415-425.
Hoos, J. J., & Harley, C. D. (2021). The sign and magnitude of the effects of thermal extremes on an intertidal kelp depend on environmental and biological context. Climate Change Ecology, 2, 100015.
Huppe, H. C., & Turpin, D. H. (1994). Integration of carbon and nitrogen metabolism in plant and algal cells. Annual Review of Plant Biology, 45(1), 577-607.
Hurd, C., Harrison, P., Bischof, K., & Lobban, C. (2014a). Physico-chemical factors as environmental stressors in seaweed biology. Seaweed Ecology and Physiology, 2, 294-348.
Hurd, C. L., Harrison, P. J., Bischof, K., & Lobban, C. S. (2014b). Seaweed ecology and physiology. Cambridge University Press.
Hurd, C. L., Wright, J. T., Layton, C., Strain, E. M., Britton, D., Visch, W., Barrett, N., Bennett, S., Chang, K. J. L., & Edgar, G. (2023). From Tasmania to the world: Long and strong traditions in seaweed use, research, and development. Botanica Marina, 66(1), 1-36.
IPCC. (2023, Core Writing Team). Climate change 2023: Synthesis report. A report of the intergovernmental panel on climate change. In H. Lee & J. Romero (Eds.), Contribution of working groups I, II and III to the sixth assessment report of the intergovernmental panel on climate change. IPCC.
Jones, C. G., Lawton, J. H., & Shachak, M. (1994). Organisms as ecosystem engineers. Oikos, 69, 373-386.
Krumhansl, K. A., Okamoto, D. K., Rassweiler, A., Novak, M., Bolton, J. J., Cavanaugh, K. C., Connell, S. D., Johnson, C. R., Konar, B., & Ling, S. D. (2016). Global patterns of kelp forest change over the past half-century. Proceedings of the National Academy of Sciences, 113(48), 13785-13790.
Layton, C., Cameron, M. J., Tatsumi, M., Shelamoff, V., Wright, J. T., & Johnson, C. R. (2020). Habitat fragmentation causes collapse of kelp recruitment. Marine Ecology Progress Series, 648, 111-123.
Layton, C., & Johnson, C. R. (2021). Assessing the feasibility of restoring giant kelp forests in Tasmania. Report to the National Environmental Science Program, Marine Biodiversity Hub.
Layton, C., Peréz-Matus, A., González, A. V., & Coleman, M. A. (2022). Future-proofing kelp forest restoration for climate change. In A. Eger, C. Layton, T. McHugh, M. Gleason, N. Eddy, J. Caselle, & B. DeAngelis (Eds.), Kelp restoration guidebook: Lessons learned from kelp projects around the world. The Nature Conservancy.
Leggat, W. P., Camp, E. F., Suggett, D. J., Heron, S. F., Fordyce, A. J., Gardner, S., Deakin, L., Turner, M., Beeching, L. J., & Kuzhiumparambil, U. (2019). Rapid coral decay is associated with marine heatwave mortality events on reefs. Current Biology, 29(16), 2723-2730. e2724.
Lenth, R. (2023). Emmeans: Estimated marginal means, aka least-squares means. R Package Version 1.8.4-1.
Mabin, C. J., Johnson, C. R., & Wright, J. T. (2019). Physiological response to temperature, light, and nitrates in the giant kelp Macrocystis pyrifera from Tasmania, Australia. Marine Ecology Progress Series, 614, 1-19.
Mann, E., & Kirkman, H. (1981). Biomass method for measuring productivity of Ecklonia radiata, with the potential for adaptation to other large brown algae. Marine and Freshwater Research, 32(2), 297-304.
Martínez, B., Radford, B., Thomsen, M. S., Connell, S. D., Carreño, F., Bradshaw, C. J., Fordham, D. A., Russell, B. D., Gurgel, C. F. D., & Wernberg, T. (2018). Distribution models predict large contractions of habitat-forming seaweeds in response to ocean warming. Diversity and Distributions, 24(10), 1350-1366.
Marzinelli, E. M., Campbell, A. H., Zozaya Valdes, E., Vergés, A., Nielsen, S., Wernberg, T., De Bettignies, T., Bennett, S., Caporaso, J. G., & Thomas, T. (2015). Continental-scale variation in seaweed host-associated bacterial communities is a function of host condition, not geography. Environmental Microbiology, 17(10), 4078-4088.
Mellin, C., Edgar, G., Emslie, M., Barrett, N., Turak, E., Gilmour, J., & Stuart-Smith, R. (2021). A standardised national assessment of the state of coral and rocky reef biodiversity. Report to the National Environmental Science Program, Marine Biodiversity Hub. University of Tasmania.
Minich, J. J., Morris, M. M., Brown, M., Doane, M., Edwards, M. S., Michael, T. P., & Dinsdale, E. A. (2018). Elevated temperature drives kelp microbiome dysbiosis, while elevated carbon dioxide induces water microbiome disruption. PLoS ONE, 13(2), e0192772.
Mohring, M. B., Wernberg, T., Wright, J. T., Connell, S. D., & Russell, B. D. (2014). Biogeographic variation in temperature drives performance of kelp gametophytes during warming. Marine Ecology Progress Series, 513, 85-96.
Nardelli, A. E., Visch, W., Farrington, G., Sanderson, J. C., Bellgrove, A., Wright, J. T., MacLeod, C., & Hurd, C. L. (2023). A new nursery approach enhances at-sea performance in the kelp Lessonia corrugata. Journal of Applied Phycology, 1-13.
Nardelli, A. E., Visch, W., Wright, J. T., & Hurd, C. L. (2023). Concise review of genus Lessonia Bory. Journal of Applied Phycology, 35, 1-14.
Nguyen, H. M., Ralph, P. J., Marín-Guirao, L., Pernice, M., & Procaccini, G. (2021). Seagrasses in an era of ocean warming: A review. Biological Reviews, 96(5), 2009-2030.
Oliver, E. C., Benthuysen, J. A., Bindoff, N. L., Hobday, A., J., Holbrook, N. J., Mundy, C. N., & Perkins-Kirkpatrick, S. E. (2017). The unprecedented 2015/16 Tasman Sea marine heatwave. Nature Communications, 8(1), 16101.
Padfield, D., O'Sullivan, H., & Pawar, S. (2021). rTPC and nls. Multstart: A new pipeline to fit thermal performance curves in R. Methods in Ecology and Evolution, 12(6), 1138-1143.
Paine, E. R., Schmid, M., Gaitán-Espitia, J. D., Castle, J., Jameson, I., Sanderson, J. C., & Hurd, C. L. (2021). Narrow range of temperature and irradiance supports optimal development of Lessonia corrugata (Ochrophyta) gametophytes: Implications for kelp aquaculture and responses to climate change. Journal of Applied Phycology, 33, 1721-1730.
Paine, E. R., Schmid, M., Revill, A. T., & Hurd, C. L. (2021). Light regulates inorganic nitrogen uptake and storage, but not nitrate assimilation, by the red macroalga Hemineura frondosa (Rhodophyta). European Journal of Phycology, 56(2), 174-185.
Qiu, Z., Coleman, M. A., Provost, E., Campbell, A. H., Kelaher, B. P., Dalton, S. J., Thomas, T., Steinberg, P. D., & Marzinelli, E. M. (2019). Future climate change is predicted to affect the microbiome and condition of habitat-forming kelp. Proceedings of the Royal Society B, 286(1896), 20181887.
R Core Team. (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/
Saunders, M. I., Doropoulos, C., Bayraktarov, E., Babcock, R. C., Gorman, D., Eger, A. M., Vozzo, M. L., Gillies, C. L., Vanderklift, M. A., & Steven, A. D. (2020). Bright spots in coastal marine ecosystem restoration. Current Biology, 30(24), R1500-R1510.
Schiel, D. R., & Foster, M. S. (2015). The biology and ecology of giant kelp forests. University of California Press.
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., & Schmid, B. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9(7), 676-682.
Singh, R. P., & Reddy, C. R. K. (2016). Unraveling the functions of the macroalgal microbiome. Frontiers in Microbiology, 6, 1488.
Smale, D. A., Wernberg, T., Oliver, E. C., Thomsen, M., Harvey, B. P., Straub, S. C., Burrows, M. T., Alexander, L. V., Benthuysen, J. A., & Donat, M. G. (2019). Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Nature Climate Change, 9(4), 306-312.
Steneck, R. S., Graham, M. H., Bourque, B. J., Corbett, D., Erlandson, J. M., Estes, J. A., & Tegner, M. J. (2002). Kelp forest ecosystems: Biodiversity, stability, resilience and future. Environmental Conservation, 29(4), 436-459.
Supratya, V. P., Coleman, L. J., & Martone, P. T. (2020). Elevated temperature affects phenotypic plasticity in the bull kelp (Nereocystis luetkeana, Phaeophyceae). Journal of Phycology, 56(6), 1534-1541.
Teagle, H., Hawkins, S. J., Moore, P. J., & Smale, D. A. (2017). The role of kelp species as biogenic habitat formers in coastal marine ecosystems. Journal of Experimental Marine Biology and Ecology, 492, 81-98.
Turpin, D. H., Elrifi, I. R., Birch, D. G., Weger, H. G., & Holmes, J. J. (1988). Interactions between photosynthesis, respiration, and nitrogen assimilation in microalgae. Canadian Journal of Botany, 66(10), 2083-2097.
Umanzor, S., Sandoval-Gil, J., Sánchez-Barredo, M., Ladah, L. B., Ramírez-García, M. M., & Zertuche-González, J. A. (2021). Short-term stress responses and recovery of giant kelp (Macrocystis pyrifera, Laminariales, Phaeophyceae) juvenile sporophytes to a simulated marine heatwave and nitrate scarcity. Journal of Phycology, 57(5), 1604-1618.
Vadillo Gonzalez, S., Vranken, S., Coleman, M. A., Wernberg, T., Steinberg, P. D., Marzinelli, E. M., & Vozzo, M. L. (2023). Host genotype and microbiome associations in co-occurring clonal and non-clonal kelp, Ecklonia radiata. Molecular Ecology, 32(16), 4584-4598. https://doi.org/10.1111/mec.17056
Van Oppen, M. J. H., Oliver, J. K., Putnam, H. M., & Gates, R. D. (2015). Building coral reef resilience through assisted evolution. Proceedings of the National Academy of Sciences, 112(8), 2307-2313.
Veenhof, R. J., Champion, C., Dworjanyn, S. A., Wernberg, T., Minne, A. J., Layton, C., Bolton, J. J., Reed, D. C., & Coleman, M. A. (2022). Kelp gametophytes in changing oceans. In S. J. Hawkins, A. L. Allcock, A. E. Bates, M. Byrne, A. J. Evans, L. B. Firth, A. J. Lemasson, C. Lucas, E. M Marzinelli, P. J. Mumby, B. D. Russell, J. Sharples, I. P. Smith, S. E. Swearer & P. A. Todd (Eds.), Oceanography and Marine Biology: An Annual Review (pp. 335-371). CRC Press.
Vergés, A., McCosker, E., Mayer-Pinto, M., Coleman, M. A., Wernberg, T., Ainsworth, T., & Steinberg, P. D. (2019). Tropicalisation of temperate reefs: Implications for ecosystem functions and management actions. Functional Ecology, 33(6), 1000-1013.
Visch, W., Layton, C., Hurd, C. L., Macleod, C., & Wright, J. T. (2023). A strategic review and research roadmap for offshore seaweed aquaculture-A case study from southern Australia. Reviews in Aquaculture, 15, 1467-1479.
Vranken, S., Wernberg, T., Scheben, A., Severn-Ellis, A. A., Batley, J., Bayer, P. E., Edwards, D., Wheeler, D., & Coleman, M. A. (2021). Genotype-environment mismatch of kelp forests under climate change. Molecular Ecology, 30(15), 3730-3746.
Wahid, A., Gelani, S., Ashraf, M., & Foolad, M. R. (2007). Heat tolerance in plants: An overview. Environmental and Experimental Botany, 61(3), 199-223.
Wernberg, T., de Bettignies, T., Joy, B. A., & Finnegan, P. M. (2016). Physiological responses of habitat-forming seaweeds to increasing temperatures. Limnology and Oceanography, 61(6), 2180-2190.
Wernberg, T., Russell, B. D., Thomsen, M. S., Gurgel, C. F. D., Bradshaw, C. J., Poloczanska, E. S., & Connell, S. D. (2011). Seaweed communities in retreat from ocean warming. Current Biology, 21(21), 1828-1832.
Woodhead, A. J., Hicks, C. C., Norström, A. V., Williams, G. J., & Graham, N. A. (2019). Coral reef ecosystem services in the Anthropocene. Functional Ecology, 33(6), 1023-1034.
Yan, W., & Hunt, L. A. (1999). An equation for modelling the temperature response of plants using only the cardinal temperatures. Annals of Botany, 84(5), 607-614.

Auteurs

Cody James (C)

Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia.

Cayne Layton (C)

Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia.

Catriona L Hurd (CL)

Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia.

Damon Britton (D)

Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia.

Classifications MeSH