Effects of thermal history on the heat shock response of bull kelp (Nereocystis luetkeana)
-
Shelby J. Hotz
Abstract
In 2013, a marine heatwave called the “Blob” caused northern California bull kelp (Nereocystis luetkeana) populations to decrease significantly. The loss of this foundation species motivated recent investigations on kelp thermal tolerance to understand how warming events might impact their physiological performance. We tested the effect of acclimation temperature on bull kelp by measuring the protein abundance of a molecular chaperone, heat shock protein 70 (Hsp70). Blades were collected from two sites (Big River and Russian Gulch) and acclimated for 7-days at two temperatures (13 and 17 °C) before tissues were subjected to a 1-h heat shock (13, 17, 20, 23, and 26 °C). Results showed a significant difference between acclimation temperature with 20 % greater total Hsp70 protein abundance in bull kelp acclimated to the warm treatment, while site was only marginally different. Heat shock temperature had no effect on total Hsp70 protein abundance. This study is the first to report about the heat shock response of bull kelp and found that thermal history of an organism is an important factor in determining whether an organism can mount a heat shock response. This information can help understand bull kelp’s tolerance to future marine heatwaves.
Acknowledgments
We would like to thank the faculty and staff at UC Davis Bodega Marine Lab (Dr. Brian Gaylord, Albert Carranza, and Phillip Smith) for use of their facility and assistance with this project. We appreciate the endless hours and effort Zachary Spade assisted with in maintaining the bull kelp acclimation tanks. We would also like to acknowledge Dr. Daniel Crocker for his assistance with the statistical analysis, Dr. Joseph Lin for helping to preserve some of the SDS-PAGE gels, and Dr. Lisa Bentley for her assistance in providing comments for this manuscript. Also, we appreciate all the help from former undergraduate students, Maxim Kulinich, Jasmine Richardson, and Francisco Elias, for their assistance on tank husbandry and protein extractions. We also would like to thank Hughes lab members Abbey Dias, Julieta Gómez, Vini Souza, and María Velázquez for their part in collecting sporophyte blades and setup of the acclimation experiment over the course of this study. Preparation of this manuscript was partially supported by Sonoma State University through the Koret Foundation awarded to S.J.H., and the Anthropocene Institute, and California Sea Grant awarded to M.L.Z and B.B.H.
-
Research ethics: Bull kelp collection and cultivation was permitted under the California Department of Fish and Wildlife (permit S-190060001-20113-001).
-
Informed consent: Informed consent was obtained by all individuals/authors for this publication.
-
Author contributions: SJH: conceptualization, methodology, investigation, formal analysis, validation, drafted original writing, edited and reviewed writing, accountability for aspects of work is accurate. RHK: methodology, review and editing of writing. BBH: funding acquisition, conceptualization, methodology, review and editing of writing. MLZ: funding acquisition, conceptualization, methodology, formal analysis, resources, writing- editing and reviewing of writing, accountability for aspects of work is accurate, supervisor, approval for publication. All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
-
Use of Large Language Models, AI and Machine Learning Tools: None declared.
-
Conflict of interest: The authors do not have any competing interests for the publication of this article.
-
Research funding: Preparation of this manuscript was partially supported by Sonoma State University through the Koret Foundation awarded to S.J.H., the Anthropocene Institute and California Sea Grant awarded to M.L.Z and B.B.H.
-
Data availability: Not applicable.
References
Adham, K.G., Wilkinson, M.C., Smith, C.J., and Laidman, D.L. (1991). An enzyme-linked immunosorbent assay for heat-shock protein 70 in plants. Food Agric. Immunol. 3: 29–36, https://doi.org/10.1080/09540109109354727.Suche in Google Scholar
Angilletta, M.J.Jr. (2009). Thermal adaptation: a theoretical and empirical synthesis, online ed. Oxford: Oxford Academic.10.1093/acprof:oso/9780198570875.001.1Suche in Google Scholar
Barua, D., Downs, C.A., and Heckathorn, S.A. (2003). Variation in chloroplast small heat-shock protein function is a major determinant of variation in thermotolerance of photosynthetic electron transport among ecotypes of Chenopodium album. Funct. Plant Biol. 30: 1071–1079, https://doi.org/10.1071/FP03106.Suche in Google Scholar PubMed
Beisner, B.E., Haydon, D.T., and Cuddington, K. (2003). Alternative stable states in ecology. Front. Ecol. Environ. 1: 376–382, https://doi.org/10.1890/1540-9295(2003)001[0376:assie]2.0.co;2.10.1890/1540-9295(2003)001[0376:ASSIE]2.0.CO;2Suche in Google Scholar
Boer, G. and Yu, B. (2003). Climate sensitivity and response. Clim. Dyn. 20: 415–429, https://doi.org/10.1007/s00382-002-0283-3.Suche in Google Scholar
Bond, N.A., Cronin, M.F., Freeland, H., and Mantua, N. (2015). Causes and impacts of the 2014 warm anomaly in the NE Pacific. Geophys. Res. Lett. 42: 3414–3420, https://doi.org/10.1002/2015gl063306.Suche in Google Scholar
Brokordt, K.B., González, R.C., Farías, W.J., and Winkler, F.M. (2015). Potential response to selection of HSP70 as a component of innate immunity in the abalone Haliotis rufescens. PLoS One 10, https://doi.org/10.1371/journal.pone.0141959.Suche in Google Scholar
Brown, C.R., Martin, R.L., Hansen, W.J., Beckmann, R.P., and Welch, W.J. (1993). The constitutive and stress inducible forms of hsp70 exhibit functional similarities and interact with one another in an ATP-dependent fashion. J. Cell Biol. 120: 1101–1112, https://doi.org/10.1083/jcb.120.5.1101.Suche in Google Scholar
Buckley, B.A., Owen, M.E., and Hofmann, G.E. (2001). Adjusting the thermostat: the threshold induction temperature for the heat-shock response in intertidal mussels (genus Mytilus) changes as a function of thermal history. J. Exp. Biol. 204: 3571–3579, https://doi.org/10.1242/jeb.204.20.3571.Suche in Google Scholar
Camarena-Novelo, I., Salazar-Campos, Z., Botello, A.V., Villanueva-Fragoso, S., Jiménez-Morales, I., Fierro, R., and González-Márquez, H. (2019). Potential of the HSP70 protein family as biomarker of Crassostrea virginica under natural conditions (Ostreoida: Ostreidae). Rev. Biol. Trop. 67: 572–584, https://doi.org/10.15517/rbt.v67i3.33048.Suche in Google Scholar
Catton, C., Rogers-Bennett, L., and Amrhein, A. (2016). “Perfect Storm” decimates northern California kelp forests. California Department of Fish and Wildlife, Available at: https://cdfwmarine.wordpress.com/2016/03/30/perfect-storm (Accessed 16 July 2025).Suche in Google Scholar
Clusella-Trullas, S., Boardman, L., Faulkner, K.T., Peck, L.S., and Chown, S.L. (2014). Effects of temperature on heat-shock responses and survival of two species of marine invertebrates from sub-Antarctic Marion Island. Antarct. Sci. 26: 145–152, https://doi.org/10.1017/s0954102013000473.Suche in Google Scholar
Collins, C.L., Burnett, N.P., Ramsey, M.J., Wagner, K., and Zippay, M.L. (2020). Physiological responses to heat stress in an invasive mussel Mytilus galloprovincialis depend on tidal habitat. Mar. Environ. Res. 154, https://doi.org/10.1016/j.marenvres.2019.104849.Suche in Google Scholar PubMed
Contolini, G., Flores-Miller, R., and Ray, J. (2021). Giant kelp and bull kelp, Macrocystis pyrifera and Nereocystis luetkeana, Enhanced status report. California Department of Fish and Wildlife.Suche in Google Scholar
Coppin, R., Rautenbach, C., Ponton, T.J., and Smit, A.J. (2020). Investigating waves and temperature as drivers of kelp morphology. Front. Mar. Sci. 7: 567, https://doi.org/10.3389/fmars.2020.00567.Suche in Google Scholar
Craig, E.A. and Gross, C.A. (1991). Is hsp70 the cellular thermometer? Trends Biochem. Sci. 16: 135–140, https://doi.org/10.1016/0968-0004(91)90055-z.Suche in Google Scholar PubMed
Currie, S., Schulte, P.M., and Evans, D.H. (2014). Thermal stress. In: Evans, D.H., Claiborne, J.B., and Currie, S. (Eds.). The physiology of fishes, 4th ed. CRC Press, Boca Raton, pp. 257–279.Suche in Google Scholar
Di Lorenzo, E. and Mantua, N. (2016). Multi-year persistence of the 2014/15 North Pacific marine heatwave. Nat. Clim. Change 6: 1042–1047, https://doi.org/10.1038/nclimate3082.Suche in Google Scholar
Dobkowski, K.A. and Crofts, S.B. (2021). Scaling and structural properties of juvenile bull kelp (Nereocystis luetkeana). Integr. Org. Biol. 3, https://doi.org/10.1093/iob/obab022.Suche in Google Scholar PubMed PubMed Central
Duncan, R.F. and Hershey, J.W. (1989). Protein synthesis and protein phosphorylation during heat stress, recovery, and adaptation. J. Cell Biol. 109: 1467–1481, https://doi.org/10.1083/jcb.109.4.1467.Suche in Google Scholar PubMed PubMed Central
Ellison, A.M. (2019). Foundation species, non-trophic interactions, and the value of being common. iScience 13: 254–268, https://doi.org/10.1016/j.isci.2019.02.020.Suche in Google Scholar PubMed PubMed Central
Fan, X., Xu, D., Wang, D., Wang, Y., Zhang, X., and Ye, N. (2020). Nutrient uptake and transporter gene expression of ammonium, nitrate, and phosphorus in Ulva linza: adaption to variable concentrations and temperatures. J. Appl. Phycol. 32: 1311–1322, https://doi.org/10.1007/s10811-020-02050-2.Suche in Google Scholar
Fattori, M. (2024). Temperature driven variability in bull kelp (Nereocystis luetkeana) early life stages: a comparative study of California populations, Master’s thesis. Humboldt, California State Polytechnic University.Suche in Google Scholar
Feder, M.E. and Hofmann, G.E. (1999). Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61: 243–282, https://doi.org/10.1146/annurev.physiol.61.1.243.Suche in Google Scholar PubMed
Flato, G.M. and Boer, G.J. (2001). Warming asymmetry in climate change simulations. Geophys. Res. Lett. 28: 195–198, https://doi.org/10.1029/2000gl012121.Suche in Google Scholar
Fujita, R. (2013). 5 ways climate change affecting our oceans. Environmental Defense Fund, Available at: www.edf.org/blog/2013/10/08/5-ways-climate-change-affecting-our-oceans (Accessed 16 July 2025).Suche in Google Scholar
Galland, G., Harrould-Kolieb, E., and Herr, D. (2012). The ocean and climate change policy. Clim. Policy 12: 764–771, https://doi.org/10.1080/14693062.2012.692207.Suche in Google Scholar
Giudice, G., Sconzo, G., and Roccheri, M.C. (1999). Studies on heat shock proteins in sea urchin development. Dev. Growth Differ. 41: 375–380, https://doi.org/10.1046/j.1440-169x.1999.00450.x.Suche in Google Scholar PubMed
Graham, M. and Hamilton, S. (2023). Assessment of practical methods for re-establishment of northern California bull kelp populations at an ecologically relevant scale. California Sea Grant.Suche in Google Scholar
Hammann, M., Wang, G., Boo, S.M., Aguilar-Rosas, L.E., and Weinberger, F. (2016). Selection of heat-shock resistance traits during the invasion of the seaweed Gracilaria vermiculophylla. Mar. Biol. 163: 1–11, https://doi.org/10.1007/s00227-016-2881-3.Suche in Google Scholar
Hara, Y., Otake, Y., Akita, S., Yamazaki, T., Takahashi, F., Yoshikawa, S., and Shimada, S. (2022). Gene expression of a canopy-forming kelp, Eisenia bicyclis (Laminariales, Phaeophyceae), under high temperature stress. Phycol. Res. 70: 203–211, https://doi.org/10.1111/pre.12497.Suche in Google Scholar
Harley, C.D., Randall-Hughes, A., Hultgren, K.M., Miner, B.G., Sorte, C.J., Thornber, C.S., Williams, S.L., and Tomanek, L. (2006). The impacts of climate change in coastal marine systems. Ecol. Lett. 9: 228–241, https://doi.org/10.1111/j.1461-0248.2005.00871.x.Suche in Google Scholar PubMed
Helmuth, B., Harley, C.D., Halpin, P.M., O’Donnell, M., Hofmann, G.E., and Blanchette, C.A. (2002). Climate change and latitudinal patterns of intertidal thermal stress. Science 298: 1015–1017, https://doi.org/10.1126/science.1076814.Suche in Google Scholar PubMed
Henkel, S.K. and Hofmann, G.E. (2008a). Differing patterns of hsp70 gene expression in invasive and native kelp species: evidence for acclimation-induced variation. J. Appl. Phycol. 20: 915–924, https://doi.org/10.1007/s10811-007-9275-3.Suche in Google Scholar
Henkel, S.K. and Hofmann, G.E. (2008b). Thermal ecophysiology of gametophytes cultured from invasive Undaria pinnatifida (Harvey) Suringar in coastal California harbors. J. Exp. Mar. Biol. Ecol. 367: 164–173, https://doi.org/10.1016/j.jembe.2008.09.010.Suche in Google Scholar
Henkel, S. and Hofmann, G. (2009). Interspecific and interhabitat variation in hsp70 gene expression in native and invasive kelp populations. Mar. Ecol.: Prog. Ser. 386: 1–13, https://doi.org/10.3354/meps08047.Suche in Google Scholar
Hereward, H.F., King, N.G., and Smale, D.A. (2020). Intra-annual variability in responses of a canopy forming kelp to cumulative low tide heat stress: implications for populations at the trailing range edge. J. Phycol. 56: 146–158, https://doi.org/10.1111/jpy.12927.Suche in Google Scholar PubMed
Hernández-Carmona, G., Hughes, B., and Graham, M.H. (2006). Reproductive longevity of drifting kelp Macrocystis pyrifera (Phaeophyceae) in Monterey Bay, USA 1. J. Phycol. 42: 1199–1207, https://doi.org/10.1111/j.1529-8817.2006.00290.x.Suche in Google Scholar
Hoegh-Guldberg, O. and Bruno, J.F. (2010). The impact of climate change on the world’s marine ecosystems. Science 328: 1523–1528, https://doi.org/10.1126/science.1189930.Suche in Google Scholar PubMed
Hofmann, G.E. (1999). Ecologically relevant variation in induction and function of heat shock proteins in marine organisms. Am. Zool. 39: 889–900, https://doi.org/10.1093/icb/39.6.889.Suche in Google Scholar
Hofmann, G.E. (2005). Patterns of Hsp gene expression in ectothermic marine organisms on small to large biogeographic scales. Integr. Comp. Biol. 45: 247–255, https://doi.org/10.1093/icb/45.2.247.Suche in Google Scholar PubMed
Hu, C., Yang, J., Qi, Z., Wu, H., Wang, B., Zou, F., Liu, Q., and Liu, J. (2022). Heat shock proteins: biological functions, pathological roles, and therapeutic opportunities. MedComm 3, https://doi.org/10.1002/mco2.161.Suche in Google Scholar PubMed PubMed Central
Ireland, H.E., Harding, S.J., Bonwick, G.A., Jones, M., Smith, C.J., and Williams, J.H. (2004). Evaluation of heat shock protein 70 as a biomarker of environmental stress in Fucus serratus and Lemna minor. Biomarkers 9: 139–155, https://doi.org/10.1080/13547500410001732610.Suche in Google Scholar PubMed
Jueterbock, A., Kollias, S., Smolina, I., Fernandes, J.M., Coyer, J.A., Olsen, J.L., and 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, https://doi.org/10.1016/j.margen.2013.12.008.Suche in Google Scholar PubMed
Karm, R. (2023). Warming resistance of bull kelp (Nereocystis luetkeana) at its southern range limit, Master’s thesis, Sonoma State University.Suche in Google Scholar
Kellermann, V., Chown, S.L., Schou, M.F., Aitkenhead, I., Janion-Scheepers, C., Clemson, A., Sgrò, C.M., and Sgrò, C.M. (2019). Comparing thermal performance curves across traits: how consistent are they? J. Exp. Biol. 222, https://doi.org/10.1242/jeb.193433.Suche in Google Scholar PubMed
Kenyon, K.E. (1999). North Pacific high: a hypothesis. Atmos. Res. 51: 15–34, https://doi.org/10.1016/s0169-8095(98)00110-0.Suche in Google Scholar
King, N.G., McKeown, N.J., Smale, D.A., Wilcockson, D.C., Hoelters, L., Groves, E.A., and Moore, P.J. (2019). Evidence for different thermal ecotypes in range centre and trailing edge kelp populations. J. Exp. Mar. Biol. Ecol. 514: 10–17, https://doi.org/10.1016/j.jembe.2019.03.004.Suche in Google Scholar
Korabik, A.R., Winquist, T., Grosholz, E.D., and Hollarsmith, J.A. (2023). Examining the reproductive success of bull kelp (Nereocystis luetkeana, Phaeophyceae, Laminariales) in climate change conditions. J. Phycol. 59: 989–1004, https://doi.org/10.1111/jpy.13368.Suche in Google Scholar PubMed
Kortsch, S., Primicerio, R., Fossheim, M., Dolgov, A.V., and Aschan, M. (2015). Climate change alters the structure of arctic marine food webs due to poleward shifts of boreal generalists. Proc. R. Soc. B: Biol. Sci. 282, https://doi.org/10.1098/rspb.2015.1546.Suche in Google Scholar PubMed PubMed Central
Krakowiak, J., Zheng, X., Patel, N., Feder, Z.A., Anandhakumar, J., Valerius, K., Gross, D.S., Khalil, A., and Pincus, D. (2018). Hsf1 and Hsp70 constitute a two-component feedback loop that regulates the yeast heat shock response. eLife 7, https://doi.org/10.7554/elife.31668.Suche in Google Scholar PubMed PubMed Central
Krebs, R.A. and Loeschcke, V. (1994). Costs and benefits of activation of the heat-shock response in Drosophila melanogaster. Funct. Ecol. 8: 730–737, https://doi.org/10.2307/2390232.Suche in Google Scholar
Krivoruchko, A. and Storey, K.B. (2010). Forever young: mechanisms of natural anoxia tolerance and potential links to longevity. Oxid. Med. Cell. Longev. 3: 186–198, https://doi.org/10.4161/oxim.3.3.12356.Suche in Google Scholar PubMed PubMed Central
Leising, A.W., Schroeder, I.D., Bograd, S.J., Abell, J., Durazo, R., Gaxiola-Castro, G., Bjorkstedt, E.P., Field, J., Sakuma, K., Roberston, R.R., et al.. (2015). State of the California Current 2014–15: impacts of the warm-water “Blob”. Calif. Coop. Ocean. Fish. Investig. Rep. 56: 31–68.Suche in Google Scholar
Lewis, M., Götting, M., Anttila, K., Kanerva, M., Prokkola, J.M., Seppänen, E., and Nikinmaa, M. (2016). Different relationship between hsp70 mRNA and hsp70 levels in the heat shock response of two salmonids with dissimilar temperature preference. Front. Physiol. 7: 511, https://doi.org/10.3389/fphys.2016.00511.Suche in Google Scholar PubMed PubMed Central
Lindquist, S. (1986). The heat-shock response. Annu. Rev. Biochem. 55: 1151–1191, https://doi.org/10.1146/annurev.biochem.55.1.1151.Suche in Google Scholar
Liu, F., Zhang, P., Liang, Z., Wang, W., Sun, X., and Wang, F. (2019). Dynamic profile of proteome revealed multiple levels of regulation under heat stress in Saccharina japonica. J. Appl. Phycol. 31: 3077–3089, https://doi.org/10.1007/s10811-019-01813-w.Suche in Google Scholar
Luning, K. and Freshwater, W. (1988). Temperature tolerance of northeast pacific marine algae. J. Phycol. 24: 310–515, https://doi.org/10.1111/j.1529-8817.1988.tb00178.x.Suche in Google Scholar
Mahmood, T. and Yang, P.C. (2012). Western blot: technique, theory, and trouble shooting. N. Am. J. Med. Sci. 4: 429–434, https://doi.org/10.4103/1947-2714.100998.Suche in Google Scholar PubMed PubMed Central
Makwana, K., Parmar, H.L., Sikotariya, H., Biswas, S., and Bhadarka, M.A. (2024). Review on climate change impacts on marine ecosystems: from ocean dynamics to biodiversity loss. Agrigate 4: 160–166.Suche in Google Scholar
Maloyan, A., Palmon, A., and Horowitz, M. (1999). Heat acclimation increases the basal HSP72 level and alters its production dynamics during heat stress.Am. J. Physiol. Regul. Integr. Comp. Physiol. 276, https://doi.org/10.1152/ajpregu.1999.276.5.r1506.Suche in Google Scholar PubMed
Mayer, M.P. and Bukau, B. (2005). Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62: 670–684, https://doi.org/10.1007/s00018-004-4464-6.Suche in Google Scholar PubMed PubMed Central
Minich, J.J., Morris, M.M., Brown, M., Doane, M., Edwards, M.S., Michael, T.P., and Dinsdale, E.A. (2018). Elevated temperature drives kelp microbiome dysbiosis, while elevated carbon dioxide induces water microbiome disruption. PLoS One 13, https://doi.org/10.1371/journal.pone.0192772.Suche in Google Scholar PubMed PubMed Central
Muth, A.F., Graham, M.H., Lane, C.E., and Harley, C.D.G. (2019). Recruitment tolerance to increased temperature present across multiple kelp clades. Ecology 100, https://doi.org/10.1002/ecy.2594.Suche in Google Scholar PubMed
Oliver, E.C., Burrows, M.T., Donat, M.G., Sen Gupta, A., Alexander, L.V., Perkins-Kirkpatrick, S.E., Smale, D.A., Hobday, A.J., Holbrook, N.J., Moore, P.J., et al.. (2019). Projected marine heatwaves in the 21st century and the potential for ecological impact. Front. Mar. Sci. 6: 734, https://doi.org/10.3389/fmars.2019.00734.Suche in Google Scholar
Oliver, E.C., Benthuysen, J.A., Darmaraki, S., Donat, M.G., Hobday, A.J., Holbrook, N.J., and Sen Gupta, A. (2021). Marine heatwaves. Ann. Rev. Mar. Sci. 13: 313–342, https://doi.org/10.1146/annurev-marine-032720-095144.Suche in Google Scholar PubMed
Peterson, W.T., Fisher, J.L., Strub, P.T., Du, X., Risien, C., Peterson, J., and Shaw, C.T. (2017). The pelagic ecosystem in the Northern California Current off Oregon during the 2014–2016 warm anomalies within the context of the past 20 years. J. Geophys. Res. Oceans 122: 7267–7290, https://doi.org/10.1002/2017jc012952.Suche in Google Scholar PubMed PubMed Central
Place, S.P., Zippay, M.L., and Hofmann, G.E. (2004). Constitutive roles for inducible genes: evidence for the alteration in expression of the inducible hsp70 gene in Antarctic notothenioid fishes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, https://doi.org/10.1152/ajpregu.00223.2004.Suche in Google Scholar PubMed
Reed, D., Washburn, L., Rassweiler, A., Miller, R., Bell, T., and Harrer, S. (2016). Extreme warming challenges sentinel status of kelp forests as indicators of climate change. Nat. Commun. 7, https://doi.org/10.1038/ncomms13757.Suche in Google Scholar PubMed PubMed Central
Reed, D.C., Schmitt, R.J., Burd, A.B., Burkepile, D.E., Kominoski, J.S., McGlathery, K.J., Zinnert, J.C., and Morris, J.T. (2022). Responses of coastal ecosystems to climate change: insights from long-term ecological research. BioScience 72: 871–888, https://doi.org/10.1093/biosci/biac006.Suche in Google Scholar
Rogers-Bennett, L. and Catton, C.A. (2019). Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens. Sci. Rep. 9, https://doi.org/10.1038/s41598-019-51114-y.Suche in Google Scholar PubMed PubMed Central
Ryan, J.A. and Hightower, L.E. (1999). Heat shock proteins: molecular biomarkers of effects. In: Paga, A. and Wallace, K.N. (Eds.). Molecular biology of the toxic response. Taylor & Francis, Philadelphia, pp. 449–466.Suche in Google Scholar
Schulte, P.M., Healy, T.M., and Fangue, N.A. (2011). Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr. Comp. Biol. 51: 691–702, https://doi.org/10.1093/icb/icr097.Suche in Google Scholar PubMed
Serafini, L., Hann, J.B., Kültz, D., and Tomanek, L. (2011). The proteomic response of sea squirts (genus Ciona) to acute heat stress: a global perspective on the thermal stability of proteins. Comp. Biochem. Physiol., Part D: Genomics Proteomics 6: 322–334, https://doi.org/10.1016/j.cbd.2011.07.002.Suche in Google Scholar PubMed
Shea, R. and Chopin, T. (2007). Effects of Germanium dioxide, an inhibitor of diatom growth, on the microscopic laboratory cultivation stage of the kelp, Laminaria saccharina. J. Appl. Phycol. 19: 27–32, https://doi.org/10.1007/s10811-006-9107-x.Suche in Google Scholar
Smale, D.A. (2020). Impacts of ocean warming on kelp forest ecosystems. New Phytol. 225: 1447–1454, https://doi.org/10.1111/nph.16107.Suche in Google Scholar PubMed
Smale, D.A., Wernberg, T., Oliver, E.C., Thomsen, M., Harvey, B.P., Straub, S.C., Moore, P.J., Alexander, L.V., Benthuysen, J.A., Donat, M.G., et al.. (2019). Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Nat. Clim. Change 9: 306–312, https://doi.org/10.1038/s41558-019-0412-1.Suche in Google Scholar
Smith, K.E., Burrows, M.T., Hobday, A.J., King, N.G., Moore, P.J., Sen Gupta, A., Smale, D.A., and Wernberg, T. (2023). Biological impacts of marine heatwaves. Ann. Rev. Mar. Sci. 15: 119–145, https://doi.org/10.1146/annurev-marine-032122-121437.Suche in Google Scholar PubMed
Smith, J.G., Malone, D., and Carr, M.H. (2024). Consequences of kelp forest ecosystem shifts and predictors of persistence through multiple stressors. Proc. R. Soc. Lond. Ser. B Biol. Sci. 291, https://doi.org/10.1098/rspb.2023.2749.Suche in Google Scholar PubMed PubMed Central
Somero, G.N. (2010). The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J. Exp. Biol. 213: 912–920, https://doi.org/10.1242/jeb.037473.Suche in Google Scholar PubMed
Sorte, C.J. and Hofmann, G.E. (2004). Changes in latitudes, changes in aptitudes: Nucella canaliculata (Mollusca: Gastropoda) is more stressed at its range edge. Mar. Ecol.: Prog. Ser. 274: 263–268, https://doi.org/10.3354/meps274263.Suche in Google Scholar
Springer, Y., Hays, C., Carr, M., Mackey, M., and Bloeser, J. (2007). Ecology and management of the bull kelp, Nereocystis luetkeana: a synthesis with recommendations for future research. Lenfest Ocean Program.Suche in Google Scholar
Starko, S., Epstein, G., Chalifour, L., Bruce, K., Buzzoni, D., Csordas, M., Dimoff, S., Hansen, R., Maucieri, D., McHenry, J., et al.. (2025). Ecological responses to extreme climatic events: a systematic review of the 2014–2016 Northeast Pacific marine heatwave. Oceanogr. Mar. Biol. Annu. Rev. 63, https://doi.org/10.1201/9781003589600-2.Suche in Google Scholar
Supratya, V.P. and Martone, P.T. (2024). Kelps on demand: closed-system protocols for culturing large bull kelp sporophytes for research and restoration. J. Phycol. 60: 73–82, https://doi.org/10.1111/jpy.13413.Suche in Google Scholar PubMed
Supratya, V.P., Coleman, L.J., and Martone, P.T. (2020). Elevated temperature affects phenotypic plasticity in the bull kelp (Nereocystis luetkeana, Phaeophyceae). J. Phycol. 56: 1534–1541, https://doi.org/10.1111/jpy.13049.Suche in Google Scholar PubMed
Tomanek, L. (2010). Variation in the heat shock response and its implication for predicting the effect of global climate change on species’ biogeographical distribution ranges and metabolic costs. J. Exp. Biol. 213: 971–979, https://doi.org/10.1242/jeb.038034.Suche in Google Scholar PubMed
Tomanek, L. and Somero, G.N. (1999). Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography. J. Exp. Biol. 202: 2925–2936, https://doi.org/10.1242/jeb.202.21.2925.Suche in Google Scholar PubMed
Tomanek, L. and Somero, G.N. (2002). Interspecific-and acclimation-induced variation in levels of heat-shock proteins 70 (hsp70) and 90 (hsp90) and heat-shock transcription factor-1 (HSF1) in congeneric marine snails (genus Tegula): implications for regulation of hsp gene expression. J. Exp. Biol. 205: 677–685, https://doi.org/10.1242/jeb.205.5.677.Suche in Google Scholar PubMed
Vadillo Gonzalez, S., Hurd, C.L., Britton, D., Bennett, E., Steinberg, P.D., and Marzinelli, E.M. (2024). Effects of temperature and microbial disruption on juvenile kelp Ecklonia radiata and its associated bacterial community. Front. Mar. Sci. 10, https://doi.org/10.3389/fmars.2023.1332501.Suche in Google Scholar
Vayda, M.E. and Yuan, M.L. (1994). The heat shock response of an Antarctic alga is evident at 5 C. Plant Mol. Biol. 24: 229–233, https://doi.org/10.1007/bf00040590.Suche in Google Scholar PubMed
Veenhof, R.J., Mcgrath, A.H., Champion, C., Dworjanyn, S.A., Marzinelli, E.M., and Coleman, M.A. (2025). The role of microbiota in kelp gametophyte development and resilience to thermal stress. J. Phycol. 61: 633–649, https://doi.org/10.1111/jpy.70018.Suche in Google Scholar PubMed PubMed Central
Verghese, J., Abrams, J., Wang, Y., and Morano, K.A. (2012). Biology of the heat shock response and protein chaperones: budding yeast (Saccharomyces cerevisiae) as a model system. Microbiol. Mol. Biol. Rev. 76: 115–158, https://doi.org/10.1128/mmbr.05018-11.Suche in Google Scholar PubMed PubMed Central
Vierling, E. (1991). The roles of heat shock proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 579–620, https://doi.org/10.1146/annurev.arplant.42.1.579.Suche in Google Scholar
Wheeler, W.N., Smith, R.G., and Srivastava, L.M. (1984). Seasonal photosynthetic performance of Nereocystis luetkeana. Can. J. Bot. 62: 664–670, https://doi.org/10.1139/b84-099.Suche in Google Scholar
Zhang, H., Li, W., Li, J., Fu, W., Yao, J., and Duan, D. (2012). Characterization and expression analysis of hsp70 gene from Ulva prolifera J. Agardh (Chlorophycophyta, Chlorophyceae). Mar. Genomics 5: 53–58, https://doi.org/10.1016/j.margen.2011.10.001.Suche in Google Scholar PubMed
© 2025 Walter de Gruyter GmbH, Berlin/Boston
