Microclimate predicts kelp forest extinction in the face of direct and indirect marine heatwave effects.

Laminariales biogenic habitat canopy-forming kelp climate change historical ecology marine heatwave microclimate regime shifts

Journal

Ecological applications : a publication of the Ecological Society of America
ISSN: 1051-0761
Titre abrégé: Ecol Appl
Pays: United States
ID NLM: 9889808

Informations de publication

Date de publication:
10 2022
Historique:
revised: 22 03 2022
received: 05 01 2022
accepted: 29 03 2022
pubmed: 19 5 2022
medline: 6 10 2022
entrez: 18 5 2022
Statut: ppublish

Résumé

Marine heatwaves threaten the persistence of kelp forests globally. However, the observed responses of kelp forests to these events have been highly variable on local scales. Here, we synthesize distribution data from an environmentally diverse region to examine spatial patterns of canopy kelp persistence through an unprecedented marine heatwave. We show that, although often overlooked, temperature variation occurring at fine spatial scales (i.e., a few kilometers or less) can be a critical driver of kelp forest persistence during these events. Specifically, though kelp forests nearly all persisted toward the cool outer coast, inshore areas were >3°C warmer at the surface and experienced extensive kelp loss. Although temperatures remained cool at depths below the thermocline, kelp persistence in these thermal refugia was strongly constrained by biotic interactions, specifically urchin populations that increased during the heatwave and drove transitions to urchin barrens in deeper rocky habitat. Urchins were, however, largely absent from mixed sand and cobble benthos, leading to an unexpected association between bottom substrate and kelp forest persistence at inshore sites with warm surface waters. Our findings demonstrate both that warm microclimates increase the risk of habitat loss during marine heatwaves and that biotic interactions modified by these events will modulate the capacity of cool microclimates to serve as thermal refugia.

Identifiants

pubmed: 35584048
doi: 10.1002/eap.2673
doi:

Substances chimiques

Sand 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2673

Informations de copyright

© 2022 The Ecological Society of America.

Références

Arafeh-Dalmau, N., G. Montaño-Moctezuma, J. A. Martínez, R. Beas-Luna, D. S. Schoeman, and G. Torres-Moye. 2019. “Extreme Marine Heatwaves Alter Kelp Forest Community near its Equatorward Distribution Limit.” Frontiers in Marine Science 6: 499. https://doi.org/10.3389/fmars.2019.00499.
Arias-Ortiz, A., O. Serrano, P. Masqué, P. S. Lavery, U. Mueller, G. A. Kendrick, M. Rozaimi, et al. 2018. “A Marine Heatwave Drives Massive Losses from the World's Largest Seagrass Carbon Stocks.” Nature Climate Change 8(4): 338-44. https://doi.org/10.1038/s41558-018-0096-y.
Babcock, R. C., R. H. Bustamante, E. A. Fulton, D. J. Fulton, M. D. E. Haywood, A. J. Hobday, R. Kenyon, et al. 2019. “Severe Continental-Scale Impacts of Climate Change Are Happening Now: Extreme Climate Events Impact Marine Habitat Forming Communities along 45% of Australia's Coast.” Frontiers in Marine Science 6: 411. https://doi.org/10.3389/fmars.2019.00411.
Bates, B. H., M. T. Burrows, M. I. Duncan, J. Garrabou, T. Guy-Haim, F. Lima, A. M. Queiros, R. Seabra, and R. Marsh. 2018. “Biologists Ignore Ocean Weather at their Peril.” Nature 560: 299-301.
Bates, D., M. Maechler, B. Bolker, S. Walker, R. H. B. Christensen, H. Singmann, B. Dai, G. Grothendieck, P. Green, and M. B. Bolker. 2015. “Package ‘Lme4’.” Convergence 12(1): 2.
Beas-Luna, R., C. Fiorenza Micheli, B. Woodson, M. Carr, D. Malone, J. Torre, C. Boch, et al. 2020. “Geographic Variation in Responses of Kelp Forest Communities of the California Current to Recent Climatic Changes.” Global Change Biology 26(11): 6457-73. https://doi.org/10.1111/gcb.15273.
Bennett, S., T. Wernberg, S. D. Connell, A. J. Hobday, C. R. Johnson, and E. S. Poloczanska. 2016. “The ‘Great Southern Reef’: Social, Ecological and Economic Value of Australia's Neglected Kelp Forests.” Marine and Freshwater Research 67(1): 47-56. https://doi.org/10.1071/MF15232.
Berry, H. D., T. F. Mumford, B. Christiaen, P. Dowty, M. Calloway, L. Ferrier, E. E. Grossman, and N. R. VanArendonk. 2021. “Long-Term Changes in Kelp Forests in an Inner Basin of the Salish Sea.” PLoS One 16(2): e0229703. https://doi.org/10.1371/journal.pone.0229703.
Bolton, J. J. 2010. “The Biogeography of Kelps (Laminariales, Phaeophyceae): A Global Analysis with New Insights from Recent Advances in Molecular Phylogenetics.” Helgoland Marine Research 64(4): 263-79. https://doi.org/10.1007/s10152-010-0211-6.
Bond, N. A., M. F. Cronin, H. Freeland, and N. Mantua. 2015. “Causes and Impacts of the 2014 Warm Anomaly in the NE Pacific.” Geophysical Research Letters 42(9): 3414-20.
Brook, B. W., N. S. Sodhi, and C. J. A. Bradshaw. 2008. “Synergies among Extinction Drivers under Global Change.” Trends in Ecology & Evolution 23(8): 453-60. https://doi.org/10.1016/j.tree.2008.03.011.
Brooks, M. E., K. Kristensen, K. J. Van Benthem, A. Magnusson, C. W. Berg, A. Nielsen, H. J. Skaug, M. Machler, and B. M. Bolker. 2017. “GlmmTMB Balances Speed and Flexibility among Packages for Zero-Inflated Generalized Linear Mixed Modeling.” The R Journal 9(2): 378-400.
Burt, J. M., M. Tim Tinker, D. K. Okamoto, K. W. Demes, K. Holmes, and A. K. Salomon. 2018. “Sudden Collapse of a Mesopredator Reveals its Complementary Role in Mediating Rocky Reef Regime Shifts.” Proceedings of the Royal Society B 285(1883): 20180553. https://doi.org/10.1098/rspb.2018.0553.
Cavanaugh, K. C., D. C. Reed, T. W. Bell, M. C. N. Castorani, and R. Beas-Luna. 2019. “Spatial Variability in the Resistance and Resilience of Giant Kelp in Southern and Baja California to a Multiyear Heatwave.” Frontiers in Marine Science 6: 413. https://doi.org/10.3389/fmars.2019.00413.
Cavole, L. M., A. M. Demko, R. E. Diner, A. Giddings, I. Koester, C. M. L. S. Pagniello, M.-L. Paulsen, A. Ramirez-Valdez, S. M. Schwenck, and N. K. Yen. 2016. “Biological Impacts of the 2013-2015 Warm-Water Anomaly in the Northeast Pacific: Winners, Losers, and the Future.” Oceanography 29(2): 273-85.
Chen, Z., J. Shi, Q. Liu, H. Chen, and C. Li. 2021. “A Persistent and Intense Marine Heatwave in the Northeast Pacific during 2019-2020.” Geophysical Research Letters 48(13): e2021GL093239. https://doi.org/10.1029/2021GL093239.
Claar, D. C., S. Starko, K. L. Tietjen, H. E. Epstein, R. Cunning, K. M. Cobb, A. C. Baker, R. D. Gates, and J. K. Baum. 2020. “Dynamic Symbioses Reveal Pathways to Coral Survival through Prolonged Heatwaves.” Nature Communications 11(1): 6097. https://doi.org/10.1038/s41467-020-19169-y.
Coleman, M. A., and H. D. Goold. 2019. “Harnessing Synthetic Biology for Kelp Forest Conservation1.” Journal of Phycology 55(4): 745-51. https://doi.org/10.1111/jpy.12888.
Coleman, M. A., and T. Wernberg. 2020. “The Silver Lining of Extreme Events.” Trends in Ecology & Evolution 35: 1065-7. https://doi.org/10.1016/j.tree.2020.08.013.
Coleman, M. A., G. Wood, K. Filbee-Dexter, A. J. P. Minne, H. D. Goold, A. Vergés, E. M. Marzinelli, P. D. Steinberg, and T. Wernberg. 2020. “Restore or Redefine: Future Trajectories for Restoration.” Frontiers in Marine Science 7: 237. https://doi.org/10.3389/fmars.2020.00237.
Druehl, L. D. 1978. “The Distribution of Macrocystis integrifolia in British Columbia as Related to Environmental Parameters.” Canadian Journal of Botany 56(1): 69-79.
Druehl, L. D., R. Baird, A. Lindwall, K. E. Lloyd, and S. Pakula. 1988. “Longline Cultivation of some Laminariaceae in British Columbia, Canada.” Aquaculture Research 19(3): 253-63.
Duggins, D. O., C. A. Simenstad, and J. A. Estes. 1989. “Magnification of Secondary Production by Kelp Detritus in Coastal Marine Ecosystems.” Science 245(4914): 170-3. https://doi.org/10.1126/science.245.4914.170.
Edwards, M. S. 2004. “Estimating Scale-Dependency in Disturbance Impacts: El Niños and Giant Kelp Forests in the Northeast Pacific.” Oecologia 138(3): 436-47. https://doi.org/10.1007/s00442-003-1452-8.
Fernández, P. A., J. D. Gaitán-Espitia, P. P. Leal, M. Schmid, A. T. Revill, and C. L. Hurd. 2020. “Nitrogen Sufficiency Enhances Thermal Tolerance in Habitat-Forming Kelp: Implications for Acclimation under Thermal Stress.” Scientific Reports 10(1): 3186. https://doi.org/10.1038/s41598-020-60104-4.
Ferrario, F., T. Suskiewicz, and L. E. Johnson. 2021. “A Seascape Approach for Guiding Effective Habitat Enhancement: Spatially Explicit Modeling of Kelp-Grazer Interactions.” Elementa: Science of the Anthropocene 9(1): 00013. https://doi.org/10.1525/elementa.2021.00013.
Filbee-Dexter, K., C. J. Feehan, and R. E. Scheibling. 2016. “Large-Scale Degradation of a Kelp Ecosystem in an Ocean Warming Hotspot.” Marine Ecology Progress Series 543: 141-52.
Filbee-Dexter, K., C. Feehan, D. Smale, K. Krumhansl, S. Augustine, F. de Bettignies, M. T. Burrows, J. Byrnes, J. Campbell, and D. Davoult. 2020. “Ocean Temperature Controls Kelp Decomposition and Carbon Sink Potential.” Research Square. https://doi.org/10.21203/rs.3.rs-38503/v1.
Filbee-Dexter, K., and T. Wernberg. 2018. “Rise of Turfs: A New Battlefront for Globally Declining Kelp Forests.” BioScience 68(2): 64-76. https://doi.org/10.1093/biosci/bix147.
Filbee-Dexter, K., and T. Wernberg. 2020. “Substantial Blue Carbon in Overlooked Australian Kelp Forests.” Scientific Reports 10(1): 1-6.
Filbee-Dexter, K., T. Wernberg, S. Fredriksen, K. M. Norderhaug, and M. F. Pedersen. 2019. “Arctic Kelp Forests: Diversity, Resilience and Future.” Global and Planetary Change 172(January): 1-14. https://doi.org/10.1016/j.gloplacha.2018.09.005.
Filbee-Dexter, K., T. Wernberg, S. P. Grace, J. Thormar, S. Fredriksen, C. N. Narvaez, C. J. Feehan, and K. M. Norderhaug. 2020. “Marine Heatwaves and the Collapse of Marginal North Atlantic Kelp Forests.” Scientific Reports 10(1): 13388. https://doi.org/10.1038/s41598-020-70273-x.
Finger, D. J. I., M. L. McPherson, H. F. Houskeeper, and R. M. Kudela. 2021. “Mapping Bull Kelp Canopy in Northern California Using Landsat to Enable Long-Term Monitoring.” Remote Sensing of Environment 254(March): 112243. https://doi.org/10.1016/j.rse.2020.112243.
Fredriksen, S., K. Filbee-Dexter, K. M. Norderhaug, H. Steen, T. Bodvin, M. A. Coleman, F. Moy, and T. Wernberg. 2020. “Green Gravel: A Novel Restoration Tool to Combat Kelp Forest Decline.” Scientific Reports 10(1): 3983. https://doi.org/10.1038/s41598-020-60553-x.
Gerard, V. A. 1997. “The Role of Nitrogen Nutrition in High-Temperature Tolerance of the Kelp, Laminaria Saccharina (Chromophyta)1.” Journal of Phycology 33(5): 800-10. https://doi.org/10.1111/j.0022-3646.1997.00800.x.
Gerard, V. A., and H. Kirkman. 1984. “Ecological Observations on a Branched, Loose-Lying Form of Macrocystis pyrifera (L.) C. Agardh in New Zealand.” Botanica Marina 27(3): 105-10. https://doi.org/10.1515/botm.1984.27.3.105.
Giraldo-Ospina, A., G. A. Kendrick, and R. K. Hovey. 2020. “Depth Moderates Loss of Marine Foundation Species after an Extreme Marine Heatwave: Could Deep Temperate Reefs Act as a Refuge?” Proceedings of the Royal Society B: Biological Sciences 287(1928): 20200709. https://doi.org/10.1098/rspb.2020.0709.
Graham, M. H. 2004. “Effects of Local Deforestation on the Diversity and Structure of Southern California Giant Kelp Forest Food Webs.” Ecosystems 7(4): 341-57.
Graham, M. H., B. P. Kinlan, L. D. Druehl, L. E. Garske, and S. Banks. 2007. “Deep-Water Kelp Refugia as Potential Hotspots of Tropical Marine Diversity and Productivity.” Proceedings of the National Academy of Sciences 104(42): 16576-80.
Gregr, E. J., V. Christensen, L. Nichol, R. G. Martone, R. W. Markel, J. C. Watson, C. D. G. Harley, E. A. Pakhomov, J. B. Shurin, and K. M. A. Chan. 2020. “Cascading Social-Ecological Costs and Benefits Triggered by a Recovering Keystone Predator.” Science 368(6496): 1243-7. https://doi.org/10.1126/science.aay5342.
Hamilton, S. L., T. Bell, J. Watson, K. Grorud-Colvert, and B. Menge. 2019. “Remote Sensing: Generation of Long-Term Kelp Bed Data Sets for Evaluation of Impacts of Climatic Variation.” Ecology 107: e03031. https://doi.org/10.1002/ecy.3031.
Hamilton, S. L., V. R. Saccomanno, W. N. Heady, A. L. Gehman, S. I. Lonhart, R. Beas-Luna, F. T. Francis, et al. 2021. “Disease-Driven Mass Mortality Event Leads to Widespread Extirpation and Variable Recovery Potential of a Marine Predator across the Eastern Pacific.” Proceedings of the Royal Society B: Biological Sciences 288(1957): 20211195. https://doi.org/10.1098/rspb.2021.1195.
Harley, C. D. G. 2003. “Abiotic Stress and Herbivory Interact to Set Range Limits across a Two-Dimensional Stress Gradient.” Ecology 84(6): 1477-88.
Harley, C. D. G. 2011. “Climate Change, Keystone Predation, and Biodiversity Loss.” Science 334(6059): 1124-7. https://doi.org/10.1126/science.1210199.
Harvell, C. D., D. Montecino-Latorre, J. M. Caldwell, J. M. Burt, K. Bosley, A. Keller, S. F. Heron, et al. 2019. “Disease Epidemic and a Marine Heat Wave Are Associated with the Continental-Scale Collapse of a Pivotal Predator (Pycnopodia helianthoides).” Science Advances 5(1): eaau7042. https://doi.org/10.1126/sciadv.aau7042.
Helmuth, B., C. D. G. Harley, P. M. Halpin, M. O'Donnell, G. E. Hofmann, and C. A. Blanchette. 2002. “Climate Change and Latitudinal Patterns of Intertidal Thermal Stress.” Science 298(5595): 1015-7. https://doi.org/10.1126/science.1076814.
Helmuth, B., B. D. Russell, S. D. Connell, Y. Dong, C. D. G. Harley, F. P. Lima, G. Sará, G. A. Williams, and N. Mieszkowska. 2014. “Beyond Long-Term Averages: Making Biological Sense of a Rapidly Changing World.” Climate Change Responses 1: 6. https://doi.org/10.1186/s40665-014-0006-0.
Hobday, A. J., L. V. Alexander, S. E. Perkins, D. A. Smale, S. C. Straub, E. C. J. Oliver, J. A. Benthuysen, M. T. Burrows, M. G. Donat, and M. Feng. 2016. “A Hierarchical Approach to Defining Marine Heatwaves.” Progress in Oceanography 141: 227-38.
Hollarsmith, J. A., K. Andrews, N. Naar, S. Starko, M. Calloway, A. Obaza, E. Buckner, D. Tonnes, J. Selleck, and T. W. Therriault. 2022. “Toward a Conceptual Framework for Managing and Conserving Marine Habitats: A Case Study of Kelp Forests in the Salish Sea.” Ecology and Evolution 12(1): e8510. https://doi.org/10.1002/ece3.8510.
Hughes, T. P., K. D. Anderson, S. R. Connolly, S. F. Heron, J. T. Kerry, J. M. Lough, A. H. Baird, et al. 2018. “Spatial and Temporal Patterns of Mass Bleaching of Corals in the Anthropocene.” Science 359(6371): 80-3. https://doi.org/10.1126/science.aan8048.
Hurd, C. L., K. M. Durante, F. S. Chia, and P. J. Harrison. 1994. “Effect of Bryozoan Colonization on Inorganic Nitrogen Acquisition by the Kelps Agarum Fimbriatum and Macrocystis Integrifolia.” Marine Biology 121(1): 167-73.
Hurd, C. L., K. M. Durante, and P. J. Harrison. 2000. “Influence of Bryozoan Colonization on the Physiology of the Kelp Macrocystis integrifolia (Laminariales, Phaeophyta) from Nitrogen-Rich and -Poor Sites in Barkley Sound, British Columbia, Canada.” Phycologia 39(5): 435-40. https://doi.org/10.2216/i0031-8884-39-5-435.1.
Iwabuchi, B. L., and L. A. Gosselin. 2019. “Long-Term Trends and Regional Variability in Extreme Temperature and Salinity Conditions Experienced by Coastal Marine Organisms on Vancouver Island, Canada.” Bulletin of Marine Science 95(3): 337-54.
Jayathilake, D., and M. J. Costello. 2021. “Version 2 of the World Map of Laminarian Kelp Benefits from more Arctic Data and Makes it the Largest Marine Biome.” Biological Conservation 257: 109099.
Johnson, C. R., S. C. Banks, N. S. Barrett, F. Cazassus, P. K. Dunstan, G. J. Edgar, S. D. Frusher, et al. 2011. “Climate Change Cascades: Shifts in Oceanography, Species' Ranges and Subtidal Marine Community Dynamics in Eastern Tasmania.” Journal of Experimental Marine Biology and Ecology 400(1): 17-32. https://doi.org/10.1016/j.jembe.2011.02.032.
Kohl, W. T., T. I. McClure, and B. G. Miner. 2016. “Decreased Temperature Facilitates Short-Term Sea Star Wasting Disease Survival in the Keystone Intertidal Sea Star Pisaster ochraceus.” PLoS One 11(4): e0153670. https://doi.org/10.1371/journal.pone.0153670.
Krumhansl, K. A., D. K. Okamoto, A. Rassweiler, M. Novak, J. J. Bolton, K. C. Cavanaugh, S. D. Connell, et al. 2016. “Global Patterns of Kelp Forest Change over the Past Half-Century.” Proceedings of the National Academy of Sciences 113(48): 13785-90. https://doi.org/10.1073/pnas.1606102113.
Ladah, L. B., J. A. Zertuche-González, and G. Hernández-Carmona. 1999. “Giant Kelp (Macrocystis pyrifera, Phaeophyceae) Recruitment near its Southern Limit in Baja California after Mass Disappearance during Enso 1997-1998.” Journal of Phycology 35(6): 1106-12. https://doi.org/10.1046/j.1529-8817.1999.3561106.x.
Laur, D. R., A. W. Ebeling, and D. C. Reed. 1986. “Experimental Evaluations of Substrate Types as Barriers to Sea Urchin (Strongylocentrotus spp.) Movement.” Marine Biology 93(2): 209-15. https://doi.org/10.1007/BF00508258.
Levine, A. F. Z., and M. J. McPhaden. 2016. “How the July 2014 Easterly Wind Burst Gave the 2015-2016 El Niño a Head Start.” Geophysical Research Letters 43(12): 6503-10. https://doi.org/10.1002/2016GL069204.
Ling, S. D. 2008. “Range Expansion of a Habitat-Modifying Species Leads to Loss of Taxonomic Diversity: A New and Impoverished Reef State.” Oecologia 156(4): 883-94.
Ling, S. D., R. E. Scheibling, A. Rassweiler, C. R. Johnson, N. Shears, S. D. Connell, A. K. Salomon, et al. 2015. “Global Regime Shift Dynamics of Catastrophic Sea Urchin Overgrazing.” Philosophical Transactions of the Royal Society B 370(1659): 20130269. https://doi.org/10.1098/rstb.2013.0269.
Lobban, C. S. 1978. “The Growth and Death of the Macrocystis Sporophyte (Phaeophyceae, Laminariales).” Phycologia 17(2): 196-212.
Markel, R. W., and J. B. Shurin. 2015. “Indirect Effects of Sea Otters on Rockfish (Sebastes spp.) in Giant Kelp Forests.” Ecology 96(11): 2877-90. https://doi.org/10.1890/14-0492.1.
McPherson, M. L., D. J. I. Finger, H. F. Houskeeper, T. W. Bell, M. H. Carr, L. Rogers-Bennett, and R. M. Kudela. 2021. “Large-Scale Shift in the Structure of a Kelp Forest Ecosystem Co-Occurs with an Epizootic and Marine Heatwave.” Communications Biology 4(1): 1-9. https://doi.org/10.1038/s42003-021-01827-6.
Montecino-Latorre, D., M. E. Eisenlord, M. Turner, C. Reyn Yoshioka, D. Harvell, C. V. Pattengill-Semmens, J. D. Nichols, and J. K. Gaydos. 2016. “Devastating Transboundary Impacts of Sea Star Wasting Disease on Subtidal Asteroids.” PLoS One 11(10): e0163190. https://doi.org/10.1371/journal.pone.0163190.
Mora-Soto, A., M. Palacios, E. C. Macaya, I. Gómez, P. Huovinen, A. Pérez-Matus, M. Young, et al. 2020. “A High-Resolution Global Map of Giant Kelp (Macrocystis pyrifera) Forests and Intertidal Green Algae (Ulvophyceae) with Sentinel-2 Imagery.” Remote Sensing 12(4): 694. https://doi.org/10.3390/rs12040694.
Oliver, E. C. J., M. T. Burrows, M. G. Donat, A. S. Gupta, L. V. Alexander, S. E. Perkins-Kirkpatrick, J. A. Benthuysen, et al. 2019. “Projected Marine Heatwaves in the 21st Century and the Potential for Ecological Impact.” Frontiers in Marine Science 6: 734. https://doi.org/10.3389/fmars.2019.00734.
Oliver, E. C. J., M. G. Donat, M. T. Burrows, P. J. Moore, D. A. Smale, L. V. Alexander, J. A. Benthuysen, et al. 2018. “Longer and more Frequent Marine Heatwaves over the Past Century.” Nature Communications 9(1): 1324. https://doi.org/10.1038/s41467-018-03732-9.
Palumbi, S. R., D. J. Barshis, N. Traylor-Knowles, and R. A. Bay. 2014. “Mechanisms of Reef Coral Resistance to Future Climate Change.” Science 344(6186): 895-8. https://doi.org/10.1126/science.1251336.
Peña, M. A., N. Nemcek, and M. Robert. 2019. “Phytoplankton Responses to the 2014-2016 Warming Anomaly in the Northeast Subarctic Pacific Ocean.” Limnology and Oceanography 64(2): 515-25. https://doi.org/10.1002/lno.11056.
Pfister, C. A., H. D. Berry, and T. Mumford. 2018. “The Dynamics of Kelp Forests in the Northeast Pacific Ocean and the Relationship with Environmental Drivers.” Journal of Ecology 106(4): 1520-33. https://doi.org/10.1111/1365-2745.12908.
Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar, S. Heisterkamp, B. Van Willigen, and R. Maintainer. 2017. “Package ‘Nlme’.” Linear and Nonlinear Mixed Effects Models, Version 3.
Pörtner, H.-O., D. C. Roberts, V. Masson-Delmotte, P. Zhai, M. Tignor, E. Poloczanska, M. Katja Mintenbeck, A. O. Nicolai, and J. Petzold. 2019. IPCC Special Report on the Ocean and Cryosphere in a Changing Climate. Geneva: IPCC Intergovernmental Panel on Climate Change.
Reed, D., L. Washburn, A. Rassweiler, R. Miller, T. Bell, and S. Harrer. 2016. “Extreme Warming Challenges Sentinel Status of Kelp Forests as Indicators of Climate Change.” Nature Communications 7(1): 1-7. https://doi.org/10.1038/ncomms13757.
Rogers-Bennett, L., and C. A. Catton. 2019. “Marine Heat Wave and Multiple Stressors Tip Bull Kelp Forest to Sea Urchin Barrens.” Scientific Reports 9(1): 1-9. https://doi.org/10.1038/s41598-019-51114-y.
Rosa, R., and B. A. Seibel. 2008. “Synergistic Effects of Climate-Related Variables Suggest Future Physiological Impairment in a Top Oceanic Predator.” Proceedings of the National Academy of Sciences 105(52): 20776-80. https://doi.org/10.1073/pnas.0806886105.
Schroeder, S. B., L. Boyer, F. Juanes, and M. Costa. 2020. “Spatial and Temporal Persistence of Nearshore Kelp Beds on the West Coast of British Columbia, Canada Using Satellite Remote Sensing.” Remote Sensing in Ecology and Conservation 6(3): 327-43. https://doi.org/10.1002/rse2.142.
Schultz, J. A., R. N. Cloutier, and I. M. Côté. 2016. “Evidence for a Trophic Cascade on Rocky Reefs Following Sea Star Mass Mortality in British Columbia.” PeerJ 4(April): e1980. https://doi.org/10.7717/peerj.1980.
Sharp, G. J. 1974. “The Impact of Tegula pulligo, Gmelin on Tissue Loss from Macrocystis integrifolia, Bory in Barkley Sound, Vancouver Island, British Columbia.” M.Sc. thesis, Simon Fraser University.
Simonson, E. J., R. E. Scheibling, and A. Metaxas. 2015. “Kelp in Hot Water: I. Warming Seawater Temperature Induces Weakening and Loss of Kelp Tissue.” Marine Ecology Progress Series 537: 89-104.
Smale, D. A. 2020. “Impacts of Ocean Warming on Kelp Forest Ecosystems.” New Phytologist 225(4): 1447-54. https://doi.org/10.1111/nph.16107.
Smale, D. A., T. Wernberg, E. C. J. Oliver, M. Thomsen, B. P. Harvey, S. C. Straub, M. T. Burrows, et al. 2019. “Marine Heatwaves Threaten Global Biodiversity and the Provision of Ecosystem Services.” Nature Climate Change 9(4): 306-12. https://doi.org/10.1038/s41558-019-0412-1.
Smith, J. M., M. A. Brzezinski, J. M. Melack, R. J. Miller, and D. C. Reed. 2018. “Urea as a Source of Nitrogen to Giant Kelp (Macrocystis pyrifera).” Limnology and Oceanography Letters 3(4): 365-73. https://doi.org/10.1002/lol2.10088.
Smith, J. G., J. Tomoleoni, M. Staedler, S. Lyon, J. Fujii, and M. Tim Tinker. 2021. “Behavioral Responses across a Mosaic of Ecosystem States Restructure a Sea Otter-Urchin Trophic Cascade.” Proceedings of the National Academy of Sciences 118(11): e2012493118. https://doi.org/10.1073/pnas.2012493118.
Smith, R. G., W. N. Wheeler, and L. M. Srivastava. 1983. “Seasonal Photosynthetic Performance of Macrocystis Integrifolia (Phaeophyceae)1.” Journal of Phycology 19(3): 352-9. https://doi.org/10.1111/j.0022-3646.1983.00352.x.
Starko, S., L. A. Bailey, E. Creviston, K. A. James, A. Warren, M. K. Brophy, A. Danasel, M. P. Fass, J. A. Townsend, and C. J. Neufeld. 2019. “Environmental Heterogeneity Mediates Scale-Dependent Declines in Kelp Diversity on Intertidal Rocky Shores.” PLoS One 14(3): e0213191. https://doi.org/10.1371/journal.pone.0213191.
Starko, S., and chrisjneufeld. 2022. "sstarko/BarkleySound_CanopyKelp: v1.1 (v1.1)." Zenodo. https://doi.org/10.5281/zenodo.6397743.
Steneck, R. S., M. H. Graham, B. J. Bourque, D. Corbett, J. M. Erlandson, J. A. Estes, and M. J. Tegner. 2002. “Kelp Forest Ecosystems: Biodiversity, Stability, Resilience and Future.” Environmental Conservation 29(4): 436-59. https://doi.org/10.1017/S0376892902000322.
Stephens, T. A., and C. D. Hepburn. 2016. “A Kelp with Integrity: Macrocystis pyrifera Prioritises Tissue Maintenance in Response to Nitrogen Fertilisation.” Oecologia 182(1): 71-84. https://doi.org/10.1007/s00442-016-3641-2.
Straub, S. C., T. Wernberg, M. S. Thomsen, P. J. Moore, M. T. Burrows, B. P. Harvey, and D. A. Smale. 2019. “Resistance, Extinction, and Everything in between - The Diverse Responses of Seaweeds to Marine Heatwaves.” Frontiers in Marine Science 6: 763. https://doi.org/10.3389/fmars.2019.00763.
Supratya, V. P., L. J. M. Coleman, and P. T. Martone. 2020. “Elevated Temperature Affects Phenotypic Plasticity in the Bull Kelp (Nereocystis luetkeana, Phaeophyceae).” Journal of Phycology 56(6): 1534-41. https://doi.org/10.1111/jpy.13049.
Teagle, H., S. J. Hawkins, P. J. Moore, and D. A. Smale. 2017. “The Role of Kelp Species as Biogenic Habitat Formers in Coastal Marine Ecosystems.” Journal of Experimental Marine Biology and Ecology 492(July): 81-98. https://doi.org/10.1016/j.jembe.2017.01.017.
Verdura, J., J. Santamaría, E. Ballesteros, D. A. Smale, M. E. Cefalì, R. Golo, S. de Caralt, A. Vergés, and E. Cebrian. 2021. “Local-Scale Climatic Refugia Offer Sanctuary for a Habitat-Forming Species during a Marine Heatwave.” Journal of Ecology 109(4): 1758-73. https://doi.org/10.1111/1365-2745.13599.
Vergés, A., C. Doropoulos, H. A. Malcolm, M. Skye, M. Garcia-Pizá, E. M. Marzinelli, A. H. Campbell, et al. 2016. “Long-Term Empirical Evidence of Ocean Warming Leading to Tropicalization of Fish Communities, Increased Herbivory, and Loss of Kelp.” Proceedings of the National Academy of Sciences 113(48): 13791-6. https://doi.org/10.1073/pnas.1610725113.
Vergés, A., E. McCosker, M. Mayer-Pinto, M. A. Coleman, T. Wernberg, T. Ainsworth, and P. D. Steinberg. 2019. “Tropicalisation of Temperate Reefs: Implications for Ecosystem Functions and Management Actions.” Functional Ecology 33(6): 1000-13. https://doi.org/10.1111/1365-2435.13310.
Vergés, A., P. D. Steinberg, M. E. Hay, A. G. B. Poore, A. H. Campbell, E. Ballesteros, K. L. Heck, et al. 2014. “The Tropicalization of Temperate Marine Ecosystems: Climate-Mediated Changes in Herbivory and Community Phase Shifts.” Proceedings of the Royal Society B: Biological Sciences 281(1789): 20140846. https://doi.org/10.1098/rspb.2014.0846.
von Biela, V. R., M. L. Arimitsu, J. F. Piatt, B. Heflin, S. K. Schoen, J. L. Trowbridge, and C. M. Clawson. 2019. “Extreme Reduction in Nutritional Value of a Key Forage Fish during the Pacific Marine Heatwave of 2014-2016.” Marine Ecology Progress Series 613(March): 171-82. https://doi.org/10.3354/meps12891.
Watson, J., and J. A. Estes. 2011. “Stability, Resilience, and Phase Shifts in Rocky Subtidal Communities along the West Coast of Vancouver Island, Canada.” Ecological Monographs 81(2): 215-39. https://doi.org/10.1890/10-0262.1.
Watson, J. C., M. W. Hawkes, L. C. Lee, and A. Lamb. 2021. “The Dynamics and Geographic Disjunction of the Kelp Eisenia arborea along the West Coast of Canada.” Botanica Marina 64: 395-406. https://doi.org/10.1515/bot-2021-0040.
Wernberg, T., S. Bennett, R. C. Babcock, T. de Bettignies, K. Cure, M. Depczynski, F. Dufois, et al. 2016. “Climate-Driven Regime Shift of a Temperate Marine Ecosystem.” Science 353(6295): 169-72. https://doi.org/10.1126/science.aad8745.
Wernberg, T., M. A. Coleman, S. Bennett, M. S. Thomsen, F. Tuya, and B. P. Kelaher. 2018. “Genetic Diversity and Kelp Forest Vulnerability to Climatic Stress.” Scientific Reports 8(1): 1-8. https://doi.org/10.1038/s41598-018-20009-9.
Wernberg, T., K. Krumhansl, K. Filbee-Dexter, and M. F. Pedersen. 2019. “Chapter 3 - Status and Trends for the World's Kelp Forests.” In World Seas: An Environmental Evaluation, Second ed., edited by C. Sheppard, 57-78. Cambridge, MA: Academic Press. https://doi.org/10.1016/B978-0-12-805052-1.00003-6.
Wickham, H. 2011. “Ggplot2.” Wiley Interdisciplinary Reviews: Computational Statistics 3(2): 180-5.
Wickham, H., M. Averick, J. Bryan, W. Chang, L. McGowan, R. François, G. Grolemund, A. Hayes, L. Henry, and J. Hester. 2019. “Welcome to the Tidyverse.” Journal of Open Source Software 4(43): 1686.
Wilmers, C. C., J. A. Estes, M. Edwards, K. L. Laidre, and B. Konar. 2012. “Do Trophic Cascades Affect the Storage and Flux of Atmospheric Carbon? An Analysis of Sea Otters and Kelp Forests.” Frontiers in Ecology and the Environment 10(8): 409-15. https://doi.org/10.1890/110176.
Woodson, C. B., F. Micheli, C. Boch, M. Al-Najjar, A. Espinoza, A. Hernandez, L. Vázquez-Vera, A. Saenz-Arroyo, S. G. Monismith, and J. Torre. 2019. “Harnessing Marine Microclimates for Climate Change Adaptation and Marine Conservation.” Conservation Letters 12(2): e12609. https://doi.org/10.1111/conl.12609.

Auteurs

Samuel Starko (S)

Department of Biology, University of Victoria, Victoria, British Columbia, Canada.
Bamfield Marine Sciences Centre, Bamfield, British Columbia, Canada.

Christopher J Neufeld (CJ)

Bamfield Marine Sciences Centre, Bamfield, British Columbia, Canada.
Department of Biology, University of British Columbia Okanagan, Kelowna, British Columbia, Canada.

Lianna Gendall (L)

Department of Geography, University of Victoria, Victoria, British Columbia, Canada.

Brian Timmer (B)

Department of Geography, University of Victoria, Victoria, British Columbia, Canada.

Lily Campbell (L)

Department of Biology, University of Victoria, Victoria, British Columbia, Canada.
Bamfield Marine Sciences Centre, Bamfield, British Columbia, Canada.

Jennifer Yakimishyn (J)

Pacific Rim National Park Reserve of Canada, Ucluelet, British Columbia, Canada.

Louis Druehl (L)

Bamfield Marine Sciences Centre, Bamfield, British Columbia, Canada.
Canadian Kelp Resources, Bamfield, British Columbia, Canada.

Julia K Baum (JK)

Department of Biology, University of Victoria, Victoria, British Columbia, Canada.

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