Krumhansl, K. A. et al. Global patterns of kelp forest change over the past half-century. Proc. Natl. Acad. Sci. USA 113, 13785–13790 (2016).
Google Scholar
Filbee-Dexter, K. & Scheibling, R. E. Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Mar. Ecol. Prog. Ser. 495, 1–25 (2014).
Google Scholar
Steneck, R. S. et al. Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ. Conserv. 29, 436–459 (2002).
Google Scholar
Steneck, R. S. Regular sea urchins as drivers of shallow benthic marine community structure. Dev. Aquacult. Fish. Sci. 43, 255–279 (2020).
Rogers-Bennett, L. & Catton, C. A. Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens. Sci. Rep. 9, 1–9 (2019).
Google Scholar
Pearse, J. S. Ecological role of purple sea urchins. Science 31, 940–941 (2006).
Google Scholar
Harrold, C. & Reed, D. C. Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66, 1160–1169 (1985).
Google Scholar
Kriegisch, N., Reeves, S. E., Flukes, E. B., Johnson, C. R. & Ling, S. D. Drift-kelp suppresses foraging movement of overgrazing sea urchins. Oecologia 190, 665–677 (2019).
Google Scholar
Pearse, J. S. & Hines, A. H. Long-term population dynamics of sea urchins in a central California kelp forest: rare recruitment and rapid decline. Mar. Ecol. Prog. Ser. 39, 275–283 (1987).
Google Scholar
Watanabe, J. M. & Harrold, C. Destructive grazing by sea urchins Strongylocentrotus spp. in a central California kelp forest: potential roles of recruitment, depth, and predation. Mar. Ecol. Prog. Ser. 71, 125–141 (1991).
Google Scholar
Reid, J. et al. The economic value of the recreational red abalone fishery in northern California. Calif. Fish Game 102, 119–130 (2016).
Menge, B. A. & Menge, D. N. Dynamics of coastal meta-ecosystems: the intermittent upwelling hypothesis and a test in rocky intertidal regions. Ecol. Monogr. 83, 283–310 (2013).
Google Scholar
Breitburg, D. L., Loher, T., Pacey, C. A. & Gerstein, A. Varying effects of low dissolved oxygen on trophic interactions in an estuarine food web. Ecol. Monogr. 67, 489–507 (1997).
Google Scholar
Hauri, C. et al. (2009) Ocean acidification in the California current system. Oceanography 22, 60–71 (2009).
Google Scholar
Connell, S. D. & Russell, B. D. The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc. R. Soc. B 277, 1409–1415 (2010).
Google Scholar
Sellers, A. J. et al. Seasonal upwelling reduces herbivore control of tropical rocky intertidal algal communities. Ecology e03335 https://doi.org/10.1002/ecy.3335(2021).
Moulin, L., Grosjean, P., Leblud, J., Batigny, A. & Dubois, P. Impact of elevated pCO2 on acid-base regulation of the sea urchin Echinometra mathaei and its relation to resistance to ocean acidification: a study in mesocosms. J. Exp. Mar. Biol. Ecol. 457, 97–104 (2014).
Google Scholar
Siikavuopio, S. I., Dale, T., Mortensen, A. & Foss, A. Effects of hypoxia on feed intake and gonad growth in the green sea urchin, Strongylocentrotus droebachiensis. Aquaculture 266, 112–116 (2007).
Google Scholar
Low, H. N. N. The Effects of Upwelling-driven Hypoxia on Sea Urchins in California Current Kelp Forests. PhD dissertation, Stanford University, Stanford, CA (2018).
Low, N. H. & Micheli, F. Lethal and functional thresholds of hypoxia in two key benthic grazers. Mar. Ecol. Prog. Ser. 594, 165–173 (2018).
Google Scholar
Low, N. H. & Micheli, F. Short-and long-term impacts of variable hypoxia exposures on kelp forest sea urchins. Sci. Rep. 10, 1–9 (2020).
Google Scholar
Huyer, A. Coastal upwelling in the California current system. Prog. Oceanogr. 12, 259–284 (1983).
Google Scholar
Frieder, C. A., Nam, S. H., Martz, T. R. & Levin, L. A. High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences 9, 3917–3930 (2012).
Feely, R. A. et al. The combined effects of acidification and hypoxia on pH and aragonite saturation in the coastal waters of the California current ecosystem and the northern Gulf of Mexico. Cont. Shelf Res. 152, 50–60 (2018).
Google Scholar
Chan, F. et al. Persistent spatial structuring of coastal ocean acidification in the California Current System. Sci. Rep. 7, 1–7 (2017).
Google Scholar
Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686 (2005).
Google Scholar
Feely, R. A. et al. Chemical and biological impacts of ocean acidification along the west coast of North America. Estuar. Coast. Shelf Sci. 183, 260–270 (2016).
Google Scholar
Iles, A. C. et al. Climate-driven trends and ecological implications of event-scale upwelling in the California Current System. Glob. Change Biol. 18, 783–796 (2012).
Google Scholar
CeNCOOS. Real-Time Sensor Feeds of Oceanographic and Atmospheric Models’ Online Tool to Extract Temperature, pH, and Dissolved Oxygen. https://data.cencoos.org (2020).
Bakun, A. Global climate change and intensification of coastal ocean upwelling. Science 247, 198–201 (1990).
Google Scholar
McGregor, H. V., Dima, M., Fischer, H. W. & Mulitza, S. Rapid 20th-century increase in coastal upwelling off northwest Africa. Science 315, 637–639 (2007).
Google Scholar
Narayan, N., Paul, A., Mulitza, S. & Schulz, M. Trends in coastal upwelling intensity during the late 20th century. Ocean Sci. 6, 815–823 (2010).
Google Scholar
Barton, E. D. D., Field, D. B. B. & Roy, C. Canary current upwelling: more or less?. Prog. Oceanogr. 116, 167–178 (2013).
Google Scholar
Mote, P. W. & Mantua, N. J. Coastal upwelling in a warmer future. Geophys. Res. Lett. 29, 2138 (2002).
Google Scholar
Bakun, A. et al. Anticipated effects of climate change on coastal upwelling ecosystems. Curr. Clim. Change Rep. 1, 85–93 (2015).
Google Scholar
Wang, D., Gouhier, T. C., Menge, B. A. & Ganguly, A. R. Intensification and spatial homogenization of coastal upwelling under climate change. Nature 518, 390–394 (2015).
Google Scholar
Snyder, M. A., Sloan, L. C., Diffenbaugh, N. S. & Bell, J. L. Future climate change and upwelling in the California Current. Geophys. Res. Lett. 30, 1823 (2003).
García‐Reyes, M. & Largier, J. Observations of increased wind‐driven coastal upwelling off central California. J. Geophys. Res. Oceans 115, 1–8 (2010).
Varela, R., Álvarez, I., Santos, F., DeCastro, M. & Gómez-Gesteira, M. Has upwelling strengthened along worldwide coasts over 1982–2010?. Sci. Rep. 5, 1–15 (2015).
Varela, R., Lima, F. P., Seabra, R., Meneghesso, C. & Gómez-Gesteira, M. Coastal warming and wind-driven upwelling: a global analysis. Sci. Total Environ. 639, 1501–1511 (2018).
Abrahams, A., Schlegel, R. W. & Smit, A. J. Variation and change of upwelling dynamics detected in the world’s eastern boundary upwelling systems. Front. Mar. Sci. 8, 626411 (2021).
Google Scholar
IPCC Climate change 2014: Synthesis report. In Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change Vol. 151 (eds Core Writing Team et al.) (IPCC, Geneva, 2014).
Rykaczewski, R. R. & Dunne, J. P. Enhanced nutrient supply to the California Current Ecosystem with global warming and increased stratification in an earth system model. Geophys. Res. Lett. 37, 1-5 (2010).
Somero, G. N. et al. What changes in the carbonate system, oxygen, and temperature portend for the northeastern Pacific Ocean: a physiological perspective. Bioscience 66, 14–26 (2016).
Google Scholar
Frölicher, T. L., Fischer, E. M. & Gruber, N. Marine heatwaves under global warming. Nature 560, 360–364 (2018).
Google Scholar
Filbee-Dexter, K. et al. Marine heatwaves and the collapse of marginal North Atlantic kelp forests. Sci. Rep. 10, 13388 (2020).
Google Scholar
Sokolova, I. M., Frederich, M., Bagwe, R., Lannig, G. & Sukhotin, A. A. Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar. Environ. Res. 79, 1–15 (2012).
Google Scholar
Sokolova, I. M. Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr. Comp. Biol. 53, 597–608 (2013).
Google Scholar
Fitzgerald-Dehoog, L., Browning, J. & Allen, B. J. Food and heat stress in the California mussel: evidence for an energetic trade-off between survival and growth. Biol. Bull. 223, 205–216 (2012).
Google Scholar
Ramajo, L. et al. Food supply confers calcifiers resistance to ocean acidification. Sci. Rep. 6, 19374 (2016).
Google Scholar
Brown, N. E., Bernhardt, J. R., Anderson, K. M. & Harley, C. D. Increased food supply mitigates ocean acidification effects on calcification but exacerbates effects on growth. Sci. Rep. 8, 1–9 (2018).
Wahle, R. A. & Peckham, S. H. Density-related reproductive trade-offs in the green sea urchin, Strongylocentrotus droebachiensis. Mar. Biol. 134, 127–137 (1999).
Google Scholar
Rogers-Bennett, L., Allen, B. L. & Rothaus, D. P. Status and habitat associations of the threatened northern abalone: importance of kelp and coralline algae. Aquat. Conserv. Mar. Freshw. Ecosyst. 21, 573–581 (2011).
Google Scholar
Brown, M. B., Edwards, M. S. & Kim, K. Y. Effects of climate change on the physiology of giant kelp, Macrocystis pyrifera, and grazing by purple urchin, Strongylocentrotus purpuratus. Algae 29, 203–215 (2014).
Google Scholar
Klinger, T. S. & Lawrence, J. M. Distance perception of food and the effect of food quantity on feeding behavior of Lytechinus variegatus (Lamarck) (Echinodermata: Echinoidea). Mar. Freshw. Behav. Physiol. 11, 327–344 (1985).
Google Scholar
Trowbridge, C. D. Establishment of the green alga Codium fragile ssp. tomentosoides on New Zealand rocky shores: current distribution and invertebrate grazers. J. Ecol. 83, 949–965 (1995).
Google Scholar
Meidel, S. K. & Scheibling, R. E. Effects of food type and ration on reproductive maturation and growth of the sea urchin Strongylocentrotus droebachiensis. Mar. Biol. 134, 155–166 (1999).
Google Scholar
Harianto, J., Nguyen, H. D., Holmes, S. P. & Byrne, M. The effect of warming on mortality, metabolic rate, heat-shock protein response and gonad growth in thermally acclimated sea urchins (Heliocidaris erythrogramma). Mar. Biol. 165, 1–12 (2018).
Google Scholar
Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).
Google Scholar
Hobday, A. J. et al. A hierarchical approach to defining marine heatwaves. Prog. Oceanogr. 141, 227–238 (2016).
Google Scholar
Spicer, J. I., Widdicombe, S., Needham, H. R. & Berge, J. A. Impact of CO2-acidified seawater on the extracellular acid-base balance of the northern sea urchin Strongylocentrotus dröebachiensis. J. Exp. Mar. Biol. Ecol. 407, 19–25 (2011).
Google Scholar
Catarino, A. I., Bauwens, M. & Dubois, P. Acid–base balance and metabolic response of the sea urchin Paracentrotus lividus to different seawater pH and temperatures. Environ. Sci. Pollut. Res. 19, 2344–2353 (2012).
Google Scholar
Rogers-Bennett, L., Bennett, W. A., Fastenau, H. C. & Dewees, C. M. Spatial variation in red sea urchin reproduction and morphology: implications for harvest refugia. Ecol. Appl. 5, 1171–1180 (1995).
Google Scholar
Quinn, J. F., Wing, S. R. & Botsford, L. W. Harvest refugia in marine invertebrate fisheries: models and applications to the red sea urchin, Strongylocentrotus franciscanus. Am. Zool. 33, 537–550 (1993).
Google Scholar
Eurich, J. G., Selden, R. L. & Warner, R. R. California spiny lobster preference for urchins from kelp forests: implications for urchin barren persistence. Mar. Ecol. Prog. Ser. 498, 217–225 (2014).
Google Scholar
Steneck, R. S., Leland, A., McNaught, D. C. & Vavrinec, J. Ecosystem flips, locks, and feedbacks: the lasting effects of fisheries on Maine’s kelp forest ecosystem. Bull. Mar. Sci. 89, 31–55 (2013).
Google Scholar
Gerard, V. A. Growth and utilization of internal nitrogen reserves by the giant kelp Macrocystis pyrifera in a low-nitrogen environment. Mar. Biol. 66(1), 27–35 (1982).
Google Scholar
Simonson, E. J., Scheibling, R. E. & Metaxas, A. Kelp in hot water: I. Warming seawater temperature induces weakening and loss of kelp tissue. Mar. Ecol. Prog. Ser. 537, 89–104 (2015).
Google Scholar
Thomsen, M. S. et al. Local extinction of bull kelp (Durvillaea spp.) due to a marine heatwave. Front. Mar. Sci. 6, 84 (2019).
Google Scholar
O’Donnell, M. J., Hammond, L. M. & Hofmann, G. E. Predicted impact of ocean acidification on a marine invertebrate: elevated CO2 alters response to thermal stress in sea urchin larvae. Mar. Biol. 156, 439–446 (2009).
Google Scholar
Dupont, S., Dorey, N., Stumpp, M., Melzner, F. & Thorndyke, M. Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar. Biol. 160, 1835–1843 (2013).
Google Scholar
Marcel, E. V. et al. Variable responses to large-scale climate change in European Parus populations. Proc. R. Soc. B 270, 367–372 (2003).
Google Scholar
Parker, L. M., Ross, P. M. & O’Connor, W. A. Populations of the Sydney rock oyster, Saccostrea glomerata, vary in response to ocean acidification. Mar. Biol. 158, 689–697 (2011).
Google Scholar
Kroeker, K. J., Kordas, R. L. & Harley, C. D. Embracing interactions in ocean acidification research: confronting multiple stressor scenarios and context dependence. Biol. Lett. 13, 20160802 (2017).
Google Scholar
Conor, J. J. Gonad growth in the sea urchin, Strongylocentrotus purpuratus (Stimpson) (Echinodermata: Echinoidea) and the assumptions of gonad index methods. J. Exp. Mar. Biol. Ecol. 10, 89–103 (1972).
Google Scholar
Bandstra, L., Hales, B. & Takahashi, T. High-frequency measurements of total CO2: method development and first oceanographic observations. Mar. Chem. 100, 24–38 (2006).
Google Scholar
Hales, B., Chipman, D. & Takahashi, T. High-frequency measurement of partial pressure and total concentration of carbon dioxide in seawater using microporous hydrophobic membrane contactors. Limnol. Oceanogr. Methods 2, 356–364 (2004).
Google Scholar
Lavigne, H., Epitalon, J. M. & Gattuso, J. P. Seacarb: Seawater Carbonate Chemistry with R. R package version 3.0 http://CRAN.R-project.org/package=seacarb (2011).
Gattuso, J. P., Epitalon, J. M., Lavigne, H. & Orr, J. Seacarb: seawater carbonate chemistry. R package version 3.2.10. http://CRAN.R-project.org/package=seacarb (2018).
Murie, K. A. & Bourdeau, P. E. Fragmented kelp forest canopies retain their ability to alter local seawater chemistry. Sci. Rep. 10, 1–13 (2020).
Google Scholar
R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ (2013).
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