1932

Abstract

Marine ecosystems are increasingly impacted by global environmental changes, including warming temperatures, deoxygenation, and ocean acidification. Marine scientists recognize intuitively that these environmental changes are translated into community changes via organismal physiology. However, physiology remains a black box in many ecological studies, and coexisting species in a community are often assumed to respond similarly to environmental stressors. Here, we emphasize how greater attention to physiology can improve our ability to predict the emergent effects of ocean change. In particular, understanding shifts in the intensity and outcome of species interactions such as competition and predation requires a sharpened focus on physiological variation among community members and the energetic demands and trophic mismatches generated by environmental changes. Our review also highlights how key species interactions that are sensitive to environmental change can operate as ecological leverage points through which small changes in abiotic conditions are amplified into large changes in marine ecosystems.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-marine-042021-051211
2022-01-03
2024-12-05
Loading full text...

Full text loading...

/deliver/fulltext/marine/14/1/annurev-marine-042021-051211.html?itemId=/content/journals/10.1146/annurev-marine-042021-051211&mimeType=html&fmt=ahah

Literature Cited

  1. Agostini S, Harvey BP, Wada S, Kon K, Milazzo M et al. 2018. Ocean acidification drives community shifts towards simplified non-calcified habitats in a subtropical–temperate transition zone. Sci. Rep. 8:11354
    [Google Scholar]
  2. Alexander JE Jr., McMahon RF. 2004. Respiratory response to temperature and hypoxia in the zebra mussel Dreissena polymorpha. Comp. Biochem. Physiol. A 137:425–34
    [Google Scholar]
  3. Atkinson A, Siegel V, Pakhomov E, Rothery P. 2004. Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432:100–3
    [Google Scholar]
  4. Baker AC, Glynn PW, Riegl B. 2008. Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar. Coast. Shelf Sci. 80:435–71
    [Google Scholar]
  5. Bayne BL. 1971. Ventilation, the heart beat and oxygen uptake by Mytilus edulis L. in declining oxygen tension. Comp. Biochem. Physiol. A 40:1065–85
    [Google Scholar]
  6. Bernhardt JR, Sunday JM, Thompson PL, O'Connor MI 2018. Nonlinear averaging of thermal experience predicts population growth rates in a thermally variable environment. Proc. R. Soc. B 285:20181076
    [Google Scholar]
  7. Bertness MD, Callaway R. 1994. Positive interactions in communities. Trends Ecol. Evol. 9:191–93
    [Google Scholar]
  8. Birkeland C, Lucas J. 1990. Acanthaster planci: Major Management Problem of Coral Reefs Boca Raton, FL: CRC
    [Google Scholar]
  9. Bonaviri C, Graham M, Gianguzza P, Shears NT. 2017. Warmer temperatures reduce the influence of an important keystone predator. J. Anim. Ecol. 86:490–500
    [Google Scholar]
  10. Boyd PW, Collins S, Dupont S, Fabricius K, Gattuso J-P et al. 2018. Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change—a review. Glob. Change Biol. 24:2239–61
    [Google Scholar]
  11. Boyd PW, Lennartz ST, Glover DM, Doney SC. 2015. Biological ramifications of climate-change-mediated oceanic multi-stressors. Nat. Clim. Change 5:71–79
    [Google Scholar]
  12. Breitburg D, Levin LA, Oschlies A, Grégoire M, Chavez FP et al. 2018. Declining oxygen in the global ocean and coastal waters. Science 359:eaam7240
    [Google Scholar]
  13. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB. 2004. Toward a metabolic theory of ecology. Ecology 85:1771–89
    [Google Scholar]
  14. Brown NEM, Milazzo M, Rastrick SPS, Hall-Spencer JM, Therriault TW, Harley CDG. 2018. Natural acidification changes the timing and rate of succession, alters community structure, and increases homogeneity in marine biofouling communities. Glob. Change Biol. 24:e112–27
    [Google Scholar]
  15. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL et al. 2007. Thermal stress and coral cover as drivers of coral disease outbreaks. PLOS Biol 5:e124
    [Google Scholar]
  16. Bruno JF, Stachowicz JJ, Bertness MD. 2003. Inclusion of facilitation into ecological theory. Trends Ecol. Evol. 18:119–25
    [Google Scholar]
  17. Byers JE. 2021. Marine parasites and disease in the era of global climate change. Annu. Rev. Mar. Sci. 13:397–420
    [Google Scholar]
  18. Chabot D, Dutil J-D. 1999. Reduced growth of Atlantic cod in non-lethal hypoxic conditions. J. Fish Biol. 55:472–91
    [Google Scholar]
  19. Cheng BS, Komoroske LM, Grosholz ED. 2017. Trophic sensitivity of invasive predator and native prey interactions: integrating environmental context and climate change. Funct. Ecol. 31:642–52
    [Google Scholar]
  20. Childress JJ, Seibel BA. 1998. Life at stable low oxygen levels: adaptations of animals to oceanic oxygen minimum layers. J. Exp. Biol. 201:1223–32
    [Google Scholar]
  21. Christie H, Gundersen H, Rinde E, Filbee-Dexter K, Norderhaug KM et al. 2019. Can multitrophic interactions and ocean warming influence large-scale kelp recovery?. Ecol. Evol. 9:2847–62
    [Google Scholar]
  22. Clements JC, Darrow ES. 2018. Eating in an acidifying ocean: a quantitative review of elevated CO2 effects on the feeding rates of calcifying marine invertebrates. Hydrobiologia 820:1–21
    [Google Scholar]
  23. Cohen AL, Holcomb M. 2009. Why corals care about ocean acidification: uncovering the mechanism. Oceanography 22:4118–27
    [Google Scholar]
  24. Compton TJ, Rijkenberg MJA, Drent J, Piersma T. 2007. Thermal tolerance ranges and climate variability: a comparison between bivalves from differing climates. J. Exp. Mar. Biol. Ecol. 352:200–11
    [Google Scholar]
  25. Connell JH 1975. Some mechanisms producing structure in natural communities: a model and evidence from field experiments. Ecology and Evolution of Communities ML Cody, JM Diamond 460–90 Cambridge, MA: Belknap
    [Google Scholar]
  26. Connell SD, Fernandes M, Burnell OW, Doubleday ZA, Griffin KJ et al. 2017. Testing for thresholds of ecosystem collapse in seagrass meadows. Conserv. Biol. 31:1196–201
    [Google Scholar]
  27. Connell SD, Kroeker KJ, Fabricius KE, Kline DI, Russell BD. 2013. The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance. Philos. Trans. R. Soc. Lond. B 368:20120442
    [Google Scholar]
  28. Cornwall CE, Revill AT, Hall-Spencer JM, Milazzo M, Raven JA, Hurd CL. 2017. Inorganic carbon physiology underpins macroalgal responses to elevated CO2. Sci. Rep. 7:46297
    [Google Scholar]
  29. Crain CM, Kroeker K, Halpern BS. 2008. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11:1304–15
    [Google Scholar]
  30. Cushing DH. 1969. The regularity of the spawning season of some fishes. ICES J. Mar. Sci. 33:81–92
    [Google Scholar]
  31. Cushing DH. 1990. Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv. Mar. Biol. 26:249–93
    [Google Scholar]
  32. De Zwaan A, Putzer V. 1985. Metabolic adaptations of intertidal invertebrates to environmental hypoxia (a comparison of environmental anoxia to exercise anoxia). Symp. Soc. Exp. Biol. 39:33–62
    [Google Scholar]
  33. Dell AI, Pawar S, Savage VM 2011. Systematic variation in the temperature dependence of physiological and ecological traits. PNAS 108:10591–96
    [Google Scholar]
  34. Dell AI, Pawar S, Savage VM. 2014. Temperature dependence of trophic interactions are driven by asymmetry of species responses and foraging strategy. J. Anim. Ecol. 83:70–84
    [Google Scholar]
  35. Desai DV, Prakash S. 2009. Physiological responses to hypoxia and anoxia in Balanus amphitrite (Cirripedia: Thoracica). Mar. Ecol. Prog. Ser. 390:157–66
    [Google Scholar]
  36. Deutsch C, Ferrel A, Seibel B, Pörtner H-O, Huey RB. 2015. Climate change tightens a metabolic constraint on marine habitats. Science 348:1132–35
    [Google Scholar]
  37. Diaz RJ, Rosenberg R. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321:926–29
    [Google Scholar]
  38. Doubleday ZA, Nagelkerken I, Coutts MD, Goldenberg SU, Connell SD. 2019. A triple trophic boost: how carbon emissions indirectly change a marine food chain. Glob. Change Biol. 25:978–84
    [Google Scholar]
  39. Dowd WW, King FA, Denny MW. 2015. Thermal variation, thermal extremes, and the physiological performance of individuals. J. Exp. Biol. 218:1956–67
    [Google Scholar]
  40. Edwards M, Richardson AJ. 2004. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–84
    [Google Scholar]
  41. Enochs IC, Manzello DP, Donham EM, Kolodziej G, Okano R et al. 2015. Shift from coral to macroalgae dominance on a volcanically acidified reef. Nat. Clim. Change 5:1083–88
    [Google Scholar]
  42. Fagerli CW, Norderhaug KM, Christie H, Pedersen MF, Fredriksen S. 2014. Predators of the destructive sea urchin Strongylocentrotus droebachiensis on the Norwegian coast. Mar. Ecol. Prog. Ser. 502:207–18
    [Google Scholar]
  43. Falkenberg LJ, Russell BD, Connell SD. 2013. Future herbivory: the indirect effects of enriched CO2 may rival its direct effects. Mar. Ecol. Prog. Ser. 492:85–95
    [Google Scholar]
  44. Ferrari MCO, McCormick MI, Munday PL, Meekan MG, Dixson DL et al. 2011. Putting prey and predator into the CO2 equation—qualitative and quantitative effects of ocean acidification on predator-prey interactions. Ecol. Lett. 14:1143–48
    [Google Scholar]
  45. Figueira WF, Curley B, Booth DJ. 2019. Can temperature-dependent predation rates regulate range expansion potential of tropical vagrant fishes?. Mar. Biol. 166:73
    [Google Scholar]
  46. Franco JN, Wernberg T, Bertocci I, Duarte P, Jacinto D et al. 2015. Herbivory drives kelp recruits into “hiding” in a warm ocean climate. Mar. Ecol. Prog. Ser. 536:1–9
    [Google Scholar]
  47. Frieder CA, Applebaum SL, Pan T-CF, Manahan DT. 2018. Shifting balance of protein synthesis and degradation sets a threshold for larval growth under environmental stress. Biol. Bull. 234:45–57
    [Google Scholar]
  48. Gaylord B, Barclay KM, Jellison BM, Jurgens LJ, Ninokawa AT et al. 2019. Ocean change within shoreline communities: from biomechanics to behaviour and beyond. Conserv. Physiol. 7:coz077
    [Google Scholar]
  49. Gaylord B, Hill TM, Sanford E, Lenz EA, Jacobs LA et al. 2011. Functional impacts of ocean acidification in an ecologically critical foundation species. J. Exp. Biol. 214:2586–94
    [Google Scholar]
  50. Gilbert B, Tunney TD, McCann KS, DeLong JP, Vasseur DAet al 2014. A bioenergetic framework for the temperature dependence of trophic interactions. Ecol. Lett 17:90214
    [Google Scholar]
  51. Gilman SE. 2017. Predicting indirect effects of predator-prey interactions. Integr. Comp. Biol. 57:148–58
    [Google Scholar]
  52. Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD. 2010. A framework for community interactions under climate change. Trends Ecol. Evol. 25:325–31
    [Google Scholar]
  53. Gooding RA, Harley CDG, Tang E 2009. Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. PNAS 106:9316–21
    [Google Scholar]
  54. Gray JS, Wu RS, Or YY. 2002. Effects of hypoxia and organic enrichment on the coastal marine environment. Mar. Ecol. Prog. Ser. 238:249–79
    [Google Scholar]
  55. Harley CDG, Anderson KM, Demes KW, Jorve JP, Kordas KL et al. 2012. Effects of climate change on global seaweed communities. J. Phycol. 48:1064–78
    [Google Scholar]
  56. Harley CDG, Connell SD, Doubleday ZA, Kelaher B, Russell BD et al. 2017. Conceptualizing ecosystem tipping points within a physiological framework. Ecol. Evol. 7:6035–45
    [Google Scholar]
  57. Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB et al. 2006. The impacts of climate change in coastal marine systems: climate change in coastal marine systems. Ecol. Lett. 9:228–41
    [Google Scholar]
  58. Harvey BP, Moore PJ. 2017. Ocean warming and acidification prevent compensatory response in a predator to reduced prey quality. Mar. Ecol. Prog. Ser. 563:111–22
    [Google Scholar]
  59. Haszprunar G, Vogler C, Wörheide G. 2017. Persistent gaps of knowledge for naming and distinguishing multiple species of Crown-of-Thorns-Seastar in the Acanthaster planci species complex. Diversity 9:22
    [Google Scholar]
  60. Helmuth B, Mieszkowska N, Moore P, Hawkins SJ. 2006. Living on the edge of two changing worlds: forecasting the response of rocky intertidal ecosystems to climate change. Annu. Rev. Ecol. Evol. Syst. 37:373–404
    [Google Scholar]
  61. Hobbs J-PA, Frisch AJ, Newman SJ, Wakefield CB. 2015. Selective impact of disease on coral communities: outbreak of white syndrome causes significant total mortality of Acropora plate corals. PLOS ONE 10:e0132528
    [Google Scholar]
  62. Hoegh-Guldberg O, Bruno JF. 2010. The impact of climate change on the world's marine ecosystems. Science 328:1523–28
    [Google Scholar]
  63. Hofmann GE, Todgham AE. 2010. Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annu. Rev. Physiol. 72:127–45
    [Google Scholar]
  64. Hughes AR, Hanley TC, Moore AFP, Ramsay-Newton C, Zerebecki RA, Sotka EE. 2018. Predicting the sensitivity of marine populations to rising temperatures. Front. Ecol. Environ. 17:17–24
    [Google Scholar]
  65. Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A et al. 2018. Global warming transforms coral reef assemblages. Nature 556:492–96
    [Google Scholar]
  66. Hutchins DA, Fu F-X, Webb EA, Walworth N, Tagliabue A. 2013. Taxon-specific response of marine nitrogen fixers to elevated carbon dioxide concentrations. Nat. Geosci. 6:790–95
    [Google Scholar]
  67. Iles AC. 2014. Toward predicting community-level effects of climate: relative temperature scaling of metabolic and ingestion rates. Ecology 95:2657–68
    [Google Scholar]
  68. Inoue S, Kayanne H, Yamamoto S, Kurihara H. 2013. Spatial community shift from hard to soft corals in acidified water. Nat. Clim. Change 3:683–87
    [Google Scholar]
  69. Jellison BM, Gaylord B. 2019. Shifts in seawater chemistry disrupt trophic links within a simple shoreline food web. Oecologia 190:955–67
    [Google Scholar]
  70. Jellison BM, Ninokawa AT, Hill TM, Sanford E, Gaylord B 2016. Ocean acidification alters the response of intertidal snails to a key sea star predator. Proc. R. Soc. B 283:20160890
    [Google Scholar]
  71. Jensen JLWV. 1906. Sur les fonctions convexes et les inégalitiés entre les valeurs moyennes. Acta Math 30:175–93
    [Google Scholar]
  72. Johnson CR, Banks SC, Barrett NS, Cazassus F, Dunstan PK et al. 2011. Climate change cascades: shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania. J. Exp. Mar. Biol. Ecol. 400:17–32
    [Google Scholar]
  73. Jurriaans S, Hoogenboom MO. 2019. Thermal performance of scleractinian corals along a latitudinal gradient on the Great Barrier Reef. Philos. Trans. R. Soc. Lond. B 374:20180546
    [Google Scholar]
  74. Kamya PZ, Byrne M, Mos B, Dworjanyn SA. 2018. Enhanced performance of juvenile crown of thorns starfish in a warm-high CO2 ocean exacerbates poor growth and survival of their coral prey. Coral Reefs 37:751–62
    [Google Scholar]
  75. Kamya PZ, Byrne M, Mos B, Hall L, Dworjanyn SA. 2017. Indirect effects of ocean acidification drive feeding and growth of juvenile crown-of-thorns starfish, Acanthaster planci. . Proc. R. Soc. B 284:20170778
    [Google Scholar]
  76. Kawaguchi S, Ishida A, King R, Raymond B, Waller N et al. 2013. Risk maps for Antarctic krill under projected Southern Ocean acidification. Nat. Clim. Change 3:843–47
    [Google Scholar]
  77. Kearney M, Shine R, Porter WP 2009. The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. PNAS 106:3835–40
    [Google Scholar]
  78. Keesing JK, Lucas JS. 1992. Field measurement of feeding and movement rates of the crown-of-thorns starfish Acanthaster planci (L.). J. Exp. Mar. Biol. Ecol. 156:89–104
    [Google Scholar]
  79. Kenyon JC, Aeby GS. 2009. Localized outbreak and feeding preferences of the crown-of-thorns seastar Acanthaster planci (Echinodermata, Asteroidea) on reefs off Oahu, Hawaii. Bull. Mar. Sci. 84:199–209
    [Google Scholar]
  80. Kingsolver JG, Buckley LB. 2017. Quantifying thermal extremes and biological variation to predict evolutionary responses to changing climate. Philos. Trans. R. Soc. Lond. B 372:20160147
    [Google Scholar]
  81. Kitchell JF, Boggs CH, He P, Walters CJ. 1999. Keystone predators in the Central Pacific. Ecosystem Approaches for Fisheries Management665–83 Fairbanks: Univ. Alsk. Sea Grant Coll. Program
    [Google Scholar]
  82. Koch M, Bowes G, Ross C, Zhang X-H. 2013. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob. Change Biol. 19:103–32
    [Google Scholar]
  83. Kordas RL, Harley CDG, O'Connor MI 2011. Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. J. Exp. Mar. Biol. Ecol. 400:218–26
    [Google Scholar]
  84. Kroeker KJ, Bell LE, Donham EM, Hoshijima U, Lummis S et al. 2020a. Ecological change in dynamic environments: accounting for temporal environmental variability in studies of ocean change biology. Glob. Change Biol. 26:54–67
    [Google Scholar]
  85. Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L et al. 2013a. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19:1884–96
    [Google Scholar]
  86. Kroeker KJ, Kordas RL, Harley CDG. 2017. Embracing interactions in ocean acidification research: confronting multiple stressor scenarios and context dependence. Biol. Lett. 13:20160802
    [Google Scholar]
  87. Kroeker KJ, Micheli F, Gambi MC. 2013b. Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat. Clim. Change 3:156–59
    [Google Scholar]
  88. Kroeker KJ, Powell C, Donham EM. 2020b. Windows of vulnerability: seasonal mismatches in exposure and resource identity determine ocean acidification's effect on a primary consumer at high latitude. Glob. Change Biol. 27:1042–51
    [Google Scholar]
  89. Kroeker KJ, Sanford E, Jellison BM, Gaylord B. 2014. Predicting the effects of ocean acidification on predator-prey interactions: a conceptual framework based on coastal molluscs. Biol. Bull. 226:211–22
    [Google Scholar]
  90. Kroeker KJ, Sanford E, Rose JM, Blanchette CA, Chan F et al. 2016. Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability. Ecol. Lett. 19:771–79
    [Google Scholar]
  91. Le Moullac G, Bacca H, Huvet A, Moal J, Pouvreau S, Van Wormhoudt A 2007. Transcriptional regulation of pyruvate kinase and phosphoenolpyruvate carboxykinase in the adductor muscle of the oyster Crassostrea gigas during prolonged hypoxia. J. Exp. Zool. A 307:371–82
    [Google Scholar]
  92. Lefevre S, McKenzie DJ, Nilsson GE. 2017. Models projecting the fate of fish populations under climate change need to be based on valid physiological mechanisms. Glob. Change Biol. 23:3449–59
    [Google Scholar]
  93. Leiva FP, Garcés C, Verberk WCEP, Care M, Paschke K, Gebauer P. 2018. Differences in the respiratory response to temperature and hypoxia across four life-stages of the intertidal porcelain crab Petrolisthes laevigatus. Mar. Biol. 165:146
    [Google Scholar]
  94. Lemoine NP, Burkepile DE. 2012. Temperature-induced mismatches between consumption and metabolism reduce consumer fitness. Ecology 93:2483–89
    [Google Scholar]
  95. Levin LA, Breitburg DL. 2015. Linking coasts and seas to address ocean deoxygenation. Nat. Clim. Change 5:401–3
    [Google Scholar]
  96. Liao M-L, Li G-Y, Wang J, Marshall DJ, Hui TY et al. 2021. Physiological determinants of biogeography: the importance of metabolic depression to heat tolerance. Glob. Change Biol. 27:2561–79
    [Google Scholar]
  97. Ling SD. 2008. Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state. Oecologia 156:883–94
    [Google Scholar]
  98. Loeb V, Siegel V, Holm-Hansen O, Hewitt R, Fraser W et al. 1997. Effects of sea-ice extent and krill or salp dominance on the Antarctic food web. Nature 387:897–900
    [Google Scholar]
  99. Lord J, Whitlatch R. 2015. Predicting competitive shifts and responses to climate change based on latitudinal distributions of species assemblages. Ecology 96:1264–74
    [Google Scholar]
  100. Low NHN, Micheli F. 2018. Lethal and functional thresholds of hypoxia in two key benthic grazers. Mar. Ecol. Prog. Ser. 594:165–73
    [Google Scholar]
  101. Lubchenco J, Petes LE. 2010. The interconnected biosphere: science at the ocean's tipping points. Oceanography 23:2115–29
    [Google Scholar]
  102. McCoy SJ, Pfister CA. 2014. Historical comparisons reveal altered competitive interactions in a guild of crustose coralline algae. Ecol. Lett. 17:475–83
    [Google Scholar]
  103. McCoy SJ, Ragazzola F. 2014. Skeletal trade-offs in coralline algae in response to ocean acidification. Nat. Clim. Change 4:719–23
    [Google Scholar]
  104. McCulloch M, Falter J, Trotter J, Montagna P. 2012. Coral resilience to ocean acidification and global warming through pH up-regulation. Nat. Clim. Change 2:623–27
    [Google Scholar]
  105. Meadows DH. 2008. Thinking in Systems: A Primer White River Junction, VT: Chelsea Green
    [Google Scholar]
  106. Melzner F, Buchholz B, Wolf F, Panknin U, Wall M. 2020. Ocean winter warming induced starvation of predator and prey. Proc. R. Soc. B 287:20200970
    [Google Scholar]
  107. Melzner F, Gutowska MA, Langenbuch M, Dupont S, Lucassen M et al. 2009. Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny?. Biogeosciences 6:2313–31
    [Google Scholar]
  108. Melzner F, Stange P, Trübenbach K, Thomsen J, Casties I et al. 2011. Food supply and seawater pCO2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis. PLOS ONE 6:e24223
    [Google Scholar]
  109. Menge BA, Olson AM. 1990. Role of scale and environmental factors in regulation of community structure. Trends Ecol. Evol. 5:52–57
    [Google Scholar]
  110. Menge BA, Sutherland JP. 1976. Species diversity gradients: synthesis of the roles of predation, competition, and temporal heterogeneity. Am. Nat. 110:351–69
    [Google Scholar]
  111. Menge BA, Sutherland JP. 1987. Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am. Nat. 130:730–57
    [Google Scholar]
  112. Mislan KAS, Deutsch CA, Brill RW, Dunne JP, Sarmiento JL. 2017. Projections of climate-driven changes in tuna vertical habitat based on species-specific differences in blood oxygen affinity. Glob. Change Biol. 23:4019–28
    [Google Scholar]
  113. Monaco CJ, Helmuth B 2011. Tipping points, thresholds and the keystone role of physiology in marine climate change research. Adv. Mar. Biol. 60:123–60
    [Google Scholar]
  114. Mouritsen KN, Poulin R. 2002. Parasitism, climate oscillations and the structure of natural communities. Oikos 97:462–68
    [Google Scholar]
  115. Mouritsen KN, Tompkins DM, Poulin R. 2005. Climate warming may cause a parasite-induced collapse in coastal amphipod populations. Oecologia 146:476–83
    [Google Scholar]
  116. Mueller CA, Seymour RS. 2011. The regulation index: a new method for assessing the relationship between oxygen consumption and environmental oxygen. Physiol. Biochem. Zool. 84:522–32
    [Google Scholar]
  117. Muth AF, Graham MH, Lane CE, Harley CDG. 2019. Recruitment tolerance to increased temperature present across multiple kelp clades. Ecology 100:e02594
    [Google Scholar]
  118. Noisette F, Egilsdottir H, Davoult D, Martin S 2013. Physiological responses of three temperate coralline algae from contrasting habitats to near-future ocean acidification. J. Exp. Mar. Biol. Ecol. 448:179–87
    [Google Scholar]
  119. Ockendon N, Baker DJ, Carr JA, White EC, Almond REA et al. 2014. Mechanisms underpinning climatic impacts on natural populations: altered species interactions are more important than direct effects. Glob. Change Biol. 20:2221–29
    [Google Scholar]
  120. O'Connor MI 2009. Warming strengthens a plant-herbivore interaction. Ecology 90:38898
    [Google Scholar]
  121. Paine RT. 1980. Food webs: linkage, interaction strength and community infrastructure. J. Anim. Ecol. 49:667–85
    [Google Scholar]
  122. Paine RT. 1992. Food-web analysis through field measurement of per capita interaction strength. Nature 355:73–75
    [Google Scholar]
  123. Pan T-CF, Applebaum SL, Manahan DT 2015. Experimental ocean acidification alters the allocation of metabolic energy. PNAS 112:4696–701
    [Google Scholar]
  124. Park T. 1954. Experimental studies of interspecies competition II. Temperature, humidity, and competition in two species of Tribolium. Physiol. Zool. 27:177–238
    [Google Scholar]
  125. Philippart CJM, van Aken HM, Beukema JJ, Bos OG, Cadee GC, Dekker R. 2003. Climate-related changes in recruitment of the bivalve Macoma balthica. Limnol. Oceanogr. 48:2171–85
    [Google Scholar]
  126. Pincebourde S, Sanford E, Helmuth B 2008. Body temperature during low tide alters the feeding performance of a top intertidal predator. Limnol. Oceanogr. 53:1562–73
    [Google Scholar]
  127. Piñones A, Fedorov AV. 2016. Projected changes of Antarctic krill habitat by the end of the 21st century. Geophys. Res. Lett. 43:8580–89
    [Google Scholar]
  128. Pinsky ML, Eikeset AM, McCauley DJ, Payne JL, Sunday JM. 2019. Greater vulnerability to warming of marine versus terrestrial ectotherms. Nature 569:108–11
    [Google Scholar]
  129. Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS et al. 2013. Global imprint of climate change on marine life. Nat. Clim. Change 3:919–25
    [Google Scholar]
  130. Poore AGB, Graba-Landry A, Favret M, Sheppard Brennand H, Byrne M, Dworjanyn SA 2013. Direct and indirect effects of ocean acidification and warming on a marine plant-herbivore interaction. Oecologia 173:1113–24
    [Google Scholar]
  131. Power ME, Tilman D, Estes JA, Menge BA, Bond WJ et al. 1996. Challenges in the quest for keystones. Bioscience 46:609–20
    [Google Scholar]
  132. Prince ED, Goodyear CP. 2006. Hypoxia-based habitat compression of tropical pelagic fishes. Fish. Oceanogr. 15:451–64
    [Google Scholar]
  133. Prosser CL. 1955. Physiological variation in animals. Biol. Rev. Camb. Philos. Soc. 30:229–61
    [Google Scholar]
  134. Randall CJ, van Woesik R. 2015. Contemporary white-band disease in Caribbean corals driven by climate change. Nat. Clim. Change 5:375–79
    [Google Scholar]
  135. Rasher DB, Steneck RS, Halfar J, Kroeker KJ, Ries JB et al. 2020. Keystone predators govern the pathway and pace of climate impacts in a subarctic marine ecosystem. Science 369:1351–54
    [Google Scholar]
  136. Ries JB, Cohen AL, McCorkle DC. 2009. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–34
    [Google Scholar]
  137. Rodríguez A, Clemente S, Brito A, Hernández JC. 2018. Effects of ocean acidification on algae growth and feeding rates of juvenile sea urchins. Mar. Environ. Res. 140:382–89
    [Google Scholar]
  138. Rogers-Bennett L, Catton CA 2019. Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens. Sci. Rep. 9:15050
    [Google Scholar]
  139. Saba GK, Schofield O, Torres JJ, Ombres EH, Steinberg DK. 2012. Increased feeding and nutrient excretion of adult Antarctic krill, Euphausia superba, exposed to enhanced carbon dioxide (CO2). PLOS ONE 7:e52224
    [Google Scholar]
  140. Sagarin RD, Barry JP, Gilman SE, Baxter CH. 1999. Climate-related change in an intertidal community over short and long time scales. Ecol. Monogr. 69:465–90
    [Google Scholar]
  141. Sanford E. 1999. Regulation of keystone predation by small changes in ocean temperature. Science 283:2095–97
    [Google Scholar]
  142. Sanford E 2002a. Community responses to climate change: links between temperature and keystone predation in a rocky intertidal system. Wildlife Responses to Climate Change: North American Case Studies SH Schneider, TL Root 165–200 Washington, DC: Island
    [Google Scholar]
  143. Sanford E. 2002b. Water temperature, predation, and the neglected role of physiological rate effects in rocky intertidal communities. Integr. Comp. Biol. 42:881–91
    [Google Scholar]
  144. Sanford E, Kelly MW. 2011. Local adaptation in marine invertebrates. Annu. Rev. Mar. Sci. 3:509–35
    [Google Scholar]
  145. Sanford E, Sones JL, García-Reyes M, Goddard JHR, Largier JL. 2019. Widespread shifts in the coastal biota of northern California during the 2014–2016 marine heatwaves. Sci. Rep. 9:4216
    [Google Scholar]
  146. Schulte PM. 2014. What is environmental stress? Insights from fish living in a variable environment. J. Exp. Biol. 217:23–24
    [Google Scholar]
  147. Schulte PM, Healy TM, Fangue NA. 2011. Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr. Comp. Biol. 51:691–702
    [Google Scholar]
  148. Seibel BA, Walsh PJ. 2003. Biological impacts of deep-sea carbon dioxide injection inferred from indices of physiological performance. J. Exp. Biol. 206:641–50
    [Google Scholar]
  149. Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA et al. 2002. A cross-ecosystem comparison of the strength of trophic cascades. Ecol. Lett. 5:785–91
    [Google Scholar]
  150. Sinclair BJ, Marshall KE, Sewell MA, Levesque DL, Willett CS et al. 2016. Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures?. Ecol. Lett. 19:1372–85
    [Google Scholar]
  151. Smith TB. 2008. Temperature effects on herbivory for an Indo-Pacific parrotfish in Panamá: implications for coral-algal competition. Coral Reefs 27:397–405
    [Google Scholar]
  152. Sobral P, Widdows J. 1997. Influence of hypoxia and anoxia on the physiological responses of the clam Ruditapes decussatus from southern Portugal. Mar. Biol. 127:455–61
    [Google Scholar]
  153. Sokolova IM. 2013. Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr. Comp. Biol. 53:597–608
    [Google Scholar]
  154. Somero GN. 2002. Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integr. Comp. Biol. 42:780–89
    [Google Scholar]
  155. Somero GN. 2005. Linking biogeography to physiology: evolutionary and acclimatory adjustments of thermal limits. Front. Zool. 2:1
    [Google Scholar]
  156. Somero GN. 2010. The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine “winners” and “losers. J. Exp. Biol. 213:912–20
    [Google Scholar]
  157. Somero GN. 2011. Comparative physiology: a “crystal ball” for predicting consequences of global change. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301:R1–14
    [Google Scholar]
  158. Somero GN, Beers JM, Chan F, Hill TM, Klinger T, Litvin SY. 2016. What changes in the carbonate system, oxygen, and temperature portend for the northeastern Pacific Ocean: a physiological perspective. BioScience 66:14–26
    [Google Scholar]
  159. Somero GN, Lockwood BL, Tomanek L. 2017. Biochemical Adaptation: Response to Environmental Challenges from Life's Origins to the Anthropocene Sunderland, MA: Sinauer
    [Google Scholar]
  160. Soniat TM, Hofmann EE, Klinck JM, Powell EN. 2008. Differential modulation of eastern oyster (Crassostrea virginica) disease parasites by the El-Niño-Southern Oscillation and the North Atlantic Oscillation. Int. J. Earth Sci. 98:99114
    [Google Scholar]
  161. Sorte CJB, Stachowicz JJ. 2011. Patterns and processes of compositional change in a California epibenthic community. Mar. Ecol. Prog. Ser. 435:63–74
    [Google Scholar]
  162. Sorte CJB, White JW. 2013. Competitive and demographic leverage points of community shifts under climate warming. Proc. R. Soc. B 280:20130572
    [Google Scholar]
  163. Spicer JI, Gaston KJ. 1999. Physiological Diversity and Its Ecological Implications Oxford, UK: Blackwell Sci.
    [Google Scholar]
  164. Stillman JH. 2003. Acclimation capacity underlies susceptibility to climate change. Science 301:65
    [Google Scholar]
  165. Strahl J, Francis DS, Doyle J, Humphrey C, Fabricius KE. 2015. Biochemical responses to ocean acidification contrast between tropical corals with high and low abundances at volcanic carbon dioxide seeps. ICES J. Mar. Sci. 73:897–909
    [Google Scholar]
  166. Stramma L, Prince ED, Schmidtko S, Luo J, Hoolihan JP et al. 2011. Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes. Nat. Clim. Change 2:33–37
    [Google Scholar]
  167. Strong DR. 1992. Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73:747–54
    [Google Scholar]
  168. Stuart-Smith RD, Edgar GJ, Barrett NS, Kininmonth SJ, Bates AE. 2015. Thermal biases and vulnerability to warming in the world's marine fauna. Nature 528:88–92
    [Google Scholar]
  169. Sunday JM, Bates AE, Dulvy NK. 2011. Global analysis of thermal tolerance and latitude in ectotherms. Proc. R. Soc. B 278:1823–30
    [Google Scholar]
  170. Sunday JM, Fabricius KE, Kroeker KJ, Anderson KM, Brown NE et al. 2017. Ocean acidification can mediate biodiversity shifts by changing biogenic habitat. Nat. Clim. Change 7:81–85
    [Google Scholar]
  171. Teagle H, Smale DA. 2018. Climate-driven substitution of habitat-forming species leads to reduced biodiversity within a temperate marine community. Divers. Distrib. 24:1367–80
    [Google Scholar]
  172. Thomas Y, Flye-Sainte-Marie J, Chabot D, Aguirre-Velarde A, Marques GM, Pecquerie L. 2019. Effects of hypoxia on metabolic functions in marine organisms: observed patterns and modelling assumptions within the context of Dynamic Energy Budget (DEB) theory. J. Sea Res. 143:231–42
    [Google Scholar]
  173. Thomsen J, Casties I, Pansch C, Körtzinger A, Melzner F. 2013. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments. Glob. Change Biol. 19:1017–27
    [Google Scholar]
  174. Tomanek L. 2008. The importance of physiological limits in determining biogeographical range shifts due to global climate change: the heat-shock response. Physiol. Biochem. Zool. 81:709–17
    [Google Scholar]
  175. Tomanek L, Somero GN. 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. 202:2925–36
    [Google Scholar]
  176. Tylianakis JM, Didham RK, Bascompte J, Wardle DA. 2008. Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11:1351–63
    [Google Scholar]
  177. Urban MC, Zarnetske PL, Skelly DK. 2017. Searching for biotic multipliers of climate change. Integr. Comp. Biol. 57:134–47
    [Google Scholar]
  178. Uthicke S, Logan M, Liddy M, Francis D, Hardy N, Lamare M. 2015. Climate change as an unexpected co-factor promoting coral eating seastar (Acanthaster planci) outbreaks. Sci. Rep. 5:8402
    [Google Scholar]
  179. Vergés A, Doropoulos C, Malcolm HA, Skye M, Garcia-Piza M et al. 2016. Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. PNAS 113:13791–96
    [Google Scholar]
  180. Vergés A, Steinberg PD, Hay ME, Poore AGB, Campbell AH et al. 2014. The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc. R. Soc. B 281:20140846
    [Google Scholar]
  181. Vizzini S, Martínez-Crego B, Andolina C, Massa-Gallucci A, Connell SD, Gambi MC. 2017. Ocean acidification as a driver of community simplification via the collapse of higher-order and rise of lower-order consumers. Sci. Rep. 7:4018
    [Google Scholar]
  182. Voigt W, Perner J, Davis AJ, Eggers T, Schumacher J et al. 2003. Trophic levels are differentially sensitive to climate. Ecology 84:2444–53
    [Google Scholar]
  183. Waldbusser GG, Hales B, Langdon CJ, Haley BA, Schrader P et al. 2015. Saturation-state sensitivity of marine bivalve larvae to ocean acidification. Nat. Clim. Change 5:273–80
    [Google Scholar]
  184. Wernberg T, Russell BD, Thomsen MS, Gurgel CFD, Bradshaw CJA et al. 2011. Seaweed communities in retreat from ocean warming. Curr. Biol. 21:1828–32
    [Google Scholar]
  185. Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ et al. 2013. An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat. Clim. Change 3:78–82
    [Google Scholar]
  186. Wootton JT, Pfister CA, Forester JD 2008. Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. PNAS 105:18848–53
    [Google Scholar]
  187. Wu RSS. 2002. Hypoxia: from molecular responses to ecosystem responses. Mar. Pollut. Bull. 45:35–45
    [Google Scholar]
  188. Yee EH, Murray SN. 2004. Effects of temperature on activity, food consumption rates, and gut passage times of seaweed-eating Tegula species (Trochidae) from California. Mar. Biol. 145:895–903
    [Google Scholar]
  189. Zacher K, Bernard M, Moreno AD, Bartsch I. 2019. Temperature mediates the outcome of species interactions in early life-history stages of two sympatric kelp species. Mar. Biol. 166:161
    [Google Scholar]
  190. Zarnetske PL, Skelly DK, Urban MC. 2012. Biotic multipliers of climate change. Science 336:1516–18
    [Google Scholar]
  191. Zhang G, Li L, Meng J, Qi H, Qu T et al. 2016. Molecular basis for adaptation of oysters to stressful marine intertidal environments. Annu. Rev. Anim. Biosci. 4:357–81
    [Google Scholar]
/content/journals/10.1146/annurev-marine-042021-051211
Loading
/content/journals/10.1146/annurev-marine-042021-051211
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error