Abiotic conditions (e.g., temperature and pH) fluctuate through time in most marine environments, sometimes passing intensity thresholds that induce physiological stress. Depending on habitat and season, the peak intensity of different abiotic stressors can occur in or out of phase with one another. Thus, some organisms are exposed to multiple stressors simultaneously, whereas others experience them sequentially. Understanding these physicochemical dynamics is critical because how organisms respond to multiple stressors depends on the magnitude and relative timing of each stressor. Here, we first discuss broad patterns of covariation between stressors in marine systems at various temporal scales. We then describe how these dynamics will influence physiological responses to multi-stressor exposures. Finally, we summarize how multi-stressor effects are currently assessed. We find that multi-stressor experiments have rarely incorporated naturalistic physicochemical variation into their designs, and emphasize the importance of doing so to make ecologically relevant inferences about physiological responses to global change.


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Literature Cited

  1. Aarset A, Aunaas T. 1987. Physiological adaptations to low temperature and brine exposure in the circumpolar amphipod Gammarus wilkitzkii. Polar Biol. 8:129–33 [Google Scholar]
  2. Albright R, Mason B. 2013. Projected near-future levels of temperature and pCO2 reduce coral fertilization success. PLOS ONE 8:e56468 [Google Scholar]
  3. Anestis A, Pörtner HO, Lazou A, Michaelidis B. 2008. Metabolic and molecular stress responses of sublittoral bearded horse mussel Modiolus barbatus to warming sea water: implications for vertical zonation. J. Exp. Biol. 211:2889–98 [Google Scholar]
  4. Anlauf H, D'Croz L, O'Dea A. 2011. A corrosive concoction: the combined effects of ocean warming and acidification on the early growth of a stony coral are multiplicative. J. Exp. Mar. Biol. Ecol. 397:13–20 [Google Scholar]
  5. Barnes DKA, Fuentes V, Clarke A, Schloss IR, Wallace MI. 2006. Spatial and temporal variation in shallow seawater temperatures around Antarctica. Deep-Sea Res. II 53:853–65 [Google Scholar]
  6. Barua D, Heckathorn SA. 2004. Acclimation of the temperature set-points of the heat-shock response. J. Therm. Biol. 29:185–93 [Google Scholar]
  7. Baruah K, Ranjan J, Sorgeloos P, Bossier P. 2010. Efficacy of heterologous and homologous heat shock protein 70s as protective agents to Artemia franciscana challenged with Vibrio campbellii. Fish Shellfish Immunol. 29:733–39 [Google Scholar]
  8. Baruah K, Ranjan J, Sorgeloos P, MacRae TH, Bossier P. 2011. Priming the prophenoloxidase system of Artemia franciscana by heat shock proteins protects against Vibrio campbellii challenge. Fish Shellfish Immunol. 31:134–41 [Google Scholar]
  9. Bates NR. 2002. Seasonal variability of the effect of coral reefs on seawater CO2 and air-sea CO2 exchange. Limnol. Oceanogr. 47:43–52 [Google Scholar]
  10. Bates NR, Michaels AF, Knap AH. 1996. Seasonal and interannual variability of oceanic carbon dioxide species at the US JGOFS Bermuda Atlantic Time-series Study (BATS) site. Deep-Sea Res. II 43:347–83 [Google Scholar]
  11. Bates NR, Takahashi T, Chipman DW, Knap AH. 1998. Variability of pCO2 on diel to seasonal timescales in the Sargasso Sea near Bermuda. J. Geophys. Res. Oceans 103:15567–85 [Google Scholar]
  12. Beaugrand G, Reid PC, Ibanez F, Lindley JA, Edwards M. 2002. Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296:1692–94 [Google Scholar]
  13. Bednarsek N, Feely RA, Reum JCP, Peterson B, Menkel J. et al. 2014. Limacina helicina shell dissolution as an indicator of declining habitat suitability owing to ocean acidification in the California Current Ecosystem. Proc. R. Soc. B 281:20140123 [Google Scholar]
  14. Benner I, Diner RE, Lefebvre SC, Li D, Komada T. et al. 2013. Emiliania huxleyi increases calcification but not expression of calcification-related genes in long-term exposure to elevated temperature and pCO2. Philos. Trans. R. Soc. B 368:20130049 [Google Scholar]
  15. Bernhardt JR, Leslie HM. 2013. Resilience to climate change in coastal marine ecosystems. Annu. Rev. Mar. Sci. 5:371–92 [Google Scholar]
  16. Bond JA, Bradley BP. 1995. Heat-shock reduces the toxicity of malathion in Daphnia magna. Mar. Environ. Res. 39:209–12 [Google Scholar]
  17. Bopp L, Resplandy L, Orr JC, Doney SC, Dunne JP. et al. 2013. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10:6225–45 [Google Scholar]
  18. 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]
  19. Breitbarth E, Bellerby RJ, Neill CC, Ardelan MV, Meyerhofer M. et al. 2010. Ocean acidification affects iron speciation during a coastal seawater mesocosm experiment. Biogeosciences 7:1065–73 [Google Scholar]
  20. Brown MA, Upender RP, Hightower LE, Renfro JL. 1992. Thermoprotection of a functional epithelium: heat stress effects on transepithelial transport by flounder renal tubule in primary monolayer culture. PNAS 89:3246–50 [Google Scholar]
  21. Brun NT, Bricelj VM, MacRae TH, Ross NW. 2008. Heat shock protein responses in thermally stressed bay scallops, Argopecten irradians, and sea scallops, Placopecten magellanicus. J. Exp. Mar. Biol. Ecol. 358:151–62 [Google Scholar]
  22. Buckley BA, Owen M-E, Hofmann GE. 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. 204:3571–79 [Google Scholar]
  23. Burleson ML, Silva PE. 2011. Cross tolerance to environmental stressors: effects of hypoxic acclimation on cardiovascular responses of channel catfish (Ictalurus punctatus) to a thermal challenge. J. Therm. Biol. 36:250–54 [Google Scholar]
  24. Burrows MT, Schoeman DS, Buckley LB, Moore P, Poloczanska ES. et al. 2011. The pace of shifting climate in marine and terrestrial ecosystems. Science 334:652–55 [Google Scholar]
  25. Byrne M, Przeslawski R. 2013. Multistressor impacts of warming and acidification of the ocean on marine invertebrates' life histories. Integr. Comp. Biol. 53:582–96 [Google Scholar]
  26. Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S. et al. 2008. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–63 [Google Scholar]
  27. Carter HA, Ceballos-Osuna L, Miller NA, Stillman JH. 2013. Impact of ocean acidification on metabolism and energetics during early life stages of the intertidal porcelain crab Petrolisthes cinctipes. J. Exp. Biol. 216:1412–22 [Google Scholar]
  28. Ceballos-Osuna L, Carter HA, Miller NA, Stillman JH. 2013. Effects of ocean acidification on early life-history stages of the intertidal porcelain crab Petrolisthes cinctipes. J. Exp. Biol. 216:1405–11 [Google Scholar]
  29. Cellura C, Toubiana M, Parrinello N, Roch P. 2006. HSP70 gene expression in Mytilus galloprovincialis hemocytes is triggered by moderate heat shock and Vibrio anguillarum, but not by V. splendidus or Micrococcus lysodeikticus. Dev. Comp. Immunol. 30:984–97 [Google Scholar]
  30. Chen X, Stillman JH. 2012. Multigenerational analysis of temperature and salinity variability affects on metabolic rate, generation time, and acute thermal and salinity tolerance in Daphnia pulex. J. Therm. Biol. 37:185–94 [Google Scholar]
  31. Cheng P, Liu X, Zhang G, He J. 2007. Cloning and expression analysis of a HSP70 gene from Pacific abalone (Haliotis discus hannai). Fish Shellfish Immunol. 22:77–87 [Google Scholar]
  32. Cheung WW, Lam VW, Sarmiento JL, Kearney K, Watson R, Pauly D. 2009. Projecting global marine biodiversity impacts under climate change scenarios. Fish Fish. 10:235–51 [Google Scholar]
  33. Cornwall CE, Hepburn CD, McGraw CM, Currie KI, Pilditch CA. et al. 2013. Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proc. R. Soc. B 280:20132201 [Google Scholar]
  34. Cottin D, Shillito B, Chertemps T, Thatje S, Léger N, Ravaux J. 2010. Comparison of heat-shock responses between the hydrothermal vent shrimp Rimicaris exoculata and the related coastal shrimp Palaemonetes varians. J. Exp. Mar. Biol. Ecol. 393:9–16 [Google Scholar]
  35. 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]
  36. Crossin GT, Al-Ayoub SA, Jury SH, Howell WH, Watson W. 1998. Behavioral thermoregulation in the American lobster Homarus americanus. J. Exp. Biol. 201:365–74 [Google Scholar]
  37. de la Vega E, Hall MR, Degnan BM, Wilson KJ. 2006. Short-term hyperthermic treatment of Penaeus monodon increases expression of heat shock protein 70 (HSP70) and reduces replication of gill associated virus (GAV). Aquaculture 253:82–90 [Google Scholar]
  38. Denny MW, Dowd WW, Bilir L, Mach KJ. 2011. Spreading the risk: small-scale body temperature variation among intertidal organisms and its implications for species persistence. J. Exp. Mar. Biol. Ecol. 400:175–90 [Google Scholar]
  39. Denny MW, Gaylord B. 2010. Marine ecomechanics. Annu. Rev. Mar. Sci. 2:89–114 [Google Scholar]
  40. Dierssen HM, Smith RC, Vernet M. 2002. Glacial meltwater dynamics in coastal waters west of the Antarctic Peninsula. PNAS 99:1790–95 [Google Scholar]
  41. Dietz TJ, Somero GN. 1992. The threshold induction temperature of the 90-kDa heat shock protein is subject to acclimatization in eurythermal goby fishes (genus Gillichthys). PNAS 89:3389–93 [Google Scholar]
  42. Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F. et al. 2012. Climate change impacts on marine ecosystems. Annu. Rev. Mar. Sci. 4:11–37 [Google Scholar]
  43. Dong C-W, Zhang Y-B, Zhang Q-Y, Gui J-F. 2006. Differential expression of three Paralichthys olivaceus Hsp40 genes in responses to virus infection and heat shock. Fish Shellfish Immunol. 21:146–58 [Google Scholar]
  44. Dore JE, Lukas R, Sadler DW, Church MJ, Karl DM. 2009. Physical and biogeochemical modulation of ocean acidification in the central North Pacific. PNAS 106:12235–40 [Google Scholar]
  45. Dorts J, Kestemont P, Thezenas ML, Raes M, Silvestre F. 2014. Effects of cadmium exposure on the gill proteome of Cottus gobio: modulatory effects of prior thermal acclimation. Aquat. Toxicol. 154:87–96 [Google Scholar]
  46. DuBeau SF, Pan F, Tremblay GC, Bradley TM. 1998. Thermal shock of salmon in vivo induces the heat shock protein hsp 70 and confers protection against osmotic shock. Aquaculture 168:311–23 [Google Scholar]
  47. Eby LA, Crowder LB. 2002. Hypoxia-based habitat compression in the Neuse River Estuary: context-dependent shifts in behavioral avoidance thresholds. Can. J. Fish. Aquat. Sci. 59:952–65 [Google Scholar]
  48. England MH, McGregor S, Spence P, Meehl GA, Timmermann A. et al. 2014. Recent intensification of wind-driven circulation in the Pacific and the ongoing warming hiatus. Nat. Clim. Change 4:222–27 [Google Scholar]
  49. Feely RA, Sabine CL, Hernandez-Ayon JM, Ianson D, Hales B. 2008. Evidence for upwelling of corrosive “acidified” water onto the continental shelf. Science 320:1490–92 [Google Scholar]
  50. Feidantsis K, Portner HO, Antonopoulou E, Michaelidis B. 2015. Synergistic effects of acute warming and low pH on cellular stress responses of the gilthead seabream Sparus aurata. J. Comp. Physiol. B 185:185–205 [Google Scholar]
  51. Frieder CA, Nam SH, Martz TR, Levin LA. 2012. High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences 9:3917–30 [Google Scholar]
  52. Ganning B. 1971. Studies on chemical, physical and biological conditions in Swedish rockpool ecosystems. Ophelia 9:51–105 [Google Scholar]
  53. Gleckler P, Santer B, Domingues C, Pierce D, Barnett T. et al. 2012. Human-induced global ocean warming on multidecadal timescales. Nat. Clim. Change 2:524–29 [Google Scholar]
  54. Green AL, Fernandes L, Almany G, Abesamis R, McLeod E. et al. 2014. Designing marine reserves for fisheries management, biodiversity conservation, and climate change adaptation. Coast. Manag. 42:143–59 [Google Scholar]
  55. Harley CDG, Paine RT. 2009. Contingencies and compounded rare perturbations dictate sudden distributional shifts during periods of gradual climate change. PNAS 106:11172–76 [Google Scholar]
  56. Harms L, Frickenhaus S, Schiffer M, Mark FC, Storch D. et al. 2014. Gene expression profiling in gills of the great spider crab Hyas araneus in response to ocean acidification and warming. BMC Genomics 15:789 [Google Scholar]
  57. Harvey BP, Gwynn-Jones D, Moore PJ. 2013. Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecol. Evol. 3:1016–30 [Google Scholar]
  58. Hauri C, Doney SC, Takahashi T, Erickson M, Jiang G, Ducklow HW. 2015. Two decades of inorganic carbon dynamics along the Western Antarctic Peninsula. Biogeosci. Discuss. 12:6929–69 [Google Scholar]
  59. Hauri C, Gruber N, Vogt M, Doney SC, Feely RA. et al. 2013. Spatiotemporal variability and long-term trends of ocean acidification in the California Current System. Biogeosciences 10:193–216 [Google Scholar]
  60. Helmuth B, Broitman BR, Yamane L, Gilman SE, Mach K. et al. 2010. Organismal climatology: analyzing environmental variability at scales relevant to physiological stress. J. Exp. Biol. 213:995–1003 [Google Scholar]
  61. Hochachka P, Somero GN. 2002. Biochemical Adaptation: Mechanism and Process in Physiological Evolution Oxford, UK: Oxford Univ. Press [Google Scholar]
  62. Hofmann GE, Evans TG, Kelly MW, Padilla-Gamino JL, Blanchette CA. et al. 2014. Exploring local adaptation and the ocean acidification seascape—studies in the California Current Large Marine Ecosystem. Biogeosciences 11:1053–64 [Google Scholar]
  63. Hofmann GE, Smith JE, Johnson KS, Send U, Levin LA. et al. 2011. High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLOS ONE 6:e28983 [Google Scholar]
  64. 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]
  65. Holmstrup M, Bindesbøl A-M, Oostingh GJ, Duschl A, Scheil V. et al. 2010. Interactions between effects of environmental chemicals and natural stressors: a review. Sci. Total Environ. 408:3746–62 [Google Scholar]
  66. Huey RB, Deutsch CA, Tewksbury JJ, Vitt LJ, Hertz PE. et al. 2009. Why tropical forest lizards are vulnerable to climate warming. Proc. R. Soc. B 276:1939–48 [Google Scholar]
  67. Huggett J, Griffiths C. 1986. Some relationships between elevation, physico-chemical variables and biota of intertidal rock pools. Mar. Ecol. Prog. Ser. 29:189–97 [Google Scholar]
  68. Karl DM, Church MJ. 2014. Microbial oceanography and the Hawaii Ocean Time-series programme. Nat. Rev. Microbiol. 12:699–713 [Google Scholar]
  69. Keeling CD, Brix H, Gruber N. 2004. Seasonal and long-term dynamics of the upper ocean carbon cycle at Station ALOHA near Hawaii. Glob. Biogeochem. Cycles 18:GB4006 [Google Scholar]
  70. Keeling RF, Körtzinger A, Gruber N. 2010. Ocean deoxygenation in a warming world. Annu. Rev. Mar. Sci. 2:199–229 [Google Scholar]
  71. Korhonen M, Rudels B, Marnela M, Wisotzki A, Zhao J. 2013. Time and space variability of freshwater content, heat content and seasonal ice melt in the Arctic Ocean from 1991 to 2011. Ocean Sci. 9:1015–55 [Google Scholar]
  72. Kültz D. 2005. Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 67:225–57 [Google Scholar]
  73. Le Campion-Alsumard T, Romano J-C, Peyrot-Clausade M, Le Campion J, Paul R. 1993. Influence of some coral reef communities on the calcium carbonate budget of Tiahura reef (Moorea, French Polynesia). Mar. Biol. 115:685–93 [Google Scholar]
  74. Lefebvre SC, Benner I, Stillman JH, Parker AE, Drake MK. et al. 2012. Nitrogen source and pCO2 synergistically affect carbon allocation, growth and morphology of the coccolithophore Emiliania huxleyi: potential implications of ocean acidification for the carbon cycle. Glob. Change Biol. 18:493–503 [Google Scholar]
  75. Lund SG, Lund ME, Tufts BL. 2003. Red blood cell Hsp 70 mRNA and protein as bio-indicators of temperature stress in the brook trout (Salvelinus fontinalis). Can. J. Fish. Aquat. Sci. 60:460–70 [Google Scholar]
  76. Lund SG, Ruberté MR, Hofmann GE. 2006. Turning up the heat: the effects of thermal acclimation on the kinetics of hsp70 gene expression in the eurythermal goby, Gillichthys mirabilis. Comp. Biochem. Physiol. A 143:435–46 [Google Scholar]
  77. Manchado M, Salas-Leiton E, Infante C, Ponce M, Asensio E. et al. 2008. Molecular characterization, gene expression and transcriptional regulation of cytosolic HSP90 genes in the flatfish Senegalese sole (Solea senegalensis Kaup). Gene 416:77–84 [Google Scholar]
  78. McBryan TL, Anttila K, Healy TM, Schulte PM. 2013. Responses to temperature and hypoxia as interacting stressors in fish: implications for adaptation to environmental change. Integr. Comp. Biol. 53:648–59 [Google Scholar]
  79. McCauley DJ, Pinsky ML, Palumbi SR, Estes JA, Joyce FH, Warner RR. 2015. Marine defaunation: animal loss in the global ocean. Science 347:1255641 [Google Scholar]
  80. McGaw IJ. 2003. Behavioral thermoregulation in Hemigrapsus nudus, the amphibious purple shore crab. Biol. Bull. 204:38–49 [Google Scholar]
  81. McPhaden MJ, Hayes SP. 1990. Variability in the eastern equatorial Pacific Ocean during 1986–1988. J. Geophys. Res. Oceans 95:13195–208 [Google Scholar]
  82. Melzner F, Thomsen J, Koeve W, Oschlies A, Gutowska MA. et al. 2013. Future ocean acidification will be amplified by hypoxia in coastal habitats. Mar. Biol. 160:1875–88 [Google Scholar]
  83. Milazzo M, Mirto S, Domenici P, Gristina M. 2012. Climate change exacerbates interspecific interactions in sympatric coastal fishes. J. Anim. Ecol. 82:468–77 [Google Scholar]
  84. Millero FJ, Woosley R, Ditrolio B, Waters J. 2009. Effect of ocean acidification on the speciation of metals in seawater. Oceanography 22:472–85 [Google Scholar]
  85. Ming J, Xie J, Xu P, Liu W, Ge X. et al. 2010. Molecular cloning and expression of two HSP70 genes in the Wuchang bream (Megalobrama amblycephala Yih). Fish Shellfish Immunol. 28:407–18 [Google Scholar]
  86. Mohrholz V, Eggert A, Junker T, Nausch G, Ohde T, Schmidt M. 2014. Cross shelf hydrographic and hydrochemical conditions and their short term variability at the northern Benguela during a normal upwelling season. J. Mar. Syst. 140:92–110 [Google Scholar]
  87. Morris S, Taylor S. 1983. Diurnal and seasonal variation in physico-chemical conditions within intertidal rock pools. Estuar. Coast. Shelf Sci. 17:339–55 [Google Scholar]
  88. Müller WE, Koziol C, Dapper J, Kurelec B, Batel R, Rinkevich B. 1995. Combinatory effects of temperature stress and nonionic organic pollutants on stress protein (hsp70) gene expression in the freshwater sponge Ephydatia fluviatilis. Environ. Toxicol. Chem. 14:1203–8 [Google Scholar]
  89. Niu C, Rummer J, Brauner C, Schulte P. 2008. Heat shock protein (Hsp70) induced by a mild heat shock slightly moderates plasma osmolarity increases upon salinity transfer in rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. C 148:437–44 [Google Scholar]
  90. Ohde S, van Woesik R. 1999. Carbon dioxide flux and metabolic processes of a coral reef, Okinawa. Bull. Mar. Sci. 65:559–76 [Google Scholar]
  91. Paganini AW, Miller NA, Stillman JH. 2014. Temperature and acidification variability reduce physiological performance in the intertidal zone porcelain crab Petrolisthes cinctipes. J. Exp. Biol. 217:3974–80 [Google Scholar]
  92. Pan F, Zarate JM, Tremblay GC, Bradley TM. 2000. Cloning and characterization of salmon hsp90 cDNA: upregulation by thermal and hyperosmotic stress. J. Exp. Zool. 287:199–212 [Google Scholar]
  93. Peck LS, Morley SA, Richard J, Clark MS. 2014. Acclimation and thermal tolerance in Antarctic marine ectotherms. J. Exp. Biol. 217:16–22 [Google Scholar]
  94. Perry AL, Low PJ, Ellis JR, Reynolds JD. 2005. Climate change and distribution shifts in marine fishes. Science 308:1912–15 [Google Scholar]
  95. Pincebourde S, Sanford E, Casas J, Helmuth B. 2012. Temporal coincidence of environmental stress events modulates predation rates. Ecol. Lett. 15:680–88 [Google Scholar]
  96. Pinkster S, Broodbakker NW. 1980. The influence of environmental factors on distribution and reproductive success of Eulimnogammarus obtusatus (Dahl, 1938) and other estuarine gammarids. Crustac. Suppl. 6:225–41 [Google Scholar]
  97. Przeslawski R, Byrne M, Mellin C. 2015. A review and meta-analysis of the effects of multiple abiotic stressors on marine embryos and larvae. Glob. Change Biol. 21:2122–40 [Google Scholar]
  98. Przeslawski R, Davis A. 2007. Does spawning behavior minimize exposure to environmental stressors for encapsulated gastropod embryos on rocky shores?. Mar. Biol. 152:991–1002 [Google Scholar]
  99. Rautenberger R, Bischof K. 2006. Impact of temperature on UV-susceptibility of two Ulva (Chlorophyta) species from Antarctic and Subantarctic regions. Polar Biol. 29:988–96 [Google Scholar]
  100. Ravaux J, Léger N, Rabet N, Morini M, Zbinden M. et al. 2012. Adaptation to thermally variable environments: capacity for acclimation of thermal limit and heat shock response in the shrimp Palaemonetes varians. J. Comp. Physiol. B 182:899–907 [Google Scholar]
  101. Reum JCP, Alin SR, Feely RA, Newton J, Warner M, McElhany P. 2014. Seasonal carbonate chemistry covariation with temperature, oxygen, and salinity in a fjord estuary: implications for the design of ocean acidification experiments. PLOS ONE 9:e89619 [Google Scholar]
  102. Sanford E. 1999. Regulation of keystone predation by small changes in ocean temperature. Science 283:2095–97 [Google Scholar]
  103. Schalkhausser B, Bock C, Portner HO, Lannig G. 2014. Escape performance of temperate king scallop, Pecten maximus under ocean warming and acidification. Mar. Biol. 161:2819–29 [Google Scholar]
  104. Schluter L, Lohbeck KT, Gutowska MA, Groger JP, Riebesell U, Reusch TBH. 2014. Adaptation of a globally important coccolithophore to ocean warming and acidification. Nat. Clim. Change 4:1024–30 [Google Scholar]
  105. Schulte PM. 2014. What is environmental stress? Insights from fish living in a variable environment. J. Exp. Biol. 217:23–34 [Google Scholar]
  106. Shaw EC, McNeil BI, Tilbrook B, Matear R, Bates ML. 2013. Anthropogenic changes to seawater buffer capacity combined with natural reef metabolism induce extreme future coral reef CO2 conditions. Glob. Change Biol. 19:1632–41 [Google Scholar]
  107. Shi DL, Xu Y, Hopkinson BM, Morel FMM. 2010. Effect of ocean acidification on iron availability to marine phytoplankton. Science 327:676–79 [Google Scholar]
  108. Sinclair BJ, Ferguson LV, Salehipour-Shirazi G, MacMillan HA. 2013. Cross-tolerance and cross-talk in the cold: relating low temperatures to desiccation and immune stress in insects. Integr. Comp. Biol. 53:545–56 [Google Scholar]
  109. 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]
  110. Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA. 2012. Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar. Environ. Res. 79:1–15 [Google Scholar]
  111. Specchiulli A, Focardi S, Renzi M, Scirocco T, Cilenti L. et al. 2008. Environmental heterogeneity patterns and assessment of trophic levels in two Mediterranean lagoons: Orbetello and Varano, Italy. Sci. Total Environ. 402:285–98 [Google Scholar]
  112. Sunday JM, Bates AE, Dulvy NK. 2012. Thermal tolerance and the global redistribution of animals. Nat. Clim. Change 2:686–90 [Google Scholar]
  113. Sung YY, Pineda C, MacRae TH, Sorgeloos P, Bossier P. 2008. Exposure of gnotobiotic Artemia franciscana larvae to abiotic stress promotes heat shock protein 70 synthesis and enhances resistance to pathogenic Vibrio campbellii. Cell Stress Chaperones 13:59–66 [Google Scholar]
  114. Sung YY, Van Damme EJM, Sorgeloos P, Bossier P. 2007. Non-lethal heat shock protects gnotobiotic Artemia franciscana larvae against virulent Vibrios. Fish Shellfish Immunol. 22:318–26 [Google Scholar]
  115. Sweeney C, Gnanadesikan A, Griffies SM, Harrison MJ, Rosati AJ, Samuels BL. 2005. Impacts of shortwave penetration depth on large-scale ocean circulation and heat transport. J. Phys. Oceanogr. 35:1103–19 [Google Scholar]
  116. Takahashi T, Olafsson J, Goddard JG, Chipman DW, Sutherland SC. 1993. Seasonal-variation of CO2 and nutrients in the high-latitude surface oceans—a comparative study. Glob. Biogeochem. Cycles 7:843–78 [Google Scholar]
  117. Takahashi T, Sutherland SC, Sweeney C, Poisson A, Metzl N. et al. 2002. Global sea-air CO2 flux based on climatological surface ocean pCO2, and seasonal biological and temperature effects. Deep-Sea Res. II 49:1601–22 [Google Scholar]
  118. Taylor AC. 1986. Seasonal and diel variations of some physico-chemical parameters of boulder shore habitats. Ophelia 25:83–95 [Google Scholar]
  119. Tedengren M, Olsson B, Bradley B, Zhou LZ. 1999. Heavy metal uptake, physiological response and survival of the blue mussel (Mytilus edulis) from marine and brackish waters in relation to the induction of heat-shock protein 70. Hydrobiologia 393:261–69 [Google Scholar]
  120. Thomas H. 2002. Remineralization ratios of carbon, nutrients, and oxygen in the North Atlantic Ocean: a field databased assessment. Glob. Biogeochem. Cycles 16:1051 [Google Scholar]
  121. Thompson RM, Beardall J, Beringer J, Grace M, Sardina P. 2013. Means and extremes: building variability into community-level climate change experiments. Ecol. Lett. 16:799–806 [Google Scholar]
  122. Todgham AE, Schulte PM, Iwama GK. 2005. Cross-tolerance in the tidepool sculpin: the role of heat shock proteins. Physiol. Biochem. Zool. 78:133–44 [Google Scholar]
  123. Todgham AE, Stillman JH. 2013. Physiological responses to shifts in multiple environmental stressors: relevance in a changing world. Integr. Comp. Biol. 53:539–44 [Google Scholar]
  124. Tomanek L, Somero GN. 2000. Time course and magnitude of synthesis of heat-shock proteins in congeneric marine snails (genus Tegula) from different tidal heights. Physiol. Biochem. Zool. 73:249–56 [Google Scholar]
  125. Truchot J-P, Duhamel-Jouve A. 1980. Oxygen and carbon dioxide in the marine intertidal environment: diurnal and tidal changes in rockpools. Respir. Physiol. 39:241–54 [Google Scholar]
  126. Vincenzi S. 2014. Extinction risk and eco-evolutionary dynamics in a variable environment with increasing frequency of extreme events. J. R. Soc. Interface 11:20140441 [Google Scholar]
  127. Walker CH, Livingstone DR. 1992. Persistent Pollutants in Marine Ecosystems Oxford, UK: Pergamon [Google Scholar]
  128. Wannamaker CM, Rice JA. 2000. Effects of hypoxia on movements and behavior of selected estuarine organisms from the southeastern United States. J. Exp. Mar. Biol. Ecol. 249:145–63 [Google Scholar]
  129. Wernberg T, Smale DA, Thomsen MS. 2012. A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob. Change Biol. 18:1491–98 [Google Scholar]
  130. Wethey DS, Woodin SA, Hilbish TJ, Jones SJ, Lima FP, Brannock PM. 2011. Response of intertidal populations to climate: effects of extreme events versus long term change. J. Exp. Mar. Biol. Ecol. 400:132–44 [Google Scholar]
  131. Zhenyu G, Chuanzhen J, Jianhai X. 2004. Heat-shock protein 70 expression in shrimp Fenneropenaeus chinensis during thermal and immune-challenged stress. Chin. J. Oceanol. Limnol. 22:386–91 [Google Scholar]

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  • Article Type: Review Article
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