1932

Abstract

To better understand life in the sea, marine scientists must first quantify how individual organisms experience their environment, and then describe how organismal performance depends on that experience. In this review, we first explore marine environmental variation from the perspective of pelagic organisms, the most abundant life forms in the ocean. Generation time, the ability to move relative to the surrounding water (even slowly), and the presence of environmental gradients at all spatial scales play dominant roles in determining the variation experienced by individuals, but this variation remains difficult to quantify. We then use this insight to critically examine current understanding of the environmental physiology of pelagic marine organisms. Physiologists have begun to grapple with the complexity presented by environmental variation, and promising frameworks exist for predicting and/or interpreting the consequences for physiological performance. However, new technology needs to be developed and much difficult empirical work remains, especially in quantifying response times to environmental variation and the interactions among multiple covarying factors. We call on the field of global-change biology to undertake these important challenges.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-marine-040221-115454
2022-01-03
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/marine/14/1/annurev-marine-040221-115454.html?itemId=/content/journals/10.1146/annurev-marine-040221-115454&mimeType=html&fmt=ahah

Literature Cited

  1. Angilletta MJ Jr. 2009. Thermal Adaptation: A Theoretical and Empirical Synthesis Oxford, UK: Oxford Univ. Press
  2. Bar-On YM, Phillips R, Milo R 2018. The biomass distribution on Earth. PNAS 115:6506–11A monumental effort to account for the distribution of biomass among all organisms on Earth.
    [Google Scholar]
  3. Bates AE, Helmuth B, Burrows MT, Duncan MI, Garrabou J et al. 2018. Biologists ignore ocean weather at their peril. Nature 560:299–301
    [Google Scholar]
  4. Bendat JS, Piersol AG. 1986. Random Data: Analysis and Measurement Procedures New York: Wiley-Intersci.
  5. Benedetti-Cecchi L. 2005. Unanticipated impacts of spatial variance of biodiversity on plant productivity. Ecol. Lett. 8:791–99
    [Google Scholar]
  6. Bergland AO, Behrman EL, O'Brien KR, Schmidt PS, Petrov DA 2014. Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila. PLOS Genet 10:e1004775
    [Google Scholar]
  7. 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]
  8. Bonnefond H, Moelants N, Talec A, Bernard O, Sciandra A. 2016. Concomitant effects of light and temperature diel variations on the growth rate and lipid production of Dunaliella salina. Algal Res 14:72–78
    [Google Scholar]
  9. Boyd PW, Cornwall CE, Davison A, Doney SC, Fourquez M et al. 2016. Biological responses to environmental heterogeneity under future ocean conditions. Glob. Change Biol. 22:2633–50
    [Google Scholar]
  10. Broitman BR, Szathmary PL, Mislan KAS, Blanchette CA, Helmuth B 2009. Predator-prey interactions under climate change: the importance of habitat versus body temperature. Oikos 118:219–24
    [Google Scholar]
  11. Burrell RB, Keppel AG, Clark VM, Breitburg DL. 2016. An automated monitoring and control system for flow-through co-cycling hypoxia and pH experiments. Limnol. Oceanogr. Methods 14:168–85
    [Google Scholar]
  12. Calosi P, Turner LM, Hawkins M, Bertolini C, Nightingale G et al. 2013. Multiple physiological responses to multiple environmental challenges: an individual approach. Integr. Comp. Biol. 53:660–70
    [Google Scholar]
  13. Chesson P, Donahue MJ, Melobourne B, Sears AL 2005. Scale transition theory for understanding mechanisms in metacommunities. Metacommunities: Spatial Dynamics and Ecological Communities M Holyoak, MA Leibold, RD Holt 279–306 Chicago: Univ. Chicago Press
    [Google Scholar]
  14. Coffey DM, Royer MA, Meyer CG, Holland KN. 2020. Diel patterns in swimming behavior of a vertically migrating deepwater shark, the bluntnose sixgill (Hexanchus griseus). PLOS ONE 15:e0228253
    [Google Scholar]
  15. Connor KM, Gracey AY 2011. Circadian cycles are the dominant transcriptional rhythm in the intertidal mussel Mytilus californianus. PNAS 108:16110–15
    [Google Scholar]
  16. Cossins AR, MacDonald AG. 1984. Homeoviscous theory under pressure: II. The molecular order of membranes from deep-sea fish. Biochim. Biophys. Acta Biomembr. 776:144–50
    [Google Scholar]
  17. Cossins AR, MacDonald AG. 1986. Homeoviscous adaptation under pressure. III. The fatty acid composition of liver mitochondrial phospholipids of deep-sea fish. Biochim. Biophys. Acta Biomembr. 860:325–35
    [Google Scholar]
  18. Costa IASF, Driedzic WR, Gamperl AK. 2013. Metabolic and cardiac responses of cunner Tautogolabrus adspersus to seasonal and acute changes in temperature. Physiol. Biochem. Zool. 86:233–44
    [Google Scholar]
  19. Crain CM, Kroeker KJ, Halpern BS. 2008. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11:1304–15
    [Google Scholar]
  20. Cresswell KA, Tarling GA, Thorpe SE, Burrows MT, Wiedenmann J, Mangel M. 2009. Diel vertical migration of Antarctic krill (Euphausia superba) is flexible during advection across the Scotia Sea. J. Plankton Res. 31:1265–81
    [Google Scholar]
  21. Cullen JJ. 1985. Diel vertical migration by dinoflagellates: roles of carbohydrate metabolism and behavioral flexibility. Contrib. Mar. Sci. 27:Suppl.135–52
    [Google Scholar]
  22. Dan X-M, Yan G-J, Zhang A-J, Cao Z-D, Fu S-J 2014. Effects of stable and diel-cycling hypoxia on hypoxia tolerance, postprandial metabolic response, and growth performance in juvenile qingbo (Spinibarbus sinensis). Aquaculture 428–29:21–28
    [Google Scholar]
  23. D'Asaro EA. 2001. Turbulent vertical kinetic energy in the ocean mixed layer. J. Phys. Oceanogr. 31:3530–37
    [Google Scholar]
  24. Denman KL, Gargett AE. 1983. Time and space scales of vertical mixing and advection of phytoplankton in the upper ocean. Limnol. Oceanogr. 28:801–15
    [Google Scholar]
  25. Denman KL, Marra J. 1986. Modelling the time dependent photoadaptation of phytoplankton to fluctuating light. Marine Interfaces Ecohydrodynamics JCJ Nihoul 341–59 Elsevier Oceanogr. Ser. 42 Amsterdam: Elsevier
    [Google Scholar]
  26. Denny MW. 1993. Air and Water: The Physics of Life's Media Princeton, NJ: Princeton Univ. Press
  27. Denny MW. 2008. How the Ocean Works: An Introduction to Oceanography Princeton, NJ: Princeton Univ. Press
  28. Denny MW. 2016. Ecological Mechanics: Principles of Life's Physical Interaction Princeton, NJ: Princeton Univ. Press
  29. 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]
  30. Denny MW, Hunt LJH, Miller LP, Harley CDG. 2009. On the prediction of extreme ecological events. Ecol. Monogr. 79:397–421
    [Google Scholar]
  31. Diggle PJ. 1990. Time Series: A Biostatistical Introduction Oxford, UK: Clarendon
  32. Dillon ME, Woods HA, Wang G, Fey SB, Vasseur DA et al. 2016. Life in the frequency domain: the biological impacts of changes in climate variability at multiple time scales. Integr. Comp. Biol. 56:14–30
    [Google Scholar]
  33. Dinh KV, Cuevas-Sanchez AY, Buhl KS, Moeser EA, Dowd WW. 2020. Heat tolerance and thermal preference of the copepod Tigriopus californicus are insensitive to ecologically relevant dissolved oxygen levels. Sci. Rep. 10:18885
    [Google Scholar]
  34. Doney SC, Fabry VJ, Feely RA, Kleypas JA. 2009. Ocean acidification: the other CO2 problem. Annu. Rev. Mar. Sci. 1:169–92
    [Google Scholar]
  35. 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]
  36. Dong Y, Li X, Choi FMP, Williams GA, Somero GN, Helmuth B. 2017. Untangling the roles of microclimate, behaviour and physiological polymorphism in governing vulnerability of intertidal snails to heat stress. Proc. R. Soc. B 284:20162367
    [Google Scholar]
  37. Dowd WW, Denny MW. 2020. A series of unfortunate events: characterizing the contingent nature of physiological extremes using long-term environmental records. Proc. R. Soc. B 287:20192333
    [Google Scholar]
  38. 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]
  39. Elder LE, Seibel BA. 2015. The thermal stress response to diel vertical migration in the hyperiid amphipod Phronima sedentaria. Comp. Biochem. Physiol. A 187:20–26
    [Google Scholar]
  40. Estay SA, Lima M, Bozinovic F. 2014. The role of temperature variability on insect performance and population dynamics in a warming world. Oikos 123:131–40
    [Google Scholar]
  41. Frölicher TL, Fischer EM, Gruber N. 2018. Marine heatwaves under global warming. Nature 560:360–64
    [Google Scholar]
  42. Frost BW. 1988. Variability and possible adaptive significance of diel vertical migration in Calanus pacificus, a planktonic marine copepod. Bull. Mar. Sci. 43:675–94
    [Google Scholar]
  43. Gary SF, Fox AD, Biastoch A, Roberts JM, Cunningham SA. 2020. Larval behaviour, dispersal and population connectivity in the deep sea. Sci. Rep. 10:10675
    [Google Scholar]
  44. Gates DM. 1980. Biophysical Ecology New York: Springer
  45. Gemmell BJ, Oh G, Buskey EJ, Villareal TA. 2016. Dynamic sinking behavior in marine phytoplankton: rapid changes in buoyancy may aid nutrient uptake. Proc. R. Soc. B 283:20161126
    [Google Scholar]
  46. Gerhard M, Koussoroplis AM, Hillebrand H, Striebel M. 2019. Phytoplankton community responses to temperature fluctuations under different nutrient concentrations and stoichiometry. Ecology 100:e02834
    [Google Scholar]
  47. Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL. 2001. Effects of size and temperature on metabolic rate. Science 293:2248–51
    [Google Scholar]
  48. Gilly WF, Beman J, Litvin SY, Robison BH. 2013. Oceanographic and biological effects of shoaling of the oxygen minimum zone. Annu. Rev. Mar. Sci. 5:393–420
    [Google Scholar]
  49. Goldbogen JA, Cade DE, Boersma AT, Calambokidis J, Kahane-Rapport SR et al. 2017. Using digital tags with integrated video and inertial sensors to study moving morphology and associated function in large aquatic vertebrates. Anat. Rec. 300:1935–41
    [Google Scholar]
  50. Goldbogen JA, Calambokidis J, Oleson E, Potvin J, Pyeson ND et al. 2011. Mechanics, hydrodynamics and energetics of blue whale lunge feeding efficiency: dependence on krill density. J. Exp. Biol. 214:131–46
    [Google Scholar]
  51. Gough WT, Segre PS, Bierlich KC, Cade DE, Potvin J et al. 2019. Scaling of swimming performance in baleen whales. J. Exp. Biol. 222:jeb204172
    [Google Scholar]
  52. Graham PJ, Nguyen B, Burdyny T, Sinton D. 2017. A penalty on photosynthetic growth in fluctuating light. Sci. Rep. 7:12513
    [Google Scholar]
  53. Gunderson AR, Armstrong EJ, Stillman JH 2016. Multiple stressors in a changing world: the need for an improved perspective on physiological responses to the dynamic marine environment. Annu. Rev. Mar. Sci. 8:357–78
    [Google Scholar]
  54. Gunderson AR, Stillman JH. 2015. Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming. Proc. R. Soc. B 282:20150401
    [Google Scholar]
  55. Häfker NS, Meyer B, Last KS, Pond DW, Hüppe L, Teschke M. 2017. Circadian clock involvement in zooplankton diel vertical migration. Curr. Biol. 27:2194–201.e3
    [Google Scholar]
  56. Halsey KH, Jones BM. 2015. Phytoplankton strategies for photosynthetic energy allocation. Annu. Rev. Mar. Sci. 7:265–97
    [Google Scholar]
  57. Harris RMB, Beaumont LJ, Vance TR, Tozer CR, Remenyi TA et al. 2018. Biological responses to the press and pulse of climate trends and extreme events. Nat. Clim. Change 8:579–87
    [Google Scholar]
  58. Hays GC. 2003. A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Hydrobiologia 503:163–70
    [Google Scholar]
  59. Helmuth B. 2002. How do we measure the environment? Linking intertidal thermal physiology and ecology through biophysics. Integr. Comp. Biol. 42:83745
    [Google Scholar]
  60. 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]
  61. Hopkins TE, Cech JJ Jr. 1994. Effect of temperature on oxygen consumption of the bat ray, Myliobatis californica (Chondrichthyes, Myliobatididae). Copeia 1994:529–32
    [Google Scholar]
  62. Howell EA, Hawn DR, Polovina JJ. 2010. Spatiotemporal variability in bigeye tuna (Thunnus obesus) dive behavior in the central Pacific Ocean. Prog. Oceanogr. 86:81–93
    [Google Scholar]
  63. Huesemann M, Dale T, Chavis A, Crowe B, Twary S et al. 2017. Simulation of outdoor pond cultures using indoor LED-lighted and temperature-controlled raceway ponds and Phenometrics photobioreactors. Algal Res 21:178–90
    [Google Scholar]
  64. Huey RB, Stevenson RD. 1979. Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Am. Zool. 19:357–66
    [Google Scholar]
  65. Jerlov NG. 1976. Marine Optics Amsterdam: Elsevier
  66. Juneau P, Harrison PJ. 2005. Comparison by PAM fluorometry of photosynthetic activity of nine marine phytoplankton grown under identical conditions. Photochem. Photobiol. 81:649–53
    [Google Scholar]
  67. Jutfelt F, Norin T, Ern R, Overgaard J, Wang T et al. 2018. Oxygen- and capacity-limited thermal tolerance: blurring ecology and physiology. J. Exp. Biol. 221:jeb169615
    [Google Scholar]
  68. Kelly MW, Sanford E, Grosberg RK 2011. Limited potential for adaptation to climate change in a broadly distributed marine crustacean. Proc. R. Soc. B 279:20110542
    [Google Scholar]
  69. Kennish MJ. 1989. Practical Handbook of Marine Science Boca Raton, FL: CRC
  70. Kerr LA, Secor DH, Kraus RT. 2007. Stable isotope (δ13C and δ18O) and Sr/Ca composition of otoliths as proxies for environmental salinity experienced by an estuarine fish. Mar. Ecol. Prog. Ser. 349:245–53
    [Google Scholar]
  71. Key T, McCarthy A, Campbell DA, Six C, Roy S, Finkel ZV 2010. Cell size trade-offs govern light exploitation strategies in marine phytoplankton. Environ. Microbiol. 12:95–104
    [Google Scholar]
  72. Kingsolver JG, Higgins JK, Augustine KE. 2015. Fluctuating temperatures and ectotherm growth: distinguishing non-linear and time-dependent effects. J. Exp. Biol. 218:2218–25
    [Google Scholar]
  73. Kingsolver JG, Woods HA. 2016. Beyond thermal performance curves: modeling time-dependent effects of thermal stress on ectotherm growth rates. Am. Nat. 187:283–94
    [Google Scholar]
  74. Kiørboe T. 2008. A Mechanistic Approach to Plankton Ecology Princeton, NJ: Princeton Univ. PressAn innovative and thorough explanation of how mechanistic approaches can provide insight into plankton ecology.
  75. Kiørboe T. 2011. How zooplankton feed: mechanisms, traits and trade-offs. Biol. Rev. 86:311–39
    [Google Scholar]
  76. Kooijman SALM. 2010. Dynamic Energy Budget Theory for Metabolic Organisation Cambridge, UK: Cambridge Univ. Press
  77. Koussoroplis A-M, Pincebourde S, Wacker A. 2017. Understanding and predicting physiological performance of organisms in fluctuating and multifactorial environments. Ecol. Monogr. 87:178–97An innovative extension of scale-transition theory that incorporates temporal covariation among multiple environmental drivers.
    [Google Scholar]
  78. Kroeker KJ, Sanford E. 2022. Ecological leverage points: species interactions amplify the physiological effects of global environmental change in the ocean. Annu. Rev. Mar. Sci. 14:75–103
    [Google Scholar]
  79. Lawson GL, Castelton MR, Block BA. 2010. Movements and diving behavior of Atlantic bluefin tuna Thunnus thynnus in relation to water column structure in the northwestern Atlantic. Mar. Ecol. Prog. Ser. 400:245–65
    [Google Scholar]
  80. Lehahn Y, d'Ovidio F, Koren I 2018. A satellite-based Lagrangian view on phytoplankton dynamics. Annu. Rev. Mar. Sci. 10:99–119
    [Google Scholar]
  81. Lesser MP, Farrell JH. 2004. Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23:367–77
    [Google Scholar]
  82. Levin LA, Le Bris N 2015. The deep ocean under climate change. Science 350:766–68
    [Google Scholar]
  83. Lewis MR, Horne EPW, Cullen JJ, Oakey NS, Platt T. 1984. Turbulent motions may control phytoplankton photosynthesis in the upper ocean. Nature 311:49–50
    [Google Scholar]
  84. Liszka CM, Robinson C, Manno C, Stowasser G, Tarling GA. 2021. Diel vertical migration of a Southern Ocean euphausiid, Euphausia triacantha, and its metabolic response to consequent short-term temperature changes. Mar. Ecol. Prog. Ser. 660:37–52
    [Google Scholar]
  85. Maas AE, Blanco-Bercial L, Lo A, Tarrant AM, Timmins-Schiffman E. 2018. Variations in copepod proteome and respiration rate in association with diel vertical migration and circadian cycle. Biol. Bull. 235:30–42
    [Google Scholar]
  86. Madigan DJ, Carlisle AB, Gardner LD, Jayasundara N, Micheli F et al. 2015. Assessing niche width of endothermic fish from genes to ecosystem. PNAS 112:8350–55
    [Google Scholar]
  87. Marshall KE, Anderson KM, Brown NEM, Dytnerski JK, Flynn KL et al. 2021. Whole-organism responses to constant temperatures do not predict responses to variable temperatures in the ecosystem engineer Mytilus trossulus. Proc. R. Soc. B 288:20202968
    [Google Scholar]
  88. Martin TL, Huey RB. 2008. Why “suboptimal” is optimal: Jensen's inequality and ectotherm thermal preferences. Am. Nat. 171:E102–18
    [Google Scholar]
  89. McHenry MJ, Jed J 2003. The ontogenetic scaling of hydrodynamics and swimming performance in jellyfish (Aurelia aurita). J. Exp. Biol. 206:4125–37
    [Google Scholar]
  90. McVeigh DM, Eggleston DB, Todd AC, Young CM, He R. 2017. The influence of larval migration and dispersal depth on potential trajectories of a deep-sea bivalve. Deep-Sea Res. I 127:57–64
    [Google Scholar]
  91. Miklasz KA, Denny MW. 2010. Diatom sinking speeds: improved predictions and insight from a modified Stokes’ law. Limnol. Oceanogr. 55:2513–25
    [Google Scholar]
  92. Morash AJ, Neufeld C, MacCormack TJ, Currie S. 2018. The importance of incorporating natural thermal variation when evaluating physiological performance in wild species. J. Exp. Biol. 221:jeb164673
    [Google Scholar]
  93. Moyen NE, Crane RL, Somero GN, Denny MW. 2020a. A single heat-stress bout induces rapid and prolonged heat acclimation in the California mussel, Mytilus californianus. Proc. R. Soc. B 287:20202561
    [Google Scholar]
  94. Moyen NE, Somero GN, Denny MW. 2020b. Mussel acclimatization to high, variable temperatures is lost slowly upon transfer to benign conditions. J. Exp. Biol. 223:jeb222893
    [Google Scholar]
  95. Neer JA, Carlson JK, Thompson BA. 2006. Standard oxygen consumption of seasonally acclimatized cownose rays, Rhinoptera bonasus (Mitchill 1815), in the northern Gulf of Mexico. Fish Physiol. Biochem. 32:67–71
    [Google Scholar]
  96. Niehaus AC, Angilletta MJ, Sears MW, Franklin CE, Wilson RS. 2012. Predicting the physiological performance of ectotherms in fluctuating thermal environments. J. Exp. Biol. 215:694–701
    [Google Scholar]
  97. Nisbet RM, Jusup M, Klanjscek T, Pecquerie L. 2012. Integrating dynamic energy budget (DEB) theory with traditional bioenergetic models. J. Exp. Biol. 215:892–902
    [Google Scholar]
  98. Ogonowski M, Duberg J, Hansson S, Gorokhova E. 2013. Behavioral, ecological and genetic differentiation in an open environment—a study of a mysid population in the Baltic Sea. PLOS ONE 8:e57210
    [Google Scholar]
  99. Oliver ECJ, Benthuysen JA, Darmaraki S, Donat MG, Hobday AJ et al. 2021. Marine heatwaves. Annu. Rev. Mar. Sci. 13:313–42
    [Google Scholar]
  100. Oliver TA, Palumbi SR. 2011. Do fluctuating temperature environments elevate coral thermal tolerance?. Coral Reefs 30:429–40
    [Google Scholar]
  101. PacIOOS (Pac. Isl. Ocean Obs. Syst.) 2021. Water temperature forecast: western North Pacific. PacIOOS http://www.pacioos.hawaii.edu/water/model-temperature-wnpacific
    [Google Scholar]
  102. 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]
  103. Pickard GL. 1964. Descriptive Physical Oceanography Oxford, UK: Pergamon
  104. Pörtner HO. 2010. Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J. Exp. Biol. 213:881–93
    [Google Scholar]
  105. Rahmstorf S, Coumou D 2011. Increase of extreme events in a warming world. PNAS 108:17905–9
    [Google Scholar]
  106. Ralph PJ, Gademann R. 2005. Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat. Bot. 82:222–37
    [Google Scholar]
  107. Rhein M, Rintoul SR, Aoki S, Campos E, Chambers RA et al. 2013. Observations: ocean. Climate Change 2013: The Physical Science Basis; Contribution of Working Group 1 to the Fifth Assessment of the Intergovernmental Panel on Climate Change TF Stocker, D Qin, G-K Plattner, M Tignor, SK Allen et al.255–315 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  108. Rivera HE, Chen C-Y, Gibson MC, Tarrant AM. 2021. Plasticity in parental effects confers rapid larval thermal tolerance in the estuarine anemone Nematostella vectensis. J. Exp. Biol. 224:jeb236745
    [Google Scholar]
  109. Roitberg BD, Mangel M. 2016. Cold snaps, heatwaves, and arthropod growth. Ecol. Entomol. 41:653–59
    [Google Scholar]
  110. Rosa R, Seibel BA 2008. Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator. PNAS 105:20776–80
    [Google Scholar]
  111. Rosa R, Seibel BA. 2010. Metabolic physiology of the Humboldt squid, Dosidicus gigas: implications for vertical migration in a pronounced oxygen minimum zone. Prog. Oceanogr. 86:72–80
    [Google Scholar]
  112. Ruel JJ, Ayres MP. 1999. Jensen's inequality predicts effects of environmental variation. Trends Ecol. Evol. 14:361–66
    [Google Scholar]
  113. Ryu T, Veilleux HD, Donelson JM, Munday PL, Ravasi T. 2018. The epigenetic landscape of transgenerational acclimation to ocean warming. Nat. Clim. Change 8:504–9
    [Google Scholar]
  114. Saborowski R, Salomon M, Buchholz F. 2000. The physiological response of Northern krill (Meganyctiphanes norvegica) to temperature gradients in the Kattegat. Hydrobiologia 426:157–60
    [Google Scholar]
  115. Salinas S, Munch SB. 2012. Thermal legacies: transgenerational effects of temperature on growth in a vertebrate. Ecol. Lett. 15:159–63
    [Google Scholar]
  116. Schaefer KM, Fuller DW, Block BA. 2007. Movements, behavior, and habitat utilization of yellowfin tuna (Thunnus albacares) in the northeastern Pacific Ocean, ascertained through archival tag data. Mar. Biol. 152:503–25
    [Google Scholar]
  117. Schaum CE, Collins S 2014. Plasticity predicts evolution in a marine alga. Proc. R. Soc. B 281:20141486
    [Google Scholar]
  118. Schaum CE, Rost B, Collins S 2016. Environmental stability affects phenotypic evolution in a globally distributed marine picoplankton. ISME J 10:75–84
    [Google Scholar]
  119. Schubert H, Sagert S, Forster RM. 2001. Evaluation of the different levels of variability in the underwater light field of a shallow estuary. Helgol. Mar. Res. 55:12–22
    [Google Scholar]
  120. 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]
  121. Seibel BA. 2011. Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones. J. Exp. Biol. 214:326–36
    [Google Scholar]
  122. Somero GN. 1992. Adaptations to high hydrostatic pressure. Annu. Rev. Physiol. 54:557–77
    [Google Scholar]
  123. 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]
  124. Somero GN, Lockwood BL, Tomanek L. 2017. Biochemical Adaptation: Response to Environmental Challenges from Life's Origins to the Anthropocene Sunderland, MA: Sinauer
  125. Southwood AL, Andrews RD, Lutcavage ME, Paladino FV, West NH et al. 1999. Heart rates and diving behavior of leatherback sea turtles in the eastern Pacific Ocean. J. Exp. Biol. 202:1115–25
    [Google Scholar]
  126. Spicer JI, Strömberg J-O. 2002. Diel vertical migration and the haemocyanin of krill Meganyctiphanes norvegica. Mar. Ecol. Prog. Ser. 238:153–62
    [Google Scholar]
  127. Spicer JI, Thomasson MA, Strömberg J-O. 1999. Possessing a poor anaerobic capacity does not prevent the diel vertical migration of Nordic krill Meganyctiphanes norvegica into hypoxic waters. Mar. Ecol. Prog. Ser. 185:181–87
    [Google Scholar]
  128. Steele JH. 1985. A comparison of terrestrial and marine ecological systems. Nature 313:355–58
    [Google Scholar]
  129. Stramski D, Rosenberg G, Legendre L. 1993. Photosynthetic and optical properties of the marine chlorophyte Dunaliella tertiolecta grown under fluctuating light caused by surface-wave focusing. Mar. Biol. 115:363–72
    [Google Scholar]
  130. Strömberg J-O, Spicer JI. 2000. Cold comfort for krill? Respiratory consequences of diel vertical migration by Meganyctiphanes norvegica into deep hypoxic waters. Ophelia 53:213–17
    [Google Scholar]
  131. Suggett DJ, Smith DJ. 2020. Coral bleaching patterns are the outcome of complex biological and environmental networking. Glob. Change Biol. 26:68–79
    [Google Scholar]
  132. Sutherland KR, Madin LP. 2010. Comparative jet wake structure and swimming performance of salps. J. Exp. Biol. 213:2967–75
    [Google Scholar]
  133. Sutton AJ, Feely RA, Maenner-Jones S, Musielwicz S, Osborne J et al. 2019. Autonomous seawater pCO2 and pH time series from 40 surface buoys and the emergence of anthropogenic trends. Earth Syst. Sci. Data 11:421–39
    [Google Scholar]
  134. Svetlichny LS, Hubareva ES, Erkan F, Gucu AC. 2000. Physiological and behavioral aspects of Calanus euxinus females (Copepoda: Calanoida) during vertical migration across temperature and oxygen gradients. Mar. Biol. 137:963–71
    [Google Scholar]
  135. Tanner RL, Dowd WW. 2019. Inter-individual physiological variation in responses to environmental variation and environmental change: integrating across traits and time. Comp. Biochem. Physiol. A 238:110577
    [Google Scholar]
  136. 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]
  137. Tutasi P, Escribano R. 2020. Zooplankton diel vertical migration and downward C flux into the oxygen minimum zone in the highly productive upwelling region off northern Chile. Biogeosciences 17:455–73
    [Google Scholar]
  138. van Haren H, Compton TJ. 2013. Diel vertical migration in deep sea plankton is finely tuned to latitudinal and seasonal day length. PLOS ONE 8:e64435
    [Google Scholar]
  139. Vasseur DA, DeLong JP, Gilbert B, Greig HS, Harley CDG et al. 2014. Increased temperature variation poses a greater risk to species than climate warming. Proc. R. Soc. B 281:20132612
    [Google Scholar]
  140. Vasseur DA, Yodzis P. 2004. The color of environmental noise. Ecology 85:1146–52
    [Google Scholar]
  141. Videler J. 1993. Fish Swimming New York: Chapman & Hall
  142. Villareal TA, Carpenter EJ. 2003. Buoyancy regulation and the potential for vertical migration in the oceanic cyanobacterium Trichodesmium. Microb. Ecol. 45:1–10
    [Google Scholar]
  143. Wahl M, Saderne V, Sawall Y. 2015. How good are we at assessing the impact of ocean acidification in coastal systems? Limitations, omissions and strengths of commonly used experimental approaches with special emphasis on the neglected role of fluctuations. Mar. Freshw. Res. 67:25–36
    [Google Scholar]
  144. Walsh P, Legendre L. 1983. Photosynthesis of natural phytoplankton under high frequency light fluctuations simulating those induced by sea surface waves. Limnol. Oceanogr. 28:688–97
    [Google Scholar]
  145. Watanabe M, Kohata K, Kunugi M. 1988. Phosphate accumulation and metabolism by Heterosigma akashiwo (Raphidophyceae) during diel vertical migration in a stratified microcosm. J. Phycol. 24:22–28
    [Google Scholar]
  146. Webb PW. 1975. Hydrodynamics and Energetics of Fish Propulsion Bull. Fish. Res. Board Can. 190 Ottawa: Fish. Res. Board Can.
  147. White CR, Marshall DJ, Alton LA, Arnold PA, Beaman JE et al. 2019. The origin and maintenance of metabolic allometry in animals. Nat. Ecol. Evol. 3:598–603
    [Google Scholar]
  148. Williams CM, Buckley LB, Sheldon KS, Vickers M, Pörtner H-O et al. 2016. Biological impacts of thermal extremes: mechanisms and costs of functional responses matter. Integr. Comp. Biol. 56:73–84
    [Google Scholar]
  149. Woods HA, Dillon ME, Pincebourde S. 2015. The roles of microclimatic diversity and of behavior in mediating the responses of ectotherms to climate change. J. Therm. Biol. 54:86–97
    [Google Scholar]
  150. Woods HA, Martin LB, Ghalambor CK 2014. Conclusions: the central role of the organism in biology. Integrative Organismal Biology LB Martin, CK Ghalambor, HA Woods 309–17 New York: Wiley & Sons
    [Google Scholar]
  151. Yancey PH. 2020. Cellular responses in marine animals to hydrostatic pressure. J. Exp. Zool. 333A:398–420
    [Google Scholar]
  152. Yancey PH, Gerringer ME, Drazen JC, Rowden AA, Jamieson A 2014. Marine fish may be biochemically constrained from inhabiting the deepest ocean depths. PNAS 111:4461–65
    [Google Scholar]
/content/journals/10.1146/annurev-marine-040221-115454
Loading
/content/journals/10.1146/annurev-marine-040221-115454
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