Abstract
Though much attention has focused on single environmental variables, most notably temperature and acidification, global climate change is most realistically to manifest as co-occurring and sustained variations in multiple environmental variables or in more frequent, but episodic, fluctuations in environmental conditions. Environmental variability is likely to produce physiological stress to organisms and may supersede the organismic capacity to handle stressor(s) when their rate or magnitude of change is high. Unfortunately, multiple stressor experiments predictive of natural systems remain difficult to perform. Multiple stressors may produce additive, synergistic, or antagonistic effects that are not always predictable from the impacts of the stressors in isolation. Furthermore, physiological variation is harbored within species and individuals, and this natural variation for resistance or resilience to one stressor may be attenuated by co-occurrence of additional stressors. As such, the combination of factors that limit physiological resilience in at-risk populations remains elusive.
After a brief description of stress biology, this chapter will describe the sources of ocean acidification and its biological impacts on the biota of marine systems. It will next describe the major drivers of oceanic deoxygenation and temperature warming as well as provide a brief discussion of the effects of these environmental stressors on aquatic animals. Next, it will discuss the environmental conditions that favor co-occurrence of these stressors in nature and how global climate change has exacerbated the magnitude and frequency of these multiple stressor interactions in nature. Finally, it will investigate how chronic exposure to new baselines in baselines in environments will sensitize or buffer organisms from acute fluctuations in environmental parameters and discuss how natural evolved variation among populations and species may sensitize or buffer wild animals from altered environments. This will address one of the grand challenges in organismal biology, which is the effective integration of molecular through whole animal responses to natural systems.
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References
Alfaro ME, Santini F, Brock C, Alamillo H, Dornburg A, Rabosky DL, Carnevale G, Harmon LJ (2009) Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc Natl Acad Sci 106:13410–13414
Andersson AJ, Gledhill D (2013) Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Annu Rev Mar Sci 5:321–348
Baumann H, Talmage SC, Gobler CJ (2012) Reduced early life growth and survival in a fish in direct response to increased carbon dioxide. Nat Clim Chang 2:38–41
Baumann H, Wallace RB, Tagliaferri T, Gobler CJ (2015) Large natural pH, CO2 and O2 fluctuations in a temperate tidal salt marsh on diel, seasonal, and interannual time scales. Estuar Coasts 38:220–231
Beaufort L, Probert I, De Garidel-Thoron T, Bendif EM, Ruiz-Pino D, Metzl N, Goyet C, Buchet N, Coupel P, Grelaud M, Rost B, Rickaby RE, De Vargas C (2011) Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature 476:80–83
Bignami S, Enochs IC, Manzello DP, Sponaugle S, Cowen RK (2013) Ocean acidification alters the otoliths of a pantropical fish species with implications for sensory function. Proc Natl Acad Sci 110:7366–7370
Bignami S, Sponaugle S, Cowen RK (2014) Effects of ocean acidification on the larvae of a high-value pelagic fisheries species, mahi-mahi Coryphaena hippurus. Aquat Biol 21:249–260
Boutilier RG (2001) Mechanisms of cell survival in hypoxia and hypothermia. J Exp Biol 204:3171–3181
Brauner CJ, Rombough PJ (2012) Ontogeny and Paleophysiology of the gill: new insights from larval and air-breathing fish. Respir Physiol Neurobiol 184:293–300
Briffa M, De La Haye K, Munday PL (2012) High CO2 and marine animal behaviour: potential mechanisms and ecological consequences. Mar Pollut Bull 64:1519–1528
Burnett KG, Bain LJ, Baldwin WS, Callard GV, Cohen S, Di Giulio RT, Evans DH, Gomez-Chiarri M, Hahn ME, Hoover CA, Karchner SI, Katoh F, Maclatchy DL, Marshall WS, Meyer JN, Nacci DE, Oleksiak MF, Rees BB, Singer TD, Stegeman JJ, Towle DW, Van Veld PA, Vogelbein WK, Whitehead A, Winn RN, Crawford DL (2007) Fundulus as the premier teleost model in environmental biology: opportunities for new insights using genomics. Comp Biochem Physiol Part D Genomics Proteomics 2:257–286
Cai W-J, Hu X, Huang W-J, Murrell MC, Lehrter JC, Lohrenz SE, Chou W-C, Zhai W, Hollibaugh JT, Wang Y, Zhao P, Guo X, Gundersen K, Dai M, Gong G-C (2011) Acidification of subsurface coastal waters enhanced by eutrophication. Nat Geosci 4:766–770
Caldeira K, Wickett ME (2003) Oceanography: anthropogenic carbon and ocean pH. Nature 425:365
Cannon WB, de la Paz D (1911) Emotional stimulation of adrenal secretion. Am J Physiol 28:64–70
Capone DG, Hutchins DA (2013) Microbial biogeochemistry of coastal upwelling regimes in a changing ocean. Nat Geosci 6:711–717
Chambers R, Candelmo AC, Habeck EA, Poach EM, Wieczorek D, Cooper K, Greenfield CE, Phelan B (2013) Ocean acidification effects in the early life-stages of summer flounder, Paralichthys dentatus. Biogeosci Discuss 10:13897–13929
Chevin LM, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol 8:E1000357
Chown SL, Hoffmann AA, Kristensen TN, Angilletta MJ, Stenseth NC, Pertoldi C (2010) Adapting to climate change: a perspective from evolutionary physiology. Clim Res 43:3–15
Christensen MR, Graham MD, Vinebrooke RD, Findlay DL, Paterson MJ, Turner MA (2006) Multiple anthropogenic stressors cause ecological surprises in boreal lakes. Glob Chang Biol 12:2316–2322
Chu JWF, Tunnicliffe V (2015) Oxygen limitations on marine animal distributions and the collapse of epibenthic community structure during shoaling hypoxia. Glob Chang Biol 21:2989–3004
Claiborne JB, Edwards SL, Morrison-Shetlar AI (2002) Acid-Base regulation in fishes: cellular and molecular mechanisms. J Exp Zool 293:302–319
Clark TD, Sandblom E, Jutfelt F (2013) Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J Exp Biol 216:2771–2782
Cole VJ, Parker LM, O'connor SJ, O'connor WA, Scanes E, Byrne M, Ross PM (2016) Effects of multiple climate change stressors: ocean acidification interacts with warming, hyposalinity, and low food supply on the larvae of the brooding flat oyster Ostrea angasi. Mar Biol 163:17
Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315
Cripps IL, Munday PL, Mccormick MI (2011) Ocean acidification affects prey detection by a predatory reef fish. PLoS One 6:E22736
Davis MB, Shaw RG, Etterson JR (2005) Evolutionary responses to changing climate. Ecology 86:1704–1714
Devine BM, Munday PL, Jones GP (2012) Homing ability of adult cardinalfish is affected by elevated carbon dioxide. Oecologia 168:269–276
Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929
Dixson DL, Munday PL, Jones GP (2010) Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol Lett 13:68–75
Domenici P, Allan B, Mccormick MI, Munday PL (2012) Elevated carbon dioxide affects behavioural lateralization in a coral reef fish. Biol Lett 8:78–81
Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192
Dupont S, Ortega-Martinez O, Thorndyke M (2010) Impact of near-future ocean acidification on echinoderms. Ecotoxicology 19:449–462
Duvernell DD, Lindmeier JB, Faust KE, Whitehead A (2008) Relative influences of historical and contemporary forces shaping the distribution of genetic variation in the Atlantic killifish, Fundulus heteroclitus. Mol Ecol 17:1344–1360
Ejbye-Ernst R, Michaelsen TY, Tirsgaard B, Wilson JM, Jensen LF, Steffensen JF, Pertoldi C, Aarestrup K, Svendsen JC (2016) Partitioning the metabolic scope: the importance of anaerobic metabolism and implications for the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis. Conserv Physiol 4:13
Eliason EJ, Clark TD, Hague MJ, Hanson LM, Gallagher ZS, Jeffries KM, Gale MK, Patterson DA, Hinch SG, Farrell AP (2011) Differences in thermal tolerance among sockeye salmon populations. Science 332:109–112
Engle VD, Summers JK, Macauley JM (1999) Dissolved oxygen conditions in northern Gulf of Mexico estuaries. Environ Monit Assess 57:1–20
Ern R, Norin T, Gamperl AK, Esbaugh AJ (2016) Oxygen dependence of upper thermal limits in fishes. J Exp Biol 219:3376–3383
Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177
Everett MV, Crawford DL (2010) Adaptation versus allometry: population and body mass effects on hypoxic metabolism in Fundulus grandis. Physiol Biochem Zool 83:182–190
Fangue NA, Hofmeister M, Schulte PM (2006) Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. J Exp Biol 209:2859–2872
Farrell AP (2009) Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids. J Exp Biol 212:3771–3780
Farrell AP (2016) Pragmatic perspective on aerobic scope: peaking, plummeting, pejus and apportioning. J Fish Biol 88:322–343
Farrell AP, Eliason EJ, Sandblom E, Clark TD (2009) Fish cardiorespiratory physiology in an era of climate change. Can J Zool 87:835–851
Ferrari MCO, Manassa RP, Dixson DL, Munday PL, Mccormick MI, Meekan MG, Sih A, Chivers DP (2012) Effects of ocean acidification on learning in coral reef fishes. PLoS One 7:10
Forsgren E, Dupont S, Jutfelt F, Amundsen T (2013) Elevated CO2 affects embryonic development and larval phototaxis in a temperate marine fish. Ecol Evol 3:3637–3646
Frommel AY, Schubert A, Piatkowski U, Clemmesen C (2013) Egg and early larval stages of Baltic cod, Gadus morhua, are robust to high levels of ocean acidification. Mar Biol 160:1825–1834
Fuller A, Dawson T, Helmuth B, Hetem RS, Mitchell D, Maloney SK (2010) Physiological mechanisms in coping with climate change. Physiol Biochem Zool 83:713–720
Gamperl AK, Farrell AP (2004) Cardiac plasticity in fishes: environmental influences and intraspecific differences. J Exp Biol 207:2539–2550
Gobler CJ, Baumann H (2016) Hypoxia and acidification in ocean ecosystems: coupled dynamics and effects on marine life. Biol Lett 12:8
Gobler CJ, Depasquale EL, Griffith AW, Baumann H (2014) Hypoxia and acidification have additive and synergistic negative effects on the growth, survival, and metamorphosis of early life stage bivalves. PLoS One 9:E83648
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 8:357–378
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 3:1016–1030
Hassell KL, Coutin PC, Nugegoda D (2008) Hypoxia impairs embryo development and survival in black bream (Acanthopagrus butcheri). Mar Pollut Bull 57:302–306
Healy TM, Schulte PM (2012) Thermal acclimation is not necessary to maintain a wide thermal breadth of aerobic scope in the common killifish (Fundulus heteroclitus). Physiol Biochem Zool 85:107–119
Helmuth B (2009) From cells to coastlines: how can we use physiology to forecast the impacts of climate change? J Exp Biol 212:753–760
Heuer RM, Grosell M (2014) Physiological impacts of elevated carbon dioxide and ocean acidification on fish. Am J Phys Regul Integr Comp Phys 307:R1061–R1084
Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York
Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485
Holmstrup M, Bindesbol AM, Oostingh GJ, Duschl A, Scheil V, Kohler HR, Loureiro S, Soares A, Ferreira ALG, Kienle C, Gerhardt A, Laskowski R, Kramarz PE, Bayley M, Svendsen C, Spurgeon DJ (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408:3746–3762
Houde ED (1989) Subtleties and episodes in the early life of fishes. J Fish Biol 35:29–38
IPCC (2014) Climate change 2014: synthesis report. In: Pachauri RK, Meyer LA (eds) Contribution of working groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland
Ivanina AV, Sokolova IM (2016) Effects of intermittent hypoxia on oxidative stress and protein degradation in molluscan mitochondria. J Exp Biol 219:3794–3802
Jorgensen LB, Macmillan HA, Overgaard J (2017) Cold mortality is not caused by oxygen limitation or loss of ion homeostasis in the tropical freshwater shrimp macrobrachium rosenbergii. Cryobiology 76:146–149
Jump AS, Penuelas J (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett 8:1010–1020
Kassahn KS, Crozier RH, Portner HO, Caley MJ (2009) Animal performance and stress: responses and tolerance limits at different levels of biological organisation. Biol Rev 84:277–292
Krebs HA (1975) The August Krogh principle: “for many problems there is an animal on which it can be most conveniently studied”. J Exp Zool 194:221–226
Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso J-P (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Chang Biol 19:1884–1896
Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434
Lockwood BL, Sanders JG, Somero GN (2010) Transcriptomic responses to heat stress in invasive and native blue mussels (genus Mytilus): molecular correlates of invasive success. J Exp Biol 213:3548–3558
Lockwood BL, Somero GN (2011) Transcriptomic responses to salinity stress in invasive and native blue mussels (genus Mytilus). Mol Ecol 20:517–529
Mahony CR, Cannon AJ, Wang TL, Aitken SN (2017) A closer look at novel climates: new methods and insights at continental to landscape scales. Glob Chang Biol 23:3934–3955
Marshall WS, Grosell M (2005) Ion transport, osmoregulation, and acid-base balance. In: Evans DH, Claiborne JB (eds) Physiology of fishes. CRC Press, Boca Raton
Martins EG, Hinch SG, Patterson DA, Hague MJ, Cooke SJ, Miller KM, Lapointe MF, English KK, Farrell AP (2011) Effects of river temperature and climate warming on stock-specific survival of adult migrating Fraser River sockeye salmon (Oncorhynchus nerka). Glob Chang Biol 17:99–114
Melzner F, Gobel S, Langenbuch M, Gutowska MA, Portner HO, Lucassen M (2009) Swimming performance in Atlantic Cod (Gadus morhua) following long-term (4–12 months) acclimation to elevated seawater PCO2. Aquat Toxicol 92:30–37
Melzner F, Gutowska MA, Langenbuch M, Dupont S, Lucassen M, Thorndyke MC, Bleich M, Pörtner HO (2009) Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6:2313–2331
Mu J, Jin F, Wang JY, Zheng N, Cong Y (2015) Effects of CO2-driven ocean acidification on early life stages of marine medaka (Oryzias melastigma). Biogeosciences 12(12):3861–3868. https://doi.org/10.5194/Bg-12-3861-2015
Munday PL, Crawley NE, Nilsson GE (2009) Interacting effects of elevated temperature and ocean acidification on the aerobic performance of coral reef fishes. Mar Ecol Prog Ser 388:235–242
Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS, Devitsina GV, Doving KB (2009) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc Natl Acad Sci 106:1848–1852
Murray CS, Fuiman LA, Baumann H (2016) Consequences of elevated CO2 exposure across multiple life stages in a coastal forage fish. ICES J Mar Sci 74:1051
Mykles DL, Ghalambor CK, Stillman JH, Tomanek L (2010) Grand challenges in comparative physiology: integration across disciplines and across levels of biological organization. Integr Comp Biol 50:6–16
Nilsson GE, Dixson DL, Domenici P, Mccormick MI, Sorensen C, Watson S-A, Munday PL (2012) Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat Clim Chang 2:201–204
Nordlie FG (2006) Physicochemical environments and tolerances of cyprinodontoid fishes found in estuaries and salt marshes of eastern North America. Rev Fish Biol Fish 16:51–106
Norin T, Malte H, Clark TD (2014) Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures. J Exp Biol 217:244–251
Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner G-K, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig M-F, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686
Payan P, Edeyer A, De Pontual H, Borelli G, Boeuf G, Mayer-Gostan N (1999) Chemical composition of saccular endolymph and otolith in fish inner ear: lack of spatial uniformity. Am J Phys Regul Integr Comp Phys 277:R123–R131
Payan P, Kossmann H, Watrin A, Mayer-Gostan N, Boeuf G (1997) Ionic composition of endolymph in teleosts: origin and importance of endolymph alkalinity. J Exp Biol 200:1905–1912
Pelster B (2002) Developmental plasticity in the cardiovascular system of fish, with special reference to the zebrafish. Comp Biochem Physiol A Mol Integr Physiol 133:547–553
Perry SF, Gilmour KM (2006) Acid-base balance and CO2 excretion in fish: unanswered questions and emerging models. Respir Physiol Neurobiol 154:199–215
Pimentel MS, Faleiro F, Dionisio G, Repolho T, Pousao-Ferreira P, Machado J, Rosa R (2014) Defective skeletogenesis and oversized otoliths in fish early stages in a changing ocean. J Exp Biol 217:2062–2070
Portner HO (2010) Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213:881–893
Pörtner H-O, Bock C, Mark FC (2017) Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology. J Exp Biol 220:2685–2696
Pörtner HO, Farrell AP (2008) Ecology physiology and climate change. Science 322:690–692
Portner HO, Farrell AP, Knust R, Lannig G, Mark FC, Storch D (2009) Adapting to climate change response. Science 323:876–877
Portner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97
Pörtner HO, Langenbuch M, Michaelidis B (2005) Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: from earth history to global change. J Geophys Res Oceans 110:C09s10
Portner HO, Peck MA (2010) Climate change effects on fishes and fisheries: towards a cause-and-effect understanding. J Fish Biol 77:1745–1779
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 Chang Biol 21:2122–2140
Rankin PS, Hannah RW, Blume MTO (2013) Effect of hypoxia on rockfish movements: implications for understanding the roles of temperature, toxins and site fidelity. Mar Ecol Prog Ser 492:223–234
Regan MD, Turko AJ, Heras J, Andersen MK, Lefevre S, Wang T, Bayley M, Brauner CJ, Huong DTT, Phuong NT, Nilsson GE (2016) Ambient CO2, fish behaviour and altered GABAergic neurotransmission: exploring the mechanism of CO2-altered behaviour by taking a hypercapnia dweller down to low CO2 levels. J Exp Biol 219:109–118
Reid NM, Proestou DA, Clark BW, Warren WC, Colbourne JK, Shaw JR, Karchner SI, Hahn ME, Nacci D, Oleksiak MF, Crawford DL, Whitehead A (2016) The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science 354:1305–1308
Richards JG (2011) Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia. J Exp Biol 214:191–199
Ries JB (2010) Geological and experimental evidence for secular variation in seawater Mg/Ca (calcite-aragonite seas) and its effects on marine biological calcification. Biogeosciences 7:2795–2849
Rogers NJ, Urbina MA, Reardon EE, Mckenzie DJ, Wilson RW (2016) A new analysis of hypoxia tolerance in fishes using a database of critical oxygen level (P crit). Conserv Physiol 4:Cow012
Rombough P (2007) The functional ontogeny of the teleost gill: which comes first, gas or ion exchange? Comp Biochem Physiol A Mol Integr Physiol 148:732–742
Scavia D, Bertani I, Obenour DR, Turner RE, Forrest DR, Katin A (2017) Ensemble modeling informs hypoxia management in the northern Gulf of Mexico. Proc Natl Acad Sci 114:8823–8828
Schade FM, Clemmesen C, Wegner KM (2014) Within- and transgenerational effects of ocean acidification on life history of marine three-spined stickleback (Gasterosteus aculeatus). Mar Biol 161:1667–1676
Schloss CA, Nuñez TA, Lawler JJ (2012) Dispersal will limit ability of mammals to track climate change in the western hemisphere. Proc Natl Acad Sci 109:8606–8611
Schulte PM (2014) What is environmental stress? Insights from fish living in a variable environment. J Exp Biol 217:23–34
Schwenk K, Padilla DK, Bakken GS, Full RJ (2009) Grand challenges in organismal biology. Integr Comp Biol 49:7–14
Scott GR, Rogers JT, Richards JG, Wood CA, Schulte PM (2004) Intraspecific divergence of ionoregulatory physiology in the euryhaline teleost Fundulus heteroclitus: possible mechanisms of freshwater adaptation. J Exp Biol 207:3399–3410
Seibel BA, Maas AE, Dierssen HM (2012) Energetic plasticity underlies a variable response to ocean acidification in the pteropod, Limacina helicina antarctica. PLoS One 7:E30464
Selye H (1936) A syndrome produced by diverse nocuous agents. Nature 138:32–33
Simpson SD, Munday PL, Wittenrich ML, Manassa R, Dixson DL, Gagliano M, Yan HY (2011) Ocean acidification erodes crucial auditory behaviour in a marine fish. Biol Lett 7:917–920
Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J Exp Biol 213:912–920
Somero GN (2011) Comparative physiology: a “crystal ball” for predicting consequences of global change. Am J Phys Regul Integr Comp Phys 301:R1–R14
Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65–65
Stillman JH, Somero GN (2000) A comparative analysis of the upper thermal tolerance limits of eastern Pacific porcelain crabs, genus Petrolisthes: influences of latitude, vertical zonation, acclimation, and phylogeny. Physiol Biochem Zool 73:200–208
Talmage SC, Gobler CJ (2010) Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. Proc Natl Acad Sci 107:17246–17251
Tomanek L, Zuzow MJ (2010) The proteomic response of the mussel congeners Mytilus galloprovincialis and M. trossulus to acute heat stress: implications for thermal tolerance limits and metabolic costs of thermal stress. J Exp Biol 213:3559–3574
Tresguerres M, Hamilton TJ (2017) Acid–base physiology, neurobiology and behaviour in relation to CO2-induced ocean acidification. J Exp Biol 220:2136–2148
Uthicke S, Momigliano P, Fabricius KE (2013) High risk of extinction of benthic foraminifera in this century due to ocean acidification. Sci Rep 3:1769
Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci 105:15452–15457
Virani NA, Rees BB (2000) Oxygen consumption, blood lactate and inter-individual variation in the gulf killifish, Fundulus grandis, during hypoxia and recovery. Comp Biochem Physiol A Physiol 126:397–405
Whitehead A (2010) The evolutionary radiation of diverse osmotolerant physiologies in killifish (Fundulus sp.) Evolution 64:2070–2085
Whitehead A, Galvez F, Zhang SJ, Williams LM, Oleksiak MF (2011) Functional genomics of physiological plasticity and local adaptation in killifish. J Hered 102:499–511
Whitehead A, Pilcher W, Champlin D, Nacci D (2012) Common mechanism underlies repeated evolution of extreme pollution tolerance. Proc R Soc Lond B Biol Sci 279:427–433
Whitehead A, Roach JL, Zhang S, Galvez F (2011) Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient. Proc Natl Acad Sci 108:6193–6198
Whitehead A, Roach JL, Zhang SJ, Galvez F (2012) Salinity- and population-dependent genome regulatory response during osmotic acclimation in the killifish (Fundulus heteroclitus) gill. J Exp Biol 215:1293–1305
Whitehead A, Zhang S, Roach JL, Galvez F (2013) Common functional targets of adaptive micro- and macro-evolutionary divergence in killifish. Mol Ecol 22:3780–3796
Whiteley NM (2011) Physiological and ecological responses of crustaceans to ocean acidification. Mar Ecol Prog Ser 430:257
Williams DA, Brown SD, Crawford DL (2008) Contemporary and historical influences on the genetic structure of the estuarine-dependent gulf killifish Fundulus grandis. Mar Ecol Prog Ser 373:111–121
Wolanski E (2007) Estuarine ecohydrology. Elsevier, Amsterdam
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Galvez, F. (2018). Physiological and Genomic Mechanisms of Resilience to Multiple Environmental Stressors. In: Burggren, W., Dubansky, B. (eds) Development and Environment. Springer, Cham. https://doi.org/10.1007/978-3-319-75935-7_8
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