Climate Action

Living Edition
| Editors: Walter Leal Filho, Anabela Marisa Azul, Luciana Brandli, Pinar Gökcin Özuyar, Tony Wall

Climate Change, Multiple Stressors, and Responses of Marine Biota

  • Eduardo SampaioEmail author
  • Rui Rosa
Living reference work entry



Human-exacerbated emissions of greenhouse gases and nutrients are creating a multitude of chemical, physical, and biological stressors, disrupting the natural equilibrium within individual homeostasis, multi-species communities, and entire ecosystems.


Climate change is ongoing and will be further aggravated if greenhouse gas emissions, and other anthropogenic pressures, remain unabated (IPCC 2013). Such scenario will imply a marked change on several abiotic parameters caused by said gases, with a special highlight for carbon dioxide (CO2), which constitutes the majority of anthropogenic emissions. These abiotic alterations occur in all physical realms on the planet, with the oceans and the life they sustain being threatened by multiple fronts. Coined as “the deadly trio,” climate change is expressed via three main stressors in the...

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The authors, and the work for producing this entry, were funded by PTDC/BIA-BMA/28317/2017, PTDC/AAG-GLO/1926/2014, and MAR-01.04.02-FEAMP-0007.


  1. Altieri AH, Harrison SB, Seemann J, Collin R, Diaz RJ, Knowlton N (2017) Tropical dead zones and mass mortalities on coral reefs. Proc Natl Acad Sci 114:3660–3665. Scholar
  2. Angilletta M (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, OxfordCrossRefGoogle Scholar
  3. Anthony KRN, Maynard JA, Diaz-Pulido G, Mumby PJ, Marshall PA, Cao L, Hoegh-Guldberg O (2011) Ocean acidification and warming will lower coral reef resilience. Glob Chang Biol 17:1798–1808. Scholar
  4. Arias-Ortiz A, Serrano O, Masqué P, Lavery PS, Mueller U, Kendrick GA, Rozaimi M, Esteban A, Fourqurean JW, Marbà N, Mateo MA, Murray K, Rule MJ, Duarte CM (2018) A marine heatwave drives massive losses from the world’s largest seagrass carbon stocks. Nat Clim Chang 8:1–7. Scholar
  5. Beaugrand G, Mcquatters-Gollop A, Edwards M, Goberville E (2013) Long-term responses of North Atlantic calcifying plankton to climate change. Nat Clim Chang 3:263–267. Scholar
  6. Bell JJ, Davy SK, Jones T, Taylor MW, Webster NS (2013) Could some coral reefs become sponge reefs as our climate changes? Glob Chang Biol 19:2613–2624. Scholar
  7. Breitburg D, Levin LA, Oschlies A, Grégoire M, Chavez FP, Conley DJ, Garçon V, Gilbert D, Gutiérrez D, Isensee K, Jacinto GS, Limburg KE, Montes I, Naqvi SWA, Pitcher GC, Rabalais NN, Roman MR, Rose KA, Seibel BA, Telszewski M, Yasuhara M, Zhang J (2018) Declining oxygen in the global ocean and coastal waters. Science 359:eaam7240. Scholar
  8. Chan F, Barth JA, Lubchenco J, Kirincich A, Weeks H, Peterson WT, Menge BA (2008) Emergence of anoxia in the California current large marine ecosystem. Science 319:920. Scholar
  9. Connell SD, Russell BD (2010) The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc Biol Sci 277:1409–1415. Scholar
  10. Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929. Scholar
  11. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Chang 1:165–169. Scholar
  12. Frazão-Santos C, Agardy T, Andrade F, Barange M, Crowder LB, Ehler CN, Orbach MK, Rosa R (2016) Ocean planning in a changing climate. Nat Geosci 9:730. Scholar
  13. Frommel AY, Maneja R, Lowe D, Malzahn AM, Geffen AJ, Folkvord A, Piatkowski U, Reusch TBH, Clemmesen C (2011) Severe tissue damage in Atlantic cod larvae under increasing ocean acidification. Nat Clim Chang 2:42–46. Scholar
  14. Gobler CJ, Baumann H (2016) Hypoxia and acidification in ocean ecosystems: coupled dynamics and effects on marine life. Biol Lett 12:20150976. Scholar
  15. Goldenberg SU, Nagelkerken I, Marangon E, Bonnet A, Camilo M (2018) Ecological complexity buffers the impacts of future climate on marine animals. Nat Clim Chang 8:1–19Google Scholar
  16. Grantham BA, Chan F, Nielsen KJ, Fox DS, Barth JA, Huyer A, Lubchenco J, Menge BA (2004) Upwelling-driven nearshore hypoxia signals ecosystem and oceanographic changes in the Northeast Pacific. Nature 429:749–754. Scholar
  17. Hepburn CD, Pritchard DW, Cornwall CE, Mcleod RJ, Beardall J, Raven JA, Hurd CL (2011) Diversity of carbon use strategies in a kelp forest community: implications for a high CO2 ocean. Glob Chang Biol 17:2488–2497. Scholar
  18. Heuer RM, Grosell M (2014) Physiological impacts of elevated carbon dioxide and ocean acidification on fish. AJP Regul Integr Comp Physiol 307:R1061–R1084. Scholar
  19. Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Liu G, McWilliam MJ, Pears RJ, Pratchett MS, Skirving WJ, Stella JS, Torda G (2018) Global warming transforms coral reef assemblages. Nature 556:492–496. Scholar
  20. IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, UK/New YorkAGoogle Scholar
  21. Keeling RF, Körtzinger A, Gruber N (2010) Ocean deoxygenation in a warming world. Annu Rev Mar Sci 2:199–229. Scholar
  22. Kingsolver JG (2009) The well-temperatured biologist. Am Nat 174:755–768. Scholar
  23. 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. Scholar
  24. Kroeker KJ, Micheli F, Gambi MC (2012) Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat Clim Chang 3:156–159. Scholar
  25. Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso JP (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Chang Biol 19:1884–1896. Scholar
  26. Kwiatkowski L, Cox P, Halloran PR, Mumby PJ, Wiltshire AJ (2015) Coral bleaching under unconventional scenarios of climate warming and ocean acidification. Nat Clim Chang 5:777–781. Scholar
  27. Levin LA, Breitburg DL (2015) Linking coasts and seas to address ocean deoxygenation. Nat Clim Chang 5:401–403. Scholar
  28. Levin LA, Bris NL (2015) The deep ocean under climate change. Science 350:766–768. Scholar
  29. Levin LA, Ekau W, Gooday AJ, Jorissen F, Middelburg JJ, Naqvi SWA, Neira C, Rabalais NN, Zhang J (2009) Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences 6:2063–2098. Scholar
  30. Lima FP, Wethey DS (2012) Three decades of high-resolution coastal sea surface temperatures reveal more than warming. Nat Commun 3:1–13. Scholar
  31. Lopes AR, Sampaio E, Santos C, Couto A, Pegado MR, Diniz M, Munday PL, Rummer JL, Rosa R (2018) Absence of cellular damage in tropical newly hatched sharks (Chiloscyllium plagiosum) under ocean acidification conditions. Cell Stress Chaperones 23(5):837–846CrossRefGoogle Scholar
  32. Meehl GA et al (2007) Global climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK, pp 747–845Google Scholar
  33. Melzner F, Thomsen J, Koeve W, Oschlies A, Gutowska MA, Bange HW, Hansen HP, Kortzinger A (2013) Future ocean acidification will be amplified by hypoxia in coastal habitats. Mar Biol 160:1875–1888. Scholar
  34. Mertens N, Russell B, Connell S (2015) Escaping herbivory: ocean warming as a refuge for primary producers where consumer metabolism and consumption cannot pursue. Oecologia 173:1223–1229. Scholar
  35. Munday PL, Cheal AJ, Dixson DL, Rummer JL, Fabricius KE (2014) Behavioural impairment in reef fishes caused by ocean acidification at CO2 seeps. Nat Clim Chang 4:487–492. Scholar
  36. Nilsson GE, Dixson DL, Domenici P, Mccormick MI, Sørensen C, Watson S, Munday PL (2012) Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat Clim Chang 2:201–204. Scholar
  37. O’Connor MI (2009) Warming strengthens an herbivore-plant interaction. Ecology 90:388–398. Scholar
  38. Oliver ECJ, Donat MG, Burrows MT, Moore PJ, Smale DA, Alexander LV, Benthuysen JA, Feng M, Sen Gupta A, Hobday AJ, Holbrook NJ, Perkins-Kirkpatrick SE, Scannell HA, Straub SC, Wernberg T (2018) Longer and more frequent marine heatwaves over the past century. Nat Commun 9:1–12. Scholar
  39. Pimentel MS, Faleiro F, Diniz M, Machado J, Pousão-Ferreira P, Peck MA, Pörtner HO, Rosa R (2015) Oxidative stress and digestive enzyme activity of flatfish larvae in a changing ocean. PLoS One 10:1–18. Scholar
  40. Pörtner H-O, Farrell AP (2008) Physiology and climate change. Science 322:690–692CrossRefGoogle Scholar
  41. Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–98. Scholar
  42. Prince ED, Goodyear CP (2006) Hypoxia-based habitat compression of tropical pelagic fishes. Fish Oceanogr 15:451–464. Scholar
  43. Prince ED, Luo J, Phillip Goodyear C, Hoolihan JP, Snodgrass D, Orbesen ES, Serafy JE, Ortiz M, Schirripa MJ (2010) Ocean scale hypoxia-based habitat compression of Atlantic istiophorid billfishes. Fish Oceanogr 19:448–462. Scholar
  44. Queirós AM, Fernandes JA, Faulwetter S, Nunes J, Rastrick SPS, Mieszkowska N, Artioli Y, Yool A, Calosi P, Arvanitidis C, Findlay HS, Barange M, Cheung WWL, Widdicombe S (2015) Scaling up experimental ocean acidification and warming research: from individuals to the ecosystem. Glob Chang Biol 21:130–143. Scholar
  45. Queiroz N, Humphries NE, Mucientes G, Hammerschlag N, Lima FP, Scales KL, Miller PI, Sousa LL, Seabra R, Sims DW (2016) Ocean-wide tracking of pelagic sharks reveals extent of overlap with longline fishing hotspots. Proc Natl Acad Sci 113:1582–1587. Scholar
  46. Repolho T, Duarte B, Dionísio G, Paula JR, Lopes AR, Rosa IC, Grilo TF, Caçador I, Calado R, Rosa R (2017) Seagrass ecophysiological performance under ocean warming and acidification. Sci Rep 7:41443. Scholar
  47. Riebesell U, Gattuso J-P (2015) Lessons learned from ocean acidification research. Nat Clim Chang 5:12–14. Scholar
  48. Rosa R, Seibel BA (2008) Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator. Proc Natl Acad Sci 105:20776–20780. Scholar
  49. Rosa R, Pimentel MS, Boavida-Portugal J, Teixeira T, Trübenbach K, Diniz M (2012) Ocean warming enhances malformations, premature hatching, metabolic suppression and oxidative stress in the early life stages of a keystone squid. PLoS One 7:e38282–e38282CrossRefGoogle Scholar
  50. Rosa R, Trübenbach K, Repolho T, Pimentel M, Faleiro F, Boavida-Portugal J, Baptista M, Lopes VM, Dionísio G, Leal MC, Calado R, Pörtner HO (2013) Lower hypoxia thresholds of cuttlefish early life stages living in a warm acidified ocean. Proc Biol Sci 280:20131695. Scholar
  51. Rosa R, Paula JR, Sampaio E, Pimentel M, Lopes AR, Baptista M, Guerreiro M, Santos C, Campos D, Almeida-Val VMF, Calado R, Diniz M, Repolho T (2016) Neuro-oxidative damage and aerobic potential loss of sharks under elevated CO2 and warming. Mar Biol 163.
  52. Rosa R, Rummer JL, Munday PL (2017) Biological responses of sharks to ocean acidification. Biol Lett 13:20160796. Scholar
  53. Sampaio E, Maulvault AL, Lopes VM, Paula JR, Barbosa V, Alves R, Pousão-Ferreira P, Repolho T, Marques A, Rosa R (2016) Habitat selection disruption and lateralization impairment of cryptic flatfish in a warm, acid, and contaminated ocean. Mar Biol 163:1–10. Scholar
  54. Sampaio E, Rodil IF, Vaz-Pinto F, Fernández A, Arenas F (2017) Interaction strength between different grazers and macroalgae mediated by ocean acidification over warming gradients. Mar Environ Res 125:25–33. Scholar
  55. Sampaio E, Lopes AR, Francisco S, Paula JR, Pimentel M, Maulvault AL, Repolho T, Grilo TF, Pousão-Ferreira P, Marques A, Rosa R (2018) Ocean acidification dampens physiological stress response to warming and contamination in a commercially-important fish (Argyrosomus regius). Sci Total Environ 618:388–398. Scholar
  56. Seibel BA, Hafker NS, Trubenbach K, Zhang J, Tessier SN, Portner H-O, Rosa R, Storey KB (2014) Metabolic suppression during protracted exposure to hypoxia in the jumbo squid, Dosidicus gigas, living in an oxygen minimum zone. J Exp Biol 217:2555–2568. Scholar
  57. Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65. Scholar
  58. Stramma L, Prince ED, Schmidtko S, Luo J, Hoolihan JP, Visbeck M, Wallace DWR, Brandt P, Körtzinger A (2012) Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes. Nat Clim Chang 2:33–37. Scholar
  59. Tewksbury JJ, Huey RB, Deutsch CA (2008) Putting the heat on tropical animals. Science 320:1296–1297CrossRefGoogle Scholar
  60. Van Hooidonk R, Maynard JA, Planes S (2013) Temporary refugia for coral reefs in a warming world. Nat Clim Chang 3:508–511. Scholar
  61. Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci 105:15452–15457. Scholar
  62. Vaquer-Sunyer R, Duarte CM (2011) Temperature effects on oxygen thresholds for hypoxia in marine benthic organisms. Glob Chang Biol 17:1788–1797. Scholar
  63. Wernberg T, Russell B, Moore P (2011) Impacts of climate change in a global hotspot for temperate marine biodiversity and ocean warming. J Exp Mar Bio Ecol 400:7–16. Scholar
  64. Wittmann AC, Pörtner HO (2013) Sensitivities of extant animal taxa to ocean acidification. Nat Clim Chang 3:995–1001. Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.MARE – Marine Environmental Sciences Centre & Laboratório Marítimo da Guia, Faculdade de CiênciasUniversidade de LisboaCascaisPortugal

Section editors and affiliations

  • Ulisses Azeiteiro
    • 1
  1. 1.University of AveiroAveiroPortugal