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Marine Biology

, 167:17 | Cite as

Thermal performance of the European flat oyster, Ostrea edulis (Linnaeus, 1758)—explaining ecological findings under climate change

  • Charlotte Eymann
  • Sandra Götze
  • Christian Bock
  • Helga Guderley
  • Andrew H. Knoll
  • Gisela Lannig
  • Inna M. Sokolova
  • Martin Aberhan
  • Hans-O. PörtnerEmail author
Original Paper

Abstract

Climate change challenges marine organisms by constraining their temperature-dependent scope for performance, fitness, and survival. According to the concept of Oxygen and Capacity Limited Thermal Tolerance (OCLTT), the overall thermal performance curve relates to an organism’s aerobic power budget, its overall aerobic scope for growth, exercise, reproduction, and other performances. We hypothesize that physiological principles shaping tolerance in extant ecosystems have also been operative during climatic changes in the distant past. To compare response patterns in extant fauna and their palaeo-relatives, we started here by studying the metabolic background of performance in the European flat oyster Ostrea edulis at organismic and cellular levels, focusing on the acute thermal window and the metabolic changes towards upper lethal temperatures. We investigated the response of the oysters (pre-acclimated at 12 °C) to a short-term warming protocol (by 2 °C every 48 h) from 14 to 36 °C which we identified as the lethal temperature. At the organismic level, heart and filtration rates were recorded. Gill metabolites were studied by 1H NMR spectroscopy to address thermal responses at the cellular level. Feeding activity by O. edulis (assessed by the filtration rates) was highest between 18 and 24 °C when overall energy expenditure (indicated by heart rate as a proxy for routine metabolic rate) was moderate. We conclude that this range reflects the thermal optimum of this species. Beyond 26 °C, the gill tissue of O. edulis became partly anaerobic, and cardiac dysfunction (arrhythmia) developed at 28 °C followed by an Arrhenius break point (30 °C). This mirrors performance constraints and indicates a wide temperature range of passive tolerance which may be a long-standing characteristic of ostreids supporting survival in extreme environments as well as during past and present climate oscillations.

Notes

Acknowledgements

This study was funded by the Deutsche Forschungsgemeinschaft (DFG Po278/16-1) and is embedded in the Research Unit TERSANE (FOR 2332: Temperature‐related stressors as a unifying principle in ancient extinctions). We thank I. Ketelsen, F. Feliz Moraleda, and R. Gorniak for technical support and assistance during the exposures and animal care. Furthermore, we want to thank the section Marine BioGeoScience, in particular S. Trimborn, A. Terbrüggen and T. Brenneis for providing access to the Coulter Counter and the Observer microscope. We thank the Biological station of Toralla (ECIMAT, Spain), in particular A.Villanueva and D. Costas for support in animal supply.

Compliance with ethical standards

This study was funded by the Deutsche Forschungsgemeinschaft (DFG Po278/16-1).

Conflict of interest

Authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Anestis A, Lazou A, Pörtner H-O, Michaelidis B (2007) Behavioral, metabolic, and molecular stress response of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature. Am J Physiol Regul Integr Comp Physiol 293:911–921.  https://doi.org/10.1152/ajpregu.00124.2007 CrossRefGoogle Scholar
  2. Artigaud S, Lacroic C, Pichereau V, Flye-Sainte-Marie J (2014) Respiratory response to combined heat and hypoxia in the marine bivalves Pecten maximus and Mytilis spp. Comp Biochem Physiol A 175:135–140.  https://doi.org/10.1016/j.cbpa.2014.06.005 CrossRefGoogle Scholar
  3. Bakhmet IN (2017) Cardiac activity and oxygen consumption of the blue mussel (Mytilus edulis) from the White Sea in relation to body mass, ambient temperature and food availability. Polar Biol 40:1959–1964.  https://doi.org/10.1007/s00300-017-2111-6 CrossRefGoogle Scholar
  4. Bambach RK, Knoll AH, Wang SC (2004) Origination, extinction, and mass depletions of marine diversity. Paleobiology 30:522–542.  https://doi.org/10.1666/0094-8373(2004)030%3c0522:OEAMDO%3e2.0.CO;2 CrossRefGoogle Scholar
  5. Bertolino M, Betti F, Bo M, Cattaneo-Vietti R, Pansini M, Romero J, Bavestrello G (2015) Changes and stability of a Mediterranean hard bottom benthic community over 25 years. J Mar Biol Assoc UK 96:341–350.  https://doi.org/10.1017/S0025315415001186 CrossRefGoogle Scholar
  6. Beukema JJ, Dekker R, Jansen JM (2009) Some like it cold: populations of the tellinid bivalve Macoma balthica (L.) suffer in various ways from a warming climate. Mar Ecol Prog Ser 384:135–145.  https://doi.org/10.3354/meps07952 CrossRefGoogle Scholar
  7. Bode A, Álvarez-Ossorio T, González N, Lorenzo J, Rodríguez C, Varela M, Varela MM (2005) Seasonal variability of plankton blooms in the Ria de Ferrol (NW Spain): II. Plankton abundance, composition and biomass. Estuar Coast Shelf Sci 63:285–300.  https://doi.org/10.1016/j.ecss.2004.11.021 CrossRefGoogle Scholar
  8. Braby CE, Somero GN (2006) Following the heart: temperature and salinity effects on heart rate in native and invasive species of blue mussels (genus Mytilus). J Exp Biol 209:2554–2566.  https://doi.org/10.1242/jeb.02259 CrossRefPubMedGoogle Scholar
  9. Brinkhoff W, Stöckmann K, Grieshaber M (1983) Natural occurence of anaerobiosis in molluscs from intertidal habitats. Oecol 57:151–155.  https://doi.org/10.1007/BF00379573 CrossRefGoogle Scholar
  10. Buxton CD, Newell RC, Field JG (1981) Response-surface analysis of the combined effects of exposure and acclimation temperatures on filtration, oxygen consumption and scope for growth in the oyster Ostrea edulis. Mar Ecol Prog Ser 6:73–82.  https://doi.org/10.3354/meps006073 CrossRefGoogle Scholar
  11. Calosi P, De Witt P, Thor P, Dupont S (2016) Will life find a way? Evolution of marine species under global change. Evol Appl 9:1035–1042.  https://doi.org/10.1111/eva.12418 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cattaneo-Vietti R (2018) Structural changes in Mediterranean marine communities: lessons from the Ligurian Sea. Rend Fis Acc Lincei 29:515–524.  https://doi.org/10.1007/s12210-018-0670-2 CrossRefGoogle Scholar
  13. Coughlan J (1969) The estimation of filtering rate from the clearance of suspensions. Mar Biol 2(4):356–358CrossRefGoogle Scholar
  14. De Zwaan A, Wijsmann TCM (1976) Anaerobic metabolism in bivalvia (mollusca)—characteristics of anaerobic metabolism. Comp Biochem Physiol B 54:313–324.  https://doi.org/10.1016/0305-0491(76)90247-9 CrossRefPubMedGoogle Scholar
  15. Depledge M, Andersen B (1990) A computer-aided physiological monitoring system for continuous, long-term recording of cardiac activity in selected invertebrates. Comp Biochem Physiol A 96:473–477.  https://doi.org/10.1016/0300-9629(90)90664-E CrossRefGoogle Scholar
  16. Dickson AG (1990) Standard potential of the (AgCl(s) + 1/2H2(g) = Ag(s) + HCl(aq)) cell and the dissociation constant of bisulfate ion in synthetic sea water from 273.15 to 318.15 K. J Chem Thermodyn 22:113–127CrossRefGoogle Scholar
  17. Domnik NJ, Polymeropoulos ET, Elliott NG, Frappell PB, Fisher JT (2016) Automated non-invasive video-microscopy of oyster spat heart rate during acute temperature change: impact of acclimation temperature. Front Physiol 7:236.  https://doi.org/10.3389/fphys.2016.00236 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Finnegan S, Anderson SC, Harnik PG, Simpson C, Tittensor DP, Byrnes JE, Finkel ZV, Lindberg DR, Liow LH, Lockwood R, Lotze HK, McClain CR, McGuire JL, O’Dea A, Pandolfi JM (2015) Paleontological baselines for evaluating extinction risk in the modern oceans. Science 348:567–570.  https://doi.org/10.1126/science.aaa6635 CrossRefPubMedGoogle Scholar
  19. Frederich M, Pörtner H-O (2000) Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am J Physiol Regul Integr Comp 279:R1531–R1538.  https://doi.org/10.1152/ajpregu.2000.279.5.R1531 CrossRefGoogle Scholar
  20. Garrabeu J, Coma R, Bensoussan N et al (2009) Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Global Change Biol 15:1090–1103.  https://doi.org/10.1111/j.1365-2486.2008.01823.x CrossRefGoogle Scholar
  21. Giomi F, Pörtner H-O (2013) A role for haemolymph oxygen capacity in heat tolerance of eurythermal crabs. Front Physiol 4:110.  https://doi.org/10.3389/fphys.2013.00110 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Götze S, Bock C, Eymann C, Lannig G, Steffen J, Pörtner H-O (2020) Single and combined effects of the “Deadly trio” hypoxia, hypercapnia and warming on the cellular metabolism of the great scallop Pecten maximus. Comp Biochem Physiol B (in review) Google Scholar
  23. Guderley H, Pörtner H-O (2010) Metabolic power budgeting and adaptive strategies in zoology: examples from scallops and fish. Can J Zool 88:753–763.  https://doi.org/10.1139/Z10-039 CrossRefGoogle Scholar
  24. Guo X, Li C, Wang H, Xu Z (2018) Diversity and evolution of oysters. J Shellfish Res 37:755–771.  https://doi.org/10.2983/035.037.0407 CrossRefGoogle Scholar
  25. Han G, Zhang S, Dong Y (2017) Anaerobic metabolism and thermal tolerance: the importance of opine pathways on survival of a gastropod after cardiac dysfunction. Integr Zool 12:361–370.  https://doi.org/10.1111/1749-4877.12229 CrossRefPubMedGoogle Scholar
  26. Haure J, Penisson C, Bougrier S, Baud J (1998) Influence of temperature on clearance and oxygen consumption rates of the flat oyster Ostrea edulis: determination of allometric coefficients. Aquaculture 169:211–224.  https://doi.org/10.1016/S0044-8486(98)00383-4 CrossRefGoogle Scholar
  27. Hicks DW, McMahon RF (2002) Respiratory responses to temperature and hypoxia in the nonindgenous Brown Mussel, Perna perna (Bivalvia. Mytilidae) from the Gulf of Mexico. J Exp Mar Biol Ecol 277:61–78.  https://doi.org/10.1016/S0022-0981(02)00276-9 CrossRefGoogle Scholar
  28. Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York, p 480 (ISBN 0‐195‐11702‐6) Google Scholar
  29. Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1524–1528.  https://doi.org/10.1126/science.1189930 CrossRefGoogle Scholar
  30. Joachimski MM, Lai X, Shen S, Jiang H, Luo G, Chen B, Chen J, Sun Y (2012) Climate warming in the latest Permian and the Permian-Triassic mass extinction. Geology 40:195–198.  https://doi.org/10.1130/G32707.1 CrossRefGoogle Scholar
  31. Jørgensen CB, Møhlenberg F, Sten-Knudsen O (1986) Nature of relation between ventilation and oxygen consumption in filter feeders. Mar Ecol Prog Ser 29:73–88.  https://doi.org/10.3354/meps029073 CrossRefGoogle Scholar
  32. Jørgensen CB, Larsen PS, Riisgård HU (1990) Effects of temperature on the mussel pump. Mar Ecol Prog Ser 64:89–97CrossRefGoogle Scholar
  33. Kittner C, Riisgård HU (2005) Effect of temperature on filtration rate in the mussel Mytilus edulis: no evidence for temperature compensation. Mar Ecol Prog Ser 305:147–152.  https://doi.org/10.3354/meps305147 CrossRefGoogle Scholar
  34. Knoll AH, Bambach RK, Payne JL, Pruss S, Fischer WW (2007) Paleophysiology and end-Permian mass extinction. EPSL 256:295–313.  https://doi.org/10.1016/j.epsl.2007.02.018 CrossRefGoogle Scholar
  35. Koenigstein S, Mark FC, Gößling-Reisemann S, Reuter H, Pörtner H-O (2016) Modelling climate change impacts on marine fish populations: process-based integration of ocean warming, acidification and other environmental drivers. Fish Fish 17:972–1004.  https://doi.org/10.1111/faf.12155 CrossRefGoogle Scholar
  36. Lannig G, Flores JF, Sokolova IM (2006) Temperature-dependent stress response in oysters, Crassostrea virginica: pollution reduces temperature tolerance in oysters. Aquat Toxicol 79:278–287.  https://doi.org/10.1016/j.aquatox.2006.06.017 CrossRefPubMedGoogle Scholar
  37. Lannig G, Cherkasov AS, Pörtner H-O, Bock C, Sokolova IM (2008) Cadmium-dependent oxygen limitation affects temperature tolerance in eastern oysters (Crassostrea virginica Gmelin). Am J Physiol Regul Integr Comp Physiol 294:R1338–R1346.  https://doi.org/10.1152/ajpregu.00793.2007 CrossRefPubMedGoogle Scholar
  38. Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations. United States: N.p. Technical Report ORNL/CDIAC-105, Osti.Gov.  https://doi.org/10.2172/639712
  39. Livingstone DR (1991) Origins and Evolution of pathways an anaerobic metabolism in the animal kingdom. Am Zool 31:522–534.  https://doi.org/10.1093/icb/31.3.522 CrossRefGoogle Scholar
  40. Marshall DJ, McQuaid CD (1992) Relationship between heart rate and oxygen consumption in the intertidal limets Patella granularis and Siphonaria oculus. Comp Biochem Physiol A 102:297–300.  https://doi.org/10.1016/0300-9629(92)90583-C CrossRefGoogle Scholar
  41. Melzner F, Bock C, Pörtner H-O (2007) Allometry of thermal limitation in the cephalopod Sepia officinalis. Comp Biochem Physiol A 146:149–154.  https://doi.org/10.1016/j.cbpa.2006.07.023 CrossRefGoogle Scholar
  42. Millero FJ, DiTrolio BR (2010) Use of thermodynamics in examining the effects of ocean acidification. Elements 6:299–303.  https://doi.org/10.2113/gselements.6.5.299 CrossRefGoogle Scholar
  43. Møhlenberg F, Riisgård HU (1978) Efficiency of particle retention in 13 species of suspension feeding bivalves. Ophelia 17:239–246.  https://doi.org/10.1080/00785326.1978.10425487 CrossRefGoogle Scholar
  44. Müller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu R-Y, van der Giezen M, Tielens AGM, Martin W (2012) Biochemistry and evolution of anaerobic energy metabolism in Eukaryotes. Microbiol Mol Biol Rev 76:444–495.  https://doi.org/10.1128/MMBR.05024-11 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Newell RC, Johson LG, Kofoed LH (1977) Adjustment of the components of energy balance in response to temperature change in Ostrea edulis. Oecol 30:97–110.  https://doi.org/10.1007/BF00345414 CrossRefGoogle Scholar
  46. Nicholson S (2002) Ecophysiological aspects of cardiac activity in the subtropical mussel Perna viridis (L.) (Bivalvia: Mytilidae). J Exp Mar Biol Ecol 267:207–222.  https://doi.org/10.1016/S0022-0981(01)00362-8 CrossRefGoogle Scholar
  47. Nickerson DM, Facey DE, Grossman GD (1989) Estimating physiological thresholds with continuous two-phase regression. Physiol Zool 62:866–887CrossRefGoogle Scholar
  48. Nielsen M, Hansen BW, Vismann B (2017) Feeding traits of the European flat oyster, Ostrea edulis, and the invasive Pacific oyster, Crassostrea gigas. Mar Biol 164:6.  https://doi.org/10.1007/s00227-016-3041-5 CrossRefGoogle Scholar
  49. Ortmann C, Grieshaber MK (2003) Energy metabolism and valve closure behaviour in the Asian Clam Corbidula fluminea. J Exp Biol 206:4167–4178.  https://doi.org/10.1242/jeb.00656 CrossRefPubMedGoogle Scholar
  50. Pazos AJ, Román G, Acosta CP, Abad M, Sánchez JL (1997) Seasonal changes in condition and biochemical composition of the scallop Pecten maximus L. from suspended culture in the Ria de Arousa (Galicia, N.W. Spain) in relation to environmental conditions. J Exp Mar Biol Ecol 211:169–193.  https://doi.org/10.1016/S0022-0981(96)02724-4 CrossRefGoogle Scholar
  51. Penn JL, Deutsch C, Payne JL, Sperling EA (2018) Temperature-dependent hypoxia explains biogeography and severity of end-Permian marine mass extinction. Science 362:eaat1327.  https://doi.org/10.1126/science.aat1327 CrossRefPubMedGoogle Scholar
  52. Petersen JK, Sejr MK, Larsen JEN (2003) Clearance rates in the Arctic bivalve Hiatella arctica and Mya sp. Polar Biol 26:334–341.  https://doi.org/10.1007/s00300-003-0483-2 CrossRefGoogle Scholar
  53. Poloczanska E, Brown C, Sydeman W, Kiessling W, Schoeman D, Moore P, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte C, Halpern BS, Holding J, Kappel CV, O’Connor MI, Pandolfi JM, Parmesan C, Schwing F, Thompson SA, Richardson AJ (2013) Global imprint of climate change on marine life. Nat Clim Change 3:919–925.  https://doi.org/10.1038/nclimate1958 CrossRefGoogle Scholar
  54. Pörtner H-O (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146.  https://doi.org/10.1007/s001140100216 CrossRefPubMedGoogle Scholar
  55. Pörtner H-O (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.  https://doi.org/10.1242/jeb.037523 CrossRefPubMedGoogle Scholar
  56. Pörtner H-O (2014) How and how not to investigate the oxygen and capacity limitation of thermal tolerance (OCLTT) and aerobic scope–remarks on the article by Gräns et al. J Exp Biol 217:4432–4433CrossRefGoogle Scholar
  57. Pörtner H-O, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97.  https://doi.org/10.1126/science.1135471 CrossRefPubMedGoogle Scholar
  58. Pörtner H-O, 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 C 110:C09S10.  https://doi.org/10.1029/2004JC002561 CrossRefGoogle Scholar
  59. Pörtner H-O, Farrell AP, Knust R, Lannig G, Mark FC, Storch D (2009) Adapting to climate change—response. Science 323:876–877Google Scholar
  60. Pörtner H-O, Bock C, Mark FC (2017) Oxygen-and capacity-limited thermal tolerance: bridging ecology and physiology. J Exp Biol 220:2685–2696.  https://doi.org/10.1242/jeb.134585 CrossRefPubMedGoogle Scholar
  61. Purohit PV, Rocke DM, Viant MR, Woodruff DL (2004) Discrimination models using variance-stabilizing transformation of metabolomic NMR data. OMICS 8:118–130.  https://doi.org/10.1089/1536231041388348 CrossRefPubMedGoogle Scholar
  62. Rhein M, Rintoul SR, Aoki S et al (2013) Observations: ocean. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) 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, pp 255–316Google Scholar
  63. Riebesell U, Fabry VJ, Hansson L, Gattuso JP (2011) Guide to best practices for ocean acidification research and data reporting. European Commission EUR 24872, Publications Office of the European Union, Luxembourg. ISBN: 978-92-79-20650-4.  https://doi.org/10.2777/66906 Google Scholar
  64. Riisgård HU (2001) Comment: physiological regulation vs. autonomous filtration in filter-feeding bivalves: Starting points for progress. Ophelia 54:193–209.  https://doi.org/10.1080/00785236.2001.10409465 CrossRefGoogle Scholar
  65. Riisgård HU, Larsen PS (2015) Research Note. Physiological regulated valve-closure makes mussels long-term starvation survivors: test of hypothesis. J Molluscan Stud 81:303–307CrossRefGoogle Scholar
  66. Riisgård HU, Kittner C, Seerup DF (2003) Regulation of opening state and filtration rate in filter-feeding bivalves (Cardium edule, Mytilus edulis, Mya arenaria) in response to low algal concentration. J Exp Mar Biol Ecol 284:105–127.  https://doi.org/10.1016/S0022-0981(02)00496-3 CrossRefGoogle Scholar
  67. Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CS, Wallace DR, Tilbrook B, Millero FJ, Peng T-H, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371.  https://doi.org/10.1126/science.1097403 CrossRefPubMedGoogle Scholar
  68. Schalkhausser B, Bock C, Stemmer K, Brey T, Pörtner H-O, Lannig G (2013) Impact of ocean acidification on escape performance of the king scallop, Pecten maximus, from Norway. Mar Biol 160:1995–2006.  https://doi.org/10.1007/s00227-012-2057-8 CrossRefGoogle Scholar
  69. Schiffer M, Harms L, Lucassen M, Mark FC, Pörtner H-O (2014) Temperature tolerance of different larval stages of the spider crab Hyas araneus exposed to elevated seawater PCO2. Front Zool 11:87.  https://doi.org/10.1186/s12983-014-0087-4 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Schmalenbach I, Buchholz F, Franke HD, Saborowski R (2009) Improvement of rearing conditions for juvenile lobsters (Homarus gammarus) by co-culturing with juvenile isopods (Idotea emarginata). Aquaculture 289:297–303.  https://doi.org/10.1016/j.aquaculture.2009.01.017 CrossRefGoogle Scholar
  71. Schmidt M, Windisch HS, Ludwichowski KU, Seegert SLL, Pörtner H-O, Storch D, Bock C (2017) Differences in neurochemical profiles of two gadid specied under ocean warming and acidification. Front Zool 14:49.  https://doi.org/10.1186/s12983-017-0238-5 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Shepard S, Beukers-Stewart B, Hiddink JG, Brand AR, Kaiser MJ (2010) Strengthening recruitment of exploited scallops Pecten maximus with ocean warming. Mar Biol 157:91–97.  https://doi.org/10.1007/s00227-009-1298-7 CrossRefGoogle Scholar
  73. Shumway SE, Koehn RK (1982) Oxygen consumption in the american oyster Crassostrea virginica. Mar Ecol Prog Ser 9:59–68.  https://doi.org/10.3354/meps009059 CrossRefGoogle Scholar
  74. 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.  https://doi.org/10.1016/j.marenvres.2012.04.003 CrossRefPubMedGoogle Scholar
  75. Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits and costs of living. Integr Comp Biol 42:780–789.  https://doi.org/10.1093/icb/42.4.780 CrossRefPubMedGoogle Scholar
  76. Specht JA, Fuchs HL (2018) Thermal and viscous effect of temperature on mercenaria mercenaria suspension feeding. Mar Ecol Prog Ser 589:129–140.  https://doi.org/10.3354/meps12431 CrossRefGoogle Scholar
  77. Stanley SM (2016) Estimates of the magnitudes of major marine mass extinctions in earth history. PNAS 113:E6325–E6334.  https://doi.org/10.1073/pnas.1613094113 CrossRefPubMedGoogle Scholar
  78. Stoll MHC, Bakker K, Nobbe GH, Haesel RR (2001) Continuous-Flow analysis of dissolved inorganic carbon content in seawater. Anal Chem 73:4111–4116.  https://doi.org/10.1021/ac010303r CrossRefPubMedGoogle Scholar
  79. Taylor AC (1976) The cardiac responses to shell opening and closure in the bivalve Arctica islandica (L.). J Exp Biol 64:751–759PubMedGoogle Scholar
  80. Tripp-Valdez MA, Bock C, Lucassen M, Lluch-Cota SE, Sicard MT, Lannig G, Pörtner H-O (2017) Metabolic response and thermal tolerance of green abalone juveniles (Haliotis fulgens: Gastropoda) under acute hypoxia and hypercapnia. J Exp Mar Biol Ecol 497:11–18.  https://doi.org/10.1016/j.jembe.2017.09.002 CrossRefGoogle Scholar
  81. Trueman ER, Lowe GA (1971) The effect of temperature and littoral exposure on the heart rate of a bivalve mollusc, Isognomum alatus, in tropical condtions. Comp Biochem Physiol A 38:555–564.  https://doi.org/10.1016/0300-9629(71)90122-8 CrossRefGoogle Scholar
  82. Uppström LR (1974) Boron/chlorinity ratio of deep-sea water from the Pacific Ocean. Deep-Sea Res Oceanogr Abstr 21:161–162.  https://doi.org/10.1016/0011-7471(74)90074-6 CrossRefGoogle Scholar
  83. Waters JF, Millero FJ (2013) The free proton concentration scale for seawater pH. Mar Chem 149:8–22.  https://doi.org/10.1016/j.marchem.2012.11.003 CrossRefGoogle Scholar
  84. Widdows J (1973) Effect of temperature and food on the heart beat, ventilation rate and oxygen uptake of Mytilus edulis. Mar Biol 20:269–276.  https://doi.org/10.1007/BF00354270 CrossRefGoogle Scholar
  85. Widdows J (1976) Physiological adaption of Mytilus edulis to cyclic temperatures. J Comp Physiol B 105:115–128.  https://doi.org/10.1007/BF00691115 CrossRefGoogle Scholar
  86. Wignall PB, Twitchett RJ (1996) Oceanic anoxia and the end Permian mass extinction. Science 272:1155–1158.  https://doi.org/10.1126/science.272.5265.1155 CrossRefPubMedGoogle Scholar
  87. Wilson JG (1981) Temperature tolerance of circatidal bivalves in relation to their distribution. J Therm Biol 6:279–286.  https://doi.org/10.1016/0306-4565(81)90016-4 CrossRefGoogle Scholar
  88. Wilson JG, Elkaim B (1991) Tolerances to high temperature of infaunal bivalves and the effect of geographical distribution, position on the shore and season. J Mar Biol Assoc UK 71:169–177.  https://doi.org/10.1017/S0025315400037486 CrossRefGoogle Scholar
  89. Xia J, Wishart DS (2016) Using metabo analyst 3.0 for comprehensive metabolomics data analysis. Curr Protoc Bioinform 55:14.10.1–14.10.91.  https://doi.org/10.1002/cpbi.11 CrossRefGoogle Scholar
  90. Xing Q, Li Y, Guo H, Yu Q, Huang X, Wang S, Hu X, Zhang L, Bao Z (2016) Cardiac performance: a thermal tolerance indicator in scallops. Mar Biol 163:244.  https://doi.org/10.1007/s00227-016-3021-9 CrossRefGoogle Scholar
  91. Yeager DP, Ultsch GR (1989) Phyiological regulation and conformation: a basic program for the determination of critical points. Physiol Zool 62:888–907CrossRefGoogle Scholar
  92. Zannella C, Mosca F, Mariani F, Franci G, Folliero V, Galdiero M, Tiscar PG, Galdiero M (2017) Microbial diseases of bivalve mollusks: infections, immunology and antimicrobial defense. Mar Drugs 15:E182.  https://doi.org/10.3390/md15060182 CrossRefPubMedGoogle Scholar
  93. Zittier ZM, Bock C, Lannig G, Pörtner H-O (2015) Impact of ocean acidification on thermal tolerance and acid–base regulation of Mytilus edulis (L.) from the North Sea. J Exp Mar Biol Ecol 473:16–25.  https://doi.org/10.1016/j.jembe.2015.08.001 CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Alfred Wegener Institute Helmholtz Centre for Polar and Marine ResearchBremerhavenGermany
  2. 2.Department of BiologyInstitut de Biologie Integrative et des SystemesQuebecCanada
  3. 3.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA
  4. 4.Marine Biology, Faculty of Mathematics and Natural SciencesUniversity of RostockRostockGermany
  5. 5.Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity ScienceBerlinGermany

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