Marine Biology

, 166:6 | Cite as

Thermal tolerance limits as indicators of current and future intertidal zonation patterns in a diverse mussel guild

  • Cascade J. B. SorteEmail author
  • Geneviève Bernatchez
  • K. A. S. Mislan
  • Lauren L. M. Pandori
  • Nyssa J. Silbiger
  • Piper D. Wallingford
Original paper


Climate change has driven shifts in species distributions along latitudinal and elevational gradients, and such shifts are likely to continue as warming accelerates. However, little is known about the response of strongly interacting species, including whether multiple, interacting species are likely to shift concordantly or whether climate change will promote community disassembly. In rocky shore ecosystems, mussels are dominant foundation species that provide habitat and increase diversity of associated species. The New Zealand mussel guild is uniquely diverse as four species can be found within 1 m2 of shoreline. We integrated comparative ecophysiology and population ecology to evaluate whether air temperature sets elevational range limits and to quantify mussels’ warming tolerances. Air temperature appears to set upper intertidal limits across mid-intertidal species, based on findings that (1) lethal thermal limits coincided with temperatures experienced at upper tide-height limits, (2) species with higher thermal tolerances occurred higher on shore, and (3) lethal tolerances were highest at our warmest site. Based on predicted body temperatures in year 2100, mid-elevation habitat-forming mussels are likely to experience an increase in the frequency of thermal events causing 50% mortality at their upper elevation limit. Such events are predicted to occur 3.0–4.4 times more frequently in 2100 than present at a warmer site and to increase from 0 to 0.4/0.1 days per year for Perna/Aulacomya, but not Mytilus, at a cooler site. These results indicate that the mussel species’ ranges are all likely to contract at warmer sites in the future, decreasing habitat for associated organisms.



We particularly thank M. Bracken and A. Gannett for collaborating on the 2015 fieldwork and D. Schiel and members of MERG at University of Canterbury for facilitating this New Zealand-based research. We thank H. Frenzel for technological help and M. Bracken, M. Foley, M. Peich, D. Wethey, and Sorte Lab members for additional assistance and feedback. This is CSUN Marine Biology Contribution #280.


This work was supported by start-up funds from the University of California, Irvine to CS, an Erskine Fellowship from University of Canterbury to M. Bracken, and a UCI GAANN travel grant to LP.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflicts of interest.

Ethical approval

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

Data availability

Data and code for temperature modeling and projected frequency of lethal temperature events are available on GitHub at and, respectively. Additional data (mussel abundances, maximum tide heights, and thermal tolerances) are available in Online Resource 2.

Supplementary material

227_2018_3452_MOESM1_ESM.pdf (47 kb)
Supplementary material 1 (PDF 47 kb)
227_2018_3452_MOESM2_ESM.xlsx (568 kb)
Supplementary material 2 (XLSX 567 kb)
227_2018_3452_MOESM3_ESM.pdf (40 kb)
Supplementary material 3 (PDF 39 kb)
227_2018_3452_MOESM4_ESM.pdf (86 kb)
Supplementary material 4 (PDF 86 kb)


  1. Abrams PA, Matsuda H (1996) Positive indirect effects between prey species that share predators. Ecology 77:610–616. CrossRefGoogle Scholar
  2. Angelini C, Altieri AH, Silliman BR, Bertness MD (2011) Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. Bioscience 61:782–789. CrossRefGoogle Scholar
  3. Angelini C, Van der Heide T, Griffin JN, Morton JP, Derksen-Hooijberg M, Lamers LP, Smolders AJ, Silliman BR (2015) Foundation species’ overlap enhances biodiversity and multifunctionality from the patch to landscape scale in southeastern United States salt marshes. Proc R Soc B 282:20150421. CrossRefGoogle Scholar
  4. Barron CN, Kara AB (2006) Satellite-based daily SSTs over the global ocean. Geophys Res Lett 33:L15603. CrossRefGoogle Scholar
  5. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48CrossRefGoogle Scholar
  6. Berg MP, Kiers E, Driessen G, Van Der Heijden M, Kooi BW, Kuenen F, Liefting M, Verhoef HA, Ellers J (2010) Adapt or disperse: understanding species persistence in a changing world. Glob Change Biol 16:587–598. CrossRefGoogle Scholar
  7. Blanchette CA, Miner CM, Raimondi PT, Lohse D, Heady KE, Broitman BR (2008) Biogeographical patterns of rocky intertidal communities along the Pacific coast of North America. J Biogeogr 35:1593–1607. CrossRefGoogle Scholar
  8. Borrvall C, Ebenman B, Jonsson T, Jonsson T (2000) Biodiversity lessens the risk of cascading extinction in model food webs. Ecol Lett 3:131–136. CrossRefGoogle Scholar
  9. Borthagaray AI, Carranza A (2007) Mussels as ecosystem engineers: their contribution to species richness in a rocky littoral community. Acta Oecol 31:243–250. CrossRefGoogle Scholar
  10. Bracken MES (2017) Coexistence, complementarity, and resource partitioning in a guild of marine filter feeders. In: Abstract 28403 presented at ASLO 2017 aquatic sciences meeting, Honolulu, Hawaii, USAGoogle Scholar
  11. Bracken MES, Menge BA, Foley MM, Sorte CJB, Lubchenco J, Schiel DR (2012) Mussel selectivity for high-quality food drives carbon inputs into open-coast intertidal ecosystems. Mar Ecol Prog Ser 459:53–62. CrossRefGoogle Scholar
  12. Branch GM, Steffani CN (2004) Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck). J Exp Mar Biol Ecol 300:189–215. CrossRefGoogle Scholar
  13. Broitman BR, Navarrete SA, Smith F, Gaines SD (2001) Geographic variation of southeastern Pacific intertidal communities. Mar Ecol Prog Ser 224:21–34. CrossRefGoogle Scholar
  14. Bruno JF, Bertness MD (2001) Habitat modification and facilitation in benthic marine communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 201–216Google Scholar
  15. Buchanan S (2001) Measuring reproductive condition in the Greenshell™ mussel Perna canaliculus. NZ J Mar Freshwat Res 35:859–870CrossRefGoogle Scholar
  16. Cahill AE, Aiello-Lammens ME, Fisher-Reid MC, Hua X, Karanewsky CJ, Ryu HY, Sbeglia GC, Spagnolo F, Waldron JB, Wiens JJ (2014) Causes of warm-edge range limits: systematic review, proximate factors and implications for climate change. J Biogeogr 41:429–442. CrossRefGoogle Scholar
  17. Callander DC (2012) Effects of environmental stress on gene expression in mussels. Dissertation, University of Canterbury, New ZealandGoogle Scholar
  18. Calosi P, Bilton DT, Spicer JI (2008) Thermal tolerance, acclimatory capacity and vulnerability to global climate change. Biol Lett 4:99–102. PubMedCrossRefGoogle Scholar
  19. Chen F, Dudhia J (2001) Coupling an advanced land surface-hydrology model with the Penn State-NCAR MM5 modeling system. Part I. Model implementation and sensitivity. Mon Weather Rev 129:569–585CrossRefGoogle Scholar
  20. Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026. PubMedCrossRefGoogle Scholar
  21. Chivers WJ, Walne AW, Hays GC (2017) Mismatch between marine plankton range movements and the velocity of climate change. Nat Commun 8:14434. PubMedPubMedCentralCrossRefGoogle Scholar
  22. Collins WJ, Bellouin N, Doutriaux-Boucher M, Gedney N et al (2011) Development and evaluation of an Earth-System model—HadGEM2. Geosci Model Dev 4:1051–1075CrossRefGoogle Scholar
  23. Connell JH (1961) The Influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42:710–723. CrossRefGoogle Scholar
  24. Dethier MN, Graham ES, Cohen S, Tear LM (1993) Visual versus random-point percent cover estimations: ‘objective’ is not always better. Mar Ecol Progr Ser 96:93–100CrossRefGoogle Scholar
  25. Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci USA 105:6668–6672. PubMedCrossRefGoogle Scholar
  26. Dowd WW, Somero GN (2013) Behavior and survival of Mytilus congeners following episodes of elevated body temperature in air and seawater. J Exp Biol 216:502–514PubMedCrossRefGoogle Scholar
  27. Dufresne J-L, Foujols M-A, Denvil S et al (2013) Climate change projections using the IPSL-CM5 earth system model: from CMIP3 to CMIP5. Clim Dyn 40:2123–2165CrossRefGoogle Scholar
  28. Dunne JP, John JG, Adcroft AJ et al (2012) GFDL’s ESM2 global coupled climate-carbon earth system models. Part I: physical formulation and baseline simulation characteristics. J Clim 25:6646–6665CrossRefGoogle Scholar
  29. Dunne JP, John JG, Shevliakova E et al (2013) GFDL’s ESM2 global coupled climate-carbon earth system models. Part II: carbon system formulation and baseline simulation characteristics. J Clim 26:2247–2267CrossRefGoogle Scholar
  30. Dunphy BJ, Ragg NL, Collings MG (2013) Latitudinal comparison of thermotolerance and HSP70 production in F2 larvae of the greenshell mussel (Perna canaliculus). J Exp Biol 216:1202–1209. PubMedCrossRefGoogle Scholar
  31. Dunphy BJ, Watts E, Ragg NL (2015) Identifying thermally-stressed adult green-lipped mussels (Perna canaliculus Gmelin, 1791) via metabolomic profiling. Am Malacol Bull 33:127–135. CrossRefGoogle Scholar
  32. Egbert GD, Erofeeva SY (2002) Efficient inverse modeling of barotropic ocean tides. J Atmos Ocean Technol 19:183–204CrossRefGoogle Scholar
  33. Egbert GD, Bennett A, Foreman M (1994) TOPEX/poseidon tides estimated using a global inverse model. J Geophys Res 99:24821–24852CrossRefGoogle Scholar
  34. Ek MB, Mitchell KE, Lin Y et al (2003) Implementation of NOAH land surface model advances in the National Centers for Environmental Prediction operational mesoscale Eta model. J Geophys Res 108:8851. CrossRefGoogle Scholar
  35. Ellison AM, Bank MS, Clinton BD, Colburn EA, Elliott K, Ford CR, Foster DR, Kloeppel BD, Knoepp JD, Lovett GM, Mohan J (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486.;2 CrossRefGoogle Scholar
  36. Faulkner KT, Clusella-Trullas S, Peck LS, Chown SL (2014) Lack of coherence in the warming responses of marine crustaceans. Funct Ecol 28:895–903. CrossRefGoogle Scholar
  37. Feder M, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282PubMedCrossRefGoogle Scholar
  38. Gardner J, Zbawicka M, Westfall KM, Wenne R (2016) Invasive blue mussels threaten regional scale genetic diversity in mainland and remote offshore locations: the need for baseline data and enhanced protection in the Southern Ocean. Glob Change Biol 22:3182–3195. CrossRefGoogle Scholar
  39. Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407CrossRefGoogle Scholar
  40. Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD (2010) A framework for community interactions under climate change. Trends Ecol Evol 25:325–331PubMedCrossRefGoogle Scholar
  41. Giorgetta MA, Jungclaus J, Reick CH et al (2013) Climate and carbon cycle changes from 1850 to 2100 in MPI-ESM simulations for the coupled model intercomparison project phase 5. J Adv Model Earth Syst 5:572–597CrossRefGoogle Scholar
  42. Gutiérrez JL, Jones CG, Straver DL, Iribarne OO (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101:79–90. CrossRefGoogle Scholar
  43. Harley CD, Helmuth BS (2003) Local-and regional-scale effects of wave exposure, thermal stress, and absolute versus effective shore level on patterns of intertidal zonation. Limnol Oceanogr 48:1498–1508. CrossRefGoogle Scholar
  44. Harley CD, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 2:228–241. CrossRefGoogle Scholar
  45. He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive species interactions with increasing environmental stress. Ecol Lett 16:695–706PubMedCrossRefGoogle Scholar
  46. Heath RA (1985) A review of the physical oceanography of the seas around New Zealand—1982. N Z J Mar Freshw 19:79–124. CrossRefGoogle Scholar
  47. Helmuth BS, Hofmann GE (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol Bull 201:374–384PubMedCrossRefGoogle Scholar
  48. Helmuth B, Harley CDG, Halpin PM, O’Donnell M, Hofmann GE, Blanchette CA (2002) Climate change and latitudinal patterns of intertidal thermal stress. Science 298:1015–1017PubMedCrossRefGoogle Scholar
  49. Helmuth B, Mieszkowska N, Moore P, Hawkins SJ (2006) Living on the edge of two changing worlds: forecasting the responses of rocky intertidal ecosystems to climate change. Annu Rev Ecol Evol Syst 37:373–404CrossRefGoogle Scholar
  50. Hughes AR, Williams SL, Duarte CM, Heck KL, Waycott M (2009) Associations of concern: declining seagrasses and threatened dependent species. Front Ecol Environ 7:242–246. CrossRefGoogle Scholar
  51. Ilyina T, Six KD, Segschneider J, Maier-Reimer E, Li H, Núñez-Riboni I (2013) Global ocean biogeochemistry model HAMOCC: model architecture and performance as component of the MPI-Earth system model in different CMIP5 experimental realizations. J Adv Model Earth Syst 5:287–315CrossRefGoogle Scholar
  52. Jimenez AG, Jayawardene S, Alves S, Dallmer J, Dowd WW (2015) Micro-scale environmental variation amplifies physiological variation among individual mussels. Proc R Soc B 282:20152273. PubMedCrossRefGoogle Scholar
  53. Jones SJ, Mieszkowska N, Wethey DS (2009) Linking thermal tolerances and biogeography: Mytilus edulis (L.) at its southern limit on the east coast of the United States. Biol Bull 217:73–85PubMedCrossRefGoogle Scholar
  54. Jones CD, Hughes JK, Bellouin N et al (2011) The HadGEM2-ES implementation of CMIP5 centennial simulations. Geosci Model Dev 4:543–570CrossRefGoogle Scholar
  55. Jurgens LJ, Gaylord B (2018) Physical effects of habitat-forming species override latitudinal trends in temperature. Ecol Lett 21:190–196. PubMedCrossRefGoogle Scholar
  56. Keith DA, Akçakaya HR, Thuiller W, Midgley GF, Pearson RG, Phillips SJ, Regan HM, Araújo MB, Rebelo TG (2008) Predicting extinction risks under climate change: coupling stochastic population models with dynamic bioclimatic habitat models. Biol Lett 4:560–563. PubMedPubMedCentralCrossRefGoogle Scholar
  57. Kennedy VS (1976) Desiccation, higher temperatures and upper intertidal limits of three species of sea mussels (Mollusca: Bivalvia) in New Zealand. Mar Biol 35:127–137. CrossRefGoogle Scholar
  58. Kimbro DL, Cheng BS, Grosholz ED (2013) Biotic resistance in marine environments. Ecol Lett 16:821–833PubMedCrossRefGoogle Scholar
  59. Kordas RL, Harley CD, O’Connor MI (2011) Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. J Exp Mar Biol Ecol 400:218–226CrossRefGoogle Scholar
  60. Logan CA, Kost LE, Somero GN (2012) Latitudinal differences in Mytilus californianus thermal physiology. Mar Ecol Prog Ser 450:93–105. CrossRefGoogle Scholar
  61. Lourenço CR, Zardi GI, McQuaid CD, Serrao EA, Pearson GA, Jacinto R, Nicastro KR (2016) Upwelling areas as climate change refugia for the distribution and genetic diversity of a marine macroalga. J Biogeogr 43:1595–1607. CrossRefGoogle Scholar
  62. Marsden ID, Weatherhead MA (1998) Effects of aerial exposure on oxygen consumption by the New Zealand mussel Perna canaliculus (Gmelin, 1791) from an intertidal habitat. J Exp Mar Biol Ecol 230:15–29CrossRefGoogle Scholar
  63. Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997. PubMedCrossRefGoogle Scholar
  64. Menge BA (1972) Foraging strategy of a starfish in relation to actual prey availability and environmental predictability. Ecol Monogr 42:25–50. CrossRefGoogle Scholar
  65. Menge BA (1976) Organization of the New England rocky intertidal community: role of predation, competition, and environmental heterogeneity. Ecol Monogr 46:355–393. CrossRefGoogle Scholar
  66. Menge BA, Branch GM (2001) Rocky intertidal communities. In: Bertness MD, Gaine SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 221–251Google Scholar
  67. Menge BA, Sutherland JP (1976) Species diversity gradients: synthesis of the roles of predation, competition, and temporal heterogeneity. Am Nat 110:351–369CrossRefGoogle Scholar
  68. Menge BA, Daley BA, Lubchenco J, Sanford E, Dahlhoff E, Halpin PM, Hudson G, Burnaford JL (1999) Top-down and bottom-up regulation of New Zealand rocky intertidal communities. Ecol Monogr 69:297–330.;2 CrossRefGoogle Scholar
  69. Menge BA, Daley BA, Sanford E, Dahlhoff EP, Lubchenco J (2007) Mussel zonation in New Zealand: an integrative eco-physiological approach. Mar Ecol Prog Ser 345:129–140. CrossRefGoogle Scholar
  70. Miller LP, Harley CD, Denny MW (2009) The role of temperature and desiccation stress in limiting the local-scale distribution of the owl limpet, Lottia gigantea. Funct Ecol 23:756–767. CrossRefGoogle Scholar
  71. Mislan KAS, Wethey DS (2011) Gridded meteorological data as a resource for mechanistic macroecology in coastal environments. Ecol Appl 21:2678–2690PubMedCrossRefGoogle Scholar
  72. Mislan KAS, Helmuth B, Wethey DS (2014) Geographical variation in climatic sensitivity of intertidal mussel zonation. Glob Ecol Biogeogr 23:744–756. CrossRefGoogle Scholar
  73. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. PubMedCrossRefGoogle Scholar
  74. Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915. PubMedCrossRefGoogle Scholar
  75. Petes LE, Menge BA, Murphy GD (2007) Environmental stress decreases survival, growth, and reproduction in New Zealand mussels. J Exp Mar Biol Ecol 351:83–91. CrossRefGoogle Scholar
  76. Petes LE, Menge BA, Harris AL (2008) Intertidal mussels exhibit energetic trade-offs between reproduction and stress resistance. Ecol Monogr 78:387–402. CrossRefGoogle Scholar
  77. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  78. Rilov G, Schiel DR (2006) Seascape-dependent subtidal–intertidal trophic linkages. Ecology 87:731–744. PubMedCrossRefGoogle Scholar
  79. Rogelj J, Meinshausen M, Knutti R (2012) Global warming under old and new scenarios using IPCC climate sensitivity range estimates. Nat Clim Change 2:248–253. CrossRefGoogle Scholar
  80. Saha S et al (2006) The NCEP climate forecast system. J Clim 19:2483–3517CrossRefGoogle Scholar
  81. Saha S et al (2010) The NCEP climate forecast system reanalysis. Bull Am Meterol Soc 91:1015–1057CrossRefGoogle Scholar
  82. Sanford E (1999) Regulation of keystone predation by small changes in ocean temperature. Science 283:2095–2097PubMedCrossRefGoogle Scholar
  83. Schiel DR, Steinbeck JR, Foster MS (2004) Ten years of induced ocean warming causes comprehensive changes in marine benthic communities. Ecology 85:1833–1839. CrossRefGoogle Scholar
  84. Schiel DR, Lilley SA, South PM, Coggins JH (2016) Decadal changes in sea surface temperature, wave forces and intertidal structure in New Zealand. Mar Ecol Prog Ser 548:77–95CrossRefGoogle Scholar
  85. Seabra R, Wethey DS, Santos AM, Gomes F, Lima FP (2016) Equatorial range limits of an intertidal ectotherm are more linked to water than air temperature. Glob Change Biol 22:3320–3331. CrossRefGoogle Scholar
  86. Sexton JP, McIntyre PJ, Angert AL, Rice KJ (2009) Evolution and ecology of species range limits. Annu Rev Ecol Evol Syst 40:415–436. CrossRefGoogle Scholar
  87. Smith JM (2003) Surf zone hydrodynamics. U.S. Army Corps of Engineers coastal engineering manual. Part II, chapter 4. U.S. Army Engineer Research and Development Center, VicksburgGoogle Scholar
  88. Smith JR, Fong P, Ambrose RF (2006a) Long-term change in mussel (Mytilus californianus Conrad) populations along the wave-exposed coast of southern California. Mar Biol 149:537–545. CrossRefGoogle Scholar
  89. Smith JR, Fong P, Ambrose RF (2006b) Dramatic declines in mussel bed community diversity: response to climate change? Ecology 87:1153–1161.;2 PubMedCrossRefGoogle Scholar
  90. Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integr Comp Biol 42:780–789. PubMedCrossRefGoogle Scholar
  91. Somero GN (2012) The physiology of global change: linking patterns to mechanisms. Annu Rev Mar Sci 4:39–61. CrossRefGoogle Scholar
  92. Sorte CJB, Williams SL, Carlton JT (2010) Marine range shifts and species introductions: comparative spread rates and community impacts. Glob Ecol Biogeogr 19:303–316. CrossRefGoogle Scholar
  93. Sorte CJB, Jones SJ, Miller LP (2011) Geographic variation in temperature tolerance as an indicator of potential population responses to climate change. J Exp Mar Biol Ecol 400:209–217. CrossRefGoogle Scholar
  94. Sorte CJB, Davidson VE, Franklin MC, Benes KM, Doellman MM, Etter RJ, Hannigan RE, Lubchenco J, Menge BA (2017) Long-term declines in an intertidal foundation species parallel shifts in community composition. Glob Change Biol 23:341–352. CrossRefGoogle Scholar
  95. Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459. CrossRefGoogle Scholar
  96. Stickle WB, Lindeberg M, Rice SD, Munley K, Reed V (2016) Seasonal changes in the thermal regime and gastropod tolerance to temperature and desiccation stress in the rocky intertidal zone in southeast Alaska. J Exp Mar Biol Ecol 482:56–63CrossRefGoogle Scholar
  97. Stickle WB, Carrington E, Hayford H (2017) Seasonal changes in the thermal regime and gastropod tolerance to temperature and desiccation stress in the rocky intertidal zone. J Exp Mar Biol Ecol 488:83–91CrossRefGoogle Scholar
  98. Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65. PubMedCrossRefGoogle Scholar
  99. 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. PubMedCrossRefGoogle Scholar
  100. Suchanek TH (1992) Extreme biodiversity in the marine-environment-Mussel bed communities of Mytilus californianus. Northwest Environ J 8:150–152Google Scholar
  101. Sunday JM, Bates AE, Dulvy NK (2012) Thermal tolerance and the global redistribution of animals. Nat Clim Change 2:686–690. CrossRefGoogle Scholar
  102. Taylor KE, Stouffer RJ, Meehl GA (2012) An overview of the CMIP5 and the experiment design. Bull Am Meteorol Soc 93:485–498CrossRefGoogle Scholar
  103. Tolman HL (1998) A new global wave forecast system at NCEP. In: Edge BL, Helmsley JM (eds) Ocean wave measurements and analysis. American Society of Civil Engineers, Reston, pp 777–786Google Scholar
  104. Tolman HL (2007) The 2007 release of WAVEWATCH III. NOAA/NWS/NCEP/OMB Tech Note 262Google Scholar
  105. Tolman HL (2009) User manual and system documentation of WAVEWATCH III version 3.14. NOAA/NWS/NCEP/OMB Tech Rep 276Google Scholar
  106. US Army Corps of Engineers (2002) Coastal engineering manual. Engineer manual 1110-2-1100. U.S. Army Corps of Engineers, Washington, DCGoogle Scholar
  107. Vinagre C, Leal I, Mendonca V, Madeira D, Narciso L, Diniz MS, Flores AAV (2016) Vulnerability to climate warming and acclimation capacity of tropical and temperate coastal organisms. Ecol Indic 62:317–327. CrossRefGoogle Scholar
  108. Vincent WF, Howard-Williams C, Tildesley P, Butler E (1991) Distribution and biological properties of oceanic water masses around the South Island, New Zealand. N Z J Mar Freshw 25:21–42. CrossRefGoogle Scholar
  109. Walter H, Harnickell E, Mueller-Dombois D (1975) Climate diagram maps. Supplement to vegetation monographs. Springer, New YorkCrossRefGoogle Scholar
  110. Wernberg T, Russell BD, Thomsen MS, Gurgel CFD, Bradshaw CJA, Poloczanska ES, Connell SD (2011) Seaweed communities in retreat from ocean warming. Curr Biol 21:1828–1832. PubMedCrossRefGoogle Scholar
  111. Wernberg T, Bennett S, Babcock RC, de Bettignies T, Cure K, Depczynski M, Dufois F, Fromont J, Fulton CJ, Hovey RK, Harvey ES (2016) Climate-driven regime shift of a temperate marine ecosystem. Science 353:169–172. PubMedCrossRefGoogle Scholar
  112. Westfall KM, Gardner J (2010) Genetic diversity of Southern hemisphere blue mussels (Bivalvia: Mytilidae) and the identification of non-indigenous taxa. Biol J Linn Soc 101:898–909. CrossRefGoogle Scholar
  113. Wethey DS, Brin LD, Helmuth B, Mislan KAS (2011) Predicting intertidal organism temperatures with modified land surface models. Ecol Model 222:3568–3576. CrossRefGoogle Scholar
  114. Williams JW, Jackson ST, Kutzbach JE (2007) Projected distributions of novel and disappearing climates by 2100 AD. Proc Natl Acad Sci USA 104:5738–5742. PubMedCrossRefGoogle Scholar
  115. Yakovis EL, Artemieva AV, Shunatova NN, Varfolomeeva MA (2008) Multiple foundation species shape benthic habitat islands. Oecologia 155:785–795. PubMedCrossRefGoogle Scholar
  116. Yamane L, Gilman SE (2009) Opposite responses by an intertidal predator to increasing aquatic and aerial temperatures. Mar Ecol Progr Ser 393:27–36CrossRefGoogle Scholar
  117. Zardi GI, Nicastro KR, McQuaid CD, Ng TPT, Lathlean J, Seuront L (2016) Enemies with benefits: parasitic endoliths protect mussels against heat stress. Sci Rep 6:31413PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaIrvineUSA
  2. 2.School of OceanographyUniversity of WashingtonSeattleUSA
  3. 3.Department of BiologyCalifornia State UniversityNorthridgeUSA

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