Marine Biology

, 164:207 | Cite as

Is the future as tasty as the present? Elevated temperature and hyposalinity affect the quality of Fucus (Phaeophyceae, Fucales) as food for the isopod Idotea balthica

  • Eva Rothäusler
  • Fiia Haavisto
  • Veijo Jormalainen
Original paper


Climate change is acknowledged to affect directly macroalgal performance but its indirect effect through changes in algal interaction with herbivores remains poorly understood. To study effects of climate change on a macroalga–herbivore interaction, we exposed three range-margin Baltic Sea populations of Fucus (60°N 39°E, 61°N 21°E, 62°N 21°E) in September 2015 to current (15.1 °C; 5.2 PSU) and predicted future (17.5 °C; 2.6 PSU) environments for 7 months. After 6 weeks we tested the indirect effect of climate change through food quality on growth, survival and food consumption of the isopod Idotea balthica while after 7 months we tested the direct effect on algal inducible defenses. We predicted that future stressful conditions impair constitutive and inducible defense traits in Fucus thus resulting in a higher susceptibility to herbivores. The short-term climate stress did decrease thallus toughness of Fucus in one population but isopod food consumption and performance remained unchanged. After 7 months, throughout the populations, Fucus grown in future conditions was softer and more consumed. The grazing attack induced resistance in two populations but irrespective of climate change. Our results show that Fucus can cope with short-term (6 weeks) stress without indirect effects on the interactions with herbivores. However, long-term (7 months) stressed Fucus was consumed more by isopods likely due to a decrease in constitutive resistance traits rather than changes in inducible resistance. This suggests that in near future, marginal populations of Fucus might become more vulnerable to grazing losses, with possibly adverse effects on the abundance and persistence of these populations.



This research was funded by BONUS, the joint Baltic Sea research and development programme (Art 185), funded jointly from the European Union’s Seventh Programme for research, technological development and demonstration and from the Academy of Finland (decision # 273623) for the project BAMBI-Baltic Sea Marine Biodiversity. We thank Joakim Sjöroos and Lukas Novaes Tump for assistance in sampling algae and isopods and in maintaining the aquaria system, and Iita Manninen and Nelson Vásquez for assistance with measuring isopod performance, and Carolin Uebermuth in building up choice bioassays. We are very grateful to Alistair Poore and one anonymous reviewer for many constructive comments that helped to improve this manuscript.

Compliance with ethical standards

Conflict of interest

The 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. This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

227_2017_3237_MOESM1_ESM.pdf (73 kb)
Supplementary material 1 (PDF 72 kb)
227_2017_3237_MOESM2_ESM.pdf (152 kb)
Supplementary material 2 (PDF 152 kb)


  1. Andersen GS, Pedersen MF, Nielsen SL (2013) Temperature acclimation and heat tolerance of photosynthesis in Norwegian Saccharina latissima (Laminariales, Phaeophyceae). J Phycol 49:689–700. doi: 10.1111/jpy.12077 CrossRefGoogle Scholar
  2. Ardehed A, Johansson D, Sundqvist L, Schagerström E, Zagrodzka Z, Kovaltchouk NA, Bergström L, Kautsky L, Rafajlovic M, Pereyra RT, Johannesson K (2016) Divergence within and among seaweed siblings (Fucus vesiculosus and F. radicans) in the Baltic Sea. PLoS One. doi: 10.1371/journal.pone.0161266 Google Scholar
  3. Baggett LP, Heck KL Jr, Frankovich TA, Armitage AR, Fourqurean JW (2013) Stoichiometry, growth, and fecundity responses to nutrient enrichment by invertebrate grazers in sub-tropical turtle grass (Thalassia testudinum) meadows. Mar Biol 160:169–180. doi: 10.1007/s00227-012-2075-6 CrossRefGoogle Scholar
  4. Bergström A, Tatarenkov A, Johannesson K, Jonsson RB, Kautsky L (2005) Genetic and morphological identification of Fucus radicans sp. nov. (Fucales, Phaeophyceae) in the brackish Baltic Sea. J Phycol 41:1025–1038CrossRefGoogle Scholar
  5. Bisson MA, Kirst GO (1995) Osmotic acclimation and turgor pressure regulation in algae. Naturwissenschaften 82:461–471CrossRefGoogle Scholar
  6. Bryant JP, Chapin FS III, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oecologia 86:202–209. doi: 10.2307/3544308 Google Scholar
  7. Connan S, Stengel DB (2011) Interactive effects on phenolic pool and assessment of metal binding capacity of phlorotannin. Aquat Toxicol 104(1–2):1–13CrossRefGoogle Scholar
  8. Cronin G (2001) Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defense theories. In: Mcclintock JB, Baker (eds) Marine chemical ecology. CRC Press, Washington D.C., pp 325–354CrossRefGoogle Scholar
  9. Cronin G, Hay ME (1996) Induction of seaweed chemical defenses by amphipod grazing. Ecology 77:2287–2301. doi: 10.2307/2265731 CrossRefGoogle Scholar
  10. Cruz-Rivera E, Hay M (2000) Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81:201–219. doi: 10.2307/177144 CrossRefGoogle Scholar
  11. Duarte C, Acuña K, Navarro JM, Gómez I (2011) Intra-plant differences in seaweed nutritional quality and chemical defenses: importance for the feeding behavior of the intertidal amphipod Orchestoidea tuberculata. J Sea Res 66:215–222. doi: 10.1016/j.seares.2011.07.007 CrossRefGoogle Scholar
  12. Duarte C, Lopez J, Benitez S, Manriquez PH, Navarro JM, Bonta CC, Torres R, Quijon P (2016) Ocean acidification induces changes in algal palatability and herbivore feeding behavior and performance. Oecologia 180:453–462. doi: 10.1007/s00442-015-3459-3 CrossRefGoogle Scholar
  13. Eklöf JS, Alsterberg C, Havenland JN, Sundbäck K, Wood HL, Gamfeld L (2012) Experimental climate change weakens the insurance effect of biodiversity. Ecol Lett 15:864–872. doi: 10.1111/j.1461-0248.2012.01810.x CrossRefGoogle Scholar
  14. Engel CR, Brawley S, Edwards KJ, Serrão E (2003) Isolation and cross-species amplification of microsatellite loci from the fucoid seaweeds Fucus vesiculosus, F. serratus, and Ascophyllum nodosum (Heterokontophyta, Fucaceae). Mol Ecol Notes 3:180–182CrossRefGoogle Scholar
  15. Falkenberg LJ, Russell BD, Connell SD (2013) Future herbivory: the indirect effects of enriched CO2 may rival its direct effects. Mar Ecol Progr Ser 492:85–95. doi: 10.3354/meps10491 CrossRefGoogle Scholar
  16. Flöthe C, Molis M, John U (2014) Induced resistance to periwinkle grazing in the brown seaweed Fucus vesiculosus (Phaeophyceae): molecular insights and seaweed-mediated effects on herbivore interactions. J Phycol 50:564–576. doi: 10.1111/jpy.12186 CrossRefGoogle Scholar
  17. Forslund H, Eriksson O, Kautsky L (2012) Grazing and geographic range of the Baltic seaweed Fucus radicans (Phaeophyceae). Mar Biol Res 8:386–394CrossRefGoogle Scholar
  18. Gruner DS, Smith JE, Seabloom EW, Sandin S, Ngai JT, Hillebrand H, Harpole WS, Elser JJ, Cleland EE, Bracken MES, Borer ET, Bolker BM (2008) A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecol Lett 11:1–16. doi: 10.1111/j.1461-0248.2008.01192.x CrossRefGoogle Scholar
  19. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 26–60Google Scholar
  20. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239CrossRefGoogle Scholar
  21. Gutow L, Rahman MM, Bartl K, Saborowski R, Bartsch I, Wiencke C (2014) Ocean acidification affects growth but not nutritional quality of the seaweed Fucus vesiculosus (Phaeophyceae, Fucales). J Exp Mar Biol Ecol 453:84–90. doi: 10.1016/j.jembe.2014.01.005 CrossRefGoogle Scholar
  22. Haavisto F, Jormalainen V (2014) Seasonality elicits herbivores’ escape from trophic control and favors induced resistance in a temperate macroalga. Ecology 95:3035–3045. doi: 10.1890/13-2387.1 CrossRefGoogle Scholar
  23. Haavisto F, Välikangas T, Jormalainen V (2010) Induced resistance in a brown alga: phlorotannins, genotypic variation and fitness costs for the crustacean herbivore. Oecologia 162:685–695. doi: 10.1007/s00442-009-1494-7 CrossRefGoogle Scholar
  24. Haavisto F, Koivikko R, Jormalainen V (2017) Defensive role of macroalgal phlorotannins: cost and benefits under natural herbivory. Mar Ecol Prog Ser 566:79–90. doi: 10.3354/meps12004 CrossRefGoogle Scholar
  25. Harley CDG, Anderson KM, Demes KW, Jorve JP, Kordas RL, Coyle TA, Graham MH (2012) Effects of climate change on global seaweed communities. J Phycol 48:1064–1078. doi: 10.1111/j.1529-8817.2012.01224.x CrossRefGoogle Scholar
  26. Hemmi A, Jormalainen V (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food alga. Ecology 83:1052–1064. doi:10.1890/0012-9658(2002)083[1052:NEIPOA]2.0.CO;2Google Scholar
  27. Hemmi A, Jormalainen V (2004) Geographic covariation of chemical quality of the host alga Fucus vesiculosus with fitness of the herbivorous isopod Idotea balthica. Mar Biol 145:759–768. doi: 10.1007/s00227-004-1360-4 Google Scholar
  28. Hemmi A, Honkanen T, Jormalainen V (2004) Inducible resistance to herbivory in Fucus vesiculosus—duration, spreading and variation with nutrient availability. Mar Ecol Prog Ser 273:109–120CrossRefGoogle Scholar
  29. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67(3):283–335. doi: 10.1086/417659 CrossRefGoogle Scholar
  30. Hillebrand H, Gruner DS, Borer ET, Bracken MES, Cleland EE, Elser JJ, Harpole WS, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Consumer versus resource control of producer diversity depends on ecosystem type and producer community structure. Proc Nat Acad Sci USA 104:10904–10909CrossRefGoogle Scholar
  31. Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed ecology and physiology, 2nd edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  32. Ilvessalo H, Tuomi J (1989) Nutrient availability and accumulation of phenolic compounds in the brown alga Fucus vesiculosus. Mar Biol 1:115–119. doi: 10.1007/BF00393484 CrossRefGoogle Scholar
  33. Johannesson K, Johansson D, Larsson KH, Huenchuñir CJ, Perus J, Forslund H, Kautsky L, Pereyra RT (2011) Frequent clonality in fucoids (Fucus radicans and Fucus vesiculosus; Fucales, Phaeophyceae) in the Baltic Sea. J Phycol 47:990–998. doi: 10.1111/j.1529-8817.2011.01032.x CrossRefGoogle Scholar
  34. Jormalainen V, Ramsay T (2009) Resistance of the brown alga Fucus vesiculosus to herbivory. Oikos 118:713–722. doi: 10.1111/j.1600-0706.2008.17178.x CrossRefGoogle Scholar
  35. Jormalainen V, Honkanen T, Mäkinen A, Hemmi A, Vesakoski O (2001) Why does herbivore sex matter? Sexual differences in utilization of Fucus vesiculosus by the isopod Idotea balthica. Oikos 93:77–86CrossRefGoogle Scholar
  36. Jormalainen V, Honkanen T, Vesakoski O (2008) Geographical divergence in host use ability of a marine herbivore in alga–grazer interaction. Evol Ecol 22:545–559. doi: 10.1007/s10682-007-9181-9 CrossRefGoogle Scholar
  37. Jormalainen V, Koivikko R, Ossipov V, Lindqvist M (2011) Quantifying variation and chemical correlates of bladderwrack quality—herbivore population makes a difference. Funct Ecol 25:900–909. doi: 10.1111/j.1365-2435.2011.01841.x CrossRefGoogle Scholar
  38. Kalbfleisch JD, Prentice RL (2002) The statistical analysis of failure time data, 2nd edn. Wiley, New Jersey, HobokenGoogle Scholar
  39. Korpinen S, Jormalainen V, Pettay E (2010) Nutrient availability modifies species abundance and community structure of Fucus-associated littoral benthic fauna. Mar Environ Res 70:283–292. doi: 10.1016/j.marenvres.2010.05.010 CrossRefGoogle Scholar
  40. Kraufvelin P, Salovius S, Hartvig C, Moy FE, Karez R, Pedersen MF (2006) Eutrophication-induced changes in benthic algae affect the behaviour and fitness of the marine amphipod Gammarus locusta. Aquat Bot 84:199–209. doi: 10.1016/j.aquabot.2005.08.008 CrossRefGoogle Scholar
  41. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models, 2nd edn. SAS Institute, CaryGoogle Scholar
  42. Long JD, Porturas L, Jones E, Kwan C, Trussell GC (2013) Seaweed traits linked to wave exposure determine predator avoidance. Mar Ecol Prog Ser 483:143–151. doi: 10.3354/meps10294 CrossRefGoogle Scholar
  43. Mackenzie BR, Schiedek D (2007) Daily ocean monitoring since the 1860s shows record warming of northern European seas. Glob Change Biol 123:1335–1347. doi: 10.1111/j.1365-2486.2007.01360.x CrossRefGoogle Scholar
  44. Meier HEM (2006) Baltic Sea climate in the late twenty-first century: a dynamical downscaling approach using two global models and two emission scenarios. Clim Dyn 27:39–68. doi: 10.1007/s00382-006-0124-x CrossRefGoogle Scholar
  45. Meier HEM, Eilola K (2011) Future projections of ecological patterns in the Baltic Sea. SMHI. Oceanografi nr 107Google Scholar
  46. Meier HEM, Kauker F (2003) Sensitivity of the Baltic Sea salinity to the freshwater supply. Clim Res 24:231–242CrossRefGoogle Scholar
  47. Neumann T (2010) Climate-change effects on the Baltic Sea ecosystem: A model study. J Marine Syst 81:213–224CrossRefGoogle Scholar
  48. Nylund GM, Pereyra RT, Wood HL, Johannesson K, Pavia H (2012) Increased resistance towards generalist herbivory in the new range of a habitat-forming seaweed. Ecosphere 3:125. doi: 10.1890/ES12-00203.1 CrossRefGoogle Scholar
  49. Pavia H, Toth GB (2008) Macroalgal models in testing and extending defense theories. In: Amsler CD (ed) Algal chemical ecology. Springer, Berlin, pp 147–167CrossRefGoogle Scholar
  50. Pavia H, Baumgartner F, Cervin G, Enge S, Kubanek J et al (2012) Chemical defences against herbivores. In: Brönmark C, Hansson LA (eds) Chemical ecology in aquatic systems. Oxford University Press, New York, pp 210–235CrossRefGoogle Scholar
  51. Pedersen A (1984) Studies on phenol content and heavy metal uptake in fucoids. Hydrobiologia 116(117):498–504CrossRefGoogle Scholar
  52. Pereyra RT, Bergström L, Kautsky L, Johannesson K (2009) Rapid speciation in a newly opened postglacial marine environment, the Baltic Sea. BMC Evol Biol 9:70CrossRefGoogle Scholar
  53. Perrin C, Daguin C, Van de Vliet M, Engel CR, Pearson GA, Serrão EA (2007) Implication of mating system for genetic diversity of sister algal species: Fucus spiralis and Fucus vesiculosus (Heterokontophyta, Phaeophyceae). Eur J Phycol 42:219–230CrossRefGoogle Scholar
  54. Philippart CJM, Anadon R, Danovaro R, Dippner JW, Drinkwater KF, Hawkins SJ, Oguz T, O’Sullivan G, Reid PC (2011) Impacts of climate change on European marine ecosystems: observations, expectations and indicators. J Exp Mar Biol Ecol 400:52–69CrossRefGoogle Scholar
  55. Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte CM, Halpern BS, Holding J, Kappel CV, O’Connor ML, 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. doi: 10.1038/nclimate1958 CrossRefGoogle Scholar
  56. Poore AGB, Campbell AH, Coleman RA, Edgar GJ, Jormalainen V, Reynolds PL, Sotka EE, Stachowicz JJ, Taylor RB, Vanderklift MA (2012) Global patterns in impact of marine herbivores on benthic primary producers. Ecol Lett 15:912–922. doi: 10.1111/j.1461-0248.2012.01804.x CrossRefGoogle Scholar
  57. Poore AG, Graba-Landry A, Favret M, Brennand HS, Byrne M, Dworjanyn SA (2013) Direct and indirect effects of ocean acidification and warming on a marine plant herbivore interaction. Oecologia 173:1113–1124. doi: 10.1007/s00442-013-2683-y CrossRefGoogle Scholar
  58. Poore AG, Graham SE, Byrne M, Dworjanyn SA (2016) Effects of ocean warming and lowered pH on algal growth and palatability to a grazing gastropod. Mar Biol 163:99. doi: 10.1007/s00227-016-2878-y CrossRefGoogle Scholar
  59. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  60. Raddatz S, Guy-Ham T, Rilov G, Wahl M (2017) Future warming and acidification effects on anti-fouling and anti-herbivory traits of the brown alga Fucus vesiculosus (Phaeophyceae). J Phycol 53:44–58CrossRefGoogle Scholar
  61. Raven J, Geider J (1988) Temperature and algal growth. N Phytol 110:441–461. doi: 10.1111/j.1469-8137.1988.tb00282.x CrossRefGoogle Scholar
  62. Rodil I, Lucena-Moya P, Olabarria C, Arenas F (2015) Alteration of macroalgal subsidies by climate-associated stressors affects behavior of wrack-reliant beach consumers. Ecosystems 18:428–440. doi: 10.1007/s10021-014-9836-7 CrossRefGoogle Scholar
  63. Rohde S, Wahl M (2008) Antifeeding defense in Baltic macroalgae: induction by direct versus waterborne cues. J Phycol 44:85–90. doi: 10.1111/j.1529-8817.2007.00451.x CrossRefGoogle Scholar
  64. Rohde S, Molis M, Wahl M (2004) Regulation of anti-herbivore defence by Fucus vesiculosus in response to various cues. J Ecol 92:1011–1018. doi: 10.1111/j.0022-0477.2004.00936.x CrossRefGoogle Scholar
  65. Rosenberg NE, Sirkus L (2011) Survival analysis using SAS: a practical guide. Second Edition By Paul D. Allison. Am J Epidemiol 174:503–504. doi: 10.1093/aje/kwr202 CrossRefGoogle Scholar
  66. Salemaa H (1978) Geographical variability in the colour polymorphism of Idotea baltica (isopoda) in the northern Baltic. Hereditas 88:165–182CrossRefGoogle Scholar
  67. Salemaa H (1979) Ecology of Idotea spp. in the northern Baltic. Ophelia 18:133–150CrossRefGoogle Scholar
  68. Schoenwaelder MEA (2002) The occurrence and cellular significance of physodes in brown algae. Phycologia 41:125–139CrossRefGoogle Scholar
  69. Simonson EJ, Scheibling RE, Metaxas A (2015a) Kelp in hot water: I. Warming seawater temperature induces weakening and loss of kelp tissue. Mar Ecol Prog Ser 537:89–104. doi: 10.3354/meps11438 CrossRefGoogle Scholar
  70. Simonson EJ, Metaxas A, Scheibling RE (2015b) Kelp in hot water: II. Effects of warming seawater temperature on kelp quality as a food source and settlement substrate. Mar Ecol Prog Ser 537:105–119. doi: 10.3354/meps11421 CrossRefGoogle Scholar
  71. Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78(1):23–55CrossRefGoogle Scholar
  72. Sudatti DB, Fuji MT, Rodrigues SV, Turra A, Pereira RC (2011) Effects of abiotic factors on growth and chemical defenses in cultivated clones of Laurencia dendroidea J. Agardh (Ceramiales, Rhodophyta). Mar Biol 158:1439–1446. doi: 10.1007/s00227-011-1660-4 CrossRefGoogle Scholar
  73. Tatarenkov A, Bergström L, Jönsson RB, Serrão EA, Kautsky L, Johannesson K (2005) Intriguing asexual life in marginal populations of the brown seaweed Fucus vesiculosus. Mol Ecol 14:647–651CrossRefGoogle Scholar
  74. Taylor RB, Sotka E, Hay ME (2002) Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132:68–76. doi: 10.1007/s00442-002-0944-2 CrossRefGoogle Scholar
  75. The BACC Author Team (2008) Assessment of climate change for the Baltic Sea Basin. Springer, BerlinCrossRefGoogle Scholar
  76. The MerMex Group (2011) Marine ecosystems’ responses to climatic and anthropogenic forcings in the Mediterranean. Prog Oceanogr 91:97–166CrossRefGoogle Scholar
  77. Toth GB, Pavia H (2007) Induced herbivore resistance in seaweeds: a meta-analysis. J Ecol 95:425–434CrossRefGoogle Scholar
  78. Vergés A, Steinberg PD, Hay ME, Poore AGB, Campbell AH, Ballesteros E, Heck KL, Booth DJ, Coleman MA, Feary DA, Figueira F, Langlois T, Marzinelli EM, Mizerek T, Mumby PJ, Nakamura Y, Roughan M, van Sebille E, Sen Gupta A, Smale DA, Tomas F, Wernberg T, Wilson SK (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 281:20140846. doi: 10.1098/rspb.2014.0846 CrossRefGoogle Scholar
  79. Vesakoski O, Boström C, Ramsay T, Jormalainen V (2008) Sexual and local divergence in host exploitation in the marine herbivore Idotea balthica (Isopoda). J Exp Mar Biol Ecol 367:118–126. doi: 10.1016/j.jembe.2008.09.006 CrossRefGoogle Scholar
  80. Vesakoski O, Rautanen J, Jormalainen V, Ramsay T (2009) Divergence in host use ability of a marine herbivore from two habitat types. J Evol Biol 22:1545–1555. doi: 10.1111/j.1420-9101.2009.01767.x CrossRefGoogle Scholar
  81. Warneke AM, Long JD (2015) Copper contamination impairs herbivore initiation of seaweed inducible defenses and decreases their effectiveness. PLoS One. doi: 10.1371/journal.pone.0135395 Google Scholar
  82. Weinberger F, Rohde S, Oschmann Y, Shahnaz L, Dobretsov S, Wahl M (2001) Effects of limitation stress and of disruptive stress on induced antigrazing defense in the bladder wrack Fucus vesiculosus. Mar Ecol Prog Ser 427:83–94. doi: 10.1111/j.0022-0477.2004.00936.x CrossRefGoogle Scholar
  83. Wernberg T, Smale DA, Thomsen MS (2012) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob Change Biol 18:1491–1498. doi: 10.1111/j.1365-2486.2012.02656.x CrossRefGoogle Scholar
  84. Wood HL, Nylund G, Eriksson SP (2014) Physiological plasticity is key to the presence of the isopod Idotea baltica (Pallas) in the Baltic Sea. J Sea Res 85:255–262CrossRefGoogle Scholar
  85. Zarnetske PL, Skelly DK, Urban MC (2012) Biotic multipliers of climate change. Science. doi: 10.1126/science.1222732 Google Scholar
  86. Zhou B, Tandg X, Wang Y (2010) Salicylic acid and heat acclimation pretreatment protects Laminaria japonica sporophyte (Phaeophyceae) from heat stress. Chin J Oceanol Limnol 28:924–932CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of BiologyUniversity of TurkuTurkuFinland

Personalised recommendations