Advertisement

Marine Biology

, 165:18 | Cite as

Variations in tolerance to climate change in a key littoral herbivore

  • Luca Rugiu
  • Iita Manninen
  • Joakim Sjöroos
  • Veijo Jormalainen
Original paper

Abstract

Changes in global climate patterns are affecting marine ecosystems, challenging species’ environmental tolerances, and driving shifts in their distributions. In the Baltic Sea, a brackish water body with low biodiversity, the isopod Idotea balthica is a key herbivore species that has a strong top–down effect on habitat-forming macrophytes. Our aim is to understand how the predicted future combination of hyposalinity and warming will affect the survival of this mesograzer throughout the Baltic Sea. By conducting a manipulative aquarium experiment, we simulated future conditions and measured the survival, at different spatial scales, of replicated populations from the entrance, central, and marginal Baltic Sea regions. Overall, the survival rate was strongly affected by the predicted future combination of hyposalinity and warming, but the intensity of the impact varied both among and within regions. Populations from the marginal Baltic Sea responded negatively to climate change. Populations within the entrance varied in their survival responses, with the geographic variation suggesting the existence of spatially distributed genetic variation in tolerance to climate change. In summary, the future combination of hyposalinity and warming is likely to induce a southward shift in the distribution of I. balthica in the northeast marginal region of the Baltic Sea. However, the geographic variation in tolerance shown by the entrance populations indicates that, for this Baltic region, the species may contain the potential for future adaptive responses in tolerance to climate change.

Notes

Acknowledgments

We thank S. Mikkonen, K. Riipinen, and E. Rothäusler for valuable assistance during sampling and laboratory work. We are also thankful to the Archipelago Research Institute of the University of Turku for the use of their facilities and logistical help.

Author contributions

VJ, LR and IM conceived and designed the experiment. LR, IM and JS performed the experiment. LR and IM analysed the data. LR led the writing of the manuscript; all authors contributed to the text.

Compliance with ethical standard

Funding

This study was funded by BONUS, the EU joint Baltic Sea research and development programme, Project BAMBI and the Academy of Finland Grant decision number 273623.

Conflict of interest

all authors declare that there is 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. Allison PD (2010) Survival analysis using the SAS system: a practical quide, 2nd edn. SAS. Institute Inc., GaryGoogle Scholar
  2. Altieri AH, Gedan KB (2015) Climate change and dead zones. Glob Chang Biol 21:1395–1406CrossRefGoogle Scholar
  3. Antonov JI (2002) Steric sea level variations during 1957–1994: importance of salinity. J Geophys Res 107:1–8CrossRefGoogle Scholar
  4. Bell G, Gonzalez A (2009) Evolutionary rescue can prevent extinction following environmental change. Ecol Lett 12:942–948CrossRefGoogle Scholar
  5. Bonsdorff E, Andersson A, Elmgren R (2015) Baltic Sea ecosystem-based management under climate change: integrating social and ecological perspectives. Ambio 44:333–334CrossRefGoogle Scholar
  6. Boyer TP, Levitus S, Antonov JI, Locarnini RA, Garcia HE (2005) Linear trends in salinity for the World Ocean, 1955–1998. Geophys Res Lett 32:1–4CrossRefGoogle Scholar
  7. Brierley AS, Kingsford MJ (2009) Impacts of climate change on marine organisms and ecosystems. Curr Biol 19:602–614CrossRefGoogle Scholar
  8. Bulnheim HP (1974) Respiratory metabolism of Idotea baltica (Crustacea, Isopoda) in relation to environmental variables, acclimation processes and moulting. Helgoländer Meeresunters 26:464–480CrossRefGoogle Scholar
  9. Coma R, Ribes M, Serrano E, Jimenez E, Salat J, Pascual J (2009) Global warming-enhanced stratification and mass mortality events in the Mediterranean. Proc Nat Acad Sci USA 106:6176–6181CrossRefGoogle Scholar
  10. Crain C, Francisco S, National B, Resear E (2008) Interactive and cumulative effects of multiple stressors in marine systems. Ecol Lett 11:1304–1315CrossRefGoogle Scholar
  11. Crispo E (2008) Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow. J Evol Biol 21:1460–1469CrossRefGoogle Scholar
  12. D’angelo C, Hume BC, Burt J, Smith EG, Achterberg EP, Wiedenmann J (2015) Local adaptation constrains the distribution potential of heat-tolerant Symbiodinium from the Persian/Arabian Gulf. ISME J 9:2551–2560CrossRefGoogle Scholar
  13. Defaveri J, Merila J (2014) Local adaptation to salinity in the three-spined stickleback? J Evol Biol 27:290–302CrossRefGoogle Scholar
  14. Dunn DW, Sumner JP, Goulson D (2005) The benefits of multiple mating to female seaweed flies, Coelopa frigida (Diptera: Coelpidae). Behav Ecol Sociobiol 58:128–135CrossRefGoogle Scholar
  15. Feistel R, Weinreben S, Wolf H, Seitz S, Spitzer P, Adel B, Nausch G, Schneider B, Wright DG (2010) Density and absolute salinity of the Baltic Sea 2006–2009. Ocean Sci 7:3–24CrossRefGoogle Scholar
  16. Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251CrossRefGoogle Scholar
  17. Goecker ME, Kåll SE (2003) Grazing preferences of marine isopods and amphipods on three prominent algal species of the Baltic Sea. J Sea Res 50:309–314CrossRefGoogle Scholar
  18. Gunnarsson K, Berglund A (2012) The brown alga Fucus radicans suffers heavy grazing by the isopod Idotea baltica. Mar Biol Res 8:87–89CrossRefGoogle Scholar
  19. Gutow L, Petersen I, Bartl K, Huenerlage K (2016) Marine meso-herbivore consumption scales faster with temperature than seaweed primary production. J Exp Mar Bio Ecol 477:80–85CrossRefGoogle Scholar
  20. Haahtela I (1984) A hypothesis of the decline of the bladder wrack Fucus vesiculosus L. in SW Finland in 1975–1981. Limnologica 15:345–350Google Scholar
  21. Haavisto F, Jormalainen V (2014) Seasonality elicits herbivores’ escape from trophic control and favors induced resistance in a temperate macroalga. Ecology 95:3035–3045CrossRefGoogle Scholar
  22. Harley CDG, 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 9:228–241CrossRefGoogle Scholar
  23. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hoffman EE, Lipp EK, Osterhaus ADME, Overstreet RM, Porter JW (1999) Emerging marine diseases: climate links and anthropogenic factors. Science 285:1505–1510CrossRefGoogle Scholar
  24. Harvell D, Aronson R, Baron N, Connell J, Dobson A, Ellner S, Gerber L, Kim K, Kuris A, McCallum H, Lafferty K (2004) The rising tide of ocean diseases: unsolved problems and research priorities. Front Ecol Environ 2:375–382CrossRefGoogle Scholar
  25. Harvey BP, Al-janabi B, Broszeit S, Cioffi R, Kumar A, Aranguren-Gassis M, Bailey A, Green L, Gsottbauer CM, Hall EF, Lechler M, Mancuso FP, Pereira CO, Ricevuto E, Schram JB, Stapp LS, Stenberg S, Rosa LTS (2014) Evolution of marine organisms under climate change at different levels of biological organisation. Water 6:3545–3574CrossRefGoogle Scholar
  26. 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
  27. Hoegh-Guldberg O, Mumby PJ, Hooten A, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742CrossRefGoogle Scholar
  28. Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485CrossRefGoogle Scholar
  29. Hørlyck V (1973) The osmoregulatory ability in three species of the genus Idotea (Isopoda, crustacea). Ophelia 12:129–140CrossRefGoogle Scholar
  30. Jansen KP (1970) Effect of temperature and salinity on survival and reproduction in Baltic populations of Sphaeroma hookeri Leach, 1814 and S. rugicauda Leach, 1814 (Isopoda). Ophelia 7:177–184Google Scholar
  31. Johannesson K, André C (2006) Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol Ecol 15:2013–2029CrossRefGoogle Scholar
  32. Johannesson K, Smolarz K, Grahn M, André C (2011) The future of Baltic Sea populations: local extinction or evolutionary rescue? Ambio 40:179–190CrossRefGoogle Scholar
  33. Jormalainen V, Ramsay T (2009) Resistance of the brown alga Fucus vesiculosus to herbivory. Oikos 118:713–722CrossRefGoogle Scholar
  34. Jormalainen V, Tuomi J (1989a) Sexual differences in habitat selection and activity of the colour polymorphic isopod Idotea baltica. Anim Behav 38:576–585CrossRefGoogle Scholar
  35. Jormalainen V, Tuomi J (1989b) Reproductive ecology of the isopod Idotea balthica (Pallas) in the Northern Baltic. Ophelia 3:213–223CrossRefGoogle Scholar
  36. Jormalainen V, Honkanen T, Makinen A, Hemmi A, Vesakoski O (2001) Why does herbivore sex matter? Sexual differences in utilization of Fucus vesiculosus by the isopod Idotea baltica. Oikos 93:77–86CrossRefGoogle Scholar
  37. Jormalainen V, Honkanen T, Vesakoski O, Koivikko R (2005) Polar extracts of the brown alga Fucus vesiculosus (L.) reduce assimilation efficiency but do not deter the herbivorous isopod Idotea baltica (Pallas). J Exp Mar Bio Ecol 317:143–157CrossRefGoogle Scholar
  38. Kalbfleisch JD, Prentice RL (1980) Statistical analysis of failure time data. Wiley, New YorkGoogle Scholar
  39. Kangas P, Autio H, Hällfors G, Luther H, Niemi Å, Salemaa H (1982) A general model of the decline of Fucus vesiculosus at Tvärminne, south coast of Finland in 1977–81. Acta Bot Fenn 118:1–27Google Scholar
  40. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  41. Knights AM, Firth LB, Russell BD (2017) Ecological responses to environmental change in marine systems. J Mar Biol Ecol 492:1–140CrossRefGoogle Scholar
  42. Lamichhaney S, Barrio AM, Rafati N (2012) Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring. Proc Natl Acad Sci USA 109:19345–19350CrossRefGoogle Scholar
  43. Łapucki T, Normant M (2008) Physiological responses to salinity changes of the isopod Idotea chelipes from the Baltic brackish waters. Comp Biochem Physiol: Mol Integr Physiol 149:299–305CrossRefGoogle Scholar
  44. Lass HU, Matthäus U (2008) General oceanography of the Baltic Sea. In: Feistel R, Nausch G, Wasmund N (eds) State and evolution of the Baltic Sea, 1952–2005. Wiley, Hoboken, pp 5–44Google Scholar
  45. Leidenberger S, Harding K, Jonsson PR (2012) Ecology and distribution of the isopod genus Idotea in the Baltic Sea: key species in a changing environment. J Crustac Biol 32:359–381CrossRefGoogle Scholar
  46. Lenoir J, Svenning JC (2015) Climate-related range shifts—a global multidimensional synthesis and new research directions. Ecography 38:15–28CrossRefGoogle Scholar
  47. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models, 2nd edn. SAS Institute, CaryGoogle Scholar
  48. Meier HEM, Eilola K (2011) Future projections of ecological patterns in the Baltic Sea. SMHI Reports, Oceanografi 107Google Scholar
  49. Meier HEM, Hordoir R, Andersson HC, Dieterich C, Eilola K, Gustafsson BG, Höglund A, Schimanke S (2012) Modeling the combined impact of changing climate and changing nutrient loads on the Baltic Sea environment in an ensemble of transient simulations for 1961–2099. Clim Dyn 39:2421–2441CrossRefGoogle Scholar
  50. Muir AP, Nunes FL, Dubois SF, Pernet F (2016) Lipid remodelling in the reef-building honeycomb worm, Sabellaria alveolata, reflects acclimation and local adaptation to temperature. Sci Rep 6:35669CrossRefGoogle Scholar
  51. Nilsson J, Engkvist R, Persson LE (2004) Long-term decline and recent recovery of Fucus populations along the rocky shores of southeast Sweden, Baltic Sea. Aquat Ecol 38:587–598CrossRefGoogle Scholar
  52. Normant M, Lamprecht I (2006) Does scope for growth change as a result of salinity stress in the amphipod Gammarus oceanicus? J Exp Mar Bio Ecol 334:158–163CrossRefGoogle Scholar
  53. Orav-Kotta H, Kotta J (2004) Food and habitat choice of the isopod Idotea baltica in the northeastern Baltic Sea. Hydrobiologia 514:79–85CrossRefGoogle Scholar
  54. Pauls SU, Nowak C, Bálint M, Pfenninger M (2013) The impact of global climate change on genetic diversity within populations and species. Mol Ecol 22:925–946CrossRefGoogle Scholar
  55. Poloczanska ES, Babcock RC, Butler A, Hobday AJ, Hoegh-Guldberg O, Kunz TJ, Matear R, Milton DA, Okey TA, Richardson AJ (2007) Climate change and Australian marine life. Ocean Mar Biol Annu Rev 45:407–478Google Scholar
  56. Pörtner HO (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146CrossRefGoogle Scholar
  57. Postel U, Becker W, Brandt A, Luck-Kopp S, Riestenpatt S, Weihrauch D, Siebers D (2000) Active osmoregulatory ion uptake across the pleopods of the isopod Idotea baltica (Pallas): electrophysiological measurements on isolated split endo- and exopodites mounted in a micro-ussing chamber. J Exp Biol 203:1141–1152Google Scholar
  58. Przeslawski R, Ahyong S, Byrne M, Wörheide G, Hutchings P (2008) Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs. Glob Chang Biol 14:2773–2795CrossRefGoogle Scholar
  59. Qiu J-W, Qian P-Y (1999) Tolerance of the barnacle Balanus amphitrite to salinity and temperature stress: effects of previous experience. Mar Ecol Prog Ser 188:123–132CrossRefGoogle Scholar
  60. Ravanko O (1969) Benthic algae as food for some invertebrates in the inner part of the Baltic. Limnologica 7:203–205Google Scholar
  61. Rivera-Ingraham GA, Lignot JH (2017) Osmoregulation, bioenergetics and oxidative stress in coastal marine invertebrates: raising the questions for future research. J Exp Biol 220:1749–1760CrossRefGoogle Scholar
  62. Rosenberg NE, Sirkus L (2011) Survival analysis using SAS: a practical guide. Second Edition By Paul D. Allison. Am J Epidemiol 174:503–504CrossRefGoogle Scholar
  63. Roth O, Kurtz J, Reusch TBH (2010) A summer heat wave decreases the immunocompetence of the mesograzer, Idotea balthica. Mar Biol 157:1605–1611CrossRefGoogle Scholar
  64. Saada G, Nicastro KR, Jacinto R, McQuaid CD, Serrão EA, Pearson GA, Zardi GI, Schoeman D (2016) Taking the heat: distinct vulnerability to thermal stress of central and threatened peripheral lineages of a marine macroalga. Divers Distrib 22:1060–1068CrossRefGoogle Scholar
  65. Salemaa H (1979) Ecology of Idotea spp (Isopoda) in the northern Baltic. Ophelia 18:133–150CrossRefGoogle Scholar
  66. Salemaa H (1987) Herbivory and microhabitat preferences of Idotea spp. (Isopoda) in the northern Baltic Sea. Ophelia 27:1–15CrossRefGoogle Scholar
  67. Salomon M, Buchholz F (2000) Effects of temperature on the respiration rates and the kinetics of citrate synthase in two species of Idotea (Isopoda, Crustacea). Comp Biochem Physiol: B Biochem Mol Biol 125:71–81CrossRefGoogle Scholar
  68. Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Annu Rev Mar Sci 3:509–535CrossRefGoogle Scholar
  69. Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430CrossRefGoogle Scholar
  70. Strong KW, Daborn GR (1980) The influence of temperature on energy budget variables, body size, and seasonal occurrence of the isopod Idotea balhtica (Pallas). Can J Zool 58:1992–1996CrossRefGoogle Scholar
  71. Torres G, Giménez L, Anger K (2011) Growth, tolerance to low-salinity, and osmoregulation in decapod crustacean larvae. Aquat Biol 12:249–260CrossRefGoogle Scholar
  72. Valladares F, Matesanz S, Araujo MB, Balaguer L, Benito-Garzon M, Cornwell WK, Gianoli E, Guilhaumon F, van Kleunen M, Naya D, Nicotra AB, Poorter H, Zavala MA (2014) The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol Lett 17:1351–1364CrossRefGoogle Scholar
  73. Vergés A, Steinberg PD, Hay ME, Poore AGB, Campbell AH, Ballesteros E, Heck KL, Booth DJ, Coleman MA, Feary DA, Figueira W, 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 The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 281:1–10CrossRefGoogle Scholar
  74. Wernberg T, Smale DA, Thomsen MS (2012) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob Chang Biol 18:1491–1498CrossRefGoogle Scholar
  75. Werner FJ, Graiff A, Matthiessen B (2015) Temperature effects on seaweed-sustaining top-down control vary with season. Oecologia 180:889–901CrossRefGoogle Scholar
  76. Wood HL, Nylund G, Eriksson SP (2014) Physiological plasticity is key to the presence of the isopod Idotea balthica (Pallas) in the Baltic Sea. J Sea Res 85:255–262CrossRefGoogle Scholar
  77. Wrange AL, André C, Lundh T, Lind U, Blomberg A, Jonsson PJ, Havenhand JN (2014) Importance of plasticity and local adaptation for coping with changing salinity in coastal areas: a test case with barnacles in the Baltic Sea. BMC Evol Biol 14:156CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland

Personalised recommendations