Skip to main content

Advertisement

SpringerLink
Log in

Variations in tolerance to climate change in a key littoral herbivore

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allison PD (2010) Survival analysis using the SAS system: a practical quide, 2nd edn. SAS. Institute Inc., Gary

    Google Scholar 

  • Altieri AH, Gedan KB (2015) Climate change and dead zones. Glob Chang Biol 21:1395–1406

    Article  Google Scholar 

  • Antonov JI (2002) Steric sea level variations during 1957–1994: importance of salinity. J Geophys Res 107:1–8

    Article  Google Scholar 

  • Bell G, Gonzalez A (2009) Evolutionary rescue can prevent extinction following environmental change. Ecol Lett 12:942–948

    Article  Google Scholar 

  • Bonsdorff E, Andersson A, Elmgren R (2015) Baltic Sea ecosystem-based management under climate change: integrating social and ecological perspectives. Ambio 44:333–334

    Article  Google Scholar 

  • Boyer TP, Levitus S, Antonov JI, Locarnini RA, Garcia HE (2005) Linear trends in salinity for the World Ocean, 1955–1998. Geophys Res Lett 32:1–4

    Article  Google Scholar 

  • Brierley AS, Kingsford MJ (2009) Impacts of climate change on marine organisms and ecosystems. Curr Biol 19:602–614

    Article  Google Scholar 

  • Bulnheim HP (1974) Respiratory metabolism of Idotea baltica (Crustacea, Isopoda) in relation to environmental variables, acclimation processes and moulting. Helgoländer Meeresunters 26:464–480

    Article  Google Scholar 

  • 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 106:6176–6181

    Article  CAS  Google Scholar 

  • Crain C, Francisco S, National B, Resear E (2008) Interactive and cumulative effects of multiple stressors in marine systems. Ecol Lett 11:1304–1315

    Article  Google Scholar 

  • Crispo E (2008) Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow. J Evol Biol 21:1460–1469

    Article  CAS  Google Scholar 

  • 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 9:2551–2560

    Article  Google Scholar 

  • Defaveri J, Merila J (2014) Local adaptation to salinity in the three-spined stickleback? J Evol Biol 27:290–302

    Article  CAS  Google Scholar 

  • Dunn DW, Sumner JP, Goulson D (2005) The benefits of multiple mating to female seaweed flies, Coelopa frigida (Diptera: Coelpidae). Behav Ecol Sociobiol 58:128–135

    Article  Google Scholar 

  • 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 7:3–24

    Article  Google Scholar 

  • Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251

    Article  CAS  Google Scholar 

  • Goecker ME, Kåll SE (2003) Grazing preferences of marine isopods and amphipods on three prominent algal species of the Baltic Sea. J Sea Res 50:309–314

    Article  Google Scholar 

  • Gunnarsson K, Berglund A (2012) The brown alga Fucus radicans suffers heavy grazing by the isopod Idotea baltica. Mar Biol Res 8:87–89

    Article  Google Scholar 

  • 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 477:80–85

    Article  Google Scholar 

  • Haahtela I (1984) A hypothesis of the decline of the bladder wrack Fucus vesiculosus L. in SW Finland in 1975–1981. Limnologica 15:345–350

    Google Scholar 

  • Haavisto F, Jormalainen V (2014) Seasonality elicits herbivores’ escape from trophic control and favors induced resistance in a temperate macroalga. Ecology 95:3035–3045

    Article  Google Scholar 

  • 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 9:228–241

    Article  Google Scholar 

  • 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 285:1505–1510

    Article  CAS  Google Scholar 

  • 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 2:375–382

    Article  Google Scholar 

  • 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 6:3545–3574

    Article  Google Scholar 

  • 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 37:373–404

    Article  Google Scholar 

  • 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 318:1737–1742

    Article  CAS  Google Scholar 

  • Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485

    Article  CAS  Google Scholar 

  • Hørlyck V (1973) The osmoregulatory ability in three species of the genus Idotea (Isopoda, crustacea). Ophelia 12:129–140

    Article  Google Scholar 

  • 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 7:177–184

    Google Scholar 

  • Johannesson K, André C (2006) Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol Ecol 15:2013–2029

    Article  CAS  Google Scholar 

  • Johannesson K, Smolarz K, Grahn M, André C (2011) The future of Baltic Sea populations: local extinction or evolutionary rescue? Ambio 40:179–190

    Article  CAS  Google Scholar 

  • Jormalainen V, Ramsay T (2009) Resistance of the brown alga Fucus vesiculosus to herbivory. Oikos 118:713–722

    Article  Google Scholar 

  • Jormalainen V, Tuomi J (1989a) Sexual differences in habitat selection and activity of the colour polymorphic isopod Idotea baltica. Anim Behav 38:576–585

    Article  Google Scholar 

  • Jormalainen V, Tuomi J (1989b) Reproductive ecology of the isopod Idotea balthica (Pallas) in the Northern Baltic. Ophelia 3:213–223

    Article  Google Scholar 

  • 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 93:77–86

    Article  Google Scholar 

  • 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 317:143–157

    Article  Google Scholar 

  • Kalbfleisch JD, Prentice RL (1980) Statistical analysis of failure time data. Wiley, New York

    Google Scholar 

  • 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 118:1–27

    Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Knights AM, Firth LB, Russell BD (2017) Ecological responses to environmental change in marine systems. J Mar Biol Ecol 492:1–140

    Article  Google Scholar 

  • 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 109:19345–19350

    Article  CAS  Google Scholar 

  • 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 149:299–305

    Article  Google Scholar 

  • 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 5–44

    Google Scholar 

  • 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 32:359–381

    Article  Google Scholar 

  • Lenoir J, Svenning JC (2015) Climate-related range shifts—a global multidimensional synthesis and new research directions. Ecography 38:15–28

    Article  Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models, 2nd edn. SAS Institute, Cary

    Google Scholar 

  • Meier HEM, Eilola K (2011) Future projections of ecological patterns in the Baltic Sea. SMHI Reports, Oceanografi 107

  • 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 39:2421–2441

    Article  Google Scholar 

  • 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 6:35669

    Article  CAS  Google Scholar 

  • 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 38:587–598

    Article  Google Scholar 

  • 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 334:158–163

    Article  Google Scholar 

  • Orav-Kotta H, Kotta J (2004) Food and habitat choice of the isopod Idotea baltica in the northeastern Baltic Sea. Hydrobiologia 514:79–85

    Article  Google Scholar 

  • Pauls SU, Nowak C, Bálint M, Pfenninger M (2013) The impact of global climate change on genetic diversity within populations and species. Mol Ecol 22:925–946

    Article  Google Scholar 

  • 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 45:407–478

    Google Scholar 

  • Pörtner HO (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146

    Article  Google Scholar 

  • 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 203:1141–1152

    CAS  Google Scholar 

  • 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 14:2773–2795

    Article  Google Scholar 

  • 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 188:123–132

    Article  Google Scholar 

  • Ravanko O (1969) Benthic algae as food for some invertebrates in the inner part of the Baltic. Limnologica 7:203–205

    Google Scholar 

  • Rivera-Ingraham GA, Lignot JH (2017) Osmoregulation, bioenergetics and oxidative stress in coastal marine invertebrates: raising the questions for future research. J Exp Biol 220:1749–1760

    Article  Google Scholar 

  • Rosenberg NE, Sirkus L (2011) Survival analysis using SAS: a practical guide. Second Edition By Paul D. Allison. Am J Epidemiol 174:503–504

    Article  Google Scholar 

  • Roth O, Kurtz J, Reusch TBH (2010) A summer heat wave decreases the immunocompetence of the mesograzer, Idotea balthica. Mar Biol 157:1605–1611

    Article  Google Scholar 

  • 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 22:1060–1068

    Article  Google Scholar 

  • Salemaa H (1979) Ecology of Idotea spp (Isopoda) in the northern Baltic. Ophelia 18:133–150

    Article  Google Scholar 

  • Salemaa H (1987) Herbivory and microhabitat preferences of Idotea spp. (Isopoda) in the northern Baltic Sea. Ophelia 27:1–15

    Article  Google Scholar 

  • 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 125:71–81

    Article  CAS  Google Scholar 

  • Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Annu Rev Mar Sci 3:509–535

    Article  Google Scholar 

  • Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430

    Article  Google Scholar 

  • 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 58:1992–1996

    Article  Google Scholar 

  • Torres G, Giménez L, Anger K (2011) Growth, tolerance to low-salinity, and osmoregulation in decapod crustacean larvae. Aquat Biol 12:249–260

    Article  Google Scholar 

  • 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 17:1351–1364

    Article  Google Scholar 

  • 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 281:1–10

    Article  Google Scholar 

  • Wernberg T, Smale DA, Thomsen MS (2012) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob Chang Biol 18:1491–1498

    Article  Google Scholar 

  • Werner FJ, Graiff A, Matthiessen B (2015) Temperature effects on seaweed-sustaining top-down control vary with season. Oecologia 180:889–901

    Article  Google Scholar 

  • 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 85:255–262

    Article  Google Scholar 

  • 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 14:156

    Article  Google Scholar 

Download references

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 information

Authors and Affiliations

  1. Section of Ecology, Department of Biology, University of Turku, 20014, Turku, Finland

    Luca Rugiu, Iita Manninen, Joakim Sjöroos & Veijo Jormalainen

Authors
  1. Luca Rugiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Iita Manninen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joakim Sjöroos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Veijo Jormalainen
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Corresponding author

Correspondence to Luca Rugiu.

Ethics declarations

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.

Additional information

Responsible Editor: F. Bulleri.

Reviewed by undisclosed experts.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rugiu, L., Manninen, I., Sjöroos, J. et al. Variations in tolerance to climate change in a key littoral herbivore. Mar Biol 165, 18 (2018). https://doi.org/10.1007/s00227-017-3275-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-017-3275-x

Search

Navigation