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Genotypic variation influences tolerance to warming and acidification of early life-stage Fucus vesiculosus L. (Phaeophyceae) in a seasonally fluctuating environment

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Abstract

Global change exposes brown algal Fucus vesiculosus populations to increasing temperature and pCO2, which may threaten individuals, in particular the early life-stages. Genetic diversity of F. vesiculosus populations is low in the Baltic compared to Atlantic populations. This might jeopardise their potential for adaptation to environmental changes. Here, we report on the responses of early life-stage F. vesiculosus to warming and acidification in a near-natural scenario maintaining natural and seasonal variation (spring 2013–2014) of the Kiel Fjord in the Baltic Sea, Germany (54°27ʹN, 10°11ʹW). We assessed how stress sensitivity differed among sibling groups and how genetic diversity of germling populations affected their stress tolerance. Warming increased growth rates of Fucus germlings in spring and in early summer, but led to higher photoinhibition in spring and decreased their survival in late summer. Acidification increased germlings’ growth in summer but otherwise showed much weaker effects than warming. During the colder seasons (autumn and winter), growth was slow while survival was high compared to spring and summer, all at ambient temperatures. A pronounced variation in stress response among genetically different sibling groups (full-sib families) suggests a genotypic basis for this variation and thus a potential for adaptation for F. vesiculosus populations to future conditions. Corroborating this, survival in response to warming in populations with higher diversity was better than the mean survival of single sibling groups. We conclude that impacts on early life-stages depend on the combination of stressors and season and that genetic variation is crucial for the tolerance to global change stress.

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References

  • Aguirre JD, Marshall DJ (2012) Does genetic diversity reduce sibling competition? Evolution 66:94–102. doi:10.1111/j.1558-5646.2011.01413.x

    Article  Google Scholar 

  • Allakhverdiev S, Kreslavski V, Klimov V, Los D, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550. doi:10.1007/s11120-008-9331-0

    Article  CAS  Google Scholar 

  • Beardall J, Giordano M (2002) Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms, and their regulation. Funct Plant Biol 29:335–347. doi:10.1071/PP01195

    Article  CAS  Google Scholar 

  • Berger R, Bergström L, Granéli E, Kautsky L (2004) How does eutrophication affect different life stages of Fucus vesiculosus in the Baltic Sea?—a conceptual model. Hydrobiologia 514:243–248. doi:10.1023/B:hydr.0000018222.44511.b7

    Article  Google Scholar 

  • Bertness MD, Leonard GH (1997) The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78:1976–1989

    Article  Google Scholar 

  • Bonsdorff E (2006) Zoobenthic diversity-gradients in the Baltic Sea: continuous post-glacial succession in a stressed ecosystem. J Exp Mar Biol Ecol 330:383–391

    Article  Google Scholar 

  • Caruso CM, Maherali H, Mikulyuk A, Carlson K, Jackson RB (2005) Genetic variance and covariance for physiological traits in Lobelia: are there constraints on adaptive evolution? Evolution 59:826–837

    Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143. doi:10.1111/j.1442-9993.1993.tb00438.x

    Article  Google Scholar 

  • Coelho S, Rijstenbil J, Brown M (2000) Impacts of anthropogenic stresses on the early development stages of seaweeds. J Aquat Ecosyst Stress Recovery 7:317–333. doi:10.1023/A:1009916129009

    Article  CAS  Google Scholar 

  • da Gama BAP, Plouguerné E, Pereira RC (2014) Chapter fourteen—The antifouling defence mechanisms of marine macroalgae. In: Nathalie B (ed) Adv Bot Res. Academic Press, Cambridge, pp 413–440

    Google Scholar 

  • Ehlers A, Worm B, Reusch TBH (2008) Importance of genetic diversity in eelgrass Zostera marina for its resilience to global warming. Mar Ecol Prog Ser 355:1–7. doi:10.3354/meps07369

    Article  Google Scholar 

  • Elken J, Lehmann A, Myrberg K (2015) Recent change—marine circulation and stratification. In: The BACC II Author Team (eds) Second assessment of climate change for the Baltic Sea basin. Springer, pp 131–144

  • Eriksson BK, Johansson G, Snoeijs P (1998) Long-term changes in the sublittoral zonation of brown algae in the southern Bothnian Sea. Eur J Phycol 33:241–249. doi:10.1080/09670269810001736743

    Article  Google Scholar 

  • Folt CL, Chen CY, Moore MV, Burnaford J (1999) Synergism and antagonism among multiple stressors. Limnol Oceanogr 44:864–877. doi:10.4319/lo.1999.44.3_part_2.0864

    Article  Google Scholar 

  • Forster RM, Dring MJ (1992) Interactions of blue light and inorganic carbon supply in the control of light-saturated photosynthesis in brown algae. Plant Cell Environ 15:241–247. doi:10.1111/j.1365-3040.1992.tb01478.x

    Article  CAS  Google Scholar 

  • Frankham R (2003) Genetics and conservation biology. CR Biol 326(S1):22–29. doi:10.1016/S1631-0691(03)00023-4

    Article  Google Scholar 

  • Frankham R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv 143:1919–1927. doi:10.1016/j.biocon.2010.05.011

    Article  Google Scholar 

  • Frankham R, Ballou JD, Bricoe DA (2009) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Gamfeldt L, Wallén J, Jonsson PR, Berntsson KM, Havenhand JN (2005) Increasing intraspecific diversity enhances settling success in a marine invertebrate. Ecology 86:3219–3224. doi:10.1890/05-0377

    Article  Google Scholar 

  • Gordillo FJL, Niell FX, Figueroa FL (2001) Non-photosynthetic enhancement of growth by high CO2 level in the nitrophilic seaweed Ulva rigida C. Agardh (Chlorophyta). Planta 213:64–70. doi:10.1007/s004250000468

    Article  CAS  Google Scholar 

  • Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Funct Plant Biol 22:131–160. doi:10.1071/PP9950131

    CAS  Google Scholar 

  • Graham LP, Chen D, Christensen OB, Kjellström E, Krysanova V, Meier HEM, Radziejewski M, Räisänen J, Rockel B, Ruosteenoja K (2008) Projections of future anthropogenic climate change. In: The Baltic Sea Author Team (eds) Assessment of climate change for the Baltic Sea basin

  • Graiff A, Liesner D, Karsten U, Bartsch I (2015) Temperature tolerance of western Baltic Sea Fucus vesiculosus—growth, photosynthesis and survival. J Exp Mar Biol Ecol 471:8–16. doi:10.1016/j.jembe.2015.05.009

    Article  Google Scholar 

  • Hanelt D (1998) Capability of dynamic photoinhibition in Arctic macroalgae is related to their depth distribution. Mar Biol 131:361–369. doi:10.1007/s002270050329

    Article  Google Scholar 

  • Harvey B, Al-Janabi B, Broszeit S et al (2014) Evolution of marine organisms under climate change at different levels of biological organisation. Water 6:3545–3574

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Honkanen T, Jormalainen V (2005) Genotypic variation in tolerance and resistance to fouling in the brown alga Fucus vesiculosus. Oecologia 144:196–205. doi:10.1007/s00442-005-0053-0

    Article  Google Scholar 

  • Hooper DU, Chapin FS, Ewel JJ, Hector A et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35. doi:10.1890/04-0922

    Article  Google Scholar 

  • Hughes AR, Stachowicz JJ (2004) Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc Natl Acad Sci USA 101:8998–9002. doi:10.1073/pnas.0402642101

    Article  CAS  Google Scholar 

  • IPCC (2013) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate Change. Cambridge University Press, Cambridge

    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. doi:10.1111/j.1365-294X.2006.02919.x

    Article  CAS  Google Scholar 

  • Johannesson K, Johansson D, Larsson KH et al (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

    Article  Google Scholar 

  • Johnson VR, Russell BD, Fabricius KE, Brownlee C, Hall-Spencer JM (2012) Temperate and tropical brown macroalgae thrive, despite decalcification, along natural CO2 gradients. Global Change Biol 18:2792–2803. doi:10.1111/j.1365-2486.2012.02716.x

    Article  Google Scholar 

  • Jueterbock A, Tyberghein L, Verbruggen H, Coyer JA, Olsen JL, Hoarau G (2013) Climate change impact on seaweed meadow distribution in the North Atlantic rocky intertidal. Ecol Evol 3:1356–1373. doi:10.1002/ece3.541

    Article  Google Scholar 

  • Klenell M, Snoeijs P, Pedersén M (2004) Active carbon uptake in Laminaria digitata and L. saccharina (Phaeophyta) is driven by a proton pump in the plasma membrane. Hydrobiologia 514:41–53. doi:10.1023/B:hydr.0000018205.80186.3e

    Article  CAS  Google Scholar 

  • Koch M, Bowes G, Ross C, Zhang X-H (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biol 19:103–132. doi:10.1111/j.1365-2486.2012.02791.x

    Article  Google Scholar 

  • Lamote M, Johnson L (2008) Temporal and spatial variation in the early recruitment of fucoid algae: the role of microhabitats and temporal scales. Mar Ecol Prog Ser 368:93–102. doi:10.3354/meps07592

    Article  Google Scholar 

  • Lavaud J, Rousseau B, Etienne AL (2002a) In diatoms, a transthylakoid proton gradient alone is not sufficient to induce a non-photochemical fluorescence quenching. FEBS Lett 523:163–166

    Article  CAS  Google Scholar 

  • Lavaud J, Rousseau B, van Gorkom HJ, Etienne AL (2002b) Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiol 129:1398–1406. doi:10.1104/pp.002014

    Article  CAS  Google Scholar 

  • Lehvo A, Bäck S, Kiirikki M (2001) Growth of Fucus vesiculosus L (Phaeophyta) in the northern Baltic proper: energy and nitrogen storage in seasonal environment. Bot Mar 44:345–350

    Article  Google Scholar 

  • Li R, Brawley SH (2004) Improved survival under heat stress in intertidal embryos (Fucus spp.) simultaneously exposed to hypersalinity and the effect of parental thermal history. Mar Biol 144:205–213. doi:10.1007/s00227-003-1190-9

    Article  Google Scholar 

  • Lotze HK, Worm B, Sommer U (2001) Strong bottom-up and top-down control of early life stages of macroalgae. Limnol Oceanogr 46:749–757. doi:10.4319/lo.2001.46.4.0749

    Article  Google Scholar 

  • Maczassek K (2014) Environmental drivers of fertility, fertilization and germination of Fucus vesiculosus on the German coast. Dissertation. University of Kiel

  • Nicastro K, Zardi G, Teixeira S, Neiva J, Serrão E, Pearson G (2013) Shift happens: trailing edge contraction associated with recent warming trends threatens a distinct genetic lineage in the marine macroalga Fucus vesiculosus. BMC Biol 11:1–13. doi:10.1186/1741-7007-11-6

    Article  Google Scholar 

  • Nielsen S, Nielsen H, Pedersen M (2014) Juvenile life stages of the brown alga Fucus serratus L. are more sensitive to combined stress from high copper concentration and temperature than adults. Mar Biol 161:1895–1904. doi:10.1007/s00227-014-2471-1

    Article  CAS  Google Scholar 

  • Nygård CA, Dring MJ (2008) Influence of salinity, temperature, dissolved inorganic carbon and nutrient concentration on the photosynthesis and growth of Fucus vesiculosus from the Baltic and Irish Seas. Eur J Phycol 43:253–262. doi:10.1080/09670260802172627

    Article  Google Scholar 

  • Olischläger M, Bartsch I, Gutow L, Wiencke C (2012) Effects of ocean acidification on different life-cycle stages of the kelp Laminaria hyperborea (Phaeophyceae). Bot Mar 55(5):511–525

    Article  Google Scholar 

  • Olischläger M, Bartsch I, Gutow L, Wiencke C (2013) Effects of ocean acidification on growth and physiology of Ulva lactuca (Chlorophyta) in a rockpool-scenario. Phycol Res 61:180–190. doi:10.1111/pre.12006

    Article  Google Scholar 

  • Pansch C, Schaub I, Havenhand J, Wahl M (2014) Habitat traits and food availability determine the response of marine invertebrates to ocean acidification. Global Change Biol 20:765–777. doi:10.1111/gcb.12478

    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. doi:10.1111/mec.12152

    Article  Google Scholar 

  • Pereyra R, Bergström L, Kautsky L, Johannesson K (2009) Rapid speciation in a newly opened postglacial marine environment, the Baltic Sea. BMC Evol Biol 9:70

    Article  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reusch TH, Hughes AR (2006) The emerging role of genetic diversity for ecosystem functioning: estuarine macrophytes as models. Estuar Coasts J ERF 29:159–164. doi:10.1007/BF02784707

    Article  Google Scholar 

  • Reusch TBH, Wood TE (2007) Molecular ecology of global change. Mol Ecol 16:3973–3992. doi:10.1111/j.1365-294X.2007.03454.x

    Article  CAS  Google Scholar 

  • Reusch TBH, Ehlers A, Hämmerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc Natl Acad Sci USA 102:2826–2831. doi:10.1073/pnas.0500008102

    Article  CAS  Google Scholar 

  • Rickert E, Karsten U, Pohnert G, Wahl M (2015) Seasonal fluctuations of chemical defenses against macrofouling in F. vesiculosus and F. serratus from the Baltic Sea. Biofouling 31:363–377

    Article  CAS  Google Scholar 

  • Rohde S, Hiebenthal C, Wahl M, Karez R, Bischof K (2008) Decreased depth distribution of Fucus vesiculosus (Phaeophyceae) in the Western Baltic: effects of light deficiency and epibionts on growth and photosynthesis. Eur J Phycol 43:143–150. doi:10.1080/09670260801901018

    Article  Google Scholar 

  • Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450: 575–578. http://www.nature.com/nature/journal/v450/n7169/suppinfo/nature06262_S1.html

  • Saderne V, Fietzek P, Herman PMJ (2013) Extreme variations of pCO2 and pH in a macrophyte meadow of the Baltic Sea in summer: evidence of the effect of photosynthesis and local upwelling. PLoS One 8:e62689. doi:10.1371/journal.pone.0062689

    Article  CAS  Google Scholar 

  • Sarker MY, Bartsch I, Olischläger M, Gutow L, Wiencke, C (2013) Combined effects of CO2, temperature, irradiance and time on the physiological performance of Chondrus crispus (Rhodophyta). Bot Mar 56:63–74

    Article  Google Scholar 

  • Schmid R, Mills JA, Dring MJ (1996) Influence of carbon supply on the stimulation of light-saturated photosynthesis by blue light in Laminaria saccharina: implications for the mechanism of carbon acquisition in higher brown algae. Plant Cell Environ 19:383–391. doi:10.1111/j.1365-3040.1996.tb00330.x

    Article  CAS  Google Scholar 

  • Schmidt A, Coll M, Romanuk T, Lotze H (2011) Ecosystem structure and services in eelgrass Zostera marina and rockweed Ascophyllum nodosum habitats. Mar Ecol Prog Ser 437:51–68. doi:10.3354/meps09276

    Article  Google Scholar 

  • Schneider B, Eilola K, Lukkari K, Muller-Karulis B, Neumann T (2015) Environmental impacts—Marine biogeochemistry. In: The BACC II Author Team (eds) Second assessment of climate change for the Baltic Sea basin. Springer, pp 337–361

  • Serôdio J, Lavaud J (2011) A model for describing the light response of the nonphotochemical quenching of chlorophyll fluorescence. Photosynth Res 108:61–76. doi:10.1007/s11120-011-9654-0

    Article  Google Scholar 

  • Serrão EA, Kautsky L, Brawley SH (1996) Distributional success of the marine seaweed Fucus vesiculosus L. in the brackish Baltic Sea correlates with osmotic capabilities of Baltic gametes. Oecologia 107:1–12

    Article  Google Scholar 

  • Steen H, Scrosati R (2004) Intraspecific competition in Fucus serratus and F. evanescens (Phaeophyceae: Fucales) germlings: effects of settlement density, nutrient concentration, and temperature. Mar Biol 144:61–70. doi:10.1007/s00227-003-1175-8

    Article  Google Scholar 

  • Tatarenkov A, Jönsson RB, Kautsky L, Johannesson K (2007) Genetic structure in populations of Fucus vesiculosus (Phaeophyceae) over spatial scales from 10 m to 800 km. J Phycol 43:675–685. doi:10.1111/j.1529-8817.2007.00369.x

    Article  CAS  Google Scholar 

  • Torn K, Krause-Jensen D, Martin G (2006) Present and past depth distribution of bladderwrack (Fucus vesiculosus) in the Baltic Sea. Aquat Bot 84:53–62. doi:10.1016/j.aquabot.2005.07.011

    Article  Google Scholar 

  • Violle C, Enquist BJ, McGill BJ et al (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252. doi:10.1016/j.tree.2011.11.014

    Article  Google Scholar 

  • Vogt H, Schramm W (1991) Conspicuous decline of Fucus in Kiel Bay (Western Baltic): what are the causes? Mar Ecol Prog Ser 69:189–194

    Article  Google Scholar 

  • Wahl M, Hay ME (1995) Associational resistance and shared doom: effects of epibiosis on herbivory. Oecologia 102:329–340. doi:10.1007/BF00329800

    Article  Google Scholar 

  • Wahl M, Jormalainen V, Eriksson BK et al (2011) Stress ecology in Fucus: abiotic, biotic and genetic interactions. Adv Mar Biol 59:37–105. doi:10.1016/b978-0-12-385536-7.00002-9

    Article  Google Scholar 

  • Wahl M, Molis M, Hobday AJ et al (2015a) The responses of brown macroalgae to environmental change from local to global scales: direct versus ecologically mediated effects. Perspec Phycol. doi:10.1127/pip/2015/0019

    Google Scholar 

  • Wahl M, Buchholz B, Winde V et al (2015b) A novel mesocosm concept for the simulation of shallow underwater climates: the Kiel Outdoor Benthocosms (KOB). Limnol Oceanogr Methods. doi:10.1002/lom3.10055

    Google Scholar 

  • Wahl M, Saderne V, Sawall Y (2015c) How good are we at assessing the impact of ocean acidification in coastal systems? Limitations, omissions and strengths of commonly used experimental approaches with special emphasis on the neglected role of fluctuations. Mar Freshwater Res. doi:10.1071/MF14154

    Google Scholar 

  • Walsby AE (1997) Modelling the daily integral of photosynthesis by phytoplankton: its dependence on the mean depth of the population. Hydrobiologia 349:65–74. doi:10.1023/A:1003045528581

    Article  CAS  Google Scholar 

  • Wernberg T, Russell Bayden D, Thomsen Mads S, Gurgel C, Frederico D, Bradshaw Corey JA, Poloczanska Elvira S, Connell Sean D (2011) Seaweed communities in retreat from ocean warming. Curr Biol 21:1828–1832. doi:10.1016/j.cub.2011.09.028

    Article  CAS  Google Scholar 

  • Wikström SA, Kautsky L (2007) Structure and diversity of invertebrate communities in the presence and absence of canopy-forming Fucus vesiculosus in the Baltic Sea. Estuar Coast Shelf S 72:168–176. doi:10.1016/j.ecss.2006.10.009

    Article  Google Scholar 

  • Wu H, Zou D, Gao K (2008) Impacts of increased atmospheric CO2 concentration on photosynthesis and growth of micro- and macro-algae. Sci China Ser C Life Sci 51:1144–1150. doi:10.1007/s11427-008-0142-5

    Article  Google Scholar 

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Acknowledgments

Financial support was provided by the Project BIOACID II of the German Federal Ministry of Education and Research (BMBF; FKZ 03F0655, A). We thank Laura Käse, Felix Müller and Finn Ole-Petersen for their participation in the laboratory work and Björn Buchholz for the maintenance of the Kiel Benthocosms. We also want to thank all members of the Bioacid II consortium 2 ‘Benthic assemblages’ for their cooperation, Mark Lenz for statistical advice and Trystan Sanders for the linguistic revision. We thank for the comments of two anonymous reviewers.

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Al-Janabi, B., Kruse, I., Graiff, A. et al. Genotypic variation influences tolerance to warming and acidification of early life-stage Fucus vesiculosus L. (Phaeophyceae) in a seasonally fluctuating environment. Mar Biol 163, 14 (2016). https://doi.org/10.1007/s00227-015-2804-8

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