pp 1–14 | Cite as

Response of a coastal Baltic Sea diatom-dominated phytoplankton community to experimental heat shock and changing salinity

  • Natassa StefanidouEmail author
  • Savvas Genitsaris
  • Juan Lopez-Bautista
  • Ulrich Sommer
  • Maria Moustaka-Gouni
Global change ecology – original research


Climate change has been altering the ocean environment, affecting as a consequence the biological communities including microorganisms. We performed a mesocosm experiment to test whether biodiversity loss caused by one stressor would influence plankton community sensitivity to a subsequent stressor, as envisioned in Vinebrooke’s multiple stressor concept. A natural Baltic Sea diatom-dominated phytoplankton assemblage was used as a model system where we examined whether a preceding heat shock would affect the community’s response to changing salinity. Initially, the community was treated by a short-term temperature increase of 6 °C, which resulted in a loss of species compared to the control. Thereafter, the control and the heat-shocked communities were subject to a salinity change (− 5 psu, control, + 5 psu). The species Skeletonema dohrnii, Thalassiosira anguste-lineata, Thalassiosira nordenskioeldii, Chaetoceros socialis and Ditylum brightwellii were major components of the control and heat-shocked assemblages (> 80% of the total biomass). We examined the effect on species composition and biodiversity (morphospecies and operational taxonomic units (OTUs) related to phytoplankton) and on phytoplankton biomass. In addition, we explored the single species response of five dominant diatoms on these environmental perturbations. Our results showed that increased salinity significantly reduced the OTUs richness both in the control and the less diverse heated community as well as the phytoplankton biomass in the heated community. On the other hand, decreased salinity significantly increased species richness and phytoplankton biomass in both communities and OTUs richness in the control community. The five dominant diatoms reached their highest biomass under decreased salinity and responded negatively to increased salinity (lower biomass than ambient salinity). Contrary to Vinebrooke’s multiple stressor concept, there was no indication that the heat treatment had altered the community’s sensitivity to the salinity stress in our study system.


Climate change Interactive effects 18S rRNA gene sequencing Mesocosms 



We would like to thank the editor and the two reviewers for their constructive comments and suggestions that helped improve our manuscript. We are thankful to Prof. Konstantinos Ar. Kormas for providing the equipment to perform the nucleic acid extractions. We would like to thank T. Hansen, B. Gardeler and C. Meyer for technical support. The experiments are part of the BEN-Network (Non-random Biodiversity Experiments Network) initiated by A.M. Lewandowska (University of Helsinki, Tvärminne Zoological Station). Similar experiments using the same design are conducted on other marine sites.

Author contribution statement

NS, US, and MM-G designed the research and the experiment. NS and SG carried out the molecular and the bioinformatics analysis. NS carried out the experiment, the statistical analysis, and prepared the manuscript. NS, SG, JL-B, US, and MM-G revised the manuscript.


This research was implemented through IKY scholarships program and co-financed by the European Union (European Social Fund–ESF) and Greek national funds through the action entitled “Scholarships program for postgraduates studies-2nd Study Cycle” in the framework of the Operational Program “Human Resources Development Program, Education and Lifelong Learning” of the National Strategic Reference Framework (NSRF) 2014–2020. This project was partially supported by the Alabama Greece Initiative, The University of Alabama.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

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

Supplementary material

442_2019_4502_MOESM1_ESM.pdf (232 kb)
Supplementary material 1 (PDF 232 kb)


  1. Aberle N, Malzahn AM, Lewandowska AM, Sommer U (2015) Some like it hot: the protozooplankton-copepod link in a warming ocean. Mar Ecol Prog Ser 519:103–113CrossRefGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefGoogle Scholar
  3. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligo-nucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925Google Scholar
  4. Andersson A, Meier HEM, Ripszam M, Ripzam M, Rowe O, Winker J et al (2015) Projected future climate change and Baltic Sea ecosystem management. Ambio 44(3):345CrossRefGoogle Scholar
  5. Barton AD, Irwin AJ, Finkel ZV, Stock CA (2016) Anthropogenic climate change drives shift and shuffle in north Atlantic phytoplankton communities. Proc Natl Acad Sci USA 113:964–2969CrossRefGoogle Scholar
  6. Bénard R, Levasseur M, Scarratt M, Blais MA, Mucci A, Ferreyra G et al (2018) Experimental assessment of the sensitivity of an estuarine phytoplankton fall bloom to acidification and warming. Biogeosciences 15:4883–4904CrossRefGoogle Scholar
  7. Boyd PW, Strzepek R, Chiswell S, Chang H, DeBruyn JM, Ellwood M et al (2012) Microbial control of diatom bloom dynamics in the open ocean. Geophys Res Lett 39:L18601CrossRefGoogle Scholar
  8. Boyd PW, Collins S, Dupont S, Fabricius K, Gattuso JP, Havenhand J et al (2018) Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change: a review. Glob Change Biol 24:2239–2261CrossRefGoogle Scholar
  9. Broman E, Li L, Fridlund J, Svensson F, Legrand C, Dopson M (2018) Spring and late summer phytoplankton biomass impact on the coastal sediment microbial community structure. Microb Ecol. Google Scholar
  10. Bunse C, Bertos-Fortis M, Sassenhagen I, Sildever S, Sjöqvist C, Godhe A et al (2016) Spatio-temporal interdependence of bacteria and phytoplankton during a Baltic Sea spring bloom. Front Microbiol 7:517CrossRefGoogle Scholar
  11. Burgmer T, Hillebrand H (2011) Temperature mean and variance alter phytoplankton biomass and biodiversity in a long-term microcosm experiment. Oikos 120:922–933CrossRefGoogle Scholar
  12. Bužančić M, Gladan ZN, Marasović I, Kušpilić G, Grbec B (2016) Eutrophication influence on phytoplankton community composition in three bays on the eastern Adriatic coast. Oceanologia 4:302–316Google Scholar
  13. Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992CrossRefGoogle Scholar
  14. Carstensen J, Klais R, Cloern JE (2015) Phytoplankton blooms in estuarine and coastal waters: seasonal patterns and key species. Estuar Coast Shelf Sci 162:98e109CrossRefGoogle Scholar
  15. de Vargas C, Audic S, Henry N, Decelle J, Mahe F, Logares R et al (2015) Eukaryotic plankton diversity in the sunlit ocean. Science 348:1261605CrossRefGoogle Scholar
  16. Descamps S, Aars J, Fuglei E, Kovacs KM, Lydersen C, Pavlova O et al (2017) Climate change impacts on wildlife in a high Arctic archipelago–Svalbard, Norway. Glob Change Biol 23:490–502CrossRefGoogle Scholar
  17. Dowd SE, Sun Y, Secor PR, Rhoads DD, Wolcott BM, James GA et al (2008) Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol 8:43CrossRefGoogle Scholar
  18. Eggers SL, Lewandowska AM, Barcelos e Ramos J, Blanco-Ameijeiras S, Gallo F, Matthiessen B (2014) Community composition has greater impact on the functioning of marine phytoplankton communities than ocean acidification. Glob Change Biol 20:713–723CrossRefGoogle Scholar
  19. Engel FG, Lewandowska AM, Eggers SL, Matthiessen B (2017) Manipulation of non-random species loss in natural phytoplankton: qualitative and quantitative evaluation of different approaches. Front Mar Sci 4:317CrossRefGoogle Scholar
  20. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O et al (2004) The evolution of modern eukaryotic phytoplankton. Science 305(5682):354–360CrossRefGoogle Scholar
  21. Feistel R, Weinreben S, Wolf H, Seitz S, Spitzer P, Abel B, Nausch G, Schneider B, Wright DG (2010) Density and absolute salinity of the Baltic Sea 2006–2009. Ocean Sci 6:3–24CrossRefGoogle Scholar
  22. Gliwicz ZM, Siedlar E (1980) Food size limitation and algae interfering with food collection in Daphnia. Arch Hydrobiol 88:155–177Google Scholar
  23. Godhe A, Sjöqvist C, Sildever S, Sefbom J, Harðardóttir S, Bertos-Fortis M et al (2016) Physical barriers and environmental gradients cause spatial and temporal genetic differentiation of an extensive algal bloom. J Biogeogr 43:1130–1142CrossRefGoogle Scholar
  24. Grossart HP, Meinhard S, Logan BE (1997) Formation of macroscopic organic aggregates (lake snow) in a large lake: the significance of transparent exopolymer particles, plankton, and zooplankton. Limnol Oceanogr 42:1651–1659CrossRefGoogle Scholar
  25. Gruner DS, Bracken MES, Berger SA, Eriksson BK, Gamfeldt L, Matthiesen B et al (2017) Effects of experimental warming on biodiversity depend on ecosystem type and local species composition. Oikos 126:8–17CrossRefGoogle Scholar
  26. Gunderson AR, Armstrong EJ, Stillman JH (2016) Multiple stressors in a changing world: the need for an improved perspective on physiological responses to the dynamic marine environment. Ann Rev Mar Sci 8(1):357–378CrossRefGoogle Scholar
  27. Hansen HP, Koroleff F (1999) Determination of nutrients. In: Grasshoff K, Kremling K, Ehrhardt M (eds) Methods of seawater analysis, 3rd edn. Wiley VCH, Weinheim, pp 159–228CrossRefGoogle Scholar
  28. Hevia-Orube J, Orive E, David H, Laza-Martinez A, Seoane S (2016) Skeletonema species in a temperate estuary: a morphological, molecular and physiological approach. Diatom Res 31(3):185–197CrossRefGoogle Scholar
  29. Hillebrand H, Dürselen C, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424CrossRefGoogle Scholar
  30. Hooper DU, Chapin FS, Ewel JJ et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35CrossRefGoogle Scholar
  31. Huston MA (1997) Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110:449–460CrossRefGoogle Scholar
  32. Hutchins DA, Fu F (2017) Microorganisms and ocean global change. Nat Microbiol 2:17058CrossRefGoogle Scholar
  33. Intergovernmental Panel on Climate Change (IPCC) (2014) Climate change 2014: impacts, adaptation and vulnerability. IPCC Working Group II contribution to the 5th assessment report of the International Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  34. Intergovernmental Panel on Climate Change (IPCC) (2018) Summary for Policymakers. In: Global warming of 1.5°C. An IPCC special report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. World Meteorological Organization, Geneva, SwitzerlandGoogle Scholar
  35. Javidpour J, Molinero JC, Peschutter J, Sommer U (2009) Seasonal changes and population dynamics of the ctenophore Mnemiopsis leidyi after its first year of invasion in the Kiel Fjord, western Baltic Sea. Biol Invasions 11:873–882CrossRefGoogle Scholar
  36. Kaur-Kahlon G, Kumar S, Rehnstam-Holm AS, Rai A, Bhavya PS, Edler L et al (2016) Response of a coastal tropical pelagic microbial community to changing salinity and temperature. Aquat Microb Ecol 77:37–50CrossRefGoogle Scholar
  37. Kooistra WH, Sarno D, Balzano S, Gu H, Andersen RA, Zinone A (2008) Global diversity and biogeography of Skeletonema species (bacillariophyta). Protist 159:177–193CrossRefGoogle Scholar
  38. Leitão P, Zuanon J, Villéger S, Williams SE, Baraloto C, Fortunel C et al (2016) Rare species contribute disproportionately to the functional structure of species assemblages. Proc Royal Soc B 283:20160084CrossRefGoogle Scholar
  39. Lewandowska AM, Breithaupt P, Hillebrand H, Hoppe HG, Jürgens K, Sommer U (2012) Responses of primary productivity to increased temperature and phytoplankton diversity. J Sea Res 72:87–93CrossRefGoogle Scholar
  40. Lewandowska AM, Hillebrand H, Lengfellner K, Sommer U (2014) Temperature effects on phytoplankton diversity: the zooplankton link. J Sea Res 85:359–364CrossRefGoogle Scholar
  41. Lin Y, Kang L, Shih C, Gong G, Chang J (2018) Evaluation of the relationship between the 18S rRNA/rDNA ratio and population growth in the marine diatom Skeletonema tropicum via the application of an exogenous nucleic acid standard. J Eukaryot Microbiol 65(6):792–803CrossRefGoogle Scholar
  42. Liu Y, Song S, Chen T, Li C (2017) The diversity and structure of marine protists in the coastal waters of China revealed by morphological observation and 454 pyrosequencing. Estuar Coast Shelf Sci 189:143–155CrossRefGoogle Scholar
  43. Lopez-Garcia P, Philippe H, Gail F, Moreira D (2003) Autochthonous eukaryotic diversity in hydrothermal sediment and experimental microcolonizers at the Mid-Atlantic Ridge. Proc Natl Acad Sci USA 100:697–702CrossRefGoogle Scholar
  44. Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A et al (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808CrossRefGoogle Scholar
  45. 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 27:39CrossRefGoogle Scholar
  46. Nunes S, Latasa M, Gasol JM et al (2018) Seasonal and interannual variability of phytoplankton community structure in a Mediterranean coastal site. Mar Ecol Prog Ser 592:57–75CrossRefGoogle Scholar
  47. Pannard A, Pédrono J, Bormans M, Briand E, Claquin P, Lagadeuc Y (2016) Production of exopolymers (EPS) by cyanobacteria: impact on the carbon-to-nutrient ratio of the particulate organic matter. Aquat Ecol 50:29CrossRefGoogle Scholar
  48. Passow U (2002) Transparent exopolymer particles (TEP) in aquatic environments. Prog Oceanogr 55:287–333CrossRefGoogle Scholar
  49. Passow U, Alldredge AL (1995) A dye-binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP). Limnol Oceanogr 40:1326–1335CrossRefGoogle Scholar
  50. Paul C, Sommer U, Garzke J, Moustaka-Gouni M, Paul A, Matthiensen B (2016) Effects of increased CO2 concentration on nutrient limited coastal summer plankton depend on temperature. Limnol Oceanogr 61:853–868CrossRefGoogle Scholar
  51. Pfannkuchen MD, Godrijan J, Smodlaka TM, Baričević A, Kužat N, Djakovac T et al (2018) The ecology of one cosmopolitan, one newly introduced and one occasionally advected species from the genus Skeletonema in a highly structured ecosystem, the northern Adriatic. Microb Ecol 75:674CrossRefGoogle Scholar
  52. Russo A, Maccaferri S, Djakovac T, Precali R, Degobbis D, Deserti M et al (2005) Meteorological and oceanographic conditions in the northern Adriatic Sea during the period June 1999–July 2002: influence on the mucilage phenomenon. Sci Total Environ 353:24–38CrossRefGoogle Scholar
  53. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefGoogle Scholar
  54. Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310CrossRefGoogle Scholar
  55. Sett S, Schulz KG, Bach LT, Riebesell U (2018) Shift towards larger diatoms in a natural phytoplankton assemblage under combined high-CO2 and warming conditions. J Plankton Res 40:391–406CrossRefGoogle Scholar
  56. Shade A, Peter H, Allison S, Baho DL, Berga M, Bürgmann H et al (2012) Fundamentals of microial community resistance and resilience. Front Microbiol 3:417CrossRefGoogle Scholar
  57. Sjöqvist C, Godhe A, Jonsson PR, Sundqvist L, Kremp A (2015) Local adaptation and oceanographic connectivity patterns explain genetic differentiation of a marine diatom across the North Sea–Baltic Sea salinity gradient. Mol Ecol 24:2871–2885CrossRefGoogle Scholar
  58. Sommer U, Lewandowska A (2011) Climate change and the phytoplankton spring bloom: warming and overwintering zooplankton have similar effects on phytoplankton. Glob Change Biol 17:154–162CrossRefGoogle Scholar
  59. Stefanidou N, Genitsaris S, Lopez-Bautista J, Sommer U, Moustaka-Gouni M (2018a) Effects of heat shock and salinity changes on coastal Mediterranean phytoplankton in a mesocosm experiment. Mar Biol 165:154CrossRefGoogle Scholar
  60. Stefanidou N, Genitsaris S, Lopez-Bautista J, Sommer U, Moustaka-Gouni M (2018b) Unicellular eukaryotic community response to temperature and salinity variation in mesocosm experiments. Front Microbiol 9:2444CrossRefGoogle Scholar
  61. Tatters AO, Roleda MR, Schnetzer A, Fu FX, Hurd CL, Boyd PW et al (2013) Short- and long-term conditioning of a temperate marine diatom community to acidification and warming. Philos Trans R Soc B 368(1627):20120437CrossRefGoogle Scholar
  62. Tatters AO, Schnetzer A, Xu K, Walworth NG, Fu F, Spackeen JL et al (2018) Interactive effects of temperature, CO2 and nitrogen source on a coastal California diatom assemblage. J Plankton Res 40(2):151–164CrossRefGoogle Scholar
  63. Tüfekçi V, Balkis-Ozdelice N, Beken ÇP, Ediger D, Mantikci M (2010) Phytoplankton composition and environmental conditions of a mucilage event in the sea of Marmara. Turk J Biol. Google Scholar
  64. Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt Int Ver Theor Angew Limnol 9:263–272Google Scholar
  65. Vinebrooke RD, Cottingham KL, Norberg J, Scheffer M, Dodson SI, Maberly SC et al (2004) Impacts of multiple stressors on biodiversity and ecosystem functioning: the role of species co-tolerance. Oikos 104:451–457CrossRefGoogle Scholar
  66. Wasmund N, Göbel J, Bodungen VB (2008) 100-year-changes in the phytoplankton community of Kiel Bight (Baltic Sea). J Mar Syst 73:300–322CrossRefGoogle Scholar
  67. Wasmund N, Nausch G, Feistel R (2013) Silicate consumption: an indicator for long-term trends in spring diatom development in the Baltic Sea. J Plankton Res 35:393–406CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Botany, School of BiologyAristotle University of ThessalonikiThessalonikiGreece
  2. 2.School of Economics, Business Administration & Legal StudiesInternational Hellenic UniversityThessalonikiGreece
  3. 3.Department of Biological SciencesThe University of AlabamaTuscaloosaUSA
  4. 4.Geomar Helmholtz Centre for Ocean Research KielKielGermany

Personalised recommendations