Advertisement

Marine Biology

, 167:22 | Cite as

Responses of a Mediterranean coastal lagoon plankton community to experimental warming

  • Silvia Pulina
  • Sanna Suikkanen
  • Bachisio M. PadeddaEmail author
  • Andreas Brutemark
  • Lorena M. Grubisic
  • Cecilia T. Satta
  • Tiziana Caddeo
  • Pasqualina Farina
  • Antonella Lugliè
Original Paper

Abstract

Coastal lagoons are extremely sensitive to increasing temperature, especially in the Mediterranean basin, which has been identified as a hotspot for global warming. The warming effects on the abundance and size structure of a Mediterranean coastal lagoon plankton community were investigated in this study. Water from Cabras Lagoon (Italy) was incubated in laboratory for 16 days in winter, excluding mesozooplankton. Three temperature treatments were applied: (i) the in situ winter mean water temperature; (ii) + 3 °C, as forecasted for the Mediterranean region by the next century; (iii) + 6 °C, as forecasted for the Mediterranean region by the next two centuries. A direct and positive effect of warming on ciliate density was observed in absence of their predators, as well as a taxonomic composition shift from Oligotrichs to Scuticociliatida. In turn, a decrease in heterotrophic nanoflagellate density was detected under warming. Phytoplankton (autotrophic cell size > 2 µm) density increased significantly, while their mean cell size decreased strongly throughout the experiment at the highest temperature. A significant change in phytoplankton class composition, consisting of the increase of smaller Chlorophyceae which replaced larger Bacillariophyceae, was observed under heating. Considering picoplankton (cell size < 2 µm), a decrease in larger autotrophic cell density was contemporary to an increase in smaller heterotrophic cell density, especially at the highest temperature. This work adds novel information to the predictions about plankton community responses on warming considering several trophic levels, which has been little studied in shallow coastal lagoons and in the Mediterranean basin.

Notes

Acknowledgements

The Authors thank Carlo Aresu and his team of technicians for providing and arranging the system with “Peltier cells” to regulate and maintain constant water temperature during the experiment. Dr. Harri Kuosa is acknowledged for help with nanoflagellate analysis. The Authors are grateful to the three anonymous reviewers for their constructive comments, which improved the manuscript.

Funding

Sanna Suikkanen was supported by the Academy of Finland (Grant Number 259357). Andreas Brutemark was supported by the Visiting Scientist grant Program 2014 of the University of Sassari I.D. 17 (L.R. 7/2007).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Supplementary material

227_2019_3640_MOESM1_ESM.pdf (252 kb)
Supplementary file1 (PDF 251 kb)

References

  1. Abbiati M, Mistri M, Bartoli M et al (2010) Trade-off between conservation and exploitation of the transitional water ecosystems of the northern Adriatic Sea. Chem Ecol 26:105–119.  https://doi.org/10.1080/02757541003693193 CrossRefGoogle Scholar
  2. Aberle N, Lengfellner K, Sommer U (2007) Spring bloom succession, grazing impact and herbivore selectivity of ciliate communities in response to winter warming. Oecologia 150:668–681.  https://doi.org/10.1007/s00442-006-0540-y CrossRefPubMedGoogle Scholar
  3. Barrett RDH, Schluter D (2008) Adaptation from standing genetic variation. Trends Ecol Evol 23:38–44.  https://doi.org/10.1016/j.tree.2007.09.008 CrossRefPubMedGoogle Scholar
  4. Berglund J, Müren U, Båmstedt U, Andersson A (2007) Efficiency of a phytoplankton-based and a bacterial-based food web in a pelagic marine system. Limnol Oceanogr 52:121–131.  https://doi.org/10.4319/lo.2007.52.1.0121 CrossRefGoogle Scholar
  5. Boyce DG, Worm B (2015) Patterns and ecological implications of historical marine phytoplankton change. Mar Ecol Prog Ser 534:251–272.  https://doi.org/10.3354/meps11411 CrossRefGoogle Scholar
  6. Boyce DG, Frank KT, Leggett WC (2015) From mice to elephants: overturning the ‘one size fits all’ paradigm in marine plankton food chains. Ecol Lett 18:504–515.  https://doi.org/10.1111/ele.12434 CrossRefPubMedGoogle Scholar
  7. del Giorgio PA, Bird DF, Prairie YT, Planas D (1996) Flow cytometric determination of bacterial abundance in lake plankton with the green nucleic acid stain SYTO 13. Limnol Oceanogr 41:783–789.  https://doi.org/10.4319/lo.1996.41.4.0783 CrossRefGoogle Scholar
  8. Di Poi E, Blason C, Corinaldesi C, Danovaro R, Malisana E, Fonda-Umani S (2013) Structure and interactions within the pelagic microbial food web (from viruses to microplankton) across environmental gradients in the Mediterranean Sea. Global Biogeochem Cycles 27:1034–1045.  https://doi.org/10.1002/2013GB004589 CrossRefGoogle Scholar
  9. Edler L (ed) (1979) Recommendations for marine Biological Studies in the Baltic Sea Phytoplankton and Chlorophyll. The Baltic Marine Biologists, Publ No 5, pp 1–38Google Scholar
  10. EEA European Environment Agency (2012) Climate change impacts and vulnerability in Europe. Copenhagen, EEA Report No 12/2012. 10.2800/66071Google Scholar
  11. Ferrarin C, Bajo M, Bellafiore D, Cucco A, De Pascalis F, Ghezzo M, Umgiesser G (2014) Toward homogenization of Mediterranean lagoons and their loss of hydrodiversity. Geophys Res Lett 41:5935–5941.  https://doi.org/10.1002/2014GL060843 CrossRefGoogle Scholar
  12. García-Ruiz JM, López-Moreno JI, Vicente-Serrano SM, Lasanta–Martínez T, Beguería S (2011) Mediterranean water resources in a global change scenario. Earth Sci Rev 105(3–4):121–139.  https://doi.org/10.1016/j.earscirev.2011.01.006 CrossRefGoogle Scholar
  13. Gardner JL, Peters A, Kaarney MR, Joseph L, Heinson R (2011) Declining body size: a third universal response to warming? Trends Ecol Evol 26:285–291.  https://doi.org/10.1016/j.tree.2011.03.005 CrossRefPubMedGoogle Scholar
  14. Gifford DJ (1985) Laboratory culture of marine planktonic oligotrichs (Ciliophora, Oligotrichida). Mar Ecol Prog Ser 23:257–267CrossRefGoogle Scholar
  15. Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Global Planet Change 63:90–104.  https://doi.org/10.1016/j.gloplacha.2007.09.005 CrossRefGoogle Scholar
  16. Jakobsen HH, Hansen PJ (1997) Prey size selection, grazing and growth response of the small heterotrophic dinoflagellate Gymnodinium sp. and the ciliate Balanion comatum—a comparative study. Mar Ecol Prog Ser 158:75–86.  https://doi.org/10.3354/meps158075 CrossRefGoogle Scholar
  17. Johansson M, Gorokhova E, Larsson U (2004) Annual variability in ciliate community structure potential prey and predators in the open northern Baltic Sea proper. J Plankton Res 26(1):67–80.  https://doi.org/10.1093/plankt/fbg CrossRefGoogle Scholar
  18. Koshikawa H, Harada S, Watanabe M, Kogure K, Ioriya T, Kohata K, Kimura T, Sato K, Akehata T (1999) Influence of plankton community structure on the contribution of bacterial production to metazooplankton in a coastal mesocosm. Mar Ecol Prog Ser 186:31–42.  https://doi.org/10.3354/meps186031 CrossRefGoogle Scholar
  19. Kuuppo P (1994) Annual variation in the abundance and size of heterotrophic nanoflagellates on the SW coast of Finland the Baltic Sea. J Plankton Res 16:1525–1542.  https://doi.org/10.1093/plankt/16.11.1525 CrossRefGoogle Scholar
  20. Hays GC, Richardson AJ, Robinson C (2005) Climate change and marine plankton. Trends Ecol Evol 20:337–344.  https://doi.org/10.1016/j.tree.2005.03.004 CrossRefPubMedGoogle Scholar
  21. Lenth R (2016) V: lsmeans: least-squares means R package version 222. https://CRANR-projectorg/package=lsmeansGoogle Scholar
  22. Lewandowska AM, Sommer U (2010) Climate change and the spring bloom: a mesocosm study on the influence of light and temperature on phytoplankton and mesozooplankton. Mar Ecol Prog Ser 405:101–111.  https://doi.org/10.3354/meps08520 CrossRefGoogle Scholar
  23. Lewandowska AM, Hillebrand H, Lengfellner K, Sommer U (2014) Temperature effects on phytoplankton diversity—the zooplankton link. J Sea Res 85:359–364.  https://doi.org/10.1016/j.seares.2013.07.003 CrossRefGoogle Scholar
  24. Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Annu Rev Ecol Evol Syst 39:615–639.  https://doi.org/10.1146/annurev.ecolsys.39.110707.173549 CrossRefGoogle Scholar
  25. Litchman E, Klausmeier CA, Schofield OM, Falkowski PG (2007) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol Lett 10:1170–1181.  https://doi.org/10.1111/j.1461-0248.2007.01117.x CrossRefPubMedGoogle Scholar
  26. Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationships for dinoflagellates diatoms and other protist plankton. Limnol Oceanogr 45:569–579.  https://doi.org/10.4319/lo.2000.45.3.0569 CrossRefGoogle Scholar
  27. Morabito G, Mazzocchi MG, Salmaso N et al (2018) Plankton dynamics across the freshwater transitional and marine research sites of the LTER-Italy Network Patterns fluctuations drivers. Sci Total Environ 627:373–387.  https://doi.org/10.1016/j.scitotenv.2018.01.153 CrossRefPubMedGoogle Scholar
  28. Müren U, Berglund J, Samulesson K, Andersson A (2005) Potential effects of elevated sea-water temperature on pelagic food webs. Hydrobiologia 545:153–166.  https://doi.org/10.1007/s10750-005-2742-4 CrossRefGoogle Scholar
  29. Newton A, Icely J, Cristina S et al (2014) An overview of ecological status vulnerability and future perspectives of European large shallow semi-enclosed coastal systems lagoons and transitional waters. Estuar Coast Shelf Sci 140:95–122.  https://doi.org/10.1016/j.ecss.2013.05.023 CrossRefGoogle Scholar
  30. Padedda BM, Lugliè A, Ceccherelli G, Trebini F, Sechi N (2010) Nutrient-flux evaluation by the LOICZ Biogeochemical Model in Mediterranean lagoons: the case of Cabras Lagoon (Central-Western Sardinia). Chem Ecol 26(2):147–162CrossRefGoogle Scholar
  31. Padedda BM, Pulina S, Magni P, Sechi N, Lugliè A (2012) Phytoplankton dynamics in relation to environmental changes in a phytoplankton-dominated Mediterranean lagoon (Cabras Lagoon Italy). Adv Oceanogr Limnol 3(2):147–169.  https://doi.org/10.1080/19475721.2012.716792 CrossRefGoogle Scholar
  32. Pérez-Ruzafa A, Marcos C, Pérez-Ruzafa IM (2011) Mediterranean coastal lagoons in an ecosystem and aquatic resource management context. Phys Chem Earth 36:160–166.  https://doi.org/10.1016/j.pce.2010.04.013 CrossRefGoogle Scholar
  33. Peter KH, Sommer U (2012) Phytoplankton cell size inter- and intraspecific effects of warming and grazing. PLoS ONE 7(11):e49632.  https://doi.org/10.1371/journal.pone.0049632 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Peter KH, Sommer U (2013) Phytoplankton cell size reduction in response to warming mediated by nutrient limitation. PLoS ONE 8(9):e71528.  https://doi.org/10.1371/journal.pone.0071528 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Peter KH, Sommer U (2015) Interactive effect of warming, nitrogen and phosphorus limitation on phytoplankton cell size. Ecol Evol 5:1011–1024.  https://doi.org/10.1002/ece3.1241 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Pinheiro J, Bates D, DebRoy S, Sarkar D (2012) R Development Core Team nlme: linear and nonlinear mixed effects models. R package version 3:1–105Google Scholar
  37. Polovina JJ, Woodworth PA (2012) Declines in phytoplankton cell size in the subtropical oceans estimated from satellite remotely-sensed temperature and chlorophyll 1998–2007. Deep Sea Res II 77–80:82–88.  https://doi.org/10.1016/j.dsr2.2012.04.006 CrossRefGoogle Scholar
  38. Pugnetti A, Acri F, Bernardi Aubry F et al (2013) The Italian Long-Term Ecosystem Research (LTER-Italy) network: results, opportunities and challenges for coastal transitional ecosystems. Transit Waters Bull 7(1):43–63.  https://doi.org/10.1285/i1825229Xv7n1p43 CrossRefGoogle Scholar
  39. Pulina S, Padedda BM, Sechi N, Lugliè A (2011) The dominance of cyanobacteria in Mediterranean hypereutrophic lagoons: a case study of Cabras Lagoon (Sardinia Italy). Sci Mar 75:111–120.  https://doi.org/10.3989/scimar.2011.75n1111 CrossRefGoogle Scholar
  40. Pulina S, Padedda BM, Satta CT, Sechi N, Lugliè A (2012) Long term phytoplankton dynamics in a Mediterranean eutrophic lagoon (Cabras Lagoon Italy). Plant Biosyst 146:259–272.  https://doi.org/10.1080/11263504.2012.717545 CrossRefGoogle Scholar
  41. Pulina S, Brutemark A, Suikkanen S, Padedda BM, Grubisic LM, Satta CT, Caddeo T, Farina P, Sechi N, Lugliè A (2016) Effects of warming on a Mediterranean phytoplankton community. Web Ecol 16:89–92.  https://doi.org/10.5194/we-16-89-2016 CrossRefGoogle Scholar
  42. R Core Team (2017) R: a language and environment for statistical computing. https://www.R-project.org/
  43. Reynolds CS (2006) Ecology of phytoplankton. Cambridge University Press, Cambridge, pp 1–552.  https://doi.org/10.1017/CBO9780511542145 CrossRefGoogle Scholar
  44. Rivkin R, Legendre L (2001) Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291:2398–2400.  https://doi.org/10.1126/science.291.5512.2398 CrossRefPubMedGoogle Scholar
  45. Sánchez E, Gallardo C, Gaertner MA, Arribas A, Castro M (2004) Future climate extreme events in the Mediterranean simulated by a regional climate model: a first approach. Global Planet Change 44:163–180.  https://doi.org/10.1016/j.gloplacha.2004.06.010 CrossRefGoogle Scholar
  46. Satta CT, Anglès S, Garcés E, Sechi N, Pulina S, Padedda BM, Stacca D, Lugliè A (2014) Dinoflagellate cyst assemblages in surface sediments from three shallow Mediterranean lagoons (Sardinia north western Mediterranean Sea). Estuar Coast 37:646–663.  https://doi.org/10.1007/s12237-013-9705-1 CrossRefGoogle Scholar
  47. Smetacek V (1981) Annual cycle of protozooplankton in the Kiel Bight. Mar Biol 63:1–11.  https://doi.org/10.1007/BF00394657 CrossRefGoogle Scholar
  48. Sommer U (1984) The paradox of the plankton: Fluctuations of phosphorus availability maintain diversity of phytoplankton in flow-through cultures. Limnol Oceanogr 29(3):633–636.  https://doi.org/10.4319/lo.1984.29.3.0633 CrossRefGoogle Scholar
  49. Sommer U, Aberle N, Engel A, Hansen T, Lengfellner K, Sandow M, Wohlers J, Zöllner E, Riebesell U (2007) An indoor mesocosm system to study the effect of climate change on the late winter and spring succession of Baltic Sea phyto- and zooplankton. Oecologia 150:655–667.  https://doi.org/10.1007/s00442-006-0539-4 CrossRefPubMedGoogle Scholar
  50. Sommer U, Charalampous E, Genitsaris S, Moustaka-Gouni M (2017) Benefits, costs and taxonomic distribution of marine phytoplankton body size. J Plankton Res 39(3):494–508.  https://doi.org/10.1093/plankt/fbw071 CrossRefGoogle Scholar
  51. Stibor H, Vadstein O, Diehl S et al (2004) Copepods act as a switch between alternative trophic cascades in marine pelagic food webs. Ecol Lett 7:321–328CrossRefGoogle Scholar
  52. Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Fisheries Research Board of Canada 167, Ottawa, pp 1–310Google Scholar
  53. Strom SL, Brainard MA, Holmes JL, Olson MB (2001) Phytoplankton blooms are strongly impacted by microzooplankton grazing in coastal North Pacific waters. Mar Biol 138:355–368.  https://doi.org/10.1007/s002270000461 CrossRefGoogle Scholar
  54. Suikkanen S, Laamanen M, Huttunen M (2007) Long-term changes in summer phytoplankton communities of the open northern Baltic Sea. Estuar Coast Shelf Sci 71:580–592.  https://doi.org/10.1016/j.ecss.2006.09.004 CrossRefGoogle Scholar
  55. Tillmann U (2004) Interactions between planktonic microalgae and protozoan grazers. J Eukaryot Microbiol 51:156–168.  https://doi.org/10.1111/j.1550-7408.2004.tb00540.x CrossRefPubMedGoogle Scholar
  56. Unrein F, Massana R, Alonso-Sáez L, Gasol JM (2007) Significant year-round effect of small mixotrophic flagellates on bacterioplankton in an oligotrophic coastal system. Limnol Oceanogr 52(1):456–469.  https://doi.org/10.4319/lo.2007.52.1.0456 CrossRefGoogle Scholar
  57. Utermöhl H (1958) Zur vervollkommung der quantitativen phytoplankton-methodik. Mitt Internat Verein Limnol 9:1–39.  https://doi.org/10.1080/05384680.1958.11904091 CrossRefGoogle Scholar
  58. Vidussi F, Mostajir B, Fouilland E, Le Floc’h E, Nouguier J, Roques C, Got P, Thibault-Botha D, Bouvier T, Trousselliera M (2011) Effects of experimental warming and increased ultraviolet B radiation on the Mediterranean plankton food web. Limnol Oceanogr 56:206–218.  https://doi.org/10.4319/lo.2011.56.1.0206 CrossRefGoogle Scholar
  59. Winder M, Sommer U (2012) Phytoplankton response to a changing climate. Hydrobiologia 698:5–16.  https://doi.org/10.1007/s10750-012-1149-2 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Authors and Affiliations

  • Silvia Pulina
    • 1
  • Sanna Suikkanen
    • 2
  • Bachisio M. Padedda
    • 1
    Email author
  • Andreas Brutemark
    • 3
  • Lorena M. Grubisic
    • 4
  • Cecilia T. Satta
    • 1
    • 5
  • Tiziana Caddeo
    • 1
  • Pasqualina Farina
    • 1
  • Antonella Lugliè
    • 1
  1. 1.Department of Architecture, Design and Urban PlanningUniversity of SassariSassariItaly
  2. 2.Marine Research CentreFinnish Environment InstituteHelsinkiFinland
  3. 3.Calluna ABStockholmSweden
  4. 4.Department of Ecology and Genetics, LimnologyUppsala UniversityUppsalaSweden
  5. 5.AGRIS Sardegna, Agenzia Per La Ricerca in AgricolturaSassariItaly

Personalised recommendations