, Volume 186, Issue 4, pp 1137–1152 | Cite as

Seagrass collapse due to synergistic stressors is not anticipated by phenological changes

  • Giulia CeccherelliEmail author
  • Silvia Oliva
  • Stefania Pinna
  • Luigi Piazzi
  • Gabriele Procaccini
  • Lazaro Marin-Guirao
  • Emanuela Dattolo
  • Roberto Gallia
  • Gabriella La Manna
  • Paola Gennaro
  • Monya M. Costa
  • Isabel Barrote
  • João Silva
  • Fabio Bulleri
Conservation ecology – original research


Seagrasses are globally declining and often their loss is due to synergies among stressors. We investigated the interactive effects of eutrophication and burial on the Mediterranean seagrass, Posidonia oceanica. A field experiment was conducted to estimate whether shoot survival depends on the interactive effects of three levels of intensity of both stressors and to identify early changes in plants (i.e., morphological, physiological and biochemical, and expression of stress-related genes) that may serve to detect signals of imminent shoot density collapse. Sediment burial and nutrient enrichment produced interactive effects on P. oceanica shoot survival, as high nutrient levels had the potential to accelerate the regression of the seagrass exposed to high burial (HB). After 11 weeks, HB in combination with either high or medium nutrient enrichment caused a shoot loss of about 60%. Changes in morphology were poor predictors of the seagrass decline. Likewise, few biochemical variables were associated with P. oceanica survival (the phenolics, ORAC and leaf δ34S). In contrast, the expression of target genes had the highest correlation with plant survival: photosynthetic genes (ATPa, psbD and psbA) were up-regulated in response to high burial, while carbon metabolism genes (CA-chl, PGK and GADPH) were down-regulated. Therefore, die-offs due to high sedimentation rate in eutrophic areas can only be anticipated by altered expression of stress-related genes that may warn the imminent seagrass collapse. Management of local stressors, such as nutrient pollution, may enhance seagrass resilience in the face of the intensification of extreme climate events, such as floods.


Burial Early warnings Eutrophication Multiple stressors Posidonia oceanica 



Analyses were performed at the Servizos de Apoio á Investigación-Universidade da Coruña (Leaf N, Leaf C, and corresponding isotopic signatures), Iso-Analytical Ltd (Leaf S and leaf δ34S). We are grateful to Capo Caccia-Isola Piana MPA administration for facilitating the samplings within their domains. This research was supported by MIUR, the Italian Ministry of Education and Research, (TETRIS Grant 2011–2015) and by Fondazione di Sardegna (EIMS Grant 2016–2019). PG acknowledges the support of S. Porrello and E. Persia at ISPRA laboratories for water nutrient analysis.

Author contribution statement

GC, SO, and LP conceived and designed the experiments. GC, SO, SP and LP performed the experiments. GP, LMG, ED, RG, PG, MMC, IB, JS analysed the sampled material, FB analysed the data. GC and FB led the writing of the ms. All authors contributed critically to the drafts and gave final approval for publication.

Supplementary material

442_2018_4075_MOESM1_ESM.docx (6.1 mb)
Supplementary material 1 (DOCX 6227 kb)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Giulia Ceccherelli
    • 1
    Email author
  • Silvia Oliva
    • 1
  • Stefania Pinna
    • 1
  • Luigi Piazzi
    • 1
  • Gabriele Procaccini
    • 2
  • Lazaro Marin-Guirao
    • 2
  • Emanuela Dattolo
    • 2
  • Roberto Gallia
    • 2
  • Gabriella La Manna
    • 1
    • 3
  • Paola Gennaro
    • 4
  • Monya M. Costa
    • 5
  • Isabel Barrote
    • 5
  • João Silva
    • 5
  • Fabio Bulleri
    • 6
  1. 1.Dipartimento di Scienze della Natura e del Territorio, Polo BionaturalisticoUniversity of SassariSassariItaly
  2. 2.Stazione Zoologica Anton Dohrn, Villa ComunaleNaplesItaly
  3. 3.MareTerra - Environmental Research and ConservationAlgheroItaly
  4. 4.Italian National Institute for Environmental Protection and Research (ISPRA)RomeItaly
  5. 5.CCMAR - Centre of Marine SciencesUniversity of AlgarveFaroPortugal
  6. 6.Department of BiologyUniversity of PisaPisaItaly

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