Fruit encasing preserves the dispersal potential and viability of stranded Posidonia oceanica seeds.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
14 03 2024
14 03 2024
Historique:
received:
04
05
2023
accepted:
07
03
2024
medline:
18
3
2024
pubmed:
15
3
2024
entrez:
15
3
2024
Statut:
epublish
Résumé
Posidonia oceanica meadows are the most productive coastal ecosystem in the Mediterranean. Posidonia oceanica seeds are enclosed in buoyant fleshy fruits that allow dispersal. Many fruits eventually strand on beaches, imposing a remarkable energy cost for the plant. This study aims to assess whether stranded seeds retain functional reproductive potential under a variety of environmental conditions. First, we measured the possibility that seeds could be returned to the sea, by tagging fruits and seeds. Second, we quantified the effect of air, sun and heat exposure on the viability and fitness of stranded fruits and naked seeds. The results showed that on average more than half of fruits and seeds are returned to the sea after stranding events and that fruits significantly protect from desiccation and loss of viability. Furthermore, in fruits exposed to the sun and in naked seeds, seedlings development was slower. This study indicates that a significant portion of stranded P. oceanica fruits have a second chance to recruit and develop into young seedlings, relieving the paradox of large energy investment in seed production and apparent low recruitment rate. Additionally, we provide practical indications for seed collection aimed at maximizing seedling production, useful in meadow restoration campaigns.
Identifiants
pubmed: 38486018
doi: 10.1038/s41598-024-56536-x
pii: 10.1038/s41598-024-56536-x
pmc: PMC10940675
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6218Subventions
Organisme : Ministero dell'Istruzione, dell'Università e della Ricerca (Ministry of Education, University and Research)
ID : PON03PE_00203_1
Informations de copyright
© 2024. The Author(s).
Références
Mtwana Nordlund, L., Koch, E. W., Barbier, E. B. & Creed, J. C. Seagrass ecosystem services and their variability across genera and geographical regions. PLoS ONE 11, e0163091 (2016).
doi: 10.1371/journal.pone.0163091
pubmed: 27732600
pmcid: 5061329
Duarte, C. M. & Krause-Jensen, D. Export from seagrass meadows contributes to marine carbon sequestration. Front. Mar. Sci. 4, 13 (2017).
doi: 10.3389/fmars.2017.00013
Dunic, J. C., Brown, C. J., Connolly, R. M., Turschwell, M. P. & Côté, I. M. Long-term declines and recovery of meadow area across the world’s seagrass bioregions. Glob. Chang. Biol. 27, 4096–4109 (2021).
doi: 10.1111/gcb.15684
pubmed: 33993580
Kendrick, G. A. et al. A systematic review of how multiple stressors from an extreme event drove ecosystem-wide loss of resilience in an iconic seagrass community. Front. Mar. Sci. 6, 455 (2019).
doi: 10.3389/fmars.2019.00455
Krause-Jensen, D., Duarte, C. M., Sand-Jensen, K. & Carstensen, J. Century-long records reveal shifting challenges to seagrass recovery. Glob. Chang. Biol. 27, 563–575 (2021).
doi: 10.1111/gcb.15440
pubmed: 33241657
Waycott, M. et al. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Nat. Acad. Sci. U. S. A. 106, 12377–12381 (2009).
doi: 10.1073/pnas.0905620106
de los Santos, C. B. et al. Recent trend reversal for declining European seagrass meadows. Nat. Commun. 10, 3356 (2019).
doi: 10.1038/s41467-019-11340-4
pubmed: 31848338
pmcid: 6917704
Telesca, L. et al. Seagrass meadows (Posidonia oceanica) distribution and trajectories of change. Sci. Rep. 5(1), 12505 (2015).
doi: 10.1038/srep12505
Escandell-Westcott, A., Riera, R. & Hernández-Muñoz, N. Posidonia oceanica restoration review: Factors affecting seedlings. J. Sea Res. 191, 102337 (2023).
doi: 10.1016/j.seares.2023.102337
Micheli, C. et al. Genetic input by Posidonia oceanica (L.) Delile fruits dispersed by currents in the Ligurian Sea. Plant Biosyst. 144, 333–339 (2010).
doi: 10.1080/11263501003764798
Marbà, N. & Duarte, C. M. Rhizome elongation and seagrass clonal growth. Mar. Ecol. Prog. Ser. 174, 269–280 (1998).
doi: 10.3354/meps174269
Alagna, A. et al. Taking advantage of seagrass recovery potential to develop novel and effective meadow rehabilitation methods. Mar. Pollut. Bull. 149, 110578 (2019).
doi: 10.1016/j.marpolbul.2019.110578
pubmed: 31550578
Seddon, S. Going with the flow: Facilitating seagrass rehabilitation. Ecol. Manag. Restor. 5, 167–176 (2004).
doi: 10.1111/j.1442-8903.2004.00205.x
Sullivan, B. K., Trevathan-Tackett, S. M., Neuhauser, S. & Govers, L. L. Review: Host-pathogen dynamics of seagrass diseases under future global change. Mar. Pollut. Bull. 134, 75–88 (2018).
doi: 10.1016/j.marpolbul.2017.09.030
pubmed: 28965923
Bradamante, G., Scheid, O. M. & Incarbone, M. Under siege: Virus control in plant meristems and progeny. Plant Cell 33, 2523–2537 (2021).
doi: 10.1093/plcell/koab140
pubmed: 34015140
pmcid: 8408453
Zenone, A. et al. Biological adhesion in seagrasses: The role of substrate roughness in Posidonia oceanica (L.) Delile seedling anchorage via adhesive root hairs. Mar. Environ. Res. 160, 105012 (2020).
doi: 10.1016/j.marenvres.2020.105012
pubmed: 32907731
Badalamenti, F., Alagna, A. & Fici, S. Evidences of adaptive traits to rocky substrates undermine paradigm of habitat preference of the Mediterranean seagrass Posidonia oceanica. Sci. Rep. 5, 8804 (2015).
doi: 10.1038/srep08804
pubmed: 26690845
pmcid: 4522670
Diaz-Almela, E., Marbà, N. & Duarte, C. M. Consequences of Mediterranean warming events in seagrass (Posidonia oceanica) flowering records. Glob. Chang. Biol. 13, 224–235 (2007).
doi: 10.1111/j.1365-2486.2006.01260.x
Calvo, S. et al. Seagrasses along the Sicilian coasts. Chem. Ecol. https://doi.org/10.1080/0275754100363637426,249-266 (2010).
doi: 10.1080/0275754100363637426,249-266
Balestri, E., Vallerini, F. & Lardicci, C. Recruitment and patch establishment by seed in the seagrass Posidonia oceanica: Importance and conservation implications. Front. Plant Sci. 8, 1067 (2017).
doi: 10.3389/fpls.2017.01067
pubmed: 28670323
pmcid: 5472673
Belzunce, M., Navarro, R. M. & Rapoport, H. F. Posidonia oceanica seeds from drift origin: Viability, germination and early plantlet development. Bot. Marina 51, 1–9 (2008).
doi: 10.1515/BOT.2008.005
Balestri, E. & Vallerini, F. Interannual variability in flowering of Posidonia oceanica in the North-Western Mediterranean Sea, and relationships among shoot age and flowering. Bot. Marina 46, 525–530 (2003).
doi: 10.1515/BOT.2003.054
Balestri, E. Flowering of the seagrass Posidonia oceanica in a north-western Mediterranean coastal area: Temporal and spatial variations. Mar. Biol. 145, 61-68 (2004).
doi: 10.1007/s00227-004-1301-2
Ruiz, J. M. et al. Experimental evidence of warming-induced flowering in the Mediterranean seagrass Posidonia oceanica. Mar. Pollut. Bull. 134, 49–54 (2018).
doi: 10.1016/j.marpolbul.2017.10.037
pubmed: 29102072
Marín-Guirao, L., Entrambasaguas, L., Ruiz, J. M. & Procaccini, G. Heat-stress induced flowering can be a potential adaptive response to ocean warming for the iconic seagrass Posidonia oceanica. Mol. Ecol. 28, 2486–2501 (2019).
doi: 10.1111/mec.15089
pubmed: 30938465
Jahnke, M. et al. Should we sync? Seascape-level genetic and ecological factors determine seagrass flowering patterns. J. Ecol. 103, 1464–1474 (2015).
doi: 10.1111/1365-2745.12470
Arnaud-Haond, S. et al. Vicariance patterns in the Mediterranean Sea: East–west cleavage and low dispersal in the endemic seagrass Posidonia oceanica. J. Biogeogr. 34, 963–976 (2007).
doi: 10.1111/j.1365-2699.2006.01671.x
Balestri, E. & Cinelli, F. Sexual reproductive success in Posidonia oceanica. Aquat. Bot. 75, 21–32 (2003).
doi: 10.1016/S0304-3770(02)00151-1
Balestri, E., Gobert, S., Lepoint, G. & Lardicci, C. Seed nutrient content and nutritional status of Posidonia oceanica seedlings in the northwestern Mediterranean Sea. Mar. Ecol. Prog. Ser. 388, 99–109 (2009).
doi: 10.3354/meps08104
Ruiz-Montoya, L. et al. The role of hydrodynamics on seed dispersal in seagrasses. Limnol. Oceanogr. 57(5), 1257–1265 (2012).
doi: 10.4319/lo.2012.57.5.1257
Balestri, E., Piazzi, L. & Cinelli, F. Survival and growth of transplanted and natural seedlings of Posidonia oceanica (L.) Delile in a damaged coastal area. J. Exp. Mar. Biol. Ecol. 228, 209–225 (1998).
doi: 10.1016/S0022-0981(98)00027-6
Piazzi, L., Acunto, S. & Cinelli, F. In situ survival and development of Posidonia oceanica (L.) Delile seedlings. Aquat. Bot. 63, 103–112 (1999).
doi: 10.1016/S0304-3770(98)00115-6
Ruiz-Montoya, L., Lowe, R. J. & Kendrick, G. A. Contemporary connectivity is sustained by wind-and current-driven seed dispersal among seagrass meadows. Mov. Ecol. 3, 9 (2015).
doi: 10.1186/s40462-015-0034-9
pubmed: 25897403
pmcid: 4404238
Alagna, A. et al. Assessing Posidonia oceanica seedling substrate preference: An experimental determination of seedling anchorage success in rocky vs sandy substrates. PLoS ONE 10, e125321 (2015).
doi: 10.1371/journal.pone.0125321
Campbell, M. L. An empirical evaluation of Posidonia australis (R. Br.) Hook f. Restoration in western Australia: Development of a decision-based restoration framework. Ph.D. Dissertation. Murdoch University, Perth, 167 (2000).
Buia, M. C. & Mazzella, L. Reproductive phenology of the Mediterranean seagrasses Posidonia oceanica (L.) Delile, Cymodocea nodosa (Ucria) Aschers., and Zostera noltii Hornem. Aquat. Bot. 40, 343–362 (1991).
doi: 10.1016/0304-3770(91)90080-O
Balestri, E., Piazzi, L. & Cinelli, F. In vitro germination and seedling development of Posidonia oceanica. Aquat. Bot. 60, 83–93 (1998).
doi: 10.1016/S0304-3770(97)00017-X
Negrao, S. et al. Differential leaf age-dependent thermal plasticity in the keystone seagrass Posidonia oceanica. Front. Plant Sci. 10, 1556 (2019).
doi: 10.3389/fpls.2019.01556
pubmed: 30984222
pmcid: 6449481