Effects of ocean acidification on phenology and epiphytes of the seagrass Posidonia oceanica at two CO2 vent systems of Ischia (Italy)

Published: Mar 29, 2020
Ocean acidification climate change Posidonia oceanica seagrasses morphological features epiphytic community temporal trend Mediterranean Sea.

Morphological features of the seagrass Posidonia oceanica (L.) Delile and its epiphyte community were studied in three acidified stations located in two CO2 vents systems and one control station under normal pH conditions off the island of Ischia (Italy) to highlight the possible effects of ocean acidification. Plant phenology was analyzed every two months for a year cycle (June 2016–April 2017), while epiphytes were studied in the period of highest development of both the leaf canopy and the epiphytic community (June, August, and October 2016). The shoot density of Posidonia beds in the acidified stations of the studied sites was significantly higher than that in the control area. Significant differences in the mean leaf length according to the pH condition, month, and the interaction of these two factors were observed (PERMANOVA); the mean leaf width differed also among pH conditions and months. We recorded lower leaf lengths and widths in the acidified stations in all the considered months, compared to those in the control station. These differences are consistent with the higher impact of grazing by the herbivorous fish Sarpa salpa observed on the leaves in the acidified stations. However, the overall leaf surface available for epiphytes was similar among stations because of the higher shoot density under ocean acidification conditions. Overall, the composition and structure of the epiphytic community on the Posidonia leaves showed significant differences in relation to acidification: in both acidified sites, all the calcareous forms, both encrusting red algae (Corallinales) and animals (bryozoans, foraminiferans, and spirorbids), disappeared or were strongly reduced, in favor of encrusting or erect fleshy algae, and non-calcifying invertebrates (hydrozoans, tunicates) which dominated the assemblage. Coralline algae are early species in the epiphytic colonization of P. oceanica and therefore their absence can further modify the pattern of leaf colonization by other species. Therefore, the changes found in the epiphyte community in low pH areas could have potential cascading effects on the seagrass trophic network and the functioning of the system.

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Author Biographies
SILVIA MECCA, University of Rome "La Sapienza"
Environmental Biology
EDOARDO CASOLI, Department of Environmental Biology, "La Sapienza" University of Rome
PhD student, Department of Environmental Biology
GIANDOMENICO ARDIZZONE, University of Rome "La Sapienza"
Environmental Biology
Arnold, T.M., Mealey, C., Leahey, H., Miller, A.W., Hall-Spencer, J.M. et al., 2012. Ocean acidification and the loss of phenolic substances in marine plants. PLoS ONE, 7, e35107.
Balata, D., Bertocci, I., Piazzi, L., Nesti, U., 2008. Comparison between epiphyte assemblages of leaves and rhizomes of the seagrass Posidonia oceanica subjected to different levels of anthropogenic eutrophication. Estuarine, Coastal and Shelf Science, 79, 533-540.
Buia, M.C., Gambi, M.C., Lorenti, M., Dappiano, M., Zupo, V., 2003. Aggiornamento sulla distribuzione e sullo stato ambientale dei sistemi a fanerogame marine (Posidonia oceanica e Cymodocea nodosa) delle isole Flegree. In: Ambiente marino costiero e territorio delle isole Flegree (Ischia Procida Vivara - Golfo di Napoli). Gambi, M.C., De Lauro, M., Iannuzzi, F., (Eds). Liguori Editore, Napoli.
Buia, M.C., Gambi, M.C., Dappiano, M., 2004. The seagrass systems. Biologia Marina Mediterranea, 11 (Suppl. 1), 133- 184.
Cambridge, M.L., How, J.R., Lavery, P.S., Vanderklift, M.A., 2007. Retrospective analysis of epiphyte assemblages in relation to seagrass loss in a eutrophic coastal embayment. Marine Ecology Progress Series, 346, 97-107.
Casola, E., Scardi, M., Mazzella, L., Fresi, E., 1987. Structure of the epiphytic community of Posidonia oceanica leaves in a shallow meadow. Marine Ecology, 8 (4), 285-296.
Corlett, H., Jones, B., 2007. Epiphyte communities on Thalassia testudinum from Grand Cayman, British West Indies: Their composition, structure, and contribution to lagoonal sediments. Sedimentary Geology, 194(3-4), 245-262.
Cox, T.E., Schenone, S., Delille, J., Diaz-Castaneda, V., Alliouane, S. et al., 2015. Effects of ocean acidification on Posidonia oceanica epiphytic community and shoot productivity. Journal of Ecology, 103, 1594-1609.
Cox, T.E., Gazeau, F., Alliouane, S., Hendriks, I., Mahacek, P. et al., 2016. Effects of in situ CO2 enrichment on structural characteristics, photosynthesis, and growth of the Mediterranean seagrass Posidonia oceanica. Biogeosciences, 13, 2179-2194.
Dalla Via, J., Sturmbauer, C., Schönweger, G., Sötz, E., Mathekowitsch, S. et al., 1998. Light gradients and meadow structure in Posidonia oceanica: ecomorphological and functional correlates. Marine Ecology Progress Series, 163, 267-278.
Donnarumma, L., Lombardi, C., Cocito, S., Gambi, M.C., 2014. Settlement pattern of Posidonia oceanica epibionts along a gradient of ocean acidification: an approach with mimics. Mediterranean Marine Science, 15 (3), 498-509.
Foo, S.A., Byrne, M., Ricevuto, E., Gambi, M.C., 2018. The carbon dioxide vents of Ischia, Italy, a natural laboratory to assess impacts of ocean acidification on marine ecosystems: an overview of research and comparisons with other vent systems. Oceanography and Marine Biology: An Annual Review, 56, 237-310.
Gaglioti, M., Auriemma, R., De Vittor, C., Esposito, V., Teixido, N., Gambi, M.C., 2019. A pilot study on Posidonia oceanica features of a hydrothermal system at Panarea (Aeolian Islands, Italy). Biologia Marina Mediterranea 26 (preprint), 236-237. (www.sibm.it).
Gambi, M.C., 2014. Emissioni sommerse di CO2 lungo le coste dell’isola d’Ischia. Rilievi su altre aree come possibili laboratori naturali per lo studio dell’acidificazione e cambiamento climatico a mare. Notiziario S.I.B.M., 66, 67-79.
Gambi, M.C., Gaglioti, M., Teixido, N., 2019. The CO2 vent’s systems off the island of Ischia (Tyrrhenian Sea). Memorie Descrittive della Carta Geologica d’Italia, 105, 55-64.
Garrard, S.L., 2013. The effect of ocean acidification on plant-animal interactions in a Posidonia oceanica meadow. PhD thesis. Open University and Stazione Zoologica Napoli, 289 pp.
Garrard, S.L., Gambi, M.C., Scipione, M.B., Patti, F.P., Lorenti, M. et al., 2014. Indirect effects may buffer negative responses of seagrass invertebrate communities to ocean acidification. Journal of Experimental Marine Biology and Ecology, 461, 31-38.
Giovannetti, E., Montefalcone, M., Morri, C., Bianchi, C.N., Albertelli, G., 2010. Early warning response of Posidonia oceanica epiphyte community to environmental alterations (Ligurian Sea, NW Mediterranean). Marine Pollution Bulletin, 60, 1031-1039.
Giraud, G., Boudouresque, C., Cinelli, F., Fresi, E., Mazzella, L., 1979. Observations sur l’herbier de Posidonia oceanica (L.) Delile autour de l’Ile d’Ischia (Italie). Giornale Botanico Italianio, 113, 261-274.
Gonzalez-Delgado, S., Hernadez, J.C., 2018. The importance of natural acidified systems in the study of ocean acidification: what have we learned? Advances in Marine Biology, 80, 57-99.
Guidetti, P., Bussotti, S., 1998. Juveniles of littoral fish species in shallow seagrass beds: preliminary quali-quantitative data. Biologia Marina Mediterranea, 5, 347-350.
Guilini, K., Weber, M., de Beer, D., Schneider, M., Molari, M. et al., 2017. Response of Posidonia oceanica seagrass and its epibiont communities to ocean acidification. PloS ONE 12(8):e0181531.
Hall-Spencer, J.M., Rodolfo-Metalpa, R., Martin, S., Ransome, E., Fine, M. et al., 2008. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature, 454, 96:99.
Invers, O., Zimmerman, R., Alberte, R.S., Perez, M., Romero, J., 2001. Inorganic carbon sources for seagrass photosynthesis: an experimental evaluation of bicarbonate use in species inhabiting temperate waters. Journal of Experimental Marine Biology and Ecology, 265, 203-217.
Kerrison, P., Hall-Spencer, J.M., Suggett, D., Hepburn, L.J., Steinke, M., 2011. Assessment of pH variability at coastal CO2 vent for ocean acidification studies. Estuarine Coastal and Shelf Science, 94 (2), 129-137.
Kroeker, K.J., Kordas, R.L., Crim, R.N., Singh, G.G., 2010. Meta- analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters, 13, 1419-1434.
Kroeker, K.J., Micheli, F., Gambi, M.C., Martz, T.R., 2011. Divergent ecosystem responses within a benthic marine community to ocean acidification. Proceedings of the National Academy of Sciences, 108 (35), 14515-14520.
Kroeker, K.J., Micheli, F., Gambi, M.C., 2012. Ocean acidification causes ecosystem shifts via altered competitive interactions. Nature Climate Change, 3, 156-159.
Leoni, V., Pasqualini, V., Pergent-Martini, C., Vela, A., Pergent, G., 2006. Morphological responses of Posidonia oceanica to experimental nutrient enrichment of the canopy water. Journal of Experimental Marine Biology and Ecology, 339, 1-14.
Lepoint, G., Havelange, S., Gobert, S., Bouquegneau, J.M., 1999. Fauna vs flora contribution to the leaf epiphytes biomass in a Posidonia oceanica seagrass bed (Revellata Bay, Corsica). Hydrobiologia, 394, 63-67.
Libes, M., Boudouresque, C.F., 1987. Uptake and long-distance transport of carbon in the marine phanerogam Posidonia oceanica. Marine Ecology Progress Series, 38, 177-186.
Lucey, N.M., Lombardi, C., Florio, M., Rundle, S., Calosi, P. et al., 2018. Distribution patterns of life history traits in calcifying Spirorbinae polychaetes along natural pH gradients. Marine Ecology Progress Series, 589, 145-156.
Martin, S., Rodolfo-Metalpa, R., Ransome, E., Rowley, S., Buia, M.C. et al., 2008. Effects of naturally acidified seawater on seagrass calcareous epibionts. Biology Letters, 4(6), 689-692.
Mazzella, L., Scipione, M.B., Buia, M.C., 1989. Spatio-temporal distribution of algal and animal communities in a Posidonia oceanica (L.) Delile meadow. Marine Ecology, 10, 107-131.
Mazzella, L., Buia, M.C., Gambi, M.C., Lorenti, M,. Russo, G.F. et al., 1992. Plant-animal trophic relationships in the Posidonia oceanica ecosystem of the Mediterranean Sea: a review, p. 165-187. In: Plant-Animal Interaction in the Marine Benthos. John, D.M., Hawkins, S.J., Price, J.H. (Eds). Clarendon Press, Oxford.
Migliore, L., Piccenna, A., Rotini, A., Garrard, S.L., Buia, M.C., 2012. Can ocean acidification affect chemical defence in Posidonia oceanica? p. 14. In: Proceedings 3rd Mediterranean Seagrass Workshop 2012. Essaouira, Morocco.
Milliman, J.D., 1974. Marine carbonates. Springer, Berlin, p. 375. Moschella, P., Alberto, F., Antoniadou, C., Chintiroglu, C., Azzurro, E. et al., 2010. CIESM tropical signals program - Tracking biogeographic trends in a changing sea. Commission. p. 39. CIESM Congress Proceedings, Venice.
Nelson, T.A., Waaland, J.R., 1997. Seasonality of eelgrass, epiphyte, and grazer biomass and productivity in subtidal eelgrass meadows subjected to moderate tidal amplitude. Aquatic Botany, 56, 51-74.
Nogueira, P., Gambi, M.C., Vizzini, S., Califano, G., Tavares, A.M. et al., 2017. Altered epiphyte community and sea urchin diet in Posidonia oceanica meadows in the vicinity of volcanic CO2 vents. Marine Environmental Research, 127, 102-111.
Pages, J.F., Farina, S., Gera, A., Arthur, R., Romero, J., Alcoverro, T., 2012. Indirect interactions in seagrasses: fish herbivores increase predation risk to sea urchins by modifying plant traits. Functional Ecology, 26, 1015-1023.
Pergent-Martini, C., Pergent, G., 1996. Spatio-temporal dynamics of Posidonia oceanica beds near a sewage outfall (Mediterranean-France). p. 299-306. In: Kuo J., Phillips R.C., Walker D.I., Kirkman H. (Eds), In: Seagrass Biology. Proceedings of an International Workshop. Rottnest Island, Western Australia, 25-29 January 1996.
Perry, C.T., Beavington-Penney, S.J., 2005. Epiphytic calcium carbonate production and facies development within sub-tropical seagrass beds, Inhaca Island, Mozambique. Sedimentary Geology, 174, 161-176.
Piazzi, L., Balata, D., Cinelli, F., Benedetti-Cecchi, L., 2004. Patterns of spatial variability in epiphytes of Posidonia oceanica. Differences between a disturbed and two references locations. Aquatic Botany, 79, 345-356.
Piazzi, L., Balata, D., Ceccherelli, G., 2016. Epiphyte assemblages of the Mediterranean seagrass Posidonia oceanica: an overview. Marine Ecology, 37 (1), 3-41.
Poluzzi, A., Sartori, R., 1974. Report on the carbonate mineralogy of bryozoans. p. 193-210. In: Documents des Laboratoires de Géologie Lyon. Pouyet, S. (Ed). Hors Série, France.
Porzio, L., Buia, M.C., Hall-Spencer, J.M., 2011. Effects of ocean acidification on macroalgal communities. Journal of Experimental of Marine Biology and Ecology, 400, 278-287.
Rastrick, S.S.P., Graham, H., Azetsu-Scott, K., Calosi, P., Chierici, M. et al., 2018. Using natural analogues to investigate the effects of climate change and ocean acidification on Northern ecosystems. ICES Journal of Marine Science, 75(7), 2299-2311.
Ravaglioli, C., Lauritano, C., Buia, M.C., Balestri, E., Capocchi, A. et al., 2017. Nutrient loading fosters seagrass productivity under ocean acidification. Scientific Reports, 7(1), 13732.
Ricevuto, E., Kroeker, K.J., Ferrigno, F., Micheli, F., Gambi, M.C., 2014. Spatio-temporal variability of polychaete colonization at volcanic CO2 vents (Italy) indicates high tolerance to ocean acidification. Marine Biology, 161, 2909-2919.
Ricevuto, E., Vizzini, S., Gambi, M.C., 2015. Ocean acidification effects on stable isotope signatures and trophic interactions of polychaete consumers and organic matter sources at a CO2 shallow vent system. Journal of Experimental Marine Biology and Ecology, 468, 105-117.
Rodolfo-Metalpa, R., Lombardi, C., Cocito, S., Hall-Spencer, J.M., Gambi, M.C., 2010. Effects of ocean acidification and high temperatures on the bryozoan Myriapora truncata at natural CO2 vents. Marine Ecology, 31, 447-456.
Scartazza, A., Moscatello, S., Gavrichkova, O., Buia. M.C., Lauteri, M. et al., 2017. Carbon and nitrogen allocation strategy in Posidonia oceanica is altered by seawater acidification. Science of the Total Environment, 607, 954-964.
Tedesco, D., 1996. Chemical and isotopic investigation of fumarolic gases from Ischia Island (Southern Italy): evidence of magmatic and crustal contribution. Journal of Volcanology and Geothermal Research, 74, 233-242. T-MedNet: http://www.t-mednet.org/t-sites/ (Accessed 4th November 2019).T
omas, F., Turon, X., Romero, J., 2005. Effects of herbivores on a Posidonia oceanica seagrass meadow: importance of epiphytes. Marine Ecology Progress Series, 287, 115-125.
Vizzini, S., Tomasello, A., Di Maida, G., Pirrotta, M., Mazzola, A. et al., 2010. Effect of explosive shallow hydrothermal vents on δ13C and growth performance in the seagrass Posidonia oceanica. Journal of Ecology, 98 (6), 1284-1291.
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