Abstract
Alterations in seagrass epiphytic communities are expected under future ocean acidification conditions, yet this hypothesis has been little tested in situ. A Free Ocean Carbon Dioxide Enrichment system was used to lower pH by a ~0.3 unit offset within a partially enclosed portion (1.7 m3) of a Posidonia oceanica meadow (11 m depth) between June 21 and November 3, 2014. Leaf epiphytic community composition (% cover) and bulk epiphytic mineralogy were compared every 4 weeks within three treatments, located in the same meadow: a pH-manipulated (experimental enclosure) and a control enclosure, as well as a nearby ambient area. Percent coverage of invertebrate calcifiers and crustose coralline algae (CCA) did not appear to be affected by the lowered pH. Furthermore, fleshy algae did not proliferate at lowered pH. Only Foraminifera, which covered less than 3% of leaf surfaces, declined in manner consistent with ocean acidification predictions. Bulk epiphytic magnesium carbonate composition was similar between treatments and percentage of magnesium appeared to increase from summer to autumn. CCA did not exhibit any visible skeleton dissolution or mineral alteration at lowered pH and carbonate saturation state. Negative impacts from ocean acidification on P. oceanica epiphytic communities were smaller than expected. Epiphytic calcifiers were possibly protected from the pH treatment due to host plant photosynthesis inside the enclosure where water flow is slowed. The more positive outcome than expected suggests that calcareous members of epiphytic communities may find refuge in some conditions and be resilient to environmentally relevant changes in carbonate chemistry.
Similar content being viewed by others
References
Alcoverro T, Duarte C, Romero J (1995) Annual growth dynamics of Posidonia oceanica: contribution of large-scale versus local factors to seasonality. Mar Ecol Prog Ser 120:203–210. doi:10.3354/meps120203
Anthony KRN, Kleypas J, Gattuso J-P (2011) Coral reefs modify their seawater carbon chemistry—implications for impacts of ocean acidification. Glob Change Biol 17:3655–3666. doi:10.1111/j.1365-2486.2011.02510.x
Anthony KRN, Diaz-Pulido G, Verlinden N, Tilbrook B, Andersson AJ (2013) Benthic buffers and boosters of ocean acidification on coral reefs. Biogeosciences 10:4897–4909. doi:10.5194/bg-10-4897-2013
Apostolaki ET, Vizzini S, Hendriks IE, Olsen YS (2014) Seagrass ecosystem response to long-term high CO2 in a Mediterranean volcanic vent. Mar Environ Res 99:9–15
Baggini C, Salomidi M, Voutsinas E, Bray L, Krasakopoulou E, Hall-Spencer JM (2014) Seasonality affects macroalgal community response to increases in pCO2. PLoS ONE 9:e106520. doi:10.1371/journal.pone.0106520
Beer S, Koch E (1996) Photosynthesis of marine macroalgae and seagrasses in globally changing CO2 environments. Mar Ecol Prog Ser 141:199–204
Borowitzka MA, Lavery PS, van Keulen M (2006) Seagrasses: biology, ecology and conservation. In: Larkum AWD, Orth RJ, Duarte CM (eds) Epiphytes of seagrasses. Springer, Dordrecht, pp 441–461
Bosence D (1989) Biogenic carbonate production in Florida Bay. Bull Mar Sci 44:419–433
Britton D, Cornwall CE, Revill AT, Hurd C, Johnson C (2016) Ocean acidification reverses the positive effects of seawater pH fluctuations on growth and photosynthesis of the habitat-forming kelp, Ecklonia radiata. Sci Rep. doi:10.1038/srep26036
Burnell O, Russell B, Irving A, Connell S (2014) Seagrass response to CO2 contingent on epiphytic algae: indirect effects can overwhelm direct effects. Oecologia 176:871–882
Campbell JE, Fourqurean JW (2014) Ocean acidification outweighs nutrient effects in structuring seagrass epiphyte communities. J Ecol 102:730–737. doi:10.1111/1365-2745.12233
Cebrián J, Enríquez S, Fortes MD, Agawin N, Vermaat JE, Duarte CM (1999) Epiphyte accrual on Posidonia oceanica (L.) Delile leaves: implications for light absorption. Bot Mar 42:123–128. doi:10.1515/BOT.1999.015
Chave KE, Wheeler BD (1965) Mineralogic changes during growth in the red alga, Clathromorphum compactum. Science 147:621. doi:10.1126/science.147.3658.621
Ciais P, Sabine C, Bala G, Bopp L, Brovkin V, Canadell J, Chhabra A, DeFries R, Galloway J, Heimann M, Jones C, Le Quéré C, Myneni RB, Piao S, Thornton P (2013) Carbon and other biogeochemical cycles. Cambridge University Press, Cambridge
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust Ecol 18:117–143. doi:10.1111/j.1442-9993.1993.tb00438.x
Cornwall CE, Boyd PW, McGraw CM, Hepburn C, Pilditch CA, Morris JN, Smith AM, Hurd CL (2014) Diffusion boundary layers ameliorate the negative effects of ocean acidification on the temperate coralline macroalga Arthrocardia corymbosa. PLoS ONE 9:e97235. doi:10.1371/journal.pone.0097235
Cornwall C, Pilditch C, Hepburn C, Hurd CL (2015) Canopy macroalgae influence understorey corallines’ metabolic control of near-surface pH and oxygen concentration. Mar Ecol Prog Ser 525:81–95. doi:10.3354/meps11190
Cox TE, Schenone S, Delille J, Díaz-Castañeda V, Alliouane S, Gattuso JP, Gazeau F (2015) Effects of ocean acidification on Posidonia oceanica epiphytic community and shoot productivity. J Ecol 103:1594–1609. doi:10.1111/1365-2745.12477
Cox TE, Gazeau F, Alliouane S, Hendriks IE, Mahacek P, Le Fur A, Gattuso J-P (2016) Effects of in situ CO2 enrichment on structural characteristics, photosynthesis, and growth of the Mediterranean seagrass Posidonia oceanica. Biogeosciences 13:2179–2194. doi:10.5194/bg-13-2179-2016
Davies GM, Gray A (2015) Don’t let spurious accusations of pseudoreplication limit our ability to learn from natural experiments (and other messy kinds of ecological monitoring). Ecol Evol 5:5295–5304. doi:10.1002/ece3.1782
Diaz-Pulido G, Nash MC, Anthony KRN, Bender D, Opdyke BN, Reyes-Nivia C, Troitzsch U (2014) Greenhouse conditions induce mineralogical changes and dolomite accumulation in coralline algae on tropical reefs. Nat Commun. doi:10.1038/ncomms4310
Donnarumma L, Lombardi C, Cocito S, Gambi MC (2014) Settlement pattern of Posidonia oceanica epibionts along a gradient of ocean acidification: an approach with mimics. Mediterr Mar Sci 15:498–509. doi:10.12681/mms.677
Egilsdottir H, Noisette F, Noël LM-LJ, Olafsson J, Martin S (2013) Effects of pCO2 on physiology and skeletal mineralogy in a tidal pool coralline alga Corallina elongata. Mar Biol 160:2103–2112. doi:10.1007/s00227-012-2090-7
Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432. doi:10.1093/icesjms/fsn048
Feely RA (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366. doi:10.1126/science.1097329
Frankovich TA, Zieman JC (1994) Total epiphyte and epiphytic carbonate production on Thalassia testudinum across Florida Bay. Bull Mar Sci 54:679–695
Gattuso J-P, Kirkwood W, Barry JP, Cox TE, Gazeau F, Hansson L, Hendriks I, Kline DI, Mahacek P, Martin S, McElhany P, Peltzer ET, Reeve J, Roberts D, Saderne V, Tait K, Widdicombe S, Brewer PG (2014) Free-ocean CO2 enrichment (FOCE) systems: present status and future developments. Biogeosciences 11:4057–4075
Gattuso J-P, Magnan A, Bille R, Cheung WWL, Howes EL, Joos F, Allemand D, Bopp L, Cooley SR, Eakin CM, Hoegh-Guldberg O, Kelly RP, Portner H-O, Rogers AD, Baxter JM, Laffoley D, Osborn D, Rankovic A, Rochette J, Sumaila UR, Treyer S, Turley C (2015) Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349:aac4722. doi:10.1126/science.aac4722
Gaylord B, Kroeker KJ, Sunday JM, Anderson KM, Barry JP, Brown NE, Connell SD, Dupont S, Fabricius KE, Hall-Spencer JM, Klinger T, Milazzo M, Munday PL, Russell BD, Sanford E, Schreiber SJ, Thiyagarajan V, Vaughan MLH, Widdicombe S, Harley CDG (2015) Ocean acidification through the lens of ecological theory. Ecology 96:3–15. doi:10.1890/14-0802.1
Gazeau F, Parker LM, Comeau S, Gattuso J-P, O’Connor WA, Martin S, Pörtner H-O, Ross PM (2013) Impacts of ocean acidification on marine shelled molluscs. Mar Biol 160:2207–2245. doi:10.1007/s00227-013-2219-3
Gischler E, Dietrich S, Harris D, Webster JM, Ginsburg RN (2013) A comparative study of modern carbonate mud in reefs and carbonate platforms: mostly biogenic, some precipitated. Sediment Geol 292:36–55. doi:10.1016/j.sedgeo.2013.04.003
Gorsky G, Ohman MD, Picheral M, Gasparini S, Stemmann L, Romagnan JB, Cawood A, Pesant S, Garcia-Comas C, Prejger F (2010) Digital zooplankton image analysis using the ZooScan integrated system. J Plankton Res 32:285–303
Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia MC (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99
Hemminga MA, Duarte CM (2000) Seagrass ecology. University of Cambridge, Cambridge
Hendriks IE, Duarte CM, Olsen YS, Steckbauer A, Ramajo L, Moore TS, Trotter JA, McCulloch M (2014a) Biological mechanisms supporting adaptation to ocean acidification in coastal ecosystems. Estuar Coast Shelf Sci 152:1–8. doi:10.1016/j.ecss.2014.07.019
Hendriks IE, Olsen YS, Ramajo L, Basso L, Steckbauer A, Moore TS, Howard J, Duarte CM (2014b) Photosynthetic activity buffers ocean acidification in seagrass meadows. Biogeosciences 11:333–346. doi:10.5194/bg-11-333-2014
Hofmann LC, Bischof K (2014) Ocean acidification effects on calcifying macroalgae. Aquat Biol 22:261–279
Hofmann LC, Koch M, de Beer D (2016) Biotic control of surface pH and evidence of light-induced H + pumping and Ca2+–H+ exchange in a tropical crustose coralline alga. PLoS ONE 11:e0159057
Hurd CL (2015) Slow-flow habitats as refugia for coastal calcifiers from ocean acidification. J Phycol 51:599–605. doi:10.1111/jpy.12307
Hurlbert S (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211
Jackson EL, Rees SE, Wilding C, Attrill MJ (2015) Use of a seagrass residency index to apportion commercial fishery landing values and recreation fisheries expenditure to seagrass habitat service: seagrass contribution to fishery value. Conserv Biol 29:899–909. doi:10.1111/cobi.12436
Johnson MD, Moriarty VW, Carpenter RC (2014) Acclimatization of the crustose coralline alga Porolithon onkodes to variable pCO2. PLoS ONE 9:e87678. doi:10.1371/journal.pone.0087678
Kerrison P, Hall-Spencer JM, Suggett DJ, Hepburn LJ, Steinke M (2011) Assessment of pH variability at a coastal CO2 vent for ocean acidification studies. Estuar Coast Shelf Sci 94:129–137
Keul N, Langer G, de Nooijer LJ, Bijma J (2013) Effect of ocean acidification on the benthic foraminifera Ammonia sp. is caused by a decrease in carbonate ion concentration. Biogeosciences 10:6185–6198. doi:10.5194/bg-10-6185-2013
Kleypas J, Buddemeier R, Archer D, Gattuso J-P, Langdon C, Opdyke B (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120
Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Change Biol 19:103–132. doi:10.1111/j.1365-2486.2012.02791.x
Krayesky-Self S, Richards JL, Rahmatian M, Fredericq S (2016) Aragonite infill in overgrown conceptacles of coralline Lithothamnion spp. (Hapalidiaceae, Hapalidiales, Rhodophyta): new insights in biomineralization and phylomineralogy. J Phycol 52:161–173. doi:10.1111/jpy.12392
Kroeker KJ, Kordas RL, Crim RN, Singh GG, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso J-P (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms: biological responses to ocean acidification. Ecol Lett 13:1419–1434. doi:10.1111/j.1461-0248.2010.01518.x
Kroeker KJ, Micheli F, Gambi MC (2012) Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat Clim Change 3:156–159. doi:10.1038/nclimate1680
Kroeker KJ, Kordas RL, Crim R, Singh GG (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol 19:1884–1896. doi:10.1111/gcb.12179
Land LS (1970) Carbonate mud: production by epibiont growth on Thalassia testudinum. J Sediment Petrol 40:1361–1363
Lepoint G, Havelange S, Gobert S, Bouquegneau JM (1999) Fauna vs flora contribution to the leaf epiphytes biomass in a Posidonia oceanica seagrass bed (Revellata Bay, Corsica). Hydrobiologia 394:63–67
Lepoint G, Nyssen F, Gobert S, Dauby P, Bouquegneau JM (2000) Relative impact of a seagrass bed and its adjacent epilithic algal community in consumer diets. Mar Biol 136:513–518
Lepoint G, Jacquemart J, Bouquegneau JM, Demoulin V, Gobert S (2007) Field measurements of inorganic nitrogen uptake by epiflora components of the seagrass Posidonia oceanica (Monocotyledons, Posidoniaceae). J Phycol 43:208–218
Littler M, Littler D (2013) The nature of crustose coralline algae and their interactions on reefs. Smithson Contrib Mar Sci 39:199–212
Lombardi C, Cocito S, Gambi M, Cisterna B, Flach F, Taylor P, Keltie K, Freer A, Cusack M (2011a) Effects of ocean acidification on growth, organic tissue and protein profile of the Mediterranean bryozoan Myriapora truncata. Aquat Biol 13:251–262. doi:10.3354/ab00376
Lombardi C, Gambi MC, Vasapollo C, Taylor P, Cocito S (2011b) Skeletal alterations and polymorphism in a Mediterranean bryozoan at natural CO2 vents. Zoomorphology 130:135–145. doi:10.1007/s00435-011-0127-y
Mabrouk L, Ben Brahim M, Hamza A, Mahfoudhi M, Bradai MN (2014) A comparison of abundance and diversity of epiphytic microalgal assemblages on the leaves of the seagrasses Posidonia oceanica (L.) and Cymodocea nodosa (Ucria) Asch in Eastern Tunisia. J Mar Biol 2014:1–10. doi:10.1155/2014/275305
Martin S, Gattuso J-P (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Change Biol 15:2089–2100. doi:10.1111/j.1365-2486.2009.01874.x
Martin S, Rodolfo-Metalpa R, Ransome E, Rowley S, Buia M-CC, Gattuso J-P, Hall-Spencer J (2008) Effects of naturally acidified seawater on seagrass calcareous epibionts. Biol Lett 4:689–692. doi:10.1098/rsbl.2008.0412
Martínez-Crego B, Olivé I, Santos R (2014) CO2 and nutrient-driven changes across multiple levels of organization in Zostera noltii ecosystems. Biogeosciences 11:7237–7249
McCoy SJ, Kamenos NA (2015) Coralline algae (Rhodophyta) in a changing world: integrating ecological, physiological, and geochemical responses to global change. J Phycol 51:6–24. doi:10.1111/jpy.12262
McCoy SJ, Ragazzola F (2014) Skeletal trade-offs in coralline algae in response to ocean acidification. Nat Clim Change 4:719–723. doi:10.1038/nclimate2273
Nash MC, Troitzsch U, Opdyke BN, Trafford JM, Russell BD, Kline DI (2011) First discovery of dolomite and magnesite in living coralline algae and its geobiological implications. Biogeosciences 8:3331–3340. doi:10.5194/bg-8-3331-2011
Nash MC, Opdyke BN, Wu Z, Xu H, Trafford JM (2014) Simple X-ray diffraction techniques to identify Mg-calcite, dolomite, and magnesite in tropical coralline algae and assess peak asymmetry. J Sediment Res 83:1084–1098. doi:10.2110/jsr.2013.67
Nelsen JE, Ginsburg RN (1986) Calcium carbonate production by epibionts on Thalassia in Florida Bay. J Sediment Res 56:622–628. doi:10.1306/212F89EF-2B24-11D7-8648000102C1865D
Nelson W (2009) Calcified macroalgae–critical to coastal ecosystems and vulnerable to change: a review. Mar Freshw Res 60:787–801. doi:10.1071/MF08335
Oksanen L (2001) Logic of experiments in ecology: is pseudoreplication a pseudoissue? Oikos 94:27–38. doi:10.1034/j.1600-0706.2001.11311.x
Pasqualini V, Pergent-Martini C, Clabaut P, Pergent G (1998) Mapping of Posidonia oceanica using aerial photographs and side scan sonar: application off the island of Corsica (France). Estuar Coast Shelf Sci 47:359–367
Perry CT, Beavington-Penney SJ (2005) Epiphytic calcium carbonate production and facies development within sub-tropical seagrass beds, Inhaca Island, Mozambique. Sediment Geol 174:161–176. doi:10.1016/j.sedgeo.2004.12.003
Pettit LR, Smart CW, Hart MB, Milazzo M, Hall-Spencer JM (2015) Seaweed fails to prevent ocean acidification impact on foraminifera along a shallow-water CO 2 gradient. Ecol Evol 5:1784–1793. doi:10.1002/ece3.1475
Pinckney JL, Fiorenza M (1998) Microalgae on seagrass mimics: does epiphyte community structure differ from live seagrasses? J Exp Mar Biol Ecol 221:59–70
Prado P, Alcoverro T, Romero J (2008) Seasonal response of Posidonia oceanica epiphyte assemblages to nutrient increase. Mar Ecol Prog Ser 359:89–98
Rodolfo-Metalpa R, Lombardi C, Cocito S, Hall-Spencer JM, Gambi MC (2010) Effects of ocean acidification and high temperatures on the bryozoan Myriapora truncata at natural CO2 vents. Mar Ecol 31:447–456. doi:10.1111/j.1439-0485.2009.00354.x
Roleda MY, Cornwall CE, Feng Y, McGraw CM, Smith AM, Hurd CL (2015) Effect of ocean acidification and pH Fluctuations on the growth and development of coralline algal recruits, and an associated benthic algal assemblage. PLoS ONE 10:e0140394. doi:10.1371/journal.pone.0140394
Saderne V, Wahl M (2013) Differential responses of calcifying and non-calcifying epibionts of a brown macroalga to present-day and future upwelling pCO2. PLoS ONE 8:e70455. doi:10.1371/journal.pone.0070455
Small DP, Milazzo M, Bertolini C, Graham H, Hauton C, Hall-Spencer JM, Rastrick SPS (2016) Temporal fluctuations in seawater p CO 2 may be as important as mean differences when determining physiological sensitivity in natural systems. ICES J Mar Sci 73:604–612. doi:10.1093/icesjms/fsv232
Smith AM (2014) Growth and calcification of marine bryozoans in a changing ocean. Biol Bull 226:203–210
Smith AM, Sutherland JE, Kregting L, Farr TJ, Winter DJ (2012) Phylomineralogy of the coralline red algae: correlation of skeletal mineralogy with molecular phylogeny. Phytochemistry 81:97–108. doi:10.1016/j.phytochem.2012.06.003
Steel JB, Wilson BJ (2003) Which is the phyte in epiphyte? Folia Geobot 38:97–99. doi:10.1007/BF02803129
Stewart-Oaten A, Murdoch W, Parker K (1986) Environmental impact assessment: “pseudoreplication” in time? Ecology 67:929–940
Sunday JM, Fabricius KE, Kroeker KJ, Anderson KM, Brown NE, Barry JP, Connell SD, Dupont S, Gaylord B, Hall-Spencer JM, Klinger T, Milazzo M, Munday PL, Russell BD, Sanford E, Thiyagarajan V, Vaughan MLH, Widdicombe S, Harley CDG (2016) Ocean acidification can mediate biodiversity shifts by changing biogenic habitat. Nat Clim Change 7:81–85. doi:10.1038/nclimate3161
Tomas F, Turon X, Romero J (2005) Effects of herbivores on a Posidonia oceanica seagrass meadow: importance of epiphytes. Mar Ecol Prog Ser 287:115–125
Vizzini S, Di Leonardo R, Costa V, Tramati CD, Luzzu F, Mazzola A (2013) Trace element bias in the use of CO2 vents as analogues for low pH environments: implications for contamination levels in acidified oceans. Estuar Coast Shelf Sci 134:19–30. doi:10.1016/j.ecss.2013.09.015
Acknowledgements
We would like to acknowledge the following people who assisted in the laboratory, in the field, or with engineering: E. Beck Acain, J. Acain, J. Delille, L. van der Heijden, M. Maillot, F. Moullec, S. Schenone, L. Urbini, K. Walzyńska. We are grateful to A. Elineau for help with the ZooScan. We also thank J.-J. Pangrazi, R. Patrix and E. Tanguy for aide in construction of the enclosures. G. de Liege, D. Luquet and D. Robin kindly assisted in diving collection activities. This work was funded by the ‘European Free Ocean Carbon Enrichment’ (eFOCE; BNP-Paribas Foundation), the ‘European Project on Ocean Acidification’ (EPOCA; Grant Agreement 211384) and the MISTRALS-MERMEX (INSU, CNRS) program.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interests and all applicable guidelines for the use of animals were followed.
Ethical approval
All applicable guidelines for the use of animals were followed.
Additional information
Responsible Editor: F. Weinberger.
Reviewed by J. M. Hall-Spencer and an undisclosed expert.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Cox, T.E., Nash, M., Gazeau, F. et al. Effects of in situ CO2 enrichment on Posidonia oceanica epiphytic community composition and mineralogy. Mar Biol 164, 103 (2017). https://doi.org/10.1007/s00227-017-3136-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-017-3136-7