Abstract
Quantifying the strength of non-trophic interactions exerted by foundation species is critical to understanding how natural communities respond to environmental stress. In the case of ocean acidification (OA), submerged marine macrophytes, such as seagrasses, may create local areas of elevated pH due to their capacity to sequester dissolved inorganic carbon through photosynthesis. However, although seagrasses may increase seawater pH during the day, they can also decrease pH at night due to respiration. Therefore, it remains unclear how consequences of such diel fluctuations may unfold for organisms vulnerable to OA. We established mesocosms containing different levels of seagrass biomass (Zostera marina) to create a gradient of carbonate chemistry conditions and explored consequences for growth of juvenile and adult oysters (Crassostrea gigas), a non-native species widely used in aquaculture that can co-occur, and is often grown, in proximity to seagrass beds. In particular, we investigated whether increased diel fluctuations in pH due to seagrass metabolism affected oyster growth. Seagrasses increased daytime pH up to 0.4 units but had little effect on nighttime pH (reductions less than 0.02 units). Thus, both the average pH and the amplitude of diel pH fluctuations increased with greater seagrass biomass. The highest seagrass biomass increased oyster shell growth rate (mm day−1) up to 40%. Oyster somatic tissue weight and oyster condition index exhibited a different pattern, peaking at intermediate levels of seagrass biomass. This work demonstrates the ability of seagrasses to facilitate oyster calcification and illustrates how non-trophic metabolic interactions can modulate effects of environmental change.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Angelini C, Altieri AH, Silliman BR, Bertness MD (2011) Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. Bioscience 61:782–789. https://doi.org/10.1525/bio.2011.61.10.8
Barclay KM, Gaylord B, Jellison BM et al (2019) Variation in the effects of ocean acidification on shell growth and strength in two intertidal gastropods. Mar Ecol Prog Ser 626:109–121. https://doi.org/10.3354/meps13056
Barry SC, Frazer TK, Jacoby CA (2013) Production and carbonate dynamics of Halimeda incrassata (Ellis) Lamouroux altered by Thalassia testudinum Banks and Soland ex König. J Exp Mar Bio Ecol 444:73–80. https://doi.org/10.1016/j.jembe.2013.03.012
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Sta 67:1–48. https://doi.org/10.18637/jss.v067.i01
Beer S, Vilenkin B, Weil A et al (1998) Measuring photosynthetic rates in seagrasses by pulse amplitude modulated (PAM) fluorometry. Mar Ecol Prog Ser 174:293–300. https://doi.org/10.3354/meps174293
Bergstrom E, Silva J, Martins C, Horta P (2019) Seagrass can mitigate negative ocean acidification effects on calcifying algae. Sci Rep 9:1932. https://doi.org/10.1038/s41598-018-35670-3
Bodega Ocean Observation Node (2018) Data provided by the University of California, Davis, Bodega Marine Laboratory. https://boon.ucdavis.edu/data-access/products/seawater
Buapet P, Gullström M, Björk M (2013) Photosynthetic activity of seagrasses and macroalgae in temperate shallow waters can alter seawater pH and total inorganic carbon content at the scale of a coastal embayment. Mar Freshw Res 64:1040–1048. https://doi.org/10.1071/MF12124
Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365. https://doi.org/10.1038/425365a
Carey N, Dupont S, Sigwart JD (2016) Sea hare Aplysia punctata (Mollusca: Gastropoda) can maintain shell calcification under extreme ocean acidification. Biol Bull 231:142–151. https://doi.org/10.1086/690094
Clayton TD, Byrne RH (1993) Spectrophotometric seawater pH measurements: total hydrogen ion concentration scale calibration of m-cresol purple and at-sea results. Deep Res Part I 40:2115–2129. https://doi.org/10.1016/0967-0637(93)90048-8
Clements JC, Comeau LA, Carver CE et al (2018) Short-term exposure to elevated pCO2 does not affect the valve gaping response of adult eastern oysters, Crassostrea virginica, to acute heat shock under an ad libitum feeding regime. J Exp Mar Bio Ecol 506:9–17. https://doi.org/10.1016/j.jembe.2018.05.005
Cornwall CE, Hepburn CD, Mcgraw CM et al (2013) Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proc R Soc B Biol Sci 280:20132201. https://doi.org/10.1098/rspb.2013.2201
Davenport J, Chen X (1987) A comparison of methods for the assessment of condition in the mussel (Mytilus edulis L.). J Molluscan Stud 53:293–297. https://doi.org/10.1093/mollus/53.3.293
Dayton P (1972) Toward an understanding of community resilience and the potential effects of enrichments to the benthos at McMurdo Sound, Antarctica. Proc Colloq Conserv Probl Allen Press Lawrence, Kansas, pp 81–96
Dickson AG (1990) Standard potential of the reaction: AgCl(s) + 12H2(g) = Ag(s) + HCl(aq), and and the standard acidity constant of the ion HSO4- in synthetic sea water from 273.15 to 318.15 K. J Chem Thermodyn 22:113–127. https://doi.org/10.1016/0021-9614(90)90074-Z
Duarte CM, Cebrián J (1996) The fate of marine autotrophic production. Limnol Oceanogr 41:1758–1766. https://doi.org/10.4319/lo.1996.41.8.1758
DuBois K, Abbott J, Williams S, Stachowicz J (2019) Relative performance of eelgrass genotypes shifts during an extreme warming event: disentangling the roles of multiple traits. Mar Ecol Prog Ser 615:67–77. https://doi.org/10.3354/meps12914
Easley RA, Byrne RH (2012) Spectrophotometric calibration of pH electrodes in seawater using purified m-cresol purple. Environ Sci Technol 46:5018–5024. https://doi.org/10.1021/es300491s
Ferriss BE, Conway-Cranos LL, Sanderson BL, Hoberecht L (2019) Bivalve aquaculture and eelgrass: a global meta-analysis. Aquaculture 498:254–262. https://doi.org/10.1016/j.aquaculture.2018.08.046
Gabbott PA (1976) Energy metabolism. In: Bayne BL (ed) Marine mussels: their ecology and physiology. Cambridge University Press, Cambridge, pp 293–355
Gattuso JP, Epitalon JM, Lavigne H, Orr J (2019) Seacarb: seawater Carbonate Chemistry. R Package version 3.2.12
Gaylord B, Kroeker KJ, Sunday JM et al (2015) Ocean acidification through the lens of ecological theory. Ecology 96:3–15. https://doi.org/10.1890/14-0802.1
Groner ML, Burge CA, Cox R et al (2018) Oysters and eelgrass: potential partners in a high pCO2 ocean. Ecology 99:1802–1814. https://doi.org/10.1002/ecy.2393
Ha G, Williams SL (2018) Eelgrass community dominated by native omnivores in Bodega Bay, California, USA. Bull Mar Sci 94:1333–1353. https://doi.org/10.5343/bms.2017.1091
Hale R, Calosi P, Mcneill L et al (2011) Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities. Oikos 120:661–674. https://doi.org/10.1111/j.1600-0706.2010.19469.x
Hendriks IE, Olsen YS, Ramajo L et al (2014) Photosynthetic activity buffers ocean acidification in seagrass meadows. Biogeosciences 11:333–346. https://doi.org/10.5194/bg-11-333-2014
Hendriks IE, Duarte CM, Marbà N, Krause-Jensen D (2017) pH gradients in the diffusive boundary layer of subarctic macrophytes. Polar Biol 40:2343–2348. https://doi.org/10.1007/s00300-017-2143-y
Hilbish TJ (1986) Growth trajectories of shell and soft tissue in bivalves: Seasonal variation in Mytilus edulis L. J Exp Mar Bio Ecol 96:103–113. https://doi.org/10.1016/0022-0981(86)90236-4
Hofmann GE, Smith JE, Johnson KS et al (2011) High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS ONE 6:e28983. https://doi.org/10.1371/journal.pone.0028983
Hughes AR, Stachowicz JJ, Williams SL (2009) Morphological and physiological variation among seagrass (Zostera marina) genotypes. Oecologia 159:725–733. https://doi.org/10.1007/s00442-008-1251-3
Huntington BE, Boyer KE (2008) Effects of red macroalgal (Gracilariopsis sp.) abundance on eelgrass Zostera marina in Tomales Bay, California, USA. Mar Ecol Prog Ser 367:133–142. https://doi.org/10.3354/meps07506
Hurd CL (2015) Slow-flow habitats as refugia for coastal calcifiers from ocean acidification. J Phycol 51:599–605. https://doi.org/10.1111/jpy.12307
James RK, van Katwijk MM, van Tussenbroek BI et al (2020) Water motion and vegetation control the pH dynamics in seagrass-dominated bays. Limnol Oceanogr 65:349–362. https://doi.org/10.1002/lno.11303
Jellison BM, Gaylord B (2019) Shifts in seawater chemistry disrupt trophic links within a simple shoreline food web. Oecologia 190:955–967. https://doi.org/10.1007/s00442-019-04459-0
Jurgens LJ, Gaylord B (2018) Physical effects of habitat-forming species override latitudinal trends in temperature. Ecol Lett 21:190–196. https://doi.org/10.1111/ele.12881
Kapsenberg L, Cyronak T (2019) Ocean acidification refugia in variable environments. Glob Chang Biol 25:3201–3214. https://doi.org/10.1111/gcb.14730
Kemp P, Bertness MD (1984) Snail shape and growth rates: evidence for plastic shell allometry in Littorina littorea. Proc Natl Acad Sci 81:811–813. https://doi.org/10.1073/pnas.81.3.811
Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Chang Biol 19:103–132. https://doi.org/10.1111/j.1365-2486.2012.02791.x
Koweek DA, Zimmerman RC, Hewett KM et al (2018) Expected limits on the ocean acidification buffering potential of a temperate seagrass meadow. Ecol Appl 28:1694–1714. https://doi.org/10.1002/eap.1771
Krause-Jensen D, Marbà N, Sanz-Martin M et al (2016) Long photoperiods sustain high pH in Arctic kelp forests. Sci Adv 2:e1501938
Kroeker KJ, Kordas RL, Crim R et al (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Chang Biol 19:1884–1896. https://doi.org/10.1111/gcb.12179
Kwiatkowski L, Gaylord B, Hill T et al (2016) Nighttime dissolution in a temperate coastal ocean ecosystem increases under acidification. Sci Rep 6:1–9. https://doi.org/10.1038/srep22984
Lowe AT, Kobelt J, Horwith M, Ruesink J (2019) Ability of eelgrass to alter oyster growth and physiology is spatially limited and offset by increasing predation risk. Estuaries Coasts 42:743–754. https://doi.org/10.1007/s12237-018-00488-9
Lueker TJ, Dickson AG, Keeling CD (2000) Ocean pCO2 calculated from DIC, TA, and the Mehrbach equations for K1 and K2: Validation using laboratory measurements of CO2 in gas and seawater at equilibrium. Mar Chem 70:105–119
Mahé K, Bellamy E, Lartaud F, De Rafélis M (2010) Calcein and manganese experiments for marking the shell of the common cockle (Cerastoderma edule): Tidal rhythm validation of increments formation. Aquat Living Resour 23:239–245. https://doi.org/10.1051/alr/2010025
Manzello DP, Enochs IC, Melo N et al (2012) Ocean acidification refugia of the florida reef tract. PLoS ONE 7:1–10. https://doi.org/10.1371/journal.pone.0041715
Martinez A, Crook ED, Barshis DJ et al (2019) Species-specific calcification response of Caribbean corals after 2-year transplantation to a low aragonite saturation submarine spring. Proc R Soc B Biol Sci 286:20190572. https://doi.org/10.1098/rspb.2019.0572
Middelboe AL, Hansen PJ (2007) High pH in shallow-water macroalgal habitats. Mar Ecol Prog Ser 338:107–117
Moore K, Short FT (2006) Zostera: Biology, ecology and management. In: Larkum T, Orth R, Duarte C (eds) Seagrasses: biology, ecology and conservation. Springer, The Netherlands, pp 361–386
Moran AL (2000) Calcein as a marker in experimental studies newly-hatched gastropods. Mar Biol 137:893–898. https://doi.org/10.1007/s002270000390
Nagelkerken I, Connell SD (2015) Global alteration of ocean ecosystem functioning due to increasing human CO2 emissions. Proc Natl Acad Sci U S A 112:13272–13277. https://doi.org/10.1073/pnas.1510856112
Nair PS, Robinson WE (1998) Calcium speciation and exchange between blood and extrapallial fluid of the quahog Mercenaria mercenaria (L.). Biol Bull 195:43–51. https://doi.org/10.2307/1542774
Nielsen KJ, Stachowicz JJ, Carter H, et al (2018) Emerging understanding of the potential role of seagrass and kelp as an ocean acidification management tool in California. California Ocean Science Trust, Oakland, California, USA. Oakland, California, USA
Pacella SR, Brown CA, Waldbusser GG et al (2018) Seagrass habitat metabolism increases short-term extremes and long-term offset of CO2 under future ocean acidification. Proc Natl Acad Sci U S A 115:3870–3875. https://doi.org/10.1073/pnas.1703445115
Padilla DK (2010) Context-dependent impacts of a non-native ecosystem engineer, the pacific oyster Crassostrea gigas. Integr Comp Biol 50:213–225. https://doi.org/10.1093/icb/icq080
Pan TCF, Applebaum SL, Manahan DT (2015) Experimental ocean acidification alters the allocation of metabolic energy. Proc Natl Acad Sci U S A 112:4696–4701. https://doi.org/10.1073/pnas.1416967112
Perez FF, Fraga F (1987) Association constant of fluoride and hydrogen ions in seawater. Mar Chem 21:161–168. https://doi.org/10.1016/0304-4203(87)90036-3
Peterson CH, Summerson HC, Duncan PB (1984) The influence of seagrass cover on population structure and individual growth rate of a suspension-feeding bivalve, Mercenaria mercenaria. J Mar Res 42:123–138. https://doi.org/10.1357/002224084788506194
Pettit LR, Smart CW, Hart MB et al (2015) Seaweed fails to prevent ocean acidification impact on foraminifera along a shallow-water CO2 gradient. Ecol Evol 5:1784–1793. https://doi.org/10.1002/ece3.1475
Ries JB, Ghazaleh MN, Connolly B et al (2016) Impacts of seawater saturation state (ΩA = 0.4–4.6) and temperature (10, 25 °C) on the dissolution kinetics of whole-shell biogenic carbonates. Geochim Cosmochim Acta 192:318–337. https://doi.org/10.1016/j.gca.2016.07.001
Roleda MY, Cornwall CE, Feng Y et al (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 10:1–19. https://doi.org/10.1371/journal.pone.0140394
Sanford E, Gaylord B, Hettinger A et al (2014) Ocean acidification increases the vulnerability of native oysters to predation by invasive snails. Proc R Soc B Biol Sci 281:20132681. https://doi.org/10.1098/rspb.2013.2681
Semesi I, Beer S, Björk M (2009) Seagrass photosynthesis controls rates of calcification and photosynthesis of calcareous macroalgae in a tropical seagrass meadow. Mar Ecol Prog Ser 382:41–48. https://doi.org/10.3354/meps07973
Short FT (1987) Effects of sediment nutrients on seagrasses: Literature review and mesocosm experiment. Aquat Bot 27:41–57. https://doi.org/10.1016/0304-3770(87)90085-4
Short FT, Coles RG, Pergent-Martini C (2001) Global seagrass distribution. In: Short FT, Coles RG (eds) Global seagrass research methods. Elsevier, pp 5–30t. https://doi.org/10.1016/b978-044450891-1/50002-5
Shukla P, Hill T, Gaylord B, et al (2011) Understanding impacts of ocean acidification on seagrass and salt marsh ecosystems based on studies in Bodega Harbor, California. In: 92th Western Society of Naturalists Conference. Vancouver, Washington
Sigwart JD, Lyons G, Fink A et al (2016) Elevated pCO2 drives lower growth and yet increased calcification in the early life history of the cuttlefish Sepia officinalis (Mollusca: Cephalopoda). ICES J Mar Sci 73:970–980. https://doi.org/10.1093/icesjms/fsv188
Silbiger NJ, Sorte CJB (2018) Biophysical feedbacks mediate carbonate chemistry in coastal ecosystems across spatiotemporal gradients. Sci Rep 8:1–11. https://doi.org/10.1038/s41598-017-18736-6
Smith KA, North EW, Shi F et al (2009) Modeling the effects of oyster reefs and breakwaters on seagrass growth. Estuaries Coasts 32:748–757. https://doi.org/10.1007/s12237-009-9170-z
Spencer LH, Horwith M, Lowe AT et al (2019) Pacific geoduck (Panopea generosa) resilience to natural pH variation. Comp Biochem Physiol Part D Genomics Proteomics 30:91–101. https://doi.org/10.1016/j.cbd.2019.01.010
Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235. https://doi.org/10.1641/0006-3568(2001)051[0235:mfatso]2.0.co;2
Stenzel HB (1963) Aragonite and calcite as constituents of adult oyster shells. Science 142:232–233. https://doi.org/10.1126/science.142.3589.232
Sunday JM, Fabricius KE, Kroeker KJ et al (2017) Ocean acidification can mediate biodiversity shifts by changing biogenic habitat. Nat Clim Chang 7:81–85. https://doi.org/10.1038/nclimate3161
Swezey DS, Bean JR, Ninokawa AT et al (2017) Interactive effects of temperature, food and skeletal mineralogy mediate biological responses to ocean acidification in a widely distributed bryozoan. Proc R Soc B Biol Sci 284:20162349. https://doi.org/10.1098/rspb.2016.2349
Tan K, Zheng H (2020) Ocean acidification and adaptive bivalve farming. Sci Total Environ 701:134794. https://doi.org/10.1016/j.scitotenv.2019.134794
Taylor J, Kennedy W, Hall A (1969) The shell structure and mineralogy of the Bivalvia. Introduction. Nuculacea-Trigonacea. Bull Br Mus Nat Hist Zool Suppl 3:1–125
Thomsen J, Haynert K, Wegner KM, Melzner F (2015) Impact of seawater carbonate chemistry on the calcification of marine bivalves. Biogeosciences 12:4209–4220. https://doi.org/10.5194/bg-12-4209-2015
Trimble AC, Ruesink JL, Dumbauld BR (2009) Factors preventing the recovery of a historically overexploited shellfish species, Ostrea lurida Carpenter 1864. J Shellfish Res 28:97–106. https://doi.org/10.2983/035.028.0116
Unsworth RKF, Collier CJ, Henderson GM, McKenzie LJ (2012) Tropical seagrass meadows modify seawater carbon chemistry: Implications for coral reefs impacted by ocean acidification. Environ Res Lett 7:024026. https://doi.org/10.1088/1748-9326/7/2/024026
Wahl M, Schneider Covachã S, Saderne V et al (2018) Macroalgae may mitigate ocean acidification effects on mussel calcification by increasing pH and its fluctuations. Limnol Oceanogr 63:3–21. https://doi.org/10.1002/lno.10608
Waldbusser GG, Hales B, Langdon CJ et al (2015) Saturation-state sensitivity of marine bivalve larvae to ocean acidification. Nat Clim Chang 5:273–280. https://doi.org/10.1038/nclimate2479
Worcester SE (1995) Effects of eelgrass beds on advection and turbulent mixing in low current and low shoot density environments. Mar Ecol Prog Ser 126:223–232. https://doi.org/10.3354/meps126223
Zeebe RE, Wolf-Gladrow D (2001) CO2 in seawater: equilibrium, kinetics, isotopes. Elsevier Oceanogr Ser 65:1–341
Zieman JC (1974) Methods for the study of the growth and production of turtle grass, Thalassia testudinum König. Aquaculture 4:139–143. https://doi.org/10.1016/0044-8486(74)90029-5
Acknowledgements
We thank Katie DuBois, Sarah Merolla, Norma González Buenrostro, Siena Watson, Tessa Filipczyk and Olivia Zanzonico for their help in both the field and the laboratory. We also thank Jay Stachowicz for meaningful comments and discussion on this work.
Funding
This study was supported by the California Sea Grant (Award R/HCME-03 to Hill, Gaylord, Sanford) and the California Ocean Protection Council.
Author information
Authors and Affiliations
Contributions
AMR, BG, TMH and ES conceived and designed methodology. AMR, JDS, PS, MW and AN collected the data. AMR, BG and ES analyzed the data. AMR led the writing of the manuscript. All the authors contributed critically to the drafts and gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethical approval
All applicable institutional and/or national guidelines for the care and use of animals were followed.
Additional information
Communicated by James Fourqurean.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ricart, A.M., Gaylord, B., Hill, T.M. et al. Seagrass-driven changes in carbonate chemistry enhance oyster shell growth. Oecologia 196, 565–576 (2021). https://doi.org/10.1007/s00442-021-04949-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-021-04949-0