Abstract
Ocean acidification (OA) increases aragonite shell dissolution in calcifying marine organisms. It has been proposed that bacteria associated with molluscan shell surfaces in situ could damage the periostracum and reduce its protective function against shell dissolution. However, the influence of bacteria on shell dissolution under OA conditions is unknown. In this study, dissolution in dead shells from gastropod larvae and adult pteropods (Limacina helicina) was examined following a 5-day incubation under a range of aragonite saturation states (Ωarag; values ranging from 0.5 to 1.8) both with and without antibiotics. Gastropod and pteropod specimens were collected from Puget Sound, Washington (48°33′19″N, 122°59′49″W and 47°41′11″N, 122°25′23″W, respectively), preserved, stored, and then treated in August 2015. Environmental scanning electron microscopy (ESEM) was used to determine the severity and extent of dissolution, which was scored as mild, severe, or summed (mild + severe) dissolution. Shell dissolution increased with decreasing Ωarag. In gastropod larvae, there was a significant interaction between the effects of antibiotics and Ωarag on severe dissolution, indicating that microbes could mediate certain types of dissolution among shells under low Ωarag. In L. helicina, there were no significant interactions between the effects of antibiotics and Ωarag on dissolution. These findings suggest that bacteria may differentially influence the response of some groups of shelled planktonic gastropods to OA conditions. This is the first assessment of the microbial–chemical coupling of dissolution in shells of either gastropod larvae or adult L. helicina under OA.
References
Bednaršek N, Tarling GA, Bakker DCE, Fielding S, Cohen A, Kuzirian A, McCorkle D, Lézé B, Montagna R (2012a) Description and quantification of pteropod shell dissolution: a sensitive bioindicator of ocean acidification. Glob Change Biol. https://doi.org/10.1111/j.1365-2486.2012.02668.x
Bednaršek N, Tarling GA, Bakker DCE, Fielding S, Jones EM, Venables HJ, Ward P, Kuzirian A, Lézé B, Feely RA, Murphy EJ (2012b) Extensive dissolution of live pteropods in the Southern Ocean. Nat Geosci. https://doi.org/10.1038/ngeo1635
Bednaršek N, Feely RA, Reum JC, Peterson B, Menkel J, Alin SR, Hales B (2014a) Limacina helicina shell dissolution as an indicator of declining habitat suitability owing to ocean acidification in the California Current Ecosystem. Proc Biol Sci. https://doi.org/10.1098/rspb.2014.0123
Bednaršek N, Tarling GA, Bakker DC, Fielding S, Feely RA (2014b) Dissolution dominating calcification process in polar pteropods close to the point of aragonite undersaturation. PLoS One. https://doi.org/10.1371/journal.pone.0109183
Berner RA, Honjo S (1981) Pelagic sedimentation of aragonite: its geochemical significance. Science. https://doi.org/10.1126/science.211.4485.940
Brunton LL, Chabner BA, Knollmann BC (eds) (2011) Goodman and Gilman’s the pharmacological basis of therapeutics, 12th edn. McGraw-Hill, New York
Busch DS, Maher M, Thibodeau P, McElhany P (2014) Shell condition and survival of Puget Sound pteropods are impaired by ocean acidification conditions. PLoS One. https://doi.org/10.1371/journal.pone.0105884
Clark GR II (1999) Organic matrix taphonomy in some molluscan shell microstructures. Palaeogeogr Palaeoclimatol Palaeoecol. https://doi.org/10.1016/S0031-0182(98)00208-9
Comeau S, Gorsky G, Alliouane S, Gattuso J-P (2010) Larvae of the pteropod Cavolinia inflexa exposed to aragonite undersaturation are viable but shell-less. Mar Biol. https://doi.org/10.1007/s00227-010-1493-6
Cottingham KL, Lennon JT, Brown BL (2005) Knowing when to draw the line: designing more informative ecological experiments. Front Ecol Environ. https://doi.org/10.1890/1540-9295(2005)003[0145:kwtdtl]2.0.co;2
Dickson AG (2010) The carbon dioxide system in seawater: equilibrium chemistry and measurements. In: Riebesell U, Fabry VJ, Hansson L, Gattuso JP (eds) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Luxembourg, pp 17–40
Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Pt A Oceanogr Res Pap. https://doi.org/10.1016/0198-0149(87)90021-5
Dickson AG, Riley JP (1978) The effect of analytical error on the evaluation of the components of the aquatic carbon-dioxide system. Mar Chem. https://doi.org/10.1016/0304-4203(78)90008-7
Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication. North Pacific Marine Science Organization, Sidney, BC, Canada, pp 1–191
Feely RA, Sabine CL, Hernandez-Ayon JM, Ianson D, Hales B (2008) Evidence for upwelling of corrosive “acidified” water onto the continental shelf. Science. https://doi.org/10.1126/science.1155676
Feely RA, Alin SR, Newton J, Sabine CL, Warner M, Devol A, Krembs C, Maloy C (2010) The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuar Coast Shelf Sci. https://doi.org/10.1016/j.ecss.2010.05.004
Garilli V, Rodolfo-Metalpa R, Scuderi D, Brusca L et al (2015) Physiological advantages of dwarfing in surviving extinctions in high-CO2 oceans. Nat Clim Change. https://doi.org/10.1038/nclimate2616
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. https://doi.org/10.1007/s00227-013-2219-3
Glover CP, Kidwell SM (1993) Influence of organic matrix on the post-mortem destruction of molluscan shells. Geology. https://doi.org/10.1086/648271
Harper EM (2000) Are calcitic layers an effective adaptation against shell dissolution in the Bivalvia. Zoology. https://doi.org/10.1111/j.1469-7998.2000.tb00602.x
Hunt BPV, Pakhomov EA, Hosie GW, Siegel V, Ward P, Bernard K (2008) Pteropods in southern ocean ecosystems. Prog Oceanogr. https://doi.org/10.1016/j.pocean.2008.06.001
Lischka S, Riebesell U (2012) Synergistic effects of ocean acidification and warming on overwintering pteropods in the Arctic. Glob Change Biol. https://doi.org/10.1111/gcb.12020
Lischka S, Büdenbender J, Boxhammer T, Riebesell U (2011) Impact of ocean acidification and elevated temperature on early juveniles of the polar shelled pteropod Limacina helicina: mortality, shell degradation, and shell growth. Biogeosci. https://doi.org/10.5194/bg-8-919-2011
Liu J, Weinbauer MG, Maier C, Dai M, Gattuso JP (2010) Effect of ocean acidification on microbial diversity and on microbe-driven biogeochemistry and ecosystem functioning. Aquat Microb Ecol. https://doi.org/10.3354/ame01446
Maas AE, Lawson GL, Tarrant AM (2015) Transcriptome-wide analysis of the response of the thecosome pteropod Clio pyramidata to short-term CO2 exposure. Comp Biochem Physiol Pt D Genom Proteom. https://doi.org/10.1016/j.cbd.2015.06.002
Manno C, Morata N, Primicerio R (2012) Limacina retroversa’s response to combined effects of ocean acidification and sea water freshening. Estuar Coast Shelf Sci. https://doi.org/10.1016/j.ecss.2012.07.019
Manno C, Bednaršek N, Tarling GA, Peck VL et al (2017) Shelled pteropods in peril: assessing vulnerability in a high CO2 ocean. Earth Sci Rev. https://doi.org/10.1016/j.earscirev.2017.04.005
Mehrbach C, Culberson CH, Hawley JE, Pytkowicx RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr. https://doi.org/10.4319/lo.1973.18.6.0897
Murray JW, Roberts E, Howard E, O’Donnell M, Bantam C, Carrington E, Foy M, Paul B, Fay A (2015) An inland sea high nitrate-low chlorophyll (HNLC) region with naturally high pCO2: an HNLC inland sea with high pCO2. Limnol Oceanogr. https://doi.org/10.1002/lno.10062
Peck VL, Tarling GA, Manno C, Harper EM, Tynan E (2016) Outer organic layer and internal repair mechanism protects pteropod Limacina helicina from ocean acidification. Deep Sea Res Pt II Top Stud Oceanogr. https://doi.org/10.1016/j.dsr2.2015.12.005
R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Robbins LL, Hansen ME, Kleypas JA, Meylan SC (2010) CO2calc: a user-friendly seawater carbon calculator for Windows, Max OS X, and iOS (iPhone). Open-file Rep (US Geol Surv), pp 1-17
Witt V, Wild C, Anthony KR, Diaz-Pulido G, Uthicke S (2011) Effects of ocean acidification on microbial community composition of, and oxygen fluxes through, biofilms from the Great Barrier Reef. Environ Microbiol. https://doi.org/10.1111/j.1462-2920.2011.02571.x
Bednaršek N, Johnson J, Feely RA (2016) Comment on Peck et al: vulnerability of pteropod (Limacina helicina) to ocean acidification: Shell dissolution occurs despite an intact organic layer. Deep Sea Res Pt II Top Stud Oceanogr. https://doi.org/10.1016/j.dsr2.2016.03.006
Acknowledgements
The experimental portion of this study was conducted at the University of Washington’s Friday Harbor Laboratories, Washington, USA during a graduate student summer course on ocean acidification. We would like to thank Andrew Dickson and Laura Newcomb for their advice and insights throughout the course; Jessamyn Johnson and Jan Newton for their advice and for providing the Limacina helicina specimens; Kristy Krull, Nicholas Ulacia, and Molly Roberts for their assistance in boat operations to collect the gastropod larvae specimens; Kathryn Van Alstyne and Victoria Foe for providing the antibiotics; Constance Sullivan and the Ocean Acidification Environmental Laboratory staff for their assistance with carbonate chemistry measurements; the Friday Harbor Laboratories faculty and staff for providing funding, facilities, supplies, and logistic support; and two reviewers for providing constructive comments on the manuscript.
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Gastropod and pteropod specimens were sampled and treated in accordance with the ethical standards of Friday Harbor Laboratories, University of Washington.
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Bausch, A.R., Gallego, M.A., Harianto, J. et al. Influence of bacteria on shell dissolution in dead gastropod larvae and adult Limacina helicina pteropods under ocean acidification conditions. Mar Biol 165, 40 (2018). https://doi.org/10.1007/s00227-018-3293-3
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DOI: https://doi.org/10.1007/s00227-018-3293-3