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Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 35, 2019 - Issue 8
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Original Articles

Recoverable impacts of ocean acidification on the tubeworm, Hydroides elegans: implication for biofouling in future coastal oceans

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Pages 945-957 | Received 19 Nov 2018, Accepted 19 Sep 2019, Published online: 05 Nov 2019

References

  • Asnaghi V, Mangialajo L, Gattuso J-P, Francour P, Privitera D, Chiantore M. 2014. Effects of ocean acidification and diet on thickness and carbonate elemental composition of the test of juvenile sea urchins. Mar Environ Res. 93:78–84. doi:10.1016/j.marenvres.2013.08.005
  • Baumann H, Wallace RB, Tagliaferri T, Gobler CJ. 2015. Large natural pH, CO2 and O2 fluctuations in a temperate tidal salt marsh on diel, seasonal, and interannual time scales. Estuar Coast. 38:220–231. doi:10.1007/s12237-014-9800-y
  • Beniash E, Ivanina A, Lieb NS, Kurochkin I, Sokolova IM. 2010. Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica. Mar Ecol Prog Ser. 419:95–108. doi:10.3354/meps08841
  • Borgesa AV, Gypensb N. 2010. Carbonate chemistry in the coastal zone responds more strongly to eutrophication than ocean acidification. Limnol Oceanogr. 55:346–353. doi:10.4319/lo.2010.55.1.0346
  • Brewer PG, Peltzer ET. 2009. OCEANS. Limits to marine life. Science. 324:347–348. doi:10.1126/science.1170756
  • Cai W-J, Hu X, Huang W-J, Murrell MC, Lehrter JC, Lohrenz SE, Chou W-C, Zhai W, Hollibaugh JT, Wang Y, et al. 2011. Acidification of subsurface coastal waters enhanced by eutrophication. Nature Geosci. 4:766–770. doi:10.1038/ngeo1297
  • Celenk C, Celenk P. 2012. Bone density measurement using computed tomography. In: Saba L, editor. Computed tomography – clinical applications.
  • Chan VBS, Li C, Lane AC, Wang Y, Lu X, Shih K, Zhang T, Thiyagarajan V. 2012. CO2-driven ocean acidification alters and weakens integrity of the calcareous tubes produced by the serpulid tubeworm, Hydroides elegans. PLoS One. 7:e42718. doi:10.1371/journal.pone.0042718
  • Chan VBS, Thiyagarajan V, Lu XW, Zhang T, Shih K. 2013. Temperature dependent effects of elevated CO2 on shell composition and mechanical properties of Hydroides elegans: insights from a multiple stressor experiment. PLoS One. 8:e78945. doi:10.1371/journal.pone.0078945
  • Clode PL, Lema K, Saunders M, Weiner S. 2011. Skeletal mineralogy of newly settling Acropora millepora (Scleractinia) coral recruits. Coral Reefs. 30:1–8. doi:10.1007/s00338-010-0673-7
  • Dickinson GH, Ivanina AV, Matoo OB, Portner HO, Lannig G, Bock C, Beniash E, Sokolova IM. 2012. Interactive effects of salinity and elevated CO2 levels on juvenile eastern oysters, Crassostrea virginica. J Exp Biol. 215:29–43. doi:10.1242/jeb.061481
  • Dickinson GH, Matoo OB, Tourek RT, Sokolova IM, Beniash E. 2013. Environmental salinity modulates the effects of elevated CO2 levels on juvenile hard-shell clams, Mercenaria mercenaria. J Exp Biol. 216:2607–2618. doi:10.1242/jeb.082909
  • Dickson AG, Millero FJ. 1987. A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Part A. 34:1733–1743. doi:10.1016/0198-0149(87)90021-5
  • Dobretsov S, Coutinho R, Rittschof D, Salta M, Ragazzola F, Hellio C. 2019. The oceans are changing: impact of ocean warming and acidification on biofouling communities. Biofouling. 35:585–595. doi:10.1080/08927014.2019.1624727
  • Doerner MF, Nix WD. 1986. A method for interpreting the data from depth-sensing indentation instruments. J Mater Res. 1:601–609. doi:10.1557/JMR.1986.0601
  • Doney SC, Fabry VJ, Feely RA, Kleypas JA. 2009. Ocean acidification: the other CO2 problem. Annu Rev Mar Sci. 1:169–192. doi:10.1146/annurev.marine.010908.163834
  • Duarte CM, Hendriks IE, Moore TS, Olsen YS, Steckbauer A, Ramajo L, Carstensen J, Trotter JA, McCulloch M. 2013. Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuar Coast. 36:221–236. doi:10.1007/s12237-013-9594-3
  • Dupont S, Thorndyke M. 2009. Impact of CO2-driven ocean acidification on invertebrates early life-history—what we know, what we need to know and what we can do. Biogeosci Discuss. 6:3109–3131. doi:10.5194/bgd-6-3109-2009
  • Espinel-Velasco N, Hoffmann L, Agüera A, Byrne M, Dupont S, Uthicke S, Webster NS, Lamare M. 2018. Effects of ocean acidification on the settlement and metamorphosis of marine invertebrate and fish larvae: a review. Mar Ecol Prog Ser. 606:237–257. doi:10.3354/meps12754
  • Feely RA, Orr J, Fabry VJ, Kleypas JA, Sabine CL, Langdon C. 2009. Present and future changes in seawater chemistry due to ocean acidification. Geophys Monogr Ser. 183:175–188.
  • Fine M, Tchernov D. 2007. Scleractinian coral species survive and recover from decalcification. Science. 315:1811–1811. doi:10.1126/science.1137094
  • Fitridge I, Dempster T, Guenther J, de Nys R. 2012. The impact and control of biofouling in marine aquaculture: a review. Biofouling. 28:649–669. doi:10.1080/08927014.2012.700478
  • Ghalambor CK, Mckay JK, Carroll SP, Reznick DN. 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecology. 21:394–407. doi:10.1111/j.1365-2435.2007.01283.x
  • Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J. 2008. Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol. 17:167–178. doi:10.1111/j.1365-294X.2007.03413.x
  • Hendriks IE, Duarte CM, Olsen YS, Steckbauer A, Ramajo L, Moore TS, Trotter JA, McCulloch M. 2015. Biological mechanisms supporting adaptation to ocean acidification in coastal ecosystems. Estuar Coast Shelf Sci. 152:A1–A8. doi:10.1016/j.ecss.2014.07.019
  • Holcomb M, Cohen AL, Gabitov RI, Hutter JL. 2009. Compositional and morphological features of aragonite precipitated experimentally from seawater and biogenically by corals. Geochim Cosmochim Acta. 73:4166–4179. doi:10.1016/j.gca.2009.04.015
  • Holcomb M, Venn AA, Tambutté E, Tambutté S, Allemand D, Trotter J, McCulloch M. 2014. Coral calcifying fluid pH dictates response to ocean acidification. Sci Rep. 4:5207.
  • Howarth R, Chan F, Conley DJ, Garnier J, Doney SC, Marino R, Billen G. 2011. Coupled biogeochemical cycles: eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Front Ecol Environ. 9:18–26. doi:10.1890/100008
  • Ivanina AV, Falfushynska HI, Beniash E, Piontkivska H, Sokolova IM. 2017. Biomineralization-related specialization of hemocytes and mantle tissues of the Pacific oyster Crassostrea gigas. J Exp Biol. 220:3209–3221. doi:10.1242/jeb.160861
  • Kavanagh CJ, Schultz MP, Swain GW, Stein J, Truby K, Wood CD. 2001. Variation in adhesion strength of Balanus eburneus, Crassostrea virginica and Hydroides dianthus to fouling‐release coatings. Biofouling. 17:155–167. doi:10.1080/08927010109378474
  • Lane AC, Campanati C, Dupont S, Thiyagarajan V. 2015. Trans-generational responses to low pH depend on parental gender in a calcifying tubeworm. Sci Rep. 5:10847. doi:10.1038/srep10847
  • Lane AC, Mukherjee J, Chan VBS, Thiyagarajan V. 2013. Decreased pH does not alter metamorphosis but compromises juvenile calcification of the tube worm. Mar Biol. 160:1983–1993. doi:10.1007/s00227-012-2056-9
  • Lannig G, Eilers S, Portner HO, Sokolova IM, Bock C. 2010. Impact of ocean acidification on energy metabolism of oyster, Crassostrea gigas-changes in metabolic pathways and thermal response. Mar Drugs. 8:2318–2339. doi:10.3390/md8082318
  • Li C, Chan VBS, He C, Meng Y, Yao H, Shih K, Thiyagarajan V. 2014. Weakening mechanisms of the serpulid tube in a high-CO2 world. Environ Sci Technol. 48:14158–14167. doi:10.1021/es501638h
  • Li C, Meng Y, He C, Chan VBS, Yao H, Thiyagarajan V. 2016. Mechanical robustness of the calcareous tubeworm Hydroides elegans: warming mitigates the adverse effects of ocean acidification. Biofouling. 32:191–204. doi:10.1080/08927014.2015.1129532
  • McCulloch M, Falter J, Trotter J, Montagna P. 2012. Coral resilience to ocean acidification and global warming through pH up-regulation. Nature Clim Change. 2:623–627. doi:10.1038/nclimate1473
  • McDonald MR, McClintock JB, Amsler CD, Rittschof D, Angus RA, Orihuela B, Lutostanski K. 2009. Effects of ocean acidification over the life history of the barnacle Amphibalanus amphitrite. Mar Ecol Prog Ser. 385:179–187. doi:10.3354/meps08099
  • 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. 18:897–907. doi:10.4319/lo.1973.18.6.0897
  • Meng Y, Fitzer SC, Chung P, Li CY, Thiyagarajan V, Cusack M. 2018. Crystallographic interdigitation in oyster shell folia enhances material strength. Cryst Growth Des. 18:3753–3761. doi:10.1021/acs.cgd.7b01481
  • Meng Y, Guo Z, Fitzer SC, Upadhyay A, Chan VBS, Li C, Cusack M, Yao H, Yeung KWK, Thiyagarajan V. 2018. Ocean acidification reduces hardness and stiffness of the Portuguese oyster shell with impaired microstructure: a hierarchical analysis. Biogeosciences. 15:6833–6846. doi:10.5194/bg-15-6833-2018
  • Meng Y, Guo Z, Yao H, Yeung KWK, Thiyagarajan V. 2019. Calcium carbonate unit realignment under acidification: a potential compensatory mechanism in an edible estuarine oyster. Mar Pollut Bull. 139:141–149. doi:10.1016/j.marpolbul.2018.12.030
  • Miles H, Widdicombe S, Spicer JI, Hall-Spencer J. 2007. Effects of anthropogenic seawater acidification on acid-base balance in the sea urchin Psammechinus miliaris. Mar Pollut Bull. 54:89–96. doi:10.1016/j.marpolbul.2006.09.021
  • Movilla J, Calvo E, Pelejero C, Coma R, Serrano E, Fernández-Vallejo P, Ribes M. 2012. Calcification reduction and recovery in native and non-native Mediterranean corals in response to ocean acidification. J Exp Mar Bio Ecol. 438:144–153. doi:10.1016/j.jembe.2012.09.014
  • Nardone JA, Patel S, Siegel KR, Tedesco D, McNicholl CG, O’Malley J, Herrick J, Metzler RA, Orihuela B, Rittschof D, et al. 2018. Assessing the impacts of ocean acidification on adhesion and shell formation in the barnacle Amphibalanus amphitrite. Front Mar Sci. 5 (369).
  • Oliver WC, Pharr GM. 1992. An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J Mater Res. 7:1564–1583. doi:10.1557/JMR.1992.1564
  • Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, et al. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature. 437:681–686. doi:10.1038/nature04095
  • Pansch C, Nasrolahi A, Appelhans YS, Wahl M. 2012. Impacts of ocean warming and acidification on the larval development of the barnacle Amphibalanus improvisus. J Exp Mar Bio Ecol. 420-421:48–55. doi:10.1016/j.jembe.2012.03.023
  • Peck LS, Clark MS, Power D, Reis J, Batista FM, Harper EM. 2015. Acidification effects on biofouling communities: winners and losers. Glob Change Biol. 21:1907–1913. doi:10.1111/gcb.12841
  • Pierrot D, Lewis E, Wallace D. 2006. MS Excel program developed for CO2 system calculations. Oak Ridge, TN: Carbon dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy. ORNL/CDIAC-105a.
  • Ries JB. 2011. Skeletal mineralogy in a high-CO2 world. J Exp Mar Bio Ecol. 403:54–64. doi:10.1016/j.jembe.2011.04.006
  • Ries JB, Cohen AL, McCorkle DC. 2009. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology. 37:1131–1134. doi:10.1130/G30210A.1
  • Solomon S, Qin D, Manning M, Averyt K, Marquis M. 2007. Climate change 2007- the physical science basis: working group I contribution to the fourth assessment report of the IPCC. Vol. 4. Cambridge, UK: Cambridge University Press.
  • Tanur AE, Gunari N, Sullan RMA, Kavanagh CJ, Walker GC. 2010. Insights into the composition, morphology, and formation of the calcareous shell of the serpulid Hydroides dianthus. J Struct Biol. 169:145–160. doi:10.1016/j.jsb.2009.09.008
  • Thomsen J, Gutowska MA, Saphörster J, Heinemann A, Trübenbach K, Fietzke J, Hiebenthal C, Eisenhauer A, Körtzinger A, Wahl M, et al. 2010. Calcifying invertebrates succeed in a naturally CO2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences. 7:3879–3891. doi:10.5194/bg-7-3879-2010
  • Toyofuku T, Matsuo MY, de Nooijer LJ, Nagai Y, Kawada S, Fujita K, Reichart G-J, Nomaki H, Tsuchiya M, Sakaguchi H, et al. 2017. Proton pumping accompanies calcification in foraminifera. Nat Commun. 8:14145. doi:10.1038/ncomms14145
  • Underwood AJ. 1999. Physical disturbances and their direct effect on an indirect effect: responses of an intertidal assemblage to a severe storm. J Exp Mar Bio Ecol. 232:125–140. doi:10.1016/S0022-0981(98)00105-1
  • Vinn O, Kirsimäe K, ten Hove HA. 2009. Tube ultrastructure of Pomatoceros americanus (Polychaeta, Serpulidae): implications for the tube formation of serpulids. Estonian J Earth Sci. 58:148–152. doi:10.3176/earth.2009.2.05
  • Vinn O, Kupriyanova EK. 2011. Evolution of a dense outer protective tube layer in serpulids (Polychaeta, Annelida). Carnets Géol. 5:137–147.
  • Watson DI, Shumway SE, Whitlatch RB. 2009. Biofouling and the shellfish industry. In: Shumway SE, Rodrick GE, editors. Shellfish safety and quality. Cambidge, UK: Woodhead Publishing; p. 317–336.
  • Wood HL, Spicer JI, Widdicombe S. 2008. Ocean acidification may increase calcification rates, but at a cost. Proc R Soc B. 275:1767–1773. doi:10.1098/rspb.2008.0343
  • Wootton JT, Pfister CA, Forester JD. 2008. Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proc Natl Acad Sci USA. 105:18848–18853. doi:10.1073/pnas.0810079105
  • Yuan XC, Yin K, Cai WJ, Ho AY, Xu J, Harrison PJ. 2011. Influence of seasonal monsoons on net community production and CO2 in subtropical Hong Kong coastal waters. Biogeosciences. 8:289–300. doi:10.5194/bg-8-289-2011

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