Publication Cover
Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 32, 2016 - Issue 2
576
Views
16
CrossRef citations to date
0
Altmetric
Articles

Mechanical robustness of the calcareous tubeworm Hydroides elegans: warming mitigates the adverse effects of ocean acidification

, , , , &
Pages 191-204 | Received 15 Jul 2015, Accepted 01 Dec 2015, Published online: 28 Jan 2016

References

  • Addadi L, Raz S, Weiner S. 2003. Taking advantage of disorder: amorphous calcium carbonate and its roles in biomineralization. Adv Mater. 15:959–970. doi: 10.1002/adma.200300381
  • Amaral V, Cabral HN, Bishop MJ. 2011. Resistance among wild invertebrate populations to recurrent estuarine acidification. Estuar Coast Shelf Sci. 93:460–467. doi: 10.1016/j.ecss.2011.05.024
  • Andersson AJ, Mackenzie FT, Bates NR. 2008. Life on the margin: implications of ocean acidification on Mg-calcite, high latitude and cold-water marine calcifiers. Mar Ecol Prog Ser. 373:265–273. doi: 10.3354/meps07639
  • Beniash E, Aizenberg J, Addadi L, Weiner S. 1997. Amorphous calcium carbonate transforms into calcite during sea urchin larval spicule growth. Proc R Soc Lond Ser B-Biol Sci. 264:461–465. doi: 10.1098/rspb.1997.0066
  • Beniash E, Ivanina A, Lieb NS, Kurochkin I, Sokolova IM. 2010a. 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
  • Beniash E, Ivanina A, Lieb NS, Kurochkin I, Sokolova IM. 2010b. Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica (Gmelin). Mar Ecol Prog Ser. 419:95–108. doi: 10.3354/meps08841
  • Brennand HS, Soars N, Dworjanyn SA, Davis AR, Byrne M. 2010. Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS one. 5:e11372. doi: 10.1371/journal.pone.0011372
  • Burton EA, Walter LM. 1987. Relative precipitation rates of aragonite and Mg calcite from seawater: temperature or carbonate ion control? Geology. 15:111–114. doi: 10.1130/0091-7613(1987)15<111:RPROAA>2.0.CO;2
  • Byrne M, Ho M, Wong E, Soars NA, Selvakumaraswamy P, Shepard-Brennand H, Dworjanyn SA, Davis AR. 2010. Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean. Proc R Soc Lond Ser B-Biol Sci. 2376–2383.
  • Byrne M, Ho M, Wong E, Soars NA, Selvakumaraswamy P, Shepard-Brennand H, Dworjanyn SA, Davis AR. 2011. Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean. Proc R Soc Lond Ser B-Biol Sci. 278:2376–2383. doi: 10.1098/rspb.2010.2404
  • Byrne M, Przeslawski R. 2013. Multistressor impacts of warming and acidification of the ocean on marine invertebrates’ life histories. Integr Comp Biol. 53:582–596. doi: 10.1093/icb/ict049
  • Cai WJ, Hu X, Huang WJ, Murrell MC, Lehrter JC, Lohrenz SE, Chou WC, 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
  • Caldeira K, Wickett ME. 2003. Oceanography: anthropogenic carbon and ocean pH. Nature. 425:365–365. doi: 10.1038/425365a
  • Celenk C, Celenk P. 2012. Bone density measurement using computed tomography. In: Saba L editor, Computed tomography - clinical applications. ISBN: 978-953-307-378-1. doi: http://cdn.intechweb.org/pdfs/25703.pdf
  • 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. 2013a. 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
  • Chan VBS, Thiyagarajan V, Lu XW, Zhang T, Shih K. 2013b. 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
  • Chan VBS, Vinn O, Li C, Lu X, Kudryavtsev AB, Schopf JW, Shih K, Zhang T, Thiyagarajan V. 2015. Evidence of compositional and ultrastructural shifts during the development of calcareous tubes in the biofouling tubeworm, Hydroides elegans. J Structural Biol. 189:230–237. doi: 10.1016/j.jsb.2015.01.004
  • Clode PL, Lema K, Saunders M, Weiner S. 2011. Skeletal mineralogy of newly settling Acropora millepora (Scleractinia) coral recruits. Coral Reefs. Mar 01; 30:1–8. doi: 10.1007/s00338-010-0673-7
  • Cohen AL, Holcomb M. 2009. Why corals care about ocean acidification: uncovering the mechanism. Oceanography. 22:118–127. doi: 10.5670/oceanog
  • Deng Y, Gao T, Gao H, Yao X, Xie L. 2014. Regional precipitation variability in East Asia related to climate and environmental factors during 1979-2012. Sci Rep.4. Article ID: 5693. doi: 10.1038/srep05693
  • 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
  • Digby PS. 1968. The mechanism of calcification in the molluscan shell. Proceedings of the Symposium of Zoological Society of London Studies in the Structure, physiology and ecology of molluscs. London: Academic Press.
  • Doney SC, Fabry VJ, Feely RA, Kleypas JA. 2009. Ocean acidification: the other CO2 problem. Ann Rev Mar Sci. 1:169–192. doi: 10.1146/annurev.marine.010908.163834
  • Fitzer SC, Phoenix VR, Cusack M, Kamenos NA. 2014. Ocean acidification impacts mussel control on biomineralisation. Sci Rep. 08/28/online;4.
  • Fitzer SC, Zhu W, Tanner KE, Phoenix VR, Kamenos NA, Cusack M. 2015. Ocean acidification alters the material properties of Mytilus edulis shells. Interface. 12: 20141227. doi: 10.1098/rsif.2014.1227
  • Füllenbach CS, Schöne BR, Branscheid R. 2014. Microstructures in shells of the freshwater gastropod Viviparus viviparus: a potential sensor for temperature change? Acta Biomater. 10:3911–3921. doi: 10.1016/j.actbio.2014.03.030
  • Gibson R, Atkinson R, Gordon J, Smith I, Hughes D. 2011a. Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Oceanogr Mar Biol Annu Rev. 49:1–42.
  • Gibson R, Atkinson R, Gordon J, Smith I, Hughes D. 2011b. Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Oceanogr Mar Biol Annu Rev. 49:1–42.
  • Gong YU, Killian CE, Olson IC, Appathurai NP, Amasino AL, Martin MC, Holt LJ, Wilt FH, Gilbert P. 2012. Phase transitions in biogenic amorphous calcium carbonate. Proc Natil Acad Sci. 109:6088–6093. doi: 10.1073/pnas.1118085109
  • Gutowska M, Melzner F, Langenbuch M, Bock C, Claireaux G, Pörtner HO. 2010. Acid–base regulatory ability of the cephalopod (Sepia officinalis) in response to environmental hypercapnia. J Comp Physiol B. Mar 01; 180:323–335. doi: 10.1007/s00360-009-0412-y
  • Hahn S, Rodolfo-Metalpa R, Griesshaber E, Schmahl W, Buhl D, Hall-Spencer J, Baggini C, Fehr K, Immenhauser A. 2011. Marine bivalve geochemistry and shell ultrastructure from modern low pH environments. Biogeosci Discus. 8:10351–10388. doi: 10.5194/bgd-8-10351-2011
  • Hahn S, Rodolfo-Metalpa R, Griesshaber E, Schmahl WW, Buhl D, Hall-Spencer J, Baggini C, Fehr K, Immenhauser A. 2012. Marine bivalve shell geochemistry and ultrastructure from modern low pH environments: environmental effect versus experimental bias. Biogeosciences. 9:1897–1914. doi: 10.5194/bg-9-1897-2012
  • Hamm CE, Merkel R, Springer O, Jurkojc P, Maier C, Prechtel K, Smetacek V. 2003. Architecture and material properties of diatom shells provide effective mechanical protection. Nature. 421:841–843. doi: 10.1038/nature01416
  • He C, Zhou W, Wang H, Shi SQ, Yao H. 2013. Mechanics of pharyngeal teeth of black carp (Mylopharyngodon piceus) crushing mollusk shells. Adv Eng Mat. 15:684–690. doi: 10.1002/adem.201200304
  • Hedley R. 1958. Tube formation by Pomatoceros triqueter (Polychaeta). J Mar Biol Assoc UK. 37:315–322. doi: 10.1017/S0025315400023717
  • Hill R. 1952. The elastic behaviour of a crystalline aggregate. Proc Physical Soc Sec A. 65:349. doi: 10.1088/0370-1298/65/5/307
  • Hoffmann AA, Parsons P. 1989. Selection for increased desiccation resistance in Drosophila melanogaster: additive genetic control and correlated responses for other stresses. Genetics. 122:837–845.
  • Holcomb M, Venn AA, Tambutte E, Tambutte S, Allemand D, Trotter J, McCulloch M. 2014. Coral calcifying fluid pH dictates response to ocean acidification. Sci Rep. Jun 06 online;4.
  • Jokiel P. 2013. Coral reef calcification: carbonate, bicarbonate and proton flux under conditions of increasing ocean acidification. Proc R Soc Lond Ser B-Biol Sci. 280:20130031. doi: 10.1098/rspb.2013.0031
  • Klein RT, Lohmann KC, Thayer CW. 1996. SrCa and 13C12C ratios in skeletal calcite of Mytilus trossulus: covariation with metabolic rate, salinity, and carbon isotopic composition of seawater. Geochim Cosmochim Acta. 60:4207–4221. doi: 10.1016/S0016-7037(96)00232-3
  • Landes A, Zimmer M. 2012. Acidification and warming affect both a calcifying predator and prey, but not their interaction. Mar Ecol Prog Ser. 450:1–10. doi: 10.3354/meps09666
  • Lane AC, Mukherjee J, Chan VBS, Thiyagarajan V. 2013. Decreased pH does not alter metamorphosis but compromises juvenile calcification of the tube worm Hydroides elegans. Mar Biol. 160:1983–1993. doi: 10.1007/s00227-012-2056-9
  • Lannig G, Eilers S, Pörtner 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 V, 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
  • Lombardi C, Rodolfo-Metalpa R, Cocito S, Gambi MC, Taylor PD. 2011. Structural and geochemical alterations in the Mg calcite bryozoan Myriapora truncata under elevated seawater pCO2 simulating ocean acidification. Mar Ecol. 32:211–221. doi: 10.1111/mae.2011.32.issue-2
  • Ma Z, Huang J, Sun J, Wang G, Li C, Xie L, Zhang R. 2007. A novel extrapallial fluid protein controls the morphology of nacre lamellae in the Pearl Oyster. J Biol Chem. 282:23253–23263. doi: 10.1074/jbc.M700001200
  • Mackenzie CL, Ormondroyd GA, Curling SF, Ball RJ, Whiteley NM, Malham SK. 2014. Ocean warming, more than acidification, reduces shell strength in a commercial shellfish species during food limitation. PLoS one. 9:e86764. doi: 10.1371/journal.pone.0086764
  • Martin S, Richier S, Pedrotti ML, Dupont S, Castejon C, Gerakis Y, Kerros M-E, Oberhänsli F, Teyssié JL, Jeffree R, et al. 2011. Early development and molecular plasticity in the Mediterranean sea urchin Paracentrotus lividus exposed to CO2-driven acidification. J Exp Biol. 214:1357–1368. doi: 10.1242/jeb.051169
  • McCulloch M, Falter J, Trotter J, Montagna P. 2012. Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Change. 2:623–627. doi: 10.1038/nclimate1473
  • McDonald MR, McClintock JB, Amsler CD, Angus DRA, Orihuela B, Lutostanski K. 2009. Effects of ocean acidification over the life history the barnacle Amphibalanus amphitrite. Mar Ecol Prog Ser. 385:179–187. doi: 10.3354/meps08099
  • Melatunan S, Calosi P, Rundle SD, Widdicombe S, Moody AJ. 2013. Effects of ocean acidification and elevated temperature on shell plasticity and its energetic basis in an intertidal gastropod. Mar Ecol Prog Ser. 472:155–168. doi: 10.3354/meps10046
  • Melzner F, Stange P, Trübenbach K, Thomsen J, Casties I, Panknin U, Gorb SN, Gutowska MA. 2011a. Food supply and seawater pCO2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis. PLoS one.6:e24223. doi: 10.1371/journal.pone.0024223
  • Melzner F, Stange P, Trübenbach K, Thomsen J, Casties I, Panknin U, Gorb SN, Gutowska MA. 2011b. Food supply and seawater pCO2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis. PLoS one. 6:e24223. doi: 10.1371/journal.pone.0024223
  • Metzger R, Sartoris FJ, Langenbuch M, Pörtner HO. 2007. Influence of elevated CO2 concentrations on thermal tolerance of the edible crab Cancer pagurus. J Therm Biol. 32:144–151. doi: 10.1016/j.jtherbio.2007.01.010
  • 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
  • Moran MD. 2003. Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos. 100:403–405. doi: 10.1034/j.1600-0706.2003.12010.x
  • Mount AS, Wheeler A, Paradkar RP, Snider D. 2004. Hemocyte-mediated shell mineralization in the eastern oyster. Science. 304:297–300. doi: 10.1126/science.1090506
  • Nedved BT, Hadfield MG. 2009. Hydroides elegans (Annelida: Polychaeta): a model for biofouling research. Marine and industrial biofouling. Berlin Heidelberg: Springer; p. 203–217.
  • Nudelman F, Gotliv BA, Addadi L, Weiner S. 2006. Mollusk shell formation: mapping the distribution of organic matrix components underlying a single aragonitic tablet in nacre. J Struct Biol. 153:176–187. doi: 10.1016/j.jsb.2005.09.009
  • 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
  • Pechenik JA, Pearse JS, Qian PY. 2007. Effects of salinity on spawning and early development of the tube-building polychaete Hydroides elegans in Hong Kong: not just the sperm’s fault? Biol Bull. 212:151–160. doi: 10.2307/25066592
  • Poloczanska ES, Butler AJ. 2010. Biofouling and climate change. In: Dürr S, Thomason JC, editors. Biofouling. Wiley-Blackwell; p. 333–347.
  • Pörtner HO. 2008. Ecosystem effects of ocean acidification in times of ocean warming: a physiologist s view. Mar Ecol Prog Ser. 373:203–217. doi: 10.3354/meps07768
  • Pörtner HO, Langenbuch M, Michaelidis B. 2005. Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: from Earth history to global change. J Geophysical Res. 110: C09S10. doi: 10.1029/2004JC002561
  • Qian PY, Lau S, Dahms HU, Dobretsov S, Harder T. 2007. Marine biofilms as mediators of colonization by marine macroorganisms: implications for antifouling and aquaculture. Mar Biotechnol. 9:399–410. doi: 10.1007/s10126-007-9001-9
  • Qian PY, Pechenik JA. 1998. Effects of larval starvation and delayed metamorphosis on juvenile survival and growth of the tube-dwelling polychaete Hydroides elegans (Haswell). J Exp Mar Biol Ecol. 227:169–185. doi: 10.1016/S0022-0981(97)00267-0
  • Qiu JW, Qian PY. 1997. Combined effects of salinity, temperature and food on early development of the polychaete Hydroides elegans. Mar Ecol Prog Ser. 152:79–88. doi: 10.3354/meps152079
  • Rayfield EJ. 2007. Finite element analysis and understanding the biomechanics and evolution of living and fossil organisms. Annu Rev Earth Planet Sci. 35:541–576. doi: 10.1146/annurev.earth.35.031306.140104
  • Ries JB. 2011. Skeletal mineralogy in a high-CO2 world. J Exp Mar Biol 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
  • 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.
  • Ruddy G, Feng S, Campbell G. 1975. The effect of prolonged exposure to elevated temperatures on the biochemical constituents, gonadal development and shell deposition of the American oyster, Crassostrea virginica. Comp Biochem Physiol B. 51:157–164.
  • Stanley SM. 2006. Influence of seawater chemistry on biomineralization throughout Phanerozoic time: paleontological and experimental evidence. Palaeogeogr Palaeoclimatol Palaeoecol. 232:214–236. doi: 10.1016/j.palaeo.2005.12.010
  • Stumpp M, Wren J, Melzner F, Thorndyke MC, Dupont ST. 2011. CO2 induced seawater acidification impacts sea urchin larval development I: elevated metabolic rates decrease scope for growth and induce developmental delay. Comparative Biochem Physiol A. 160:331–340. doi: 10.1016/j.cbpa.2011.06.022
  • Talmage SC, Gobler CJ. 2011. Effects of elevated temperature and carbon dioxide on the growth and survival of larvae and juveniles of three species of northwest Atlantic bivalves. PLoS one. 6:e26941. doi: 10.1371/journal.pone.0026941
  • Tanur A, Gunari N, Sullan R, Kavanagh CJ, Walker G. 2009. Insights into the composition, morphology, and formation of the calcareous shell of the serpulid Hydroides dianthus. J Struct Biol. 169:145–160.
  • Tanur AE, Gunari N, Sullan RM, 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
  • Todgham AE, Hofmann GE. 2009. Transcriptomic response of sea urchin larvae Strongylocentrotus purpuratus to CO2-driven seawater acidification. J Exp Biol. 212:2579–2594. doi: 10.1242/jeb.032540
  • Tunnicliffe V, Davies KT, Butterfield DA, Embley RW, Rose JM, Chadwick WW Jr. 2009. Survival of mussels in extremely acidic waters on a submarine volcano. Nature Geosci. 2:344–348. doi: 10.1038/ngeo500
  • Vinn O. 2011. The role of an internal organic tube lining in the biomineralization of serpulid tubes. Carnets de Géologie/Notebooks on Geology, Brest, Letter.1.
  • Vinn O. 2013. Occurrence, formation and function of organic sheets in the mineral tube structures of Serpulidae (Polychaeta, Annelida). PLoS one. 8:e75330. doi: 10.1371/journal.pone.0075330
  • Vinn O, Kupriyanova EK. 2011. Evolution of a dense outer protective tube layer in serpulids (Polychaeta, Annelida). Carnets de Géologie-Notebooks on Geology. CG2011_L05:137–147.
  • Vinn O, Ten Hove HA, Mutvei H, Kirsimae K. 2008. Ultrastructure and mineral composition of serpulid tubes (Polychaeta, Annelida). Zool J Linn Soc. 154:633–650. doi: 10.1111/zoj.2008.154.issue-4
  • Weiner S, Addadi L. 1997. Design strategies in mineralized biological materials. J Mater Chem. 7:689–702. doi: 10.1039/a604512j
  • Wolfe K, Smith AM, Trimby P, Byrne M. 2013. Microstructure of the paper nautilus (Argonauta nodosa) shell and the novel application of electron backscatter diffraction (EBSD) to address effects of ocean acidification. Mar Biol. 160:2271–2278. doi: 10.1007/s00227-012-2032-4
  • Zeebe RE, Zachos JC, Caldeira K, Tyrrell T. 2008. Oceans: carbon emissions and acidification. Science. 321:51–52. doi: 10.1126/science.1159124

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.