Abstract
Understanding the structural and mechanical properties of coral skeletons is important to assess their responses to natural and anthropogenic challenges and to predict the long-term viability of hermatypic corals in a changing ocean. Here, we describe the microstructure of the critically endangered staghorn coral (Acropora cervicornis) skeleton and its mechanical properties, spectral and fluidic behavior, including uniaxial compressive strength, resistance to plastic deformation, spectral vibrational response, and flow-field analysis. We evaluated skeletons of A. cervicornis retrieved from a nursery off Broward County, Florida, USA. Optical micrographs and X-ray computed topography revealed a complex system of canals and pores that allow rapid skeletal elongation while retaining sufficient strength to withstand currents, waves, and other physical forces. Compressive loading of the aragonite skeleton resulted in complex stress–strain deformation behavior; the unique pore arrangement resisted catastrophic cracks and prevented instantaneous failure. Vickers microhardness was 3.56 ± 0.31 GPa, which is typical for soft aragonite materials yet sufficient to withstand the hydraulic pressure of ocean waves. Impressions made by the diamond indenter had almost no cracks radiating from their corners, which again demonstrated the ability of the complex skeleton microstructure to suppress crack formation and growth (e.g., from the bites of grazers). Maps of the ν1 mode Raman peak of identation surfaces showed evidence of residual strain. However, the ν1 peak’s position barely changed (from 1083.6 cm−1 outside the impression to 1083.9 cm−1 in the center), indicating weak stress sensitivity. Flow-field analysis revealed small-scale, counter-rotating vortices formed in the skeleton’s wake, which can entrain food particles within range of polyp tentacles and facilitate transport of respiratory gases and wastes. Considered together, our results demonstrate that the perforate skeleton of A. cervicornis is well-adapted to withstand physical forces normally encountered in its shallow-water habitat, but may be susceptible to anthropogenic stressors that alter its architecture.
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References
Adrian RJ (1991) Particle-imaging techniques for experimental fluid mechanics. Annu Rev Fluid Mech 23:261–304
Albert S, Saunders MI, Roelfsema CM, Leon JX, Johnstone E, Mackenzie JR, Hoegh-Guldberg O, Grinham AR, Phinn SR, Duke NC, Mumby PJ (2017) Winners and losers as mangrove, coral and seagrass ecosystems respond to sea-level rise in Solomon Islands. Environ Res Lett 12:094009
Alvarez K, Camero S, Alarcόn ME, Rivas A, González G (2002) Physical and mechanical properties evaluation of Acropora palmata coralline species for bone substitution applications. J Mater Sci Mater Med 13:509–515
Baldock TE, Karampour H, Sleep R, Vyltla A, Albermani F, Golshani A, Callaghan DP, Roff G, Mumby PJ (2014) Resilience of branching and massive corals to wave loading under sea level rise – a coupled computational fluid dynamics-structural analysis. Mar Pollut Bull 86:91–101
Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193
Barnes DJ (1970) Coral skeletons: an explanation of their growth and structure. Science 170:1305–1308
Behrens G, Kuhn LT, Ubic R, Heuer AH (1995) Raman spectra of vateritic calcium carbonate. Spectrosc Lett 29:983–995
Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833
Benzerara K, Menguy N, Obst M, Stolarski J, Mazur M, Tylisczak T, Brown GE, Meibom A (2011) Study of the crystallographic architecture of corals at the nanoscale by scanning transmission X-ray microscopy and transmission electron microscopy. Ultamicroscopy 111:1268–1275
Bongaerts P, Riginos C, Hay KB, van Oppen MJH, Hoegh-Guldberg O, Dove S (2011) Adaptive divergence in a scleractinian coral: physiological adaptation of Seriatopora hystrix to shallow and deep reef habitats. BMC Evol Biol 11:303
Boström-Einarsson L, Babcock RC, Bayraktarov E, Ceccarelli D, Cook N, Ferse SC, Hancock B, Harrison P, Hein M, Shaver E, Smith A (2020) Coral restoration–A systematic review of current methods, successes, failures and future directions. PLoS ONE 15:e0226631
Burke LM, Reytar K, Spalding M, Perry A (2011) Reefs at risk revisited: World Resources Institute, Washington, DC, 130 pp
Byrne M, Fitzer S (2019) The impact of environmental acidification on the microstructure and mechanical integrity of marine invertebrate skeletons. Conserv Physiol 7(1):coz062
Carrasco-Peña A (2019) Mechanical properties of brittle ceramics: case study of boron rich ceramics and Acropora cervicornis coral skeleton. Ph.D. thesis, University of Central Florida, p 75
Chamberlain JA (1978) Mechanical properties of coral skeleton: compressive strength and its adaptive significance. Paleobiology 4:419–435
Chappell J (1980) Coral morphology, diversity and reef growth. Nature 286:249–252
Cohen AL, McConnaughey TA (2003) Chemical perspectives on coral mineralization. Rev Mineral Geochem 54:151–188
Cohen AL, McCorkle DC, de Putron S, Gaetani GA, Rose KA (2009) Morphological and compositional changes in the skeletons of new coral recruits reared in acidified seawater: insights into the biomineralization response to ocean acidification. Geochem Geophys 10:1–12
Coronado I, Fine M, Bosellini FR, Stolarski J (2019) Impact of ocean acidification on crystallographic vital effect of the coral skeleton. Nat Commun 10:2896–2904
Cresswell AK, Thomson DP, Haywood MD, Renton M (2020) Frequent hydrodynamic disturbances decrease the morphological diversity and structural complexity of 3D simulated coral communities. Coral Reefs 39:1147–1161
Danzer R (2002) Mechanical failure of advanced ceramics: The value of fractography. Key Eng Mater 223:1–18
DeCarlo T, D'Olivo J, Foster T, Holcomb M, Becker T, McCulloch M (2017) Coral calcifying fluid aragonite saturation states derived from Raman spectroscopy. Biogeosciences 14:5253–5269
DeCarlo TM, Comeau S, Cornwall CE, McCulloch MT (2018) Coral resistance to ocean acidification linked to increased calcium at the site of calcification. Proc Royal Soc B-Biol Sci 285:20180564
DeCarlo TM, Comeau S, Cornwall CE, Gajdzik L, Guagliardo P, Sadekov A, Thillainath EC, Trotter J, McCulloch MT (2019) Investigating marine bio-calcification mechanisms in a changing ocean with in vivo and high-resolution ex vivo Raman spectroscopy. Global Change Biol 25:1877–1888
Donath FA (1946) Effects of cohesion and granularity on deformational behavior of anisotropic rock. Geo Soc Am Bull 135:95–119
Dusza J (2000) Fractographic failure analysis of brittle materials. Inter J Mater Prod Tec 15:292–255
Edinger EN, Risk MJ (2000) Reef classification by coral morphology predicts coral reef conservation value. Biol Conserv 92:1–3
Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Change 1:165–169
Farfan GA, Cordes EE, Rhian GW, Thomas MD, Hansel CM (2018) Mineralogy of deep-sea coral aragonites as a function of aragonite saturation state. Front Mar Sci 5:1–15
Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2005) Hurricanes and Caribbean coral reefs: impacts, recovery patterns, and role in long-term decline. Ecology 86:174–184
Gladfelter EH (1982) Skeletal development in Acropora cervicornis: I. Patterns of calcium carbonate accretion in the axial corallite. Coral Reefs 1:45–51
Gladfelter EH (1984) Skeletal development in Acropora cervicornis. Coral Reefs 3:51–57
Gladfelter EH (2007) Skeletal development in Acropora palmata. Coral Reefs 26:883–892
Gregori G, Burger W, Sergo V (1999) Piezo-spectroscopic analysis of the residual stresses in zirconia-toughened alumina ceramics: the influence of the tetragonal-to-monoclinic transformation. J Mater Sci Eng A 271:401–406
Hallock P, Williams DE, Fisher EM, Toler SK (2006) Bleaching in foraminifera with algal symbionts: implications for reed monitoring and risk assessment. Anu do Inst de Geocienc 29:108
He J, Clarke DR (1995) Determination of the piezospectroscopic coefficients for chromium-doped sapphire. J Am Ceram Soc 78:1347–1353
Hein MY, Willis BL, Beeden R, Birtles A (2017) The need for broader ecological and socioeconomic tools to evaluate the effectiveness of coral restoration programs. Restor Ecol 25:873–883
Hein MY, Beeden R, Birtles A, Gardiner NM, Le Berre T, Levy J, Marshall N, Scott CM, Terry L, Willis BL (2020) Coral restoration effectiveness: multiregional snapshots of the long-term responses of coral assemblages to restoration. Diversity 12:153
Hughes TP, Graham NA, Jackson JB, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642
Jokiel PL, Jury CP, Kuffner IB (2016) Coral calcification and ocean acidification. In: Hubbard D, Rogers C, Lipps J, Stanley, Jr. G (eds) Coral reefs at the crossroads. Coral reefs of the world, vol 6. Springer, Dordrecht
Kearney C, Zhao Z, Bruet BJ, Radovitzky R, Boyce MC, Ortiz C (2006) Nanoscale anisotropic plastic deformation in single crystal aragonite. Phys Rev Lett 96(255505):1–4
Kontoyannis CG, Vagenas NV (2000) Calcium carbonate phase analysis using XRD and FT-Raman spectroscopy. Analyst 125:251–255
Kuffner IB, Bartels E, Stathakopoulos A, Enochs IC, Kolodziej G, Toth LT, Manzello DP (2017) Plasticity in skeletal characteristics of nursery-raised staghorn coral, Acropora cervicornis. Coral Reefs 36:679–684
Kruzic JJ, Kim DK, Koester KJ, Ritchie RO (2009) Indentation techniques for evaluating the fracture toughness of biomaterials and hard tissues. J Mech Behav Biomed Mater 2:384–395
Lirman D, Thyberg T, Herlan J, Hill C, Young-Lahiff C, Schopmeyer S, Huntington B, Santos R, Drury C (2010) Propagation of the threatened staghorn coral Acropora cervicornis: methods to minimize the impacts of fragment collection and maximize production. Coral Reefs 29:729–735
Lohr KE, Patterson JT (2017) Intraspecific variation in phenotype among nursery-reared staghorn coral Acropora cervicornis (Lamarck, 1816). J Exp Mar Biol Ecol 486:87–92
Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, Van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131
Lugovy M, Slyunyayev V, Subbotin V, Liang F, Gou J, Orlovskaya N, Graule T, Keubler J (2011) Mechanical behavior and failure mechanisms of boron carbide based three-layered laminates with weak interfaces. Ceram Int 37:2255–22261
Ma Q, Clarke DR (1993) Stress measurement in single-crystal and polycrystalline ceramics using their optical fluorescence. J Am Ceram Soc 76:1433–1440
Maia LF, Ferreira GR, Costa RC, Lucas NC, Teixeira RI, Fleury BG, Edwards HG, de Oliveira LF (2014) Raman spectroscopic study of antioxidant pigments from cup corals Tubastraea spp. J Phys Chem A 118:3429–3437
Marfenin NN (2015) Non-radial symmetry of the transport system of Acropora corals. Zool Bespozvon 12:53–59
Marshall PA (2000) Skeletal damage in reef corals: relating resistance to colony morphology. Mar Ecol Prog Ser 200:177–189
Mecholsky JJ, Passoja DE, Feinberg-Ringel KS (1989) Quantitative analysis of brittle fracture surface using fractal geometry. J Am Ceram Soc 72:60–65
Mumby PJ, Steneck RS (2008) Coral reef management and conservation in light of rapidly involving ecological paradigms. Trends Ecol Evol 23:555–563
Nedimyer K, Gaines K, Roach S (2011) Coral Tree Nursery: An innovative approach to growing corals in an ocean-based field nursery. Aquac Aquar Conserv Legis 4:442–446
Norzagaray-López OC, Calderon-Aguilera LE, Castro-Ceseña AB, Hirata G, Hernández-Ayón JM (2017) Skeletal dissolution kinetics and mechanical tests in response to morphology among coral genera. Facies 63:7
Noström AV, Nyström M, Jouffray JB, Folke C, Graham NA, Moberg F, Olsson P, Williams GJ (2016) Guiding coral reef futures in the Anthropocene. Front Ecol Environ 14:490–498
Ogden JC (1977) Carbonate-sediment production by parrot fish and sea urchins on Caribbean reefs. AAPG Stud Geol 4:281–288
Orlovskii VP, Komlev VS, Barinov SM (2002) Hydroxyapatite and hydroxyapatite-based ceramics. Inorg Mater 38:973–984
Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958
Parsard G, Subhash G, Jannotti P (2018) Amorphization-induced volume change and residual stresses in boron carbide. J Am Ceram Soc 101:2606–2615
Reid WV, Mooney HA, Cropper A, Capistrano D, Carpenter SR, Chopra K, Dasgupta P, Dietz T, Duraiappah AK, Hassan R, Kasperson R (2005) Ecosystems and human well-being-synthesis: a report of the Millennium Ecosystem Assessment. Island Press, 155 pp
Reidenbach MA, Koseff JR, Monismith SG (2007) Laboratory experiments of fine-scale mixing and mass transport within a coral canopy. Phys Fluids 19:075107
Rice MM, Ezzat L, Burkepile DE (2019) Corallivory in the Anthropocene: interactive effects of anthropogenic stressors and corallivory on coral reefs. Front Mar Sci 11:525–539
Robertson R (1970) Review of the predators and parasites of stony corals, with special reference to symbiotic prosobranch gastropods. Pac Sci 24:43–54
Rodgers KU, Cox E, Newston C (2003) Effects of mechanical fracturing and experimental trampling on Hawaiian corals. Environ Manage 31:173–181
Shafir S, Van Rijn J, Rinkevich B (2006) Steps in the construction of underwater coral nursery, an essential component in reef restoration acts. Mar Biol 149:679–687
Shapiro OH, Fernandez VI, Garren M, Guasto JS, Debaillon-Vesque FP, Kramarsky-Winter E, Vardi A, Stocker R (2014) Vortical ciliary flows actively enhance mass transport in reef corals. PNAS 111:13391–13396
Smith RL, Sandland GE (1922) An accurate method of determining the hardness of metals, with particular reference to those of a high degree of hardness. Proc Inst Mech Eng -J Pro I:623–641
Stadelmann R, Lugovy M, Orlovskaya N, Mchaffey P, Radovic M, Sglavo VM, Grasso S, Reece MJ (2016) Mechanical properties and residual stresses in ZrB2-SiC spark plasma sintered ceramic composites. J Eur Ceram Soc 36:1527–1537
Subhash G, Ravichandran G (1998) Mechanical behavior of a hot pressed aluminum nitride under uniaxial compression. J Mater Sci 33:1933–1939
Subhash G, Ravichandran G (2000b) Split Hopkins pressure bar testing of ceramics. In: Medlin D, Kuhn H (eds). ASM handbook 8:497–50
Swain TD, Bold EC, Osborn PC, Baird AH, Westneat MW, Backman V, Marcelino LA (2018) Physiological integration of coral colonies is correlated with bleaching resistance. Mar Ecol Progr Series 586:1–10
Tambutté S, Holcomb M, Ferrier-Pagès C, Reynaud S, Tambutté É, Zoccola D, Allemand D (2011) Coral biomineralization: from the gene to the environment. J Exp Mar Biol Ecol 408:58–78
Tanaka M (1996) Fracture toughness and crack morphology in indentation fracture of brittle materials. J Mater Sci 31:749–755
Thielicke W, Stamhuis EJ (2014) PIVlab - towards user friendly, affordable and accurate digital particle image velocimetry in MATLAB. J Open Res Softw 2:e30
Urmos J, Sharma SK, Mackenzie FT (1991) Characterization of some biogenic carbonates with Raman spectroscopy. Amer Miner 76:641–646
van Woesik R, Van Woesik K, Van Woesik L, Van Woesik S (2013) Effects of ocean acidification on the dissolution rates of reef-coral skeletons. PeerJ 21(1):e208
Vosburgh, (1982) Acropora reticulata: structure, mechanics and ecology of a reef coral. Biol Sci 214:481–499
Wall M, Nehrke G (2012) Reconstructing skeletal fiber arrangement and growth mode in the coral Porites lutea (Cnidaria, Scleractinia): a confocal Raman microscopy study. Biogeosciences 9:4885–4895
Ware M, Garfield EN, Nedimyer K, Levy J, Kaufman L, Precht W, Winters RS, Miller SL (2020) Survivorship and growth in staghorn coral (Acropora cervicornis) outplanting projects in the Florida Keys National Marine Sanctuary. PLoS ONE 6(15):e0231817
Weiner S, Levi-Kalisman Y, Raz S, Addadi L (2003) Biologically formed amorphous calcium carbonate. Connect Tissue Res 44:214–218
Williams DE, Miller MW (2012) Attributing mortality among drivers of population decline in Acropora palmata in the Florida Keys (USA). Coral Reefs 31:369–382
Williamson CHK (1996) Vortex dynamics in the cylinder wake. Annu Rev Fluid Mech 28:477–539
Young CN, Schopmeyer SA, Lirman D (2012) A review of reef restoration and coral propagation using the threatened genus Acropora in the Caribbean and western Atlantic. Bull Mar Sci 88:1075–1098
Zhang N, Chen Y (2013) Nano scale plastic deformation mechanism in single crystal aragonite. J Mater Sci 31:749–755
Acknowledgements
This research was supported in part by NSF MRI Award #133775. The GE Phoenix Nanotom-Mâ„¢ X-ray CT was acquired through NSF Award #0959511. Manuscript revision was supported in part by US Environmental Protection Agency Cooperative Agreement X701D00720 UCFL to JE Fauth. Harvest of staghorn coral fragments to establish the NSU coral nursery was authorized under Florida Fish and Wildlife Conservation Commission Special Activity License #SAL-10-1086-SCRP. The authors also provide many thanks to an anonymous reviewer for their detailed review, which helped to improve our paper tremendously.
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JF and NO planned the study; DSG provided the chemically cleaned coral skeletons; AC-P, BM, and ZS performed the uniaxial compression and Vickers indentation tests; AC-P photographed the coral skeleton; MO performed optical microscopy and collected Raman maps of the indented skeleton surfaces; TS conducted flow-field experiments and analyzed the flow-field data; BEC and SNY performed CT scans and analyzed those data; and AC-P, MO, GS, SNY, JS, SB, JF, and NO all contributed to synthesis and manuscript writing.
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Carrasco-Pena, A., Omer, M., Masa, B. et al. Mechanical properties, spectral vibrational response, and flow-field analysis of the aragonite skeleton of the staghorn coral (Acropora cervicornis). Coral Reefs 39, 1779–1792 (2020). https://doi.org/10.1007/s00338-020-02003-8
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DOI: https://doi.org/10.1007/s00338-020-02003-8