By Stephanie June, Ellen Pullekines, Monika LaPlante, and Felicia Aronson
Calcification and Acidification
Calcification is the process by which scleractinian corals grow. Stony corals consist of two layers: a living tissue layer lying over a hard, calcium carbonate skeleton. The skeleton is produced by the calicoblastic ectoderm, located at the interface between the living tissue and the calcareous structure. Scleractinians build their skeletons using the aragonite form of calcium carbonate. The skeleton is composed of three-dimensional fan-like structures that radiate from sclerodermites, fibers that form the base unit of calcification (Barnes 1970). Calcium carbonate is added around these centrally located fibers both outwards and upwards to increase the size of the coral.
Biomineralisation
The formation of aragonite crystals and the coral skeleton is dependent on available amounts of calcium and inorganic carbon (Allemand et al. 2004). Calcium is generally acquired from the seawater. Inorganic carbon can be converted from carbon dioxide present in the water or produced from respiration. In seawater, carbon shifts through the following equilibrium, depending on concentrations:
Incorporation of the two components is biologically regulated by the calicoblastic epithelium. Calcium moves passively across the oral epithelium of the coral tissue, and is then actively pumped across the calicoblastic epithelium by a Ca-ATPase, which utilizes ATP and an extra proton produced by calcification. Carbon dioxide is freely diffusible and is converted to usable bicarbonate by carbonic anhydrase. The two combine to form calcium carbonate:
Ca+2 + HCO3- ↔ CaCO3 + H+
Calcification rates are mediated by the saturation state, Ω of aragonite in the seawater (Atkinson and Cuet 2008).
ΩArag= [Ca+2][CO3-2]/ksp
Saturation values above one favor the formation of aragonite crystals; saturation values below one favor ionic forms and can hinder calcification rates or lead to the dissolution of current skeleton.
Historical Research
The mechanism of calcium carbonate formation in corals has been a subject of research for many decades, beginning extensively with Tom Goreau in the 1950s. Goreau, a pioneer in coral calcification research, was the first to measure calcification using radioactive 45C isotopes (Goreau 1959). He was the first to propose that calcium was actively pumped across the calicoblastic endoderm, and utilized inhibitors to discern the mechanism of carbon dioxide conversion via carbonic anhydrase. Research in years following also relied heavily on inhibitors to work out the details of calcification. By inhibiting known pathways, researchers were able to determine which channels and pumps were involved in regulating calcification. Such studies confirmed the presence of calcium channels and CaATPase, carbonic anhydrase, and anion transporters that are crucial to the calcification process (Allemand et al. 2004, Marshall and Clode 2003)
Effects on Calcification
No one biological process acts in isolation; physical conditions play a major role in the efficiency and rate at which calcification occurs in scleractinian corals.
Light vs. Dark
The formation of the coral skeleton is characterized as diurnal. Coral growth occurs at both during the day and at night, though to varying degrees. Growth in the dark, or at night, is vertical growth. The outer edge or tips of the coral are extended in a porous pattern. When exposed to light, quality growth of the skeleton takes place at a rate that is three to five times faster than in darkness. This period of strengthening is known as ‘light enhanced calcification’ (Cohen and McConnaughey 2003).
An explanation for the light enhanced calcification lies in the symbiotic relationship reef-building corals share with the symbiont Symbiodinium. Increased light absorption by the autotrophic Symbiodinium subsequently increases the uptake of carbon dioxide from the water column and the rate of photosynthesis. As a result, the dissolved inorganic carbon levels within the coral as well as in the ambient environment are modified, more energy and oxygen are produced and exchanged to the coral holobiont, and the symbiont releases molecules required by the coral to build the organic matrix of its skeleton (Marshall and Clode 2003, Allemand et al. 2004).
Depth
Marine environments change drastically with depth; this is due to the role it plays in light penetration. Depending on the amount of light attenuation experienced by a coral at a certain depth, the morphology and therefore calcification is adjusted. The same species of coral can be seen having different structural shapes, or morphologies, across a wide range of depths. Typically, shallow water with high light levels support mounding corals in the shape of hemispheres or shortly branched coral heads. In contrast, deep water with low light levels is dominated by flattened or plating morphologies. Additionally, corals in low light environments are typically less fleshy because the physical conditions do not allow the coral to sustain as much tissue mass (Todd 2008).
Temperature
The ideal temperature range for scleractinian corals is between 18°C and 30°C (Cohen and McConnaughey 2003, Al-Horani 2005). Calcification has been shown to increase with increasing temperature, but only to a certain point. At approximately 26°-29°C, calcification stops increasing unchecked. At this temperature threshold, other factors start to reduce the overall health of the organism making enhanced calcification futile. Such factors include but are not limited to bleaching events, increases in pH, and/or changes in dissolved CO2 (Al-Horani 2005).
Water Flow
Research of water flow in and around coral reef ecosystems has shown a positive relationship with calcification and coral growth. One coral species, Pocillopora damicornis, has been closely studied to determine the effect of flow regimes on calcification rates. Higher water velocities were found to increase not only the rate of growth in corals but also the amount of new skeleton being produced. Increased flow over the coral reduces the diffusion boundary layer making exchange with the environment easier. Therefore, increased rates of photosynthesis, respiration and enzymatic activity are observed and attributed to the enhanced calcification (Lesser et al. 1994).
Nutrient Concentration
Excess nutrients enter reef systems in a variety of ways: human inputs from pollution, upwelling, erosion, runoff that carries fertilizers etc. (McConnaughey et al. 2000). Unfortunately, these inputs have been shown to decrease or inhibit growth altogether. Changes in nutrient concentrations are linked to increased sedimentation and macro-algal growth. Both of which limit light penetration to corals, break down the symbiotic relationship with Symbiodinium and can suffocate and kill entire reefs (Allemand et al. 2004).
Acidification
Acidification begins with a buildup of excess carbon dioxide in the air. Increasing CO2 levels are caused mainly by anthropogenic forces and have been significantly increasing since the industrial revolution. They are expected to exponentially spike throughout the next century.
pH
The process of ocean acidification occurs when the ocean absorbs an increasing amount of carbon dioxide from the air. The carbon dioxide combines with water to form carbonic acid (HCO3- + H+), which forces the equilibrium away from carbonate and towards production of bicarbonate.
CO2 + H2O ↔ H2CO3 ↔ HCO3- + H+ ↔ CO32- + 2H+
The production of bicarbonate reduces the availability of carbonate in the ocean. This can be detrimental to calcifying corals and algae that need carbonate build their calcium carbonate shell (Orr et al. 2005). Reduced pH can also cause corals to expel their zooxanthellae in an acidic environment, initiating coral bleaching events. Furthermore, acidification may have effects on organic productivity (K.R.N. et al. 2008).
It is predicted that by 2100, ocean pH levels will decrease by 0.3 to 0.4 units (Orr et al. 2005) and that by 2300, pH will have dropped 1.4 units (Fine and Tchernov 2007). This will have devastating effects on ocean ecosystems as all biota will have no option but to adapt to lowering pHs or suffer extinction.
Saturation States
Calcium carbonate has two alternate forms: aragonite and calcite. The saturation state (W) of each of these calcium carbonate forms varies with temperature, salinity, pressure and mineral phase (Doney et al. 2009). Scleractinian corals, which use aragonite to construct their structures, are more susceptible to acidification because aragonite is 50% more soluble than calcite. As a result, the aragonite saturation horizon is closer to the surface and thus, impacted faster by rising pCO2 (Royal Society 2005, Doney et al. 2009). The aragonite saturation horizon currently occurs between 0.5 and 2.5 km below sea surface whereas the calcite saturation horizon occurs between 1.5 and 5km (Royal Society 2005). The movement of these saturation levels has been charted as a function of anthropogenic introduced CO2 in to ocean systems dating from the pre-industrial period to 2100.
Calcification rate is directly proportional to aragonite saturation. It has been found that by doubling pCO2 in laboratory mesocosm experiments a 3-34% reduction in carbonate production (Marubini et al. 2001, 2003, Royal Society 2005). In coral models doubling pCO2 has shown to reduce calcification rates by 10-30% (Kleypas et al. 1999).
Carbonate saturations decrease with temperature and depth. In recent years there has been evidence that that cold-water corals systems may actually exceed the cover of warm-water reefs (Freiwald et al. 2004). Corals and other calcifying organisms living in coldwater oceans (e.g. Southern Ocean, the sub-Antarctic, Polar Regions) will be affected first where saturation states are naturally the lowest occurring (Caldeira and Rau 1999, Caldeira and Wickett 2003,2005). As a result of anthropogenic carbon inputs, the aragonite saturation horizon in the North Pacific is migrating upwards in the water column at a rate of 1-2 meters per year-1 (Fabry et al. 2008).
Future Projections
If CO2 emissions continue to rise at current rates, aragonite dependant organisms will be latitude-limited by 2100. At this time, the aragonite saturation horizon in the Southern Ocean has been predicted to reach the sea surface. The Intergovernmental Panel on Climate Change (IPCC) IS92a “business-as-usual” emissions scenarios aragonite saturation levels will decrease 11.8% by 2040 and under saturations of both aragonite and calcite will occur within this century (Orr et al. 2005, Fabry et. al 2008). The IPCC model also shows that there will be a 47% decrease in aragonite saturation, when pCO2 reaches only three times that of pre-industrial levels.
A delicate balance of CO2 absorption and release keeps aragonite levels in check (Vernon et al. 2009); it is predicted that once aragonite levels drop, dramatic shifts those balances will have detrimental effects on the health of corals (Fine and Tchernov 2007).
References
Al-Horani, F. A. 2005. Effects of changing seawater temperature on photosynthesis and calcification in the scleractinian coral Galaxea fascicularis, measured with O2, Ca2+ and pH microsensors. Scientia Marina 69:347-354.
Allemand, D., C. Ferrier-Pages, P. Furla, F. Houlbreque, S. Puverel, S. Reynaud, E. Tambutte, S. Tambutte, and D. Zoccola. 2004. Biomineralisation of reef-building corals: from molecular mechanisms to environmental control. Comptes Rendus Palevol 3: 453-467
Anthony, K.R.N., D.I. Kline, G. Diaz-Pulido, S. Dove, and O. Hoegh-Guldberg. 2008. Ocean acidification causes bleaching and productivity loss in coral reef builders.
Atkinson, M. J. and P. Cuet. 2008. Possible effects of ocean acidification on coral reef biogeochemistry: topics for research. Marine Ecology Progress Series 373: 249-256.
Barnes, D. J. 1970. Coral skeletons: an explanation of their growth and structure. Science, New Series 170:1305-1308.
Caldeira K, and M. E. Wickett. 2003. Anthropogenic carbon and ocean pH. Nature 425:365
Caldeira K, and M. E. Wickett. 2005. Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. Journal of Geophysical Research: Oceans 110:C09S4
Caldeira, K. and G.H. Rau. 1999.Accelerating carbonate dissolution to sequester carbon dioxide in the ocean: Geochemical implications. Geophysical Research Letters: 27:225-228.
Cohen, A. L., and T. A. McConnaughey. 2003. Geochemical perspectives on coral mineralization. Reviews in Mineralogy and Geochemistry 54:151-187.
Doney, S.C., V.J.Fabry, R.A.Feely, and J.A.Kleypas. 2009. Ocean Acidification: The Other CO2 Problem. Anuual Review of Marine Science. 1:169-192.
Fabry, V. J., B.A. Seibel, R. A. Feely, and J. C. Orr. 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science 65: 414–432.
Fine, Maoz and Dan Tchernov. 2007. Scleractinian coral species survive and recover from decalcification. Science 315:1811.
Freiwald A, J. H. Fossa, A. Grehan, T. Koslow, J. M. Roberts. 2004. Cold-water coral reefs: out of sight no longer out of mind. UNEP–WCMC 22.
Goreau, T. F. 1959. The physiology of skeleton formation in corals. 1. A method for measuring the rate of calcium deposition by corals under different conditions. Biological Bulletin 116: 59-75.
Kleypas J. A., Feely R. A., Fabry V. J., Langdon C., Sabine C. L., Robbins L. L. 2005. Impacts of ocean acidification on coral reefs and other marine calcifiers: a guide for future research. 2008. Report of a workshop held 18–20 St Petersburg, FL: sponsored by NSF, NOAA, and the US Geological Survey 88pp.
Kleypas, J.A., R.W. Buddemeier, D. Archer, J. P. Gattuso, C. Langdon, and B. N. Opdyke. 1999. Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284: 118-120.
Lesser, M. P., V. M. Weis, M. R. Patterson, and P. L. Joklel. 1994. Effects of morphology and water movement on carbon delivery and productivity in the reef coral, Pocillopora damicornis (Linnaeus): Diffusion barriers, inorganic carbon limitation, and biochemical plasticity. Journal of Experimental Marine Biology and Ecology 178:153-179.
Marshall, A. T., and P. L. Clode. 2003. Light-regulated Ca2+ uptake and O2 secretion at the surface of a scleractinian coral Galaxea fascicularis. Comparative biochemistry and physiology part A 136: 417-426.
Marubini F., C. Ferrier-Page, J.P. Cuif. 2003. Suppression of skeletal growth in scleractinian corals by decreasing ambient carbonate-ion concentration: a cross-family comparison. Proceedings of the Royal Society of London, Series B :270:179-184.
Marubini F., H. Barnett, C. Langdon, M. J. Atkinson. 2001. Dependence of calcification on light and carbonate ion concentration for the hermatypic coral Porites compressa. Marine Ecology Progress Series 220:153-162.
McConnaughey, T. A, W. H. Adey, and A. M. Small. 2000. Community and environmental influences on reef coral calcification. Limnology and Oceanography 45:1667-1671.
Orr, J. C., V. J. Fabry, O. Aumont, L. Bopp, S. C. Doney, R. A. Feely, A. Gnanadesikan, N. Gruber, A. Ishida, F. Joos, R. M. Key, K. Lindsay, E. Maier-Reimer, R. Matear, P. Monfay, A. Mouchet, R. G. Najjar, G. K. Plattner, K. B. Rodgers, C. L. Sabine, J. L Sarmiento, R. Schlitzer, R. D. Slater, I. J. Totterdel, M. F. Weirig, Y. Yamanak, and A. Yool. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681-686.
The Royal Society. 2005. Ocean acidification due to increasing atmospheric carbon dioxide. Policy Document.
Todd, P. A. 2008. Morphological plasticity in scleractinian corals. Biological Review 83:315-337.
Veron, J.E.N., O. Hoegh-Guldberg, T.M. Lenton, J.M. Lough, D.O. Obura, P. Pearce-Kelly, C.R.C. Sheppard, M. Spalding, M.G. Stafford-Smith, A.D. Rogers. 2009. The coral reef crisis: The critical importance of <350 ppm CO2. Marine Pollution Bulletin 58:1428-1436.