Marine and Freshwater Acidification: Effects on Marine Plants
Writing in the Journal Club section of Nature, Stoll (2009) restates the IPCC’s mantra that “ocean acidification in response to excess carbon dioxide in the atmosphere could become a problem for marine organisms, especially those that make skeletons or shells out of calcium carbonate,” including “the coccolithophorids—microscopic algae that are, by volume, the most important shell producers.” She has a much more optimistic view of the subject, however, thanks in large part to the research of Langer et al. (2009).
The latter scientists—hailing from France, Germany, Spain, and the Netherlands—grew four different strains of the coccolithophore Emiliania huxleyi in dilute batch cultures of seawater with carbonate chemistries characteristic of those expected to prevail beneath an atmosphere of four different CO2 concentrations ranging from approximately 200 to 1200 ppm, while they measured particulate organic carbon content, particulate inorganic carbon content, and organic and inorganic carbon production. In doing so, they found the four strains “did not show a uniform response to carbonate chemistry changes in any of the analyzed parameters and none of the four strains displayed a response pattern previously described for this species.”
In light of these findings—plus other aspects of their earlier studies (Langer et al., 2006, 2007) and the diverse findings of others who had studied still other strains of the species—the five scientists concluded “the sensitivity of different strains of E. huxleyi to acidification differs substantially and that this likely has a genetic basis.” Stoll agrees with this assessment, stating that Langer et al. “argue convincingly” in this regard, and she adds that the work of those who foresee disastrous consequences typically “precludes the kind of natural selection and adaptation that might occur over decades and centuries in the ocean.”
In further discussing the subject, Langer et al. (2009) write, “shifts in dominance between species and/or between clones within a species might therefore be expected,” as the air’s CO2 content continues to rise; but they state that too often “the possibility of adaptation is not taken into account.” This should not be assumed away, for the great genetic diversity that exists both among and within species, in the words of Stoll, “is good insurance in a changing ocean.” Indeed, this could be interpreted as evidence that Earth’s coccolithophorids are well prepared for whatever the future may thrust at them in this regard, for as Langer et al. (2006) have more boldly and explicitly stated, “genetic diversity, both between and within species, may allow calcifying organisms to prevail in a high CO2 ocean.”
Support for that notion was, in fact, provided one year earlier. Based on data obtained from a sediment core extracted from the subpolar North Atlantic Ocean, Iglesias-Rodriguez et al. (2008) determined there had been a 40 percent increase in oceanic coccolith mass over the past 220 years, during which time the atmosphere’s CO2 concentration rose by approximately 90 ppm. They further found this response to be consistent with the results of several batch incubations of the far-ranging coccolithophore species Emiliania hyxleyi, conducted while bubbling air of several different atmospheric CO2 concentrations through the culture medium they employed for that purpose.
Working with materials derived from the same sediment core, Halloran et al. (2008) analyzed the size distribution of CaCO3 particles in the less-than-10-µm sediment fraction over the past quarter-century. This analysis revealed “a changing particle volume since the late 20th century consistent with an increase in the mass of coccoliths produced by the larger coccolithophore species,” which included Oolithotus fragilis, Calcidicus leptoporus, Coccolithus pelagicus var. pelagicus, and Helicosphaera carteri.
Commenting on their findings, Halloran et al. state their data suggest “in the real ocean the larger coccolithophore species increase their calcification in response to anthropogenic CO2 release,” and “such a calcification response could be attributed to an alleviation of CO2 limitation in species that partly rely on the diffusive supply of dissolved carbon dioxide for photosynthesis, as demonstrated by a rise in photosynthetic efficiency with increasing carbon dioxide in cultures of E. huxleyi (Rost et al., 2003).”
Examining other phytoplankton, Lombard et al. (2010) studied the effects of ocean acidification on two planktonic foraminifera, which in the words of the authors, “are widespread calcifying protozoa, responsible for 32–80% of the global deep-ocean calcite fluxes (Schiebel, 2002).” Working with specimens of Orbulina universa collected by scuba divers off the coast of Catalina Island, California, and Globigerinoides sacculifer obtained near Puerto Rico, USA, Lombard et al. cultured them under high and low irradiances in filtered sea water whose pH and carbonate ion concentration—[CO32-]—were manipulated by adding NaOH or HCl. Among other things, the data they collected in these experiments included “measurements of the initial and final size (µm), the survival time (days from collection to gametogenesis), and final weight of the shell (µg),” but only for “individuals that underwent gametogenesis and grew at least one chamber.”
The four researchers report “under the IS92a ‘business as usual’ scenario as defined by the Intergovernmental Panel on Climate Change and projected for the year 2100,” their results suggest “in 2100, the rate of calcification of G. sacculifer and O. universa could decline by 6–13% compared to recent rates.” In addition, they state “the future increase in temperature [predicted by the IPCC] could increase the production of calcite by foraminifera, counteracting the negative impact of ocean acidification.” In addition, the results of the analysis of Tans (2009), illustrated in Figure 8.2.2, suggest (1) the true decline in oceanic pH by the year 2100 is more likely to be only about half of that projected by the IPCC and (2) this drop will begin to be ameliorated after 2100, gradually returning oceanic pH to present-day values after 2500.
In another experiment on foraminifers, Kuroyanagi et al. (2009) cultured asexually produced individuals of Marginopora kudakajimensis—a calcifying microorganism that contributes to both organic and inorganic carbon production in coral reefs—under carefully controlled laboratory conditions for a period of 71 days in glass jars containing approximately 110 ml of filtered natural seawater (control pH of about 8.2) and two less-basic pH conditions of about 7.9 and 7.7, created by additions of 0.1 N HCl.
In declining from the control pH of 8.2 to a pH of 7.9, the mean maximum shell diameter of the large foraminifer actually rose by 8.6 percent, while its mean shell weight rose by a much smaller and insignificant 0.7 percent. As the seawater’s pH declined to 7.7, however, the organism’s mean maximum shell diameter fell by 12.1 percent, and its mean shell weight fell by 49.3 percent.
Based on these results, Kuroyanagi et al. conclude that if oceanic pH remains within the range of 8.2 to 7.9, the “large foraminifers should be able to maintain present calcification rates,” but they note any further drop in pH could lead to reduced rates of calcification. That said, although the IPCC’s A2 scenario predicts a maximum pH decline of approximately 0.5 pH units by about AD 2270, the more recent analysis of Tans (2009) suggests a maximum pH drop of only about 0.14 unit at about AD 2090, after which pH begins to rise to asymptotically return to its current value after several hundred years. This latter projection suggests oceanic pH will not come close to creating a major decline in the calcification rate of M. kudakajimensis. We next report the results of two ocean acidification studies on phytoplankton communities. In prefacing their work, Wyatt et al. (2010) state “the assimilation of inorganic nutrients fuels phytoplankton growth,” and, therefore, “any alteration in the bioavailability of these nutrients is likely to impact productivity and, by extension, climate regulation through the uptake of CO2 by marine algae.” They note “the reduction of surface ocean pH anticipated for the next century will alter the equilibrium coefficient between dissolved ammonia (NH3(aq)) and ammonium (NH4+) shifting the equilibrium towards NH4+ (Zeebe and Wolf-Gladrow, 2001; Bell et al., 2007, 2008),” such that the future decease in ocean pH due to the ongoing rise in the air’s CO2 content could result in the transfer of more gaseous NH3 from the overlying atmosphere to the ocean, as has been noted by Jacobson (2005).
To further explore this scenario, Wyatt et al. collected surface seawater samples from a coastal monitoring site in the western English Channel (WEC) from 17 March to 21 July 2008, which included two distinct phases of the annual spring phytoplankton bloom (a pre-bloom period of five weeks and the bloom proper of 11 weeks). In addition, they measured ambient pH for carbonate system estimates and dissolved inorganic nutrients, and they equilibrated the samples with CO2-in-air mixtures that resulted in CO2 concentrations of 380, 500, 760, and 1,000 ppm that led to pH values of 8.05, 8.01, 7.87, and 7.76, respectively, which are to be compared with the mean ambient value of 8.18.
The six scientists report their results indicated the phytoplankton community “was predominantly limited by the availability of inorganic nitrogen,” and “during early and mid-summer, NHX became the primary source of inorganic nitrogen.” Interestingly, they also report “an overall increase in NHX concentrations by 20% was observed between the present day CO2 treatment (380 ppm) and 1000 ppm.”
Given these findings, Wyatt et al. write, “as excess CO2 dissociates in the oceans, the increased hydrogen ion concentration ionizes NH3(aq) and decreases the ratio of NH3(aq):NH4+,” and this reduction in NH3(aq) “would lead to an imbalance in the equilibrium between NH3(aq) in the surface water and gaseous NH3 in the overlying atmosphere resulting in the drawdown of atmospheric NH3 to the surface ocean.” Based on this finding, they further calculate that whereas the surface waters of the WEC “are a net source of 150 µmol/m2/year of NH3 to the atmosphere at present (2009),” it is likely “the WEC will become a net sink of 300 µmol/m2/year for atmospheric NH3 as atmospheric CO2 rises to 717 ppm and the surface pH decreases to 7.83,” due to the increase in phytoplanktonic productivity driven by the increased transfer of gaseous NH3 from the air to the surface waters of the WEC. This phenomenon would (1) boost the productivity of higher oceanic trophic levels, (2) help sequester more carbon at the bottom of the sea, and thereby (3) reduce the rate of increase in radiative forcing that is speculated to fuel global warming.
In a contemporaneous study of a phytoplankton community, Breitbarth et al. (2010) write as background for their report, “studies of artificial and natural iron input have demonstrated iron control of phytoplankton productivity and CO2 drawdown over vast oceanic regions (Boyd et al., 2007; Blain et al., 2007; Pollard et al., 2009) and in coastal upwelling regions (Bruland et al., 2001; Hutchins and Bruland, 1998),” and they state “temporal control of iron on phytoplankton productivity was also observed in a Norwegian fjord system (Ozturk et al., 2002).”
The eight researchers report CO2 perturbation and phytoplanktonic bloom development resulted in pH value ranges of 7.67–7.97, 7.82–8.06, and 8.13–8.26 at 1,050, 700, and 350 ppm CO2, respectively. They state their measurements revealed significantly higher dFe concentrations in the high CO2 treatment compared to the mid and low CO2 treatments, and that the high-CO2 mesocosms showed higher values of FE(II) compared to the lower CO2 treatments.
Breitbarth et al. thus conclude “ocean acidification may lead to enhanced Fe-bioavailability due to an increased fraction of dFe and elevated Fe(II) concentrations in coastal systems ... due to pH induced changes in organic iron complexation and Fe(II) oxidation rates,” noting these phenomena “will result in increased turnover of Fe in surface seawater, potentially maintaining iron bioavailability given a sufficient supply of total Fe, since equilibrium partitioning eventually restores the biolabile Fe pools that have been depleted by biological uptake.” They suggest “these processes may further fuel increased phytoplankton carbon acquisition and export at future atmospheric CO2 levels,” citing the work of Riebesell et al. (2007). They thus reach their final conclusion that “changes in iron speciation and the resulting potential negative feedback mechanism of phytoplankton productivity on atmospheric CO2”—i.e., the drawdown of atmospheric CO2 due to enhanced phytoplanktonic growth and transferal of the carbon thus removed from the atmosphere to the ocean depths—“need to be considered when assessing the ecological effects of ocean acidification.”
Writing as background for their study, Jiang et al. (2010) note “seagrasses are flowering plants that thrive in shallow oceanic and estuarine waters around the world, and are ranked as one of the most ecologically and economically valuable biological systems on earth,” citing the work of Beer et al. (2006). They state Thalassia hemprichii “is among the most widely-distributed seagrass species in an Indo-Pacific flora, dominating in many mixed meadows,” citing the work of Short et al. (2007).
In conducting their analysis, the authors collected intact vegetative plants of T. hemprichii from Xincun Bay of Hainan Island, Southern China, which they transported to the laboratory and cultured in flow-through seawater aquaria bubbled with four different concentrations of CO2 representative of (1) the present global ocean, with a pH of 8.10, (2) the projected ocean for 2100, with a pH of 7.75, (3) the projected ocean for 2200, with a pH of 7.50, and (4) the ocean characteristic of “an extreme beyond the current predictions” (a hundredfold increase in free CO2, with a pH of 6.2).
The three researchers report the “leaf growth rate of CO2-enriched plants was significantly higher than that in the unenriched treatment,” that “nonstructural carbohydrates (NSC) of T. hemprichii, especially in belowground tissues, increased strongly with elevated CO2,” and “belowground tissues showed a similar response with NSC.”
The Chinese scientists identify several implications of their findings that “CO2 enrichment enhances photosynthetic rate, growth rate and NSC concentrations of T. hemprichii.” With higher atmospheric CO2 concentrations, they note, “colonization beyond current seagrass depth limits is possible”; the extra stored NSC “can be used to meet the carbon demands of plants during periods of low photosynthetic carbon fixation caused by severe environmental disturbance such as underwater light reduction”; it can enhance “rhizome growth, flowering shoot production and vegetative proliferation”; and it “may buffer the negative effects of transplant shock by increasing rhizome reserve capacity.” They also write, “the globally increasing CO2 may enhance seagrass survival in eutrophic coastal waters, where populations have been devastated by algal proliferation and reduced column light transparency,” and “ocean acidification will stimulate seagrass biomass and productivity, leading to more favorable habitat and conditions for associated invertebrate and fish species.”
Also researching the potential effects of ocean acidification on macroalgae were Xu et al. (2010), who write, “Gracilaria lemaneiformis (Bory) Weber-van Bosse is an economically important red seaweed that is cultivated on a large scale in China due to the quantity and quality of agar in its cell walls.” In addition, they state “much attention has been paid to the biofiltration capacity of the species (Yang et al., 2005, 2006; Zhou et al., 2006),” and that it has thus been suggested to be “an excellent species for alleviating coastal eutrophication in China (Fei, 2004).” Considering these important characteristics of this seaweed, the authors set out to examine how this aquatic plant might respond to elevated CO2.
In conducting their experiment, plants were grown from thalli—collected at 0.5 m depth from a farm located in Shen’ao Bay, Nanao Island, Shantou (China)—for 16 days in 3-L flasks of natural seawater maintained at either natural (0.5 µM) or high (30 µM) dissolved inorganic phosphorus (Pi) concentrations in contact with air of either 370 or 720 ppm CO2, while their photosynthetic rates, biomass production, and uptake of nitrate and phosphate were examined.
As best as can be determined from Xu et al.’s graphical representations of their results, algal photosynthetic rates in the natural Pi treatment were increased only by a non-significant 5 percent as a result of the 95 percent increase in the air’s CO2 concentration, and in the high Pi treatment they were increased by approximately 41 percent. In the case of growth rate or biomass production, on the other hand, the elevated CO2 treatment exhibited a 48 percent increase in the natural Pi treatment, whereas in the high Pi treatment there was no CO2-induced increase in growth, because the addition of the extra 29.5 µM Pi boosted the biomass production of the low-CO2 natural-Pi treatment by approximately 83 percent, and additional CO2 did not increase growth rates beyond that point.
The three Chinese researchers state “elevated levels of CO2 in seawater increase the growth rate of many seaweed species despite the variety of ways in which carbon is utilized in these algae,” noting “some species, such as Porphyra yezoensis Ueda (Gao et al., 1991) and Hizikia fusiforme (Harv.) Okamura (Zou, 2005) are capable of using HCO3-, but are limited by the current ambient carbon concentration in seawater,” and “enrichment of CO2 relieves this limitation and enhances growth.” Regarding the results they obtained with Gracilaria lemaneiformis, on the other hand—which they state “efficiently uses HCO3- and whose photosynthesis is saturated at the current inorganic carbon concentration of natural seawater (Zou et al., 2004)”—they write, “the enhancement of growth could be due to the increased nitrogen uptake rates at elevated CO2 levels,” which in their experiment were 40 percent in the natural Pi treatment, because “high CO2 may enhance the activity of nitrate reductase (Mercado et al., 1999; Gordillo et al., 2001; Zou, 2005) and stimulate the accumulation of nitrogen, which could contribute to growth.” Whatever strategy might be employed, these several marine macroalgae appear to be capable of benefiting greatly from increased atmospheric CO2 concentrations.
Beer, S., Mtolera, M., Lyimo, T., and Bjork, M. 2006. The photosynthetic performance of the tropical seagrass Halophila ovalis in the upper intertidal. Aquatic Botany 84: 367–371.
Bell, T.G., Johnson, M.T., Jickells, T.D., and Liss, P.S. 2007. Ammonia/ammonium dissociation coefficient in seawater: a significant numerical correction. Environmental Chemistry 4: 183–186.
Bell, T.G., Johnson, M.T., Jickells, T.D., and Liss, P.S. 2008. Ammonia/ammonium dissociation coefficient in seawater: a significant numerical correction (vol. 4 pg 183, 2007). Environmental Chemistry 5: 258 U8.
Blain, S., Queguiner, B., Armand, L., Belviso, S., Bombled, B., Bopp, L., Bowie, A., Brunet, C., Brussaard, C., Carlotti, F., Christaki, U., Corbiere, A., Durand, I., Ebersbach, F., Fuda, J.-L., Garcia, N., Gerringa, L., Griffiths, B., Guigue, C., Guillerm, C., Jacquet, S., Jeandel, C., Laan, P., Lefevere, D., Lo Monaco, C., Malits, A., Mosseri, J., Obermosterer, I., Park, Y.-H., Picheral, M., Pondaven, P., Remenyi, T., Sandroni, V., Sarthou, G., Savoye, N., Scouarnec, L., Souhaut, M., Thuiller, D., Timmermans, K., Trull, T., Uitz, J., van Beek, P., Veldhuis, M., Vincent, D., Viollier, E., Vong, L., and Wagener, T. 2007. Effect of natural iron fertilization on carbon sequestration in the Southern Ocean. Nature 446: 1070–1074.
Boyd, P.W., Jickells, T., Law, C.S., Blain, S., Boyle, E.A., Buesseler, K.O., Coale, K.H., Cullen, J.J., de Baar, H.J.W., Follows, M., Harvey, M., Lancelot, C., Levasseur, M., Owens, N.P.J., Pollard, R., Rivkin, R.B., Sarmiento, J., Schoemann, V., Smetacek, V., Takeda, S., Tsuda, A., Turner, S., and Watson, A.J. 2007. Mesoscale iron enrichment experiments 1993–2005: synthesis and future directions. Science 315: 612–617.
Breitbarth, E., Bellerby, R.J., Neill, C.C., Ardelan, M.V., Meyerhofer, M., Zollner, E., Croot, P.L., and Riebesell, U. 2010. Ocean acidification affects iron speciation during a coastal seawater mesocosm experiment. Biogeosciences 7: 1065–1073.
Bruland, K.W., Rue, E.L., and Smith, G.J. 2001. Iron and macronutrients in California coastal upwelling regimes: implications for diatom blooms. Limnology and Oceanography 46: 1661–1674.
Fei, X.G. 2004. Solving the coastal eutrophication problem by large scale seaweed cultivation. Hydrobiologia 512: 145–151. Halloran, P.R., Hall, I.R., Colmenero-Hidalgo, E., and Rickaby, R.E.M. 2008. Evidence for a multi-species coccolith volume change over the past two centuries: understanding a potential ocean acidification response. Biogeosciences 5: 1651–1655.
Gao, K., Aruga, Y., Asada, K., Ishihara, T., Akano, T., and Kiyohara, M. 1991. Enhanced growth of the red alga Porphyra yezoensis Ueda in high CO2 concentrations. Journal of Applied Phycology 3: 356–362.
Gordillo, F.J.L., Niell, F.X., and Figueroa, F.L. 2001. Non-photosynthetic enhancement of growth by high CO2 level in the nitrophilic seaweed Ulva rigida C. Agardh (Chlorophyta). Planta 213: 64–70.
Hutchins, D.A. and Bruland, K.W. 1998. Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime. Nature 393: 561–564.
Iglesias-Rodriguez, M.D., Halloran, P.R., Rickaby, R.E.M., Hall, I.R., Colmenero-Hidalgo, E., Gittins, J.R., Green, D.R.H., Tyrrell, T., Gibbs, S.J., von Dassow, P., Rehm, E., Armbrust, E.V., and Boessenkool, K.P. 2008. Phytoplankton calcification in a high-CO2 world. Science 320: 336–340.
Jacobson, M.Z. 2005. Studying ocean acidification with conservative, stable numerical schemes for non-equilibrium air-ocean exchange and ocean equilibrium chemistry. Journal of Geophysical Research 110: 10.1029/2004JD005220.
Jiang, Z.J., Huang, X.-P., and Zhang, J.-P. 2010. Effects of CO2 enrichment on photosynthesis, growth, and biochemical composition of seagrass Thalassia hemprichii (Ehrenb.) Aschers. Journal of Integrative Plant Biology 52: 904–913.
Kuroyanagi, A., Kawahata, H., Suzuki, A., Fujita, K., and Irie, T. 2009. Impacts of ocean acidification on large benthic foraminifers: Results from laboratory experiments. Marine Micropaleontology 73: 190–195.
Langer, G., Geisen, M., Baumann, K.-H., Klas, J. , Riebesell, U., Thoms, S., and Young, J.R. 2006. Species-specific responses of calcifying algae to changing seawater carbonate chemistry. Geochemistry, Geophysics, Geosystems 7: 10.1029/2005GC001227.
Langer, G., Gussone, N., Nehrke, G., Riebesell, U., Eisenhauer, A., and Thoms, S. 2007. Calcium isotope fractionation during coccolith formation in Emiliania huxleyi: Independence of growth and calcification rate. Geochemistry, Geophysics, Geosystems 8: 10.1029/2006GC001422.
Langer, G., Nehrke, G., Probert, I., Ly, J., and Ziveri, P. 2009. Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences Discussions 6: 4361–4383.
Lombard, F., da Rocha, R.E., Bijma, J., and Gattuso, J.-P. 2010. Effect of carbonate ion concentration and irradiance on calcification in planktonic foraminifera. Biogeosciences 7: 247–255.
Mercado, J.M., Javier, F., Gordillo, L., Niell, F.X., and Figueroa, F.L. 1999. Effects of different levels of CO2 on photosynthesis and cell components of the red alga Porphyra leucosticia. Journal of Applied Phycology 11: 455–461. Short, F.T., Carruthers, T.J., Dennison, W.C., and Waycott, M. 2007. Global seagrass distribution and diversity: a bioregional model. Journal of Experimental Marine Biology and Ecology 350: 3–20.
Ozturk, M., Steinnes, E., and Sakshaug, E. 2002. Iron speciation in the Trondheim Fjord from the perspective of iron limitation for phytoplankton. Estuarine, Coastal and Shelf Science 55: 197–212.
Pollard, R.T., Salter, I., Sanders, R.J., Lucas, M.I., Moore, C.M., Mills, R.A., Statham, P.J., Allen, J.T., Baker, A.R., Bakker, D.C.E., Charette, M.A., Fielding, S., Fones, G.R., French, M., Hickman, A.E., Holland, R.J., Hughes, J.A., Jickells, T.D., Lampitt, R.S., Morris, P.J., Nedelec, F.H., Nielsdottir, M., Planquette, H., Popova, E.E., Poulton, A.J., Read, J.F., Seeyave, S., Smith, T., Stinchcombe, M., Taylor, S., Thomalla, S., Venables, H.J., Williamson, R., and Zubkov, M.V. 2009. Southern Ocean deep-water carbon export enhanced by natural iron fertilization. Nature 457: 577–580.
Riebesell, U., Schulz, K., Bellerby, R., Botros, M., Fritsche, P., Meyerhofer, M., Neill, C., Nondal, G., Oschlies, A., Wohlers, J., and Zollner, E. 2007. Enhanced biological carbon consumption in a high CO2 ocean. Nature 450: 545–548.
Rost, B., Riebesell, U., Burkhart, S., and Sultemeyer, D. 2003. Carbon acquisition of bloom-forming marine phytoplankton. Limnology and Oceanography 48: 55–67.
Schiebel, R. 2002. Planktic foraminiferal sedimentation and the marine calcite budget. Global Biogeochemical Cycles 16: 1010.1029/2001GB001459.
Schulz, K.G., Riebesell, U., Bellerby, R.G.J., Biswas, H., Meyerhofer, M., Muller, M.N., Egge, J.K., Nejstgaard, J.C., Neill, C., Wohlers, J., and Zollner, E. 2008. Build-up and decline of organic matter during PeECE III. Biogeosciences 5: 707–718.
Stoll, H. 2009. A biogeochemist sees the value of diversity in a changing ocean. Nature 460: 935.
Tans, P. 2009. An accounting of the observed increase in oceanic and atmospheric CO2 and an outlook for the future. Oceanography 22: 26–35.
Wyatt, N.J., Kitidis, V., Woodward, E.M.S., Rees, A.P., Widdicombe, S., and Lohan, M. 2010. Effects of high CO2 on the fixed nitrogen inventory of the Western English Channel. Journal of Plankton Research 32: 631–641.
Xu, Z., Zou, D., and Gao, K. 2010. Effects of elevated CO2 and phosphorus supply on growth, photosynthesis and nutrient uptake in the marine macroalga Gracilaria lemaneiformis (Rhodophyta). Botanica Marina 53: 123–129.
Yang, H., Zhou, Y., Mao, Y., Li, X., Liu, Y., and Zhang, F. 2005. Growth characters and photosynthetic capacity of Gracilaria lemaneiformis as a biofilter in a shellfish farming area in Sanggou Bay, China. Journal of Applied Phycology 17: 199–206.
Yang, Y.F., Fei, X.G., Song, J.M., Hu, H.Y., Wang, G.C., and Chung, I.K. 2006. Growth of Gracilaria lemaneiformis under different cultivation conditions and its effects on nutrient removal in Chinese coastal waters. Aquaculture 254: 248–255.
Zeebe, R.E. and Wolf-Gladrow, D.A. 2001. CO2 in Seawater: Equilibrium, Kinetics, Isotopes. Amsterdam, Netherlands: Elsevier Oceanographic Book Series.
Zhou, Y., Yang, H., Hu, H., Liu, Y., Mao, Y., Zhou, H., Xu, X., and Zhang, F. 2006. Bioremediation potential of the macroalga Gracilaria lemaneiformis (Rhodophyta) integrated into fed fish culture in coastal waters of north China. Aquaculture 252: 264–276.
Zou, D. 2005. Effects of elevated atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in the economic brown seaweed, Hizikia fusiforme (Sargassaceae, Phaeophyta). Aquaculture 250: 726–735.
Zou, D., Xia, J., and Yang, Y. 2004. Photosynthetic use of exogenous inorganic carbon in the agarophyte Gracilaria lemaneiformis (Rhodophyta). Aquaculture 237: 421–431.