Browse > Article
http://dx.doi.org/10.4490/algae.2016.31.8.20

Species-specific responses of temperate macroalgae with different photosynthetic strategies to ocean acidification: a mesocosm study  

Kim, Ju-Hyoung (Faculty of Marine Applied Biosciences, Kunsan National University)
Kang, Eun Ju (Department of Oceanography, Chonnam National University)
Edwards, Matthew S. (Department of Biology, San Diego State University)
Lee, Kitack (School of Environmental Science and Engineering, Pohang University of Science and Technology)
Jeong, Hae Jin (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
Kim, Kwang Young (Department of Oceanography, Chonnam National University)
Publication Information
ALGAE / v.31, no.3, 2016 , pp. 243-256 More about this Journal
Abstract
Concerns about how ocean acidification will impact marine organisms have steadily increased in recent years, but there is a lack of knowledge on the responses of macroalgae. Here, we adopt an outdoor continuous-flowing mesocosm system designed for ocean acidification experiment that allows high CO2 conditions to vary with natural fluctuations in the environment. Following the establishment of the mesocosm, five species of macroalgae that are common along the coast of Korea (namely Ulva pertusa, Codium fragile, Sargassum thunbergii, S. horneri, and Prionitis cornea) were exposed to three different CO2 concentrations: ambient (×1) and elevated CO2 (2× and 4× ambient), over two-week period, and their ecophysiological traits were measured. Results indicated that both photosynthesis and growth exhibited species-specific responses to the different CO2 concentrations. Most notably, photosynthesis and growth increased in S. thunbergii when exposed to elevated CO2 conditions but decreased in P. cornea. The preference for different inorganic carbon species (CO2 and HCO3), which were estimated by gross photosynthesis in the presence and absence of the external carbonic anhydrase (eCA) inhibitor acetazolamide, were also found to vary among species and CO2 treatments. Specifically, the two Sargassum species exhibited decreased eCA inhibition of photosynthesis with increased growth when exposed to high CO2 conditions. In contrast, growth of U. pertusa and C. fragile were not notably affected by increased CO2. Together, these results suggest that the five species of macroalgae may respond differently to changes in ocean acidity, with species-specific responses based on their differentiated photosynthetic acclimation. Understanding these physiological changes might allow us to better predict future changes in macroalgal communities in a more acidic ocean.
Keywords
Codium fragile; eCA inhibition; macroalgae; mesocosm; ocean acidification; photosynthesis; Prionitis cornea; Sargassum horneri; Sargassum thunbergii; Ulva pertusa;
Citations & Related Records
Times Cited By KSCI : 5  (Citation Analysis)
연도 인용수 순위
1 Giordano, M., Beardall, J. & Raven, J. A. 2005. CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol. 56:99-131.   DOI
2 Giordano, M. & Maberly, S. C. 1989. Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81:534-539.   DOI
3 Golléty, C., Migné, A. & Davoult, D. 2008. Benthic metabolism on a sheltered rocky shore: role of the canopy in the carbon budget. J. Phycol. 44:1146-1153.   DOI
4 Gordillo, F. J. L., Figueroa, F. L. & Niell, F. X. 2003. Photon- and carbon-use efficiency in Ulva rigida at different CO2 and N levels. Planta 218:315-322.   DOI
5 Gordillo, F. J. L., Niell, F. X. & 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.   DOI
6 Hall-spencer, J. M., Rodolfo-Metalpa, R., Martin, S., Ransome, E., Fine, M., Turner, S. M., Rowley, S. J., Tedesco, D. & Buia, M. -C. 2008. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96-99.   DOI
7 Havenhand, J., Dupont, S. & Quinn, G. P. 2010. Designing ocean acidification experiments to maximize inference. In Riebesell, U., Fabry, V. J., Hansson, L. & Gattuso, J. -P. (Eds.) Guide to Best Practices in Ocean Acidification Research and Data Reporting. Publications Office of the European Union, Luxembourg, pp. 67-80.
8 Hepburn, C. D., Pritchard, D. W., Cornwall, C. E., McLeod, R. J., Beardall, J., Raven, J. A. & Hurd, C. L. 2011. Diversity of carbon use strategies in a kelp forest community: implications for a high CO2 ocean. Glob. Chang. Biol. 17:2488-2497.   DOI
9 Koch, M., Bowes, G., Ross, C. & Zhang, X. -H. 2013. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob. Chang. Biol. 19:103-132.   DOI
10 Kim, K. Y., Choi, T. S., Huh, S. H. & Garbary, D. J. 1998. Seasonality and community structure of subtidal benthic algae from Daedo Island, Southern Korea. Bot. Mar. 41:357-365.
11 Kroeker, K. J., Kordas, R. L., Crim, R., Hendriks, I. E., Ramajo, L., Singh, G. S., Duarte, C. M. & Gattuso, J. -P. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Chang. Biol. 19:1884-1896.   DOI
12 Lewis, E. & Wallace, D. W. R. 1998. Program developed for CO2 system calculation. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center. Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, TN, 33 pp.
13 Maberly, S. C. 1990. Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J. Phycol. 26:439-449.   DOI
14 Maberly, S. C., Raven, J. A. & Johnston, A. M. 1992. Discrimination between 12C and 13C by marine plants. Oecologia 91:481-492.   DOI
15 Mcleod, E., Chmura, G. L., Bouillon, S., Salm, R., Björk, M., Duarte, C. M., Lovelock, C. E., Schlesinger, W. H. & Silliman, B. R. 2011. A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front. Ecol. Environ. 9:552-560.   DOI
16 Brown, M. B., Edwards, M. S. & Kim, K. Y. 2014. Effects of climate change on the physiology of giant kelp, Macrocystis pyrifera, and grazing by purple urchin, Strongylocentrotus purpuratus. Algae 29:203-215.   DOI
17 Alexandre, A., Silva, J., Buapet, P., Björk, M. & Santos, R. 2012. Effects of CO2 enrichment on photosynthesis, growth, and nitrogen metabolism of the seagrass Zostera noltii. Ecol. Evol. 2:2625-2635.   DOI
18 Baker, N. R. & Oxborough, K. 2004. Chlorophyll fluorescence as a probe of photosynthetic productivity. In Papageorgiou, G. C. & Govindjee (Eds.) Chlorophyll a Fluorescence: A Signature of Photosynthesis. Springer, Dordrecht, pp. 65-82.
19 Millero, F. J., Zhang, J. -Z., Lee, K. & Campbell, D. M. 1993. Titration alkalinity of seawater. Mar. Chem. 44:153-165.   DOI
20 Murru, M. & Sandgren, C. D. 2004. Habitat matters for inorganic carbon acquisition in 38 species of red macroalgae (Rhodophyta) from Puget Sound, Washington, USA. J. Phycol. 40:837-845.   DOI
21 Choi, T. S. & Kim, K. Y. 2004. Spatial pattern of intertidal macroalgal assemblages associated with tidal levels. Hydrobiologia 512:49-56.   DOI
22 Hurlbert, S. H. 1984. Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 54:187-211.   DOI
23 Hernández-Ayón, J. M., Belli, S. L. & Zirino, A. 1999. pH, alkalinity and total CO2 in coastal seawater by potentiometric titration with a difference derivative readout. Anal. Chim. Acta 394:101-108.   DOI
24 Hofmann, L. C., Straub, S. & Bischof, K. 2012a. Competition between calcifying and noncalcifying temperate marine macroalgae under elevated CO2 levels. Mar. Ecol. Prog. Ser. 464:89-105.   DOI
25 Hofmann, L. C., Yildiz, G., Hanelt, D. & Bischof, K. 2012b. Physiological responses of the calcifying rhodophyte, Corallina officinalis (L.), to future CO2 levels. Mar. Biol. 159:783-792.   DOI
26 Israel, A. & Hophy, M. 2002. Growth, photosynthetic properties and Rubisco activities and amounts of marine macroalgae grown under current and elevated seawater CO2 concentrations. Glob. Chang. Biol. 8:831-840.   DOI
27 Israel, A., Katz, S., Dubinsky, Z., Merrill, J. E. & Friedlander, M. 1999. Photosynthetic inorganic carbon utilization and growth of Porphyra linearis (Rhodophyta). J. Appl. Phycol. 11:447-453.   DOI
28 Ní Longphuirt, S., Eschmann, C., Russell, C. & Stengel, D. B. 2013. Seasonal and species-specific response of five brown macroalgae to high atmospheric CO2. Mar. Ecol. Prog. Ser. 493:91-102.   DOI
29 Ji, Y. & Tanaka, J. 2002. Effect of desiccation on the photosynthesis of seaweeds from the intertidal zone in Honshu, Japan. Phycol. Res. 50:145-153.   DOI
30 Johnson, V. R., Russell, B. D., Fabricius, K. E., Brownlee, C. & Hall-Spencer, J. M. 2012. Temperate and tropical brown macroalgae thrive, despite decalcification, along natural CO2 gradients. Glob. Chang. Biol. 18:2792-2803.   DOI
31 Oilschläger, M. & Wiencke, C. 2013. Ocean acidification alleviates low-temperature effects on growth and photosynthesis of the red alga Neosiphonia harveyi (Rhodophyta). J. Exp. Bot. 64:5587-5597.   DOI
32 Olabarria, C., Arenas, F., Viejo, R. M., Gestoso, I., Vaz-Pinto, F., Incera, M., Rubal, M., Cacabelos, E., Veiga, P. & Sobrino, C. 2013. Response of macroalgal assemblages from rockpools to climate changes: effects of persistent increase in temperature and CO2. Oikos 122:1065-1079.   DOI
33 Petersen, J. E., Kennedy, V. S., Dennison, W. C. & Kemp, W. M. 2009. Enclosed experimental ecosystem and scale: tools for understanding and managing coastal ecosystem. Springer, New York, 222 pp.
34 Platt, T., Gallegos, C. L. & Harrison, W. G. 1980. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res. 38:687-701.
35 Raven, J. A., Beardall, J. & Giordano, M. 2014. Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms. Photosynth. Res. 121:111-124.   DOI
36 Duarte, C. M. & Cebrián, J. 1996. The fate of marine autotrophic production. Limnol. Oceanogr. 41:1758-1766.   DOI
37 Cornwall, C. E., Hepburn, C. D., McGraw, C. M., Currie, K. I., Pilditch, C. A., Hunter, K. A., Boyd, P. W. & Hurd, C. L. 2013. Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proc. Biol. Sci. 280:20132201.   DOI
38 Cornwall, C. E., Hepburn, C. D., Pritchard, D., Currie, K. I., McGraw, C. M., Hunter, K. A. & Hurd, C. L. 2012. Carbon-use strategies in macroalgae: differential responses to lowered pH and implications for ocean acidification. J. Phycol. 48:137-144.   DOI
39 Doney, S. C., Fabry, V. J., Feely, R. A. & Kleypas, J. A. 2009. Ocean acidification: the other CO2 problem. Annu. Rev. Mar. Sci. 1:169-192.   DOI
40 Falkenberg, L. J., Russell, B. D. & Connell, S. D. 2013. Contrasting resource limitations of marine primary producers: implications for competitive interactions under enriched CO2 and nutrient regimes. Oecologia 172:575-583.
41 Kang, E. J. & Kim, K. Y. 2016. Effects of future climate conditions on photosynthesis and biochemical component of Ulva pertusa (Chlorophyta). Algae 31:49-59.   DOI
42 Raven, J. A., Cockell, C. S. & De La Rocha, C. L. 2008. The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363:2641-2650.   DOI
43 Raven, J. A., Giordano, M., Beardall, J. & Marberly, S. C. 2011. Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynth. Res. 109:281-296.   DOI
44 Fu, F. -X., Warner, M. E., Zhang, Y., Feng, Y. & Hutchins, D. A. 2007. Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria). J. Phycol. 43:485-496.   DOI
45 Gao, K., Helbling, E. W., Häder, D. -P. & Hutchins, D. A. 2012. Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming. Mar. Ecol. Prog. Ser. 470:169-189.
46 Connell, S. D. & Russell, B. D. 2010. The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc. Biol. Sci. 277:1409-1415.   DOI
47 Kang, E. J., Kim, J.- H., Kim, K., Choi, H. -G. & Kim, K. Y. 2014. Re-evaluation of green tide-forming species in the Yellow Sea. Algae 29:267-277.   DOI
48 Kang, E. J., Kim, J. -H., Kim, K. & Kim, K. Y. 2016. Adaptations of a green tide forming Ulva linza (Ulvophyceae, Chlorophyta) to selected salinity and nutrients conditions mimicking representative environments in the Yellow Sea. Phycologia 55:210-218.   DOI
49 Kim, J. -H., Kang, E. J., Kim, K., Jeong, H. J., Lee, K., Edwards, M. S., Park, M. G., Lee, B. -G. & Kim, K. Y. 2015. Evaluation of carbon flux in vegetative bay based on ecosystem production and CO2 exchange driven by coastal autotrophs. Algae 30:121-137.   DOI
50 Kim, J. -H., Kang, E. J., Park, M. G., Lee, B. -G. & Kim, K. Y. 2011. Effects of temperature and irradiance on photosynthesis and growth of a green-tide-forming species (Ulva linza) in the Yellow Sea. J. Appl. Phycol. 23:421-432.   DOI
51 Kim, J. -H., Kim, K. Y., Kang, E. J., Lee, K., Kim, J. -M., Park, K. -T., Shin, K., Hyun, B. & Jeong, H. J. 2013a. Enhancement of photosynthetic carbon assimilation efficiency by phytoplankton in the future coastal ocean. Biogeosciences 10:7525-7535.   DOI
52 Xu, J. & Gao, K. 2012. Future CO2-induced ocean acidification mediates the physiological performance of a green tide alga. Plant Physiol. 160:1762-1769.   DOI
53 Kim, J. -H., Lam, S. M. N. & Kim, K. Y. 2013b. Photoacclimation strategies of the temperate coralline alga Corallina officinalis: a perspective on photosynthesis, calcification, photosynthetic pigment contents and growth. Algae 28:355-363.   DOI
54 Riebesell, U., Lee, K. & Nejstgaard, J. C. 2010. Pelagic mesocosms. In Riebesell, U., Fabry, V. J., Hansson, L. & Gattuso, J. -P. (Eds.) Guide to Best Practices in Ocean Acidification Research and Data Reporting. Publications Office of the European Union, Luxembourg, pp. 81-98.
55 Sobrino, C., Ward, M. L. & Neale, P. J. 2008. Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnol. Oceanogr. 53:494-505.   DOI
56 Widdicombe, S., Dupont, S. & Thorndyke, M. 2010. Laboratory experiments and benthic mesocosm studies. In Riebesell, U., Fabry, V. J., Hansson, L. & Gattuso, J. -P. (Eds.) Guide to Best Practices in Ocean Acidification Research and Data Reporting. Publications Office of the European Union, Luxembourg, pp. 113-122.