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Effects of climate change on the physiology of giant kelp, Macrocystis pyrifera, and grazing by purple urchin, Strongylocentrotus purpuratus

  • Brown, Matthew B. (Department of Biology, San Diego State University) ;
  • Edwards, Matthew S. (Department of Biology, San Diego State University) ;
  • Kim, Kwang Young (Department of Oceanography, Chonnam National University)
  • Received : 2014.07.30
  • Accepted : 2014.09.10
  • Published : 2014.09.15

Abstract

As global warming continues over the coming century, marine organisms will experience a warmer, more acidic ocean. Although these stressors may behave antagonistically or synergistically and will impact organisms both directly (i.e., physiologically) and indirectly (i.e., through altered species interactions), few studies have examined the complexities of these effects in combination. To address these uncertainties, we examined the independent and combined effects of elevated temperature and $pCO_2$ on the physiology of the adult sporophyte stage of giant kelp, Macrocystis pyrifera, and the grazing of the purple sea urchin Strongylocentrotus purpuratus. While elevating $pCO_2$ alone had no effect on M. pyrifera growth or photosynthetic carbon uptake, elevating temperature alone resulted in a significant reduction in both. However, when M. pyrifera was grown under elevated temperature and $pCO_2$ together, growth and photosynthetic carbon uptake significantly increased relative to ambient conditions, suggesting an interaction of these factors on photosynthetic physiology. S. purpuratus held under future conditions generally exhibited reduced growth, and smaller gonads than urchins held under present-day conditions. However, urchins fed kelp grown under future conditions showed higher growth rates, partially ameliorating this effect. Feeding rates were variable over the course of the experiment, with only the first feeding rate experiment showing significantly lower rates for urchins held under future conditions. Together, these data suggest that M. pyrifera may benefit physiologically from a warmer, more acidic (i.e., higher $pCO_2$) ocean while S. purpuratus will likely be impacted negatively. Given that kelp-urchin interactions can be important to kelp forest structure, changes to either of these populations may have serious consequences for many coastal environments.

Keywords

References

  1. Brennand, H. S., Soars, N., Dworjanyn, S. A., Davis, A. R. & Byrne, M. 2009. Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS One 5:e11372.
  2. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. 2004. Toward a metabolic theory of ecology. Ecology 85:1771-1789. https://doi.org/10.1890/03-9000
  3. Burrows, M. T., Schoeman, D. S., Richardson, A. J., Molinos, J. G., Hoffmann, A., Buckley, L. B., Moore, P. J., Brown, C. J., Bruno, J. F., Duarte, C. M., Halpern, B. S., Hoegh-Guldberg, O., Kappel, C. V., Kiessling, W., O'Connor, M. I., Pandolfi, J. M., Parmesan, C., Sydeman, W. J., Ferrier, S., Williams, K. J. & Poloczanska, E. S. 2014. Geographical limits to species-range shifts are suggested by climate velocity. Nature 507:492-495. https://doi.org/10.1038/nature12976
  4. Caldeira, K. & Wickett, M. 2003. Anthropogenic carbon and ocean pH. Nature 425:365. https://doi.org/10.1038/425365a
  5. Catarino, A. I., Bauwens, M. & Dubois, P. 2012. Acid-base balance and metabolic response of the sea urchin Paracentrotus lividus to different seawater pH and temperatures. Environ. Sci. Pollut. Res. Int. 19:2344-2353. https://doi.org/10.1007/s11356-012-0743-1
  6. Connell, S. D. & Russell, B. D. 2010. The direct effects of increasing $CO_2$ and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc. Biol. Sci. 277:1409-1415. https://doi.org/10.1098/rspb.2009.2069
  7. Crain, C. M., Kroeker, K. & Halpern, B. S. 2008. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11:1304-1315. https://doi.org/10.1111/j.1461-0248.2008.01253.x
  8. Cruz-Rivera, E. & Hay, M. E. 2000. Can quantity replace quality? Food choice, compensatory feeding, and fitness in marine mesograzers. Ecology 81:201-219. https://doi.org/10.1890/0012-9658(2000)081[0201:CQRQFC]2.0.CO;2
  9. Davison, I. 1987. Adaptation of photosynthesis in Laminaria saccharina (Phaeophyta) to changes in growth temperature. J. Phycol. 23:273-283. https://doi.org/10.1111/j.1529-8817.1987.tb04135.x
  10. Davison, I. R., Greene, R. M. & Podolak, E. J. 1991. Temperature acclimation of respiration and photosynthesis in the brown alga Laminaria saccharina. Mar. Biol. 110:449-454. https://doi.org/10.1007/BF01344363
  11. Dayton, P. K. 1985. Ecology of kelp communities. Ann. Rev. Ecol. Syst. 16:215-245. https://doi.org/10.1146/annurev.es.16.110185.001243
  12. Dean, T. A., Schroeter, S. C. & Dixon, J. D. 1984. Effects of grazing by two species of sea urchins (Strongylocentrotus franciscanus and Lytechinus anamesus) on recruitment and survival of two species of kelp (Macrocystis pyrifera and Pterygophora californica). Mar. Biol. 78:301-313. https://doi.org/10.1007/BF00393016
  13. Doney, S. C., Bopp, L. & Long, M. C. 2014. Historical and future trends in ocean climate and biogeochemistry. Oceanography 27:108-119. https://doi.org/10.5670/oceanog.2014.14
  14. Doney, S. C., Fabry, V. J., Feely, R. A. & Kleypas, J. A. 2009. Ocean acidification: the other $CO_2$ problem. Ann. Rev. Mar. Sci. 1:169-192. https://doi.org/10.1146/annurev.marine.010908.163834
  15. Estes, J. A. & Palmisano, J. F. 1974. Sea otters: their role in structuring nearshore communities. Science 185:1058-1060. https://doi.org/10.1126/science.185.4156.1058
  16. Falkenberg, L. J., Russell, B. D. & Connell, S. D. 2013. Future herbivory: the indirect effects of enriched $CO_2$ may rival its direct effects. Mar. Ecol. Prog. Ser. 492:85-95. https://doi.org/10.3354/meps10491
  17. Feely, R. A., Sabine, C. L., Lee, K., Berelson, W., Kleypas, J., Fabry, V. J. & Millero, F. J. 2004. Impact of anthropogenic $CO_2$ on the $CaCO_3$ system in the oceans. Science 305:362-366. https://doi.org/10.1126/science.1097329
  18. Gaitan-Espitia, J. D., Hancock, J. R., Padilla-Gamino, J. L., Rivest, E. B., Blanchette, C. A., Reed, D. C. & Hofmann, G. E. 2014. Interactive effects of elevated temperature and $pCO_2$ on early-life-history stages of the giant kelp Macrocystis pyrifera. J. Exp. Mar. Biol. Ecol. 457:51-58. https://doi.org/10.1016/j.jembe.2014.03.018
  19. Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. 2001. Effects of size and temperature on metabolic rate. Science 293:2248-2251. https://doi.org/10.1126/science.1061967
  20. Harley, C. D. G., Anderson, K. M., Demes, K. W., Jorve, J. P., Kordas, R. L., Coyle, T. A. & Graham, M. H. 2012. Effects of climate change on global seaweed communities. J. Phycol. 48:1064-1078. https://doi.org/10.1111/j.1529-8817.2012.01224.x
  21. Harrold, C. & Reed, D. C. 1985. Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66:1160-1169. https://doi.org/10.2307/1939168
  22. 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 $CO_2$ ocean. Glob. Chang. Biol. 17:2488-2497. https://doi.org/10.1111/j.1365-2486.2011.02411.x
  23. Hofmann, G. E., Smith, J. E., Johnson, K. S., Send, U., Levin, L. A., Micheli, F., Paytan, A., Price, N. N., Peterson, B., Takeshita, Y., Matson, P. G., Crook, E. D., Kroeker, K. J., Gambi, M. C., Ribest, E. B., Frieder, C. A., Yu, P. C. & Martz, T. R. 2011. High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLos One 6:e28983 https://doi.org/10.1371/journal.pone.0028983
  24. Hurlbert, S. H. 1984. Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 54:187-211. https://doi.org/10.2307/1942661
  25. Intergovernmental Panel on Climate Change. 2007. Technical summary. In Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K. B., Tignor, M. & Miller, H. L. (Eds.) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp. 1-91.
  26. Israel, A. & Hophy, M. 2002. Growth, photosynthetic properties and Rubisco activities and amounts of marine macroalgae grown under current and elevated seawater $CO_2$ concentrations. Glob. Chang. Biol. 8:831-840. https://doi.org/10.1046/j.1365-2486.2002.00518.x
  27. Jordan, D. B. & Ogren, W. L. 1984. The $CO_2$/$O_2$ specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase. Planta 161:308-313. https://doi.org/10.1007/BF00398720
  28. Kenner, M. C. 1992. Population dynamics of the sea urchin Strongylocentrotus purpuratus in a Central California kelp forest: recruitment, mortality, growth, and diet. Mar. Biol. 112:107-118. https://doi.org/10.1007/BF00349734
  29. Koch, M., Bowes, G., Ross, C. & Zhang, X. -H. 2013. Climate change and ocean acidifications effects on seagrasses and marine macroalgae. Glob. Chang. Biol. 19:103-132. https://doi.org/10.1111/j.1365-2486.2012.02791.x
  30. Konar, B., Edwards, M. S. & Estes, J. A. 2014. Biological interactions maintain the boundaries between kelp forests and urchin barrens in the Aleutian Archipelago. Hydrobiologia 724:91-107. https://doi.org/10.1007/s10750-013-1727-y
  31. Kurihara, H. 2008. Effects of $CO_2$-driven ocean acidification on the early developmental stages of invertebrates. Mar. Ecol. Prog. Ser. 373:275-284. https://doi.org/10.3354/meps07802
  32. Leinaas, H. P. & Christie, H. 1996. Effects of removing sea urchins (Strongylocentrotus droebachiensis): stability of the barren state and succession of kelp forest recovery in the east Atlantic. Oecologia 105:524-536. https://doi.org/10.1007/BF00330016
  33. Lemire, M. & Himmelman, J. H. 1996. Relation of food preference to fitness for the green sea urchin, Strongylocentrotus droebachiensis. Mar. Biol. 127:73-78. https://doi.org/10.1007/BF00993646
  34. Mann, K. H. 1977. Destruction of kelp-beds by sea-urchins: a cyclical phenomenon or irreversible degradation? Helgol. Weissenschaftliche Meeresunters. 30:455-467. https://doi.org/10.1007/BF02207854
  35. O'Connor, M. I. 2009. Warming strengthens an herbivore-plant interaction. Ecology 90:388-398. https://doi.org/10.1890/08-0034.1
  36. Parker, B. C. 1965. Translocation in the giant kelp Macrocystis I. rates, direction, quantity of $C^{14}$-labeled products and fluorescein. J. Phycol. 1:41-46. https://doi.org/10.1111/j.1529-8817.1965.tb04554.x
  37. Platt, T., Denman, K. L. & Jassby, A. D. 1975. The mathematical representation and prediction of phytoplankton productivity. Technical Report 523. Fisheries and Marine Services, Environment Canada, Ottawa, 110 pp.
  38. Poloczanska, E. S., Brown, C. J., Sydeman, W. J., Kiessling, W., Schoeman, D. S., Moore, P. J., Brander, K., Bruno, J. F., Buckley, L. B., Burrows, M. T., Duarte, C. M., Halpern, B. S., Holding, J., Kappel, C. V., O'Connor, M. I., Pandolfi, J. M., Parmesan, C., Schwing, F., Thompson, S. A. & Richardson, A. J. 2013. Global imprint of climate change on marine life. Nat. Clim. Chang. 3:919-925. https://doi.org/10.1038/nclimate1958
  39. Portner, H. -O. 2008. Ecosystem effects of ocean acidification in times of ocean warming: a physiologist's view. Mar. Ecol. Prog. Ser. 373:203-217. https://doi.org/10.3354/meps07768
  40. Ries, J. B., Cohen, A. L. & McCorkle, D. C. 2009. Marine calcifiers exhibit mixed responses to $CO_2$-induced ocean acidification. Geology 37:1131-1134. https://doi.org/10.1130/G30210A.1
  41. Roleda, M. Y., Morris, J. N., McGraw, C. M. & Hurd, C. L. 2012. Ocean acidification and seaweed reproduction: increased $CO_2$ ameliorates the negative effect of lowered pH on meiospore germination in the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae). Glob. Chang. Biol. 18:854-864. https://doi.org/10.1111/j.1365-2486.2011.02594.x
  42. Siikavuopio, S. I., Mortensen, A., Dale, T. & Foss, A. 2007. Effects of carbon dioxide exposure on feed intake and gonad growth in the green sea urchin, Strongylocentrotus droebachiensis. Aquaculture 266:97-101. https://doi.org/10.1016/j.aquaculture.2007.02.044
  43. Spicer, J. I., Widdicombe, S., Needhan, H. R. & Berge, J. A. 2011. Impact of $CO_2$-acidified seawater on the extracellular acid-base balance of the northern sea urchin Strongylocentrotus droebachiensis. J. Exp. Mar. Biol. Ecol. 407:19-25. https://doi.org/10.1016/j.jembe.2011.07.003
  44. Stiling, P. & Cornelissen, T. 2007. How does elevated carbon dioxide ($CO_2$) affect plant-herbivore interactions? A field experiment and meta-analysis of $CO_2$-mediated changes on plant chemistry and herbivore performance. Glob. Chang. Biol. 13:1823-1842. https://doi.org/10.1111/j.1365-2486.2007.01392.x
  45. Wernberg, T., Smale, D. A. & Thomsen, M. S. 2012. A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob. Chang. Biol. 18:1491-1498. https://doi.org/10.1111/j.1365-2486.2012.02656.x

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