Abstract
Although anthropogenic influences such as global warming, overfishing, and eutrophication may contribute to jellyfish blooms, little is known about the effects of ocean acidification on jellyfish. Most medusae form statoliths of calcium sulfate hemihydrate that are components of their balance organs (statocysts). This study was designed to test the effects of pH (7.9, within the average current range, 7.5, expected by 2100, and 7.2, expected by 2300) combined with two temperatures (9 and 15°C) on asexual reproduction and statolith formation of the moon jellyfish, Aurelia labiata. Polyp survival was 100% after 122 d in seawater in all six temperature and pH combinations. Because few polyps at 9°C strobilated, and temperature effects on budding were consistent with published results, we did not analyze data from those three treatments further. At 15°C, there were no significant effects of pH on the numbers of ephyrae or buds produced per polyp or on the numbers of statoliths per statocyst; however, statolith size was significantly smaller in ephyrae released from polyps reared at low pH. Our results indicate that A. labiata polyps are quite tolerant of low pH, surviving and reproducing asexually even at the lowest tested pH; however, the effects of small statoliths on ephyra fitness are unknown. Future research on the behavior of ephyrae with small statoliths would further our understanding of how ocean acidification may affect jellyfish survival in nature.
This is a preview of subscription content, access via your institution.



References
Arai, M. N., 1997. A Functional Biology of Scyphozoa. Chapman & Hall, London.
Attrill, M. J. & M. Edwards, 2008. Reply to Haddock. S.H.D., reconsidering evidence for potential climate-related increases in jellyfish. Limnology and Oceanography 53: 2763–2766.
Attrill, M. J., J. Wright & M. Edwards, 2007. Climate-related increases in jellyfish frequency suggest a more gelatinous future for the North Sea. Limnology and Oceanography 52: 480–485.
Becker, A., I. Sotje, C. Paulmann, F. Beckmann, T. Donath, R. Boese, O. Prymak, H. Tiemann & M. Epple, 2005. Calcium sulfate hemihydrate is the inorganic mineral in statoliths of scyphozoan medusae (Cnidaria). Dalton Transactions 1545–1550.
Bindoff, N. L., J. Willebrand, V. Artale, A. Cazenave, J. Gregory, S. Gulev, K. Hanawa, C. Le Quéré, S. Levitus, Y. Nojiri, C. K. Shum, L. D. Talley & A. Unnikrishnan, 2007. Observations: oceanic climate change and sea level. In Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor & H. L. Miller (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, UK and New York, NY, USA.
Brodeur, R. D., M. B. Decker, L. Ciannelli, J. E. Purcell, N. A. Bond, P. J. Stabeno, E. Acuna & G. L. Hunt Jr, 2008a. Rise and fall of jellyfish in the eastern Bering Sea in relation to climate regime shifts. Progress in Oceanography 77: 103–111.
Brodeur, R. D., C. L. Suchman, D. C. Reese, T. W. Miller & E. A. Daly, 2008b. Spatial overlap and trophic interactions between pelagic fish and large jellyfish in the northern California Current. Marine Biology 154: 649–659.
Caldeira, K. & M. E. Wickett, 2003. Anthropogenic carbon and ocean pH. Nature 425: 365.
Condon, R. H., M. B. Decker & J. E. Purcell, 2001. Effects of low dissolved oxygen on survival and asexual reproduction of scyphozoan polyps (Chrysaora quinquecirrha). Hydrobiologia 451: 89–95.
Doney, S. C., V. J. Fabry, R. A. Feely & J. A. Kleypas, 2009. Ocean acidification: the other CO2 problem. Annual Review of Marine Science 1: 162–192.
Fabry, V. J., B. A. Seibel, R. A. Feely & J. C. Orr, 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science 65: 414–432.
Feely, R. A., C. L. Sabine, K. Lee, W. Berelson, J. Kleypas, V. J. Fabry & F. J. Millero, 2004. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305: 362–366.
Forster, P., V. Ramaswamy, P. Artaxo, T. Berntsen, R. Betts, D. W. Fahey, J. Haywood, J. Lean, D. C. Lowe, G. Myhre, J. Nganga, R. Prinn, G. Raga, M. Schulz & R. Van Dorland, 2007. Changes in atmospheric constituents and in radiative forcing. In Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor & H. L. Miller (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, UK and New York, NY, USA.
Gamst, G., L. S. Meyers & A. J. Guarino, 2008. Analysis of Variance Designs: A Conceptual and Computational Approach with SPSS and SAS. Cambridge University Press, Cambridge.
Gattuso, J.-P. & H. Lavigne, 2009. Technical note: approaches and software tools to investigate the impact of ocean acidification. Biogeosciences 6: 2121–2133.
Gattuso, J.-P., M. Frankignoulle, I. Bourge, S. Romaine & R. W. Buddemeier, 1998. Effect of calcium carbonate saturation of seawater on coral calcification. Global and Planetary Change 18: 37–46.
Gu, L., M. Guo, H.-y. Lu, Z.-z. Sun & Y.-z. Lei, 2005. The physical-chemical factors affecting jellyfish Rhopilema esculenta breeding. Journal of Dalian Fisheries University 20: 41–44.
Haddock, H. S. D., 2008. Reconsidering evidence for potential climate-related increases in jellyfish. Limnology and Oceanography 53: 2759–2762.
Hayashi, K., J. Kita & A. Ishimatsu, 2004. Comparison of the acid–base responses to CO2 and acidification in Japanese flounder (Paralichthys olivaceus). Marine Pollution Bulletin 49: 1062–1065.
Holst, S., I. Sotje & H. Tiemann, 2007. Life cycle of the rhizostome jellyfish Rhizostoma octopus (L.) (Scyphozoa, Rhizostomeae), with studies on cnidocysts and statoliths. Marine Biology 151: 1695–1710.
Jokiel, P. L., K. S. Rodgers, I. B. Kuffner, A. J. Anderson, E. F. Fox & F. T. Mackenzie, 2008. Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27: 473–483.
Keppel, G. & T. D. Wickens, 2004. Design and Analysis: A Researcher’s Handbook, 4th ed. Prentice Hall, Upper Saddle River.
Kikkawa, T., J. Kita & A. Ishimatsu, 2004. Comparison of the lethal effect of CO2 and acidification on red sea bream (Pagrus major) during the early developmental stages. Marine Pollution Bulletin 48: 108–110.
Kleypas, J. A., R. W. Buddemeier, D. Archer, J.-P. Gattuso, C. Langdon & B. N. Opdyke, 1999. Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284: 118–120.
Kuffner, I. B., A. J. Anderson, P. L. Jokiel, K. S. Rodgers & F. T. Mackenzie, 2008. Decreased abundance of crustose coralline algae due to ocean acidification. Nature Geoscience 1: 114–117.
Langdon, C., T. Takahashi, C. Sweeney, D. Chipman & J. Goddard, 2000. Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Global Biogeochemical Cycles 14: 639–654.
Liu, W.-C., W.-T. Lo, J. E. Purcell & H.-H. Chang, 2009. Effects of temperature and light intensity on asexual reproduction of the scyphozoan, Aurelia aurita (L.) in Taiwan. Hydrobiologia 612: 247–258.
Lucas, C. H., 2001. Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment. Hydrobiologia 451: 229–246.
Lynam, C. P., S. J. Hay & A. S. Brierley, 2004. Interannual variability in abundance of North Sea jellyfish and links to the North Atlantic Oscillation. Limnology and Oceanography 49: 637–643.
Ma, X. & J. E. Purcell, 2005. Temperature, salinity and prey effects on polyp versus medusa bud production by the invasive hydrozoan Moerisia lyonsi. Marine Biology 147: 225–234.
Metzger, R., F. J. Sartoris, M. Langenbuch & H. O. Portner, 2007. Influence of elevated CO2 concentrations on thermal tolerance of the edible crab Cancer paguris. Journal of Thermal Biology 32: 144–151.
Michaelidis, B., C. Ouzounis, A. Paleras & H. O. Portner, 2005. Effects of long-term moderate hypercapnia on acid–base balance and growth rate in marine mussels Mytilus galloprovincialis. Marine Ecology and Progress Series 293: 109–118.
Mills, C. E., 2001. Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia 451: 55–68.
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. Monfray, A. Mouchet, R. G. Najjar, G.-K. Plattner, K. B. Rodgers, C. L. Sabine, J. L. Sarmiento, R. Schlitzer, R. D. Slater, I. J. Totterdell, M.-F. Weirig, Y. Yamanaka & A. Yool, 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681–686.
Palmer, M., 1992. Standard Operating Procedure for GLNPO Total Alkalinity Titration. United States Environmental Protection Agency, Chicago.
Portner, H. O., M. Langenbuch & B. Michaelidis, 2005. Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: From Earth history to global change. Journal of Geophysical Research 110: C09S10.
Purcell, J. E., 1997. Pelagic cnidarians and ctenophores as predators: selective predation, feeding rates and effects on prey populations. Annales de l’Institut océanographique, Paris 73: 125–137.
Purcell, J. E., 2005. Climate effects on formation of jellyfish and ctenophore blooms: a review. Journal of the Marine Biological Association of the United Kingdom 85: 461–476.
Purcell, J. E., 2007. Environmental effects on asexual reproduction rates of the scyphozoan Aurelia labiata. Marine Ecology Progress Series 348: 183–196.
Purcell, J. E. & J. J. Grover, 1990. Predation and food limitation as causes of mortality in larval herring at a spawning ground in British Columbia. Marine Ecology Progress Series 59: 55–61.
Purcell, J. E. & M. V. Sturdevant, 2001. Prey Selection and dietary overlap among zooplanktivorous jellyfish and juvenile fishes in Prince William Sound, Alaska. Marine Ecology Progress Series 210: 67–83.
Purcell, J. E., J. R. White, D. A. Nemazie & D. A. Wright, 1999. Temperature, salinity and food effects on asexual reproduction and abundance of the scyphozoan Chrysaora quinquecirrha. Marine Ecology Progress Series 180: 187–196.
Purcell, J. E., S.-i. Uye & W.-T. Lo, 2007. Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Marine Ecology Progress Series 350: 153–174.
Rabalais, N. N., R. E. Turner & W. J. Wiseman Jr., 2002. Gulf of Mexico hypoxia A.K.A. “the dead zone”. Annual Review of Ecology and Systematics 33: 235–263.
Richardson, A. J. & M. J. Gibbons, 2008. Are jellyfish increasing in response to ocean acidification? Limnology and Oceanography 53: 2040–2045.
Riebesell, U., I. Zondervan, B. Rost, P. D. Tortell, R. E. Zeebe & F. M. M. Morel, 2000. Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407: 364–367.
Rost, B., I. Zondervan & D. Wolf-Gladrow, 2008. Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions, and research directions. Marine Ecology Progress Series 373: 227–237.
Royal Society, 2005. Ocean Acidification Due to Increasing Atmospheric Carbon Dioxide. The Royal Society, London.
Shirayama, Y. & H. Thornton, 2005. Effect of increased atmospheric CO2 on shallow water marine benthos. Journal of Geophysical Research 110: C09S08.
Spangenberg, D. B., 1968. Statolith differentiation in Aurelia aurita. Journal of Experimental Zoology 169: 487–500.
Spangenberg, D. B., 1976. Intracellular statolith synthesis in Aurelia aurita. In Watabe, N. & K. Wilbur (eds), The Mechanisms of Mineralization in the Invertebrates and Plants. University of South Carolina Press, Columbia: 231–248.
Spangenberg, D. B., 1984. Effects of exogenous thyroxine on statolith synthesis and resorption in Aurelia. American Zoologist 24: 917–923.
Spangenberg, D. B. & C. W. Beck, 1968. Calcium sulfate dehydrate statoliths in Aurelia. Transactions of the American Microscopical Society 8: 329–335.
Spangenberg, D. B. & C. W. Beck, 1972. Tetracycline effects on statolith and nematocyst differentiation in Aurelia. Calcified Tissue Research 9: 122–133.
Thuesen, E. V., L. D. Rutherford Jr., P. L. Brommer, K. Garrison, M. A. Gutowska & T. Towanda, 2005. Intragel hypoxia promotes hypoxia tolerance of scyphomedusae. The Journal of Experimental Biology 208: 2475–2482.
Acknowledgments
We thank Dr. V. J. Fabry for inviting J. E. P. to the Ocean Carbon and Biogeochemistry Scoping Workshop on Ocean Acidification Research in 2007, and her advice on methodology for this research. We thank Drs. Gisele Muller-Parker, Benjamin Miner, and Brian Bingham for their valuable comments. We are indebted to the following people for their assistance; Rachel Garcia, Ritupreet Virk, Brandy Carpenter, Jen Moore, Dr. Gary Winans, Nathan Schwarck, Gene McKeen, Carissa Haug, Jeannie Gilbert, Peter Thut, Chandler Colahan, Alyssa Gehman, Sylvia Graham, Lauren Chomiczewski, and Carmen Guerra. Jellyfish polyps were provided by the Seattle Aquarium with help from Kathryn Kegel and Roland Anderson. We also thank Dr. K. L. Van Alstyne for sharing her information on diel intertidal pH levels. Financial support was provided by Western Washington University through the RSP Fund for the Enhancement of Graduate Research and the Biology Faculty Fellowship Fund.
Author information
Authors and Affiliations
Corresponding author
Additional information
Guest editors: J. E. Purcell & Dror Angel / Jellyfish Blooms: New Problems and Solutions
Rights and permissions
About this article
Cite this article
Winans, A.K., Purcell, J.E. Effects of pH on asexual reproduction and statolith formation of the scyphozoan, Aurelia labiata . Hydrobiologia 645, 39–52 (2010). https://doi.org/10.1007/s10750-010-0224-9
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-010-0224-9
Keywords
- Jellyfish
- Ocean acidification
- Statolith
- pH
- Reproduction