Prolonged exposure to elevated CO2 promotes growth of the algal symbiont Symbiodinium muscatinei in the intertidal sea anemone Anthopleura elegantissima

Biology Open

Volumn 1, Issue 7, 2012, Pages 615-621

  Towanda, Trisha ^a,b   Thuesen, Erik V ^a  

^a EVERGREEN STATE COLLEGE   (United States)

^b UNIVERSITY OF RHODE ISLAND   (United States)

Author keywords

Anthopleura elegantissima; Carbon dioxide; CZAR; Intertidal; Metabolic rate; Ocean acidification; Photosynthesis; Zooxanthellae

Indexed keywords

EID: 84964816566     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.2012521     Document Type: Article

References (73)

1. Allemand, D., Furla, P. and Bénazet-Tambutté, S. (1998). Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can. J. Bot. 76, 925-941.
2. Anthony, K. R. N., Kline, D. I., Diaz-Pulido, G., Dove, S. and Hoegh-Guldberg, O. (2008). Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc. Natl. Acad. Sci. USA 105, 17442-17446.
3. Ayre, D. J. and Grosberg, R. K. (1995). Aggression, habituation, and clonal coexistence in the sea anemone Anthopleura elegantissima. Am. Nat. 146, 427-453.
4. Ayre, D. J. and Grosberg, R. K. (2005). Behind anemone lines: factors affecting division of labour in the social cnidarian Anthopleura elegantissima. Anim. Behav. 70, 97-110.
5. Baghdasarian, G. and Muscatine, L. (2000). Preferential expulsion of dividing algal cells as a mechanism for regulating algal-cnidarian symbiosis. Biol. Bull. 199, 278-286.
6. 2 world: impacts of global climate change on marine phytoplankton. Plant Ecol. Divers. 2, 191-205.
7. Bidwell, J. P. and Spotte, S. (1985). Artificial Seawaters: Formulas And Methods. Boston, MA, USA: Jones and Bartlett Publishers.
8. Caldeira, K. and Wickett, M. E. (2005). Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J. Geophys. Res. 110, C09S04.
9. Childress, J. J. and Seibel, B. A. (1998). Life at stable low oxygen levels: adaptations of animals to oceanic oxygen minimum layers. J. Exp. Biol. 201, 1223-1232.
10. Crawley, A., Kline, D. I., Dunn, S., Anthony, K. and Dove, S. (2010). The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Glob. Change Biol. 16, 851-863.
11. Fabry, V. J., Seibel, B. A., Feely, R. A. and Orr, J. C. (2008). Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Sci. 65, 414-432.
12. Feely, R. A., Sabine, C. L., Hernandez-Ayon, J. M., Ianson, D. and Hales, B. (2008). Evidence for upwelling of corrosive "acidified" water onto the continental shelf. Science 320, 1490-1492.
13. Fitt, W. K., Pardy, R. L. and Littler, M. M. (1982). Photosynthesis, respiration, and contribution to community productivity of the symbiotic sea anemone Anthopleura elegantissima (Brandt, 1835). J. Exp. Mar. Biol. Ecol. 61, 213-232.
14. Frankignoulle, M., Abril, G., Borges, A., Bourge, I., Canon, C., Delille, B., Libert, E. and Théate, J. M. (1998). Carbon dioxide emission from European estuaries. Science 282, 434-436.
15. Furla, P., Allemand, D., Shick, J. M., Ferrier-Pagès, C., Richier, S., Plantivaux, A., Merle, P. L. and Tambutté, S. (2005). The symbiotic anthozoan: A physiological chimera between alga and animal. Integr. Comp. Biol. 45, 595-604.
16. Ganning, B. (1971). Studies on chemical, physical and biological conditions in Swedish rockpool ecosystems. Ophelia 9, 51-105.
17. 2 on growth and photosynthesis of the red algae Gracilaria sp. and G. chilensis. J. Appl. Phycol. 5, 563-571.
18. 2. Mar. Ecol. Prog. Ser. 373, 303-309.
19. Hall-Spencer, J. M., Rodolfo-Metalpa, R., Martin, S., Ransome, E., Fine, M., Turner, S. M., Rowley, S. J., Tedesco, D. and Buia, M. C. (2008). Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454, 96-99.
20. Hansen, P. J., Lundholm, N. and Rost, B. (2007). Growth limitation in marine red-tide dinoflagellates: effects of pH versus inorganic carbon availability. Mar. Ecol. Prog. Ser. 334, 63-71.
21. Hinga, K. R. (2002). Effects of pH on coastal marine phytoplankton. Mar. Ecol. Prog. Ser. 238, 281-300.
22. Holm-Hansen, O. and Riemann, B. (1978). Chlorophyll a determination: improvements in methodology. Oikos 30, 438-447.
23. 2 enrichment on photosynthesis, growth, and biochemical composition of seagrass Thalassia hemprichii (Ehrenb.) Aschers. J. Integr. Plant Biol. 52, 904-913.
24. Kempe, S. (1982). Valdivia cruise, October 1981: carbonate equilibria in the estuaries of Elbe, Weser, Ems and in the Southern German Bight. In Transport Of Carbon And Minerals In Major World Rivers, Part 1. (ed. E. T. Degens). Hamburg, Germany: Geologisch-Palaontologischen Institut der Universitat Hamburg.
25. 3 and daily climatic variation. Environ. Pollut. 158, 1000-1007.
26. 2 on the seaweed Lomentaria articulata. Plant Cell Environ. 22, 1303-1310.
27. La Jeunesse, T. C. and Trench, R. K. (2000). Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol. Bull. 199, 126-134.
28. Lewis, L. A. and Muller-Parker, G. (2004). Phylogenetic placement of "zoochlorellae" (Chlorophyta), algal symbiont of the temperate sea anemone Anthopleura elegantissima. Biol. Bull. 207, 87-92.
29. Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
30. Lüthi, D., Le Floch, M., Bereiter, B., Blunier, T., Barnola, J. M., Siegenthaler, U., Raynaud, D., Jouzel, J., Fischer, H., Kawamura, K. et al. (2008). High-resolution carbon dioxide concentration record 650,000-800,000 years before present. Nature 453, 379-382.
31. Martin, S., Rodolfo-Metalpa, R., Ransome, E., Rowley, S., Buia, M. C., Gattuso, J. P. and Hall-Spencer, J. (2008). Effects of naturally acidified seawater on seagrass calcareous epibionts. Biol. Lett. 4, 689-692.
32. 2 enrichment and salinity. Chemosphere 81, 725-731.
33. McCloskey, L. R., Cove, T. G. and Verde, E. A. (1996). Symbiont expulsion from the anemone Anthopleura elegantissima (Brandt) (Cnidaria; Anthozoa). J. Exp. Mar. Biol. Ecol. 195, 173-186.
34. CO2. Aquat. Toxicol. 92, 30-37.
35. 2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6, 2313-2331.
36. Menden-Deuer, S. and Lessard, E. J. (2000). Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 45, 569-579.
37. Morris, S. and Taylor, A. C. (1983). Diurnal and seasonal variation in physicochemical conditions within intertidal rock pools. Estuar. Coast. Shelf Sci. 17, 339-355.
38. 2 on grapevine (Vitis vinifera L.): physiological and yield attributes. Vitis 48, 159-165.
39. Muller-Parker, G. and Davy, S. K. (2001). Temperate and tropical algal-sea anemone symbioses. Invertebr. Biol. 120, 104-123.
40. Muller-Parker, G., Pierce-Cravens, J. and Bingham, B. L. (2007). Broad thermal tolerance of the symbiotic dinoflagellate Symbiodinium muscatinei (Dinophyta) in the sea anemone Anthopleura elegantissima (Cnidaria) from northern latitudes. J. Phycol. 43, 25-31.
41. Muscatine, L., McCloskey, L. R. and Marian, R. E. (1981). Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol. Oceanogr. 26, 601-611.
42. 2 under cold cathode fluorescent lamps. Plant Cell Rep. 29, 273-283.
43. Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C., Feely, R. A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F. et al. (2005). Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681-686.
44. 2 enrichment: possible impacts of climate change and potential for remediation of coastal habitats. Mar. Ecol. Prog. Ser. 344, 1-13.
45. Pane, E. F. and Barry, J. P. (2007). Extracellular acid-base regulation during shortterm hypercapnia is effective in a shallow-water crab, but ineffective in a deep-sea crab. Mar. Ecol. Prog. Ser. 334, 1-9.
46. 2 maximum in the oxygen minimum zone (OMZ). Biogeosciences 8, 239-252.
47. 2 System Calculations. Oak Ridge, Tennessee: U.S. Department of Energy.
48. Richards, J. G. (2011). Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia. J. Exp. Biol. 214, 191-199.
49. 2 and temperature levels projected for the year 2100 AD. Biogeosciences 7, 289-300.
50. Schneider, K. and Erez, J. (2006). The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol. Oceanogr. 51, 1284-1293.
51. Secor, S. M. (2009). Specific dynamic action: a review of the postprandial metabolic response. J. Comp. Physiol. B 179, 1-56.
52. Secord, D. and Augustine, L. (2000). Biogeography and microhabitat variation in temperate algal-invertebrate symbioses: zooxanthellae and zoochlorellae in two Pacific intertidal sea anemones, Anthopleura elegantissima and A. xanthogrammica. Invertebr. Biol. 119, 139-146.
53. Seibel, B. A. and Walsh, P. J. (2003). Biological impacts of deep-sea carbon dioxide injection inferred from indices of physiological performance. J. Exp. Biol. 206, 641-650.
54. Shick, J. M. (1991). A Functional Biology Of Sea Anemones. London, UK: Chapman and Hall.
55. Shick, J. M. and Dykens, J. A. (1984). Photobiology of the symbiotic sea anemone Anthopleura elegantissima: photosynthesis, respiration, and behavior under intertidal conditions. Biol. Bull. 166, 608-619.
56. 2-related seawater acidification on extracellular acid-base balance in the velvet swimming crab Necora puber. Mar. Biol. 151, 1117-1125.
57. Thuesen, E. V., Rutherford, L. D., Jr, Brommer, P. L., Garrison, K., Gutowska, M. A. and Towanda, T. (2005). Intragel oxygen promotes hypoxia tolerance of scyphomedusae. J. Exp. Biol. 208, 2475-2482.
58. Trench, R. K. (1987). Dinoflagellates in non-parasitic symbioses. In The Biology Of Dinoflagellates (ed. F. J. R. Taylor), pp. 530-570. London, UK: Blackwell Scientific Publications.
59. Truchot, J. P. and Duhamel-Jouve, A. (1980). Oxygen and carbon dioxide in the marine intertidal environment: diurnal and tidal changes in rockpools. Respir. Physiol. 39, 241-254.
60. 2. ISME J. 5, 1438-1450.
61. Venn, A. A., Tambutté, E., Lotto, S., Zoccola, D., Allemand, D. and Tambutté, S. (2009). Imaging intracellular pH in a reef coral and symbiotic anemone. Proc. Natl. Acad. Sci. USA 106, 16574-16579.
62. Verde, E. A. and McCloskey, L. R. (1996a). Carbon budget studies of symbiotic cnidarian anemones - evidence in support of some assumptions. J. Exp. Mar. Biol. Ecol. 195, 161-171.
63. Verde, E. A. and McCloskey, L. R. (1996b). Photosynthesis and respiration of two species of algal symbionts in the anemone Anthopleura elegantissima (Brandt) (Cnidaria; Anthozoa). J. Exp. Mar. Biol. Ecol. 195, 187-202.
64. Verde, E. A. and McCloskey, L. R. (2001). A comparative analysis of the photobiology of zooxanthellae and zoochlorellae symbiotic with the temperate clonal anemone Anthopleura elegantissima (Brandt). I. Effect of temperature. Mar. Biol. 138, 477-489.
65. Verde, E. A. and McCloskey, L. R. (2002). A comparative analysis of the photobiology of zooxanthellae and zoochlorellae symbiotic with the temperate clonal anemone Anthopleura elegantissima (Brandt) II. Effect of light intensity. Mar. Biol. 141, 225-239.
66. Verde, E. A. and McCloskey, L. R. (2007). A comparative analysis of the photobiology of zooxanthellae and zoochlorellae symbiotic with the temperate clonal anemone Anthopleura elegantissima (Brandt). III. Seasonal effects of natural light and temperature on photosynthesis and respiration. Mar. Biol. 152, 775-792.
67. Vitousek, P. M., Mooney, H. A., Lubchenco, J. and Melillo, J. M. (1997). Human domination of Earth's ecosystems. Science 277, 494-499.
68. Weis, V. M. (1993). Effect of dissolved inorganic carbon concentration on the photosynthesis of the symbiotic sea anemone Aiptasia pulchella Carlgren: role of carbonic anhydrase. J. Exp. Mar. Biol. Ecol. 174, 209-225.
69. Wilkerson, F. P., Muller-Parker, G. and Muscatine, L. (1983). Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnol. Oceanogr. 28, 1009-1014.
70. Wootton, J. T., Pfister, C. A. and Forester, J. D. (2008). Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proc. Natl. Acad. Sci. USA 105, 18848-18853.
71. 2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7, 2915-2923.
72. 2 and phosphorus supply on growth, photosynthesis and nutrient uptake in the marine macroalga Gracilaria lemaneiformis (Rhodophyta). Bot. Mar. 53, 123-129.
73. Yellowlees, D., Rees, T. A. V. and Leggat, W. (2008). Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ. 31, 679-694.