Marine Biology

, Volume 152, Issue 4, pp 775–792 | Cite as

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

  • E. Alan VerdeEmail author
  • L. R. McCloskey
Research Article


The sea anemone Anthopleura elegantissima hosts two phylogenetically different symbiotic microalgae, a dinoflagellate Symbiodinium (zooxanthellae, ZX) and a chlorophyte (zoochlorellae, ZC). The photosynthetic productivity (P), respiration (R), and contribution of algal carbon translocated to the host (CZAR) in response to a year’s seasonal ambient changes of natural light and temperature are documented for both ZX- and ZC-bearing anemones. Light and temperature both affect photosynthesis, respiration, and CZAR, as well as various algal parameters; while there are evident seasonal differences, for the most part the relative effects on P, R, and CZAR by the two environmental variables cannot be determined. Net photosynthesis (Pn) of both ZX and ZC was significantly higher during spring and summer. During these seasons, the Pn of ZX was always greater than that of ZC. Regardless of algal symbiont, anemone respiration (R) was significantly higher during the spring and summer. The annual net carbon fixation rate of anemones with ZX and ZC was 325 and 276 mg C anemone−1 year−1, respectively, which translates to annual net community productivity rates of 92 and 60 g C m−1 year−1 for anemones with ZX or ZC, respectively. CZAR did not show a clear relationship with season; however the CZAR for ZX was always significantly greater than for ZC. Lower ZX growth rates, coupled with higher photosynthetic rates and higher CZAR estimates, compared to ZC, suggest that if A. elegantissima is simply carbon limited, ZX-bearing anemones should be the dominant symbiont in the field. However ZC-bearing anemones persist in low light and reduced temperature microhabitats, therefore more than the translocation of carbon from ZC must be involved. Given that global climate change will increase water temperatures, the potential for latitudinal range shifts of both ZC and ZX (S. californium and muscatinei) might be used as biological indicators of thermal shifts in the littoral zone of the Pacific Northwest.


Carotenoid Mitotic Index Intertidal Zone Total Chlorophyll Content Algal Density 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This research was supported by the Houston Underwater Club SeaSpace Scholarship and Sigma Xi Grants-in-aid of Research (to E.A.V.), National Science Foundation grant OCE-8303513 (to L.R.M.), and the Department of Biological Sciences and Marine Station of Walla Walla College. We express our thanks to G. Muller-Parker and the staff of Shannon Point Marine Center for use of equipment, to S. Perez, L. Hauck, and D. Cowles for their pre-submission review of this document, and to three anonymous reviewers whose comments and constructive criticisms helped to improve this paper.


  1. Albrecht M, Steiger S, Sandmann G (2001) Expression of a ketolase gene mediates the synthesis of canthaxanthin in Synechococcus leading to tolerance against photoinhibition, pigment degradation and UV-B sensitivity of photosynthesis. Photochem Photobiol 73:551–555CrossRefGoogle Scholar
  2. Augustine L, Muller-Parker G (1998) Selective predation by the mosshead sculpin Clinocottus globiceps on the sea anemone Anthopleura elegantissima and its two algal symbionts. Limnol Oceanogr 43:711–715CrossRefGoogle Scholar
  3. Bachman S, Muller-Parker G (2007) Viable algae released by the Dermasterias imbricata feeding on the symbiotic sea anemone Anthopleura elegantissima. Mar Biol 150:369–375CrossRefGoogle Scholar
  4. Banaszak AT, Trench RK (1995a) Effects of ultraviolet (UV) radiation on marine microalgal-invertebrate symbioses. I. Response of the algal symbionts in culture and in hospite. J Exp Mar Biol Ecol 194:213–232CrossRefGoogle Scholar
  5. Banaszak AT, Trench RK (1995b) Effects of ultraviolet (UV) radiation on marine microalgal–invertebrate symbioses. II. The synthesis of mycosporine-like amino acids in response to exposure to UV in Anthopleura elegantissima and Cassiopeia xamachana. J Exp Mar Biol Ecol 194:233–250CrossRefGoogle Scholar
  6. Barry JP, Baxter CH, Sagarin RD, Gilman SE (1995) Climate-related, long-term faunal changes in a California rocky intertidal community. Science 267:672–674CrossRefGoogle Scholar
  7. Bates A (2000) The intertidal distribution of two algal symbionts hosted by Anthopleura xanthogrammica (Brandt 1835). J Exp Mar Biol Ecol 249:249–262CrossRefGoogle Scholar
  8. Belda CA, Lucas JS, Yellowlees D (1993) Nutrient limitation in the giant clam zooxanthellae symbiosis: effects of nutrient supplements on growth of the symbiotic partners. Mar Biol 117:655–664CrossRefGoogle Scholar
  9. Bronstein JL (2001) The costs of mutualism. Am Zool 41:825–839Google Scholar
  10. Dykens JA, Shick JM (1984) Photobiology of the symbiotic sea anemone, Anthopleura elegantissima: defenses against photodynamic effects and seasonal photoacclimatization. Biol Bull 167:683–697CrossRefGoogle Scholar
  11. Engebretson HP, Muller-Parker G (1999) Translocation of photosynthetic carbon from two algal symbionts to the sea anemone Anthopleura elegantissima. Biol Bull 197:72–81CrossRefGoogle Scholar
  12. Fagoonee I, Wilson HB, Hassell MP, Turner JR (1999) The dynamics of zooxanthellae populations: a long-term study in the field. Science 283:843–845CrossRefGoogle Scholar
  13. Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals. BioScience 43:606–611CrossRefGoogle Scholar
  14. Falkowski PG, LaRoche J (1991) Acclimation to spectral irradiance in algae. J Phycol 27:8–14CrossRefGoogle Scholar
  15. Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685CrossRefGoogle Scholar
  16. Fitt WK, Pardy RL, Littler MM (1982) Photosynthesis, respiration, and contribution to community productivity of the symbiotic sea anemone Anthopleura elegantissima (Brandt, 1835). J Exp Mar Biol Ecol 61:213–232CrossRefGoogle Scholar
  17. Gotz T, Windhovel U, Boger P, Sandmann G (1999) Protection of photosynthesis against UV-B radiation by carotenoids in transformants of the cyanobacterium Synechococcus PCC7942. Plant Physiol 120:599–604CrossRefGoogle Scholar
  18. Graham DL (1989) Response of algal populations to nutrient conditions in Anthopleura elegantissima (Brandt). Master’s thesis, Walla Walla College, WashingtonGoogle Scholar
  19. Griffiths RJ (1977a) Thermal stress and the biology of Actinia equina L. (Anthozoa). J Exp Mar Biol Ecol 27:141–154CrossRefGoogle Scholar
  20. Griffiths RJ (1977b) Temperature acclimation in Actinia equina L. (Anthozoa). J Exp Mar Biol Ecol 28:285–292CrossRefGoogle Scholar
  21. Hand C (1955) The sea anemones of central California. Part II. The endomyarian and mesomyarian anemones. Wasmann J Biol 13:37–99Google Scholar
  22. Hannack K, Kestler P, Sicken O, Westheide W (1997) The influence of UV radiation on number and ultrastructure of the endosymbiotic dinoflagellates in the sea anemone Cereus pedunculatus (Anthozoa: Actinaria). Helgolander Meeresunters 51:487–502CrossRefGoogle Scholar
  23. Helmuth B (2002) How do we measure the environment? Linking intertidal thermal physiology and ecology through biophysics. Integ Comp Biol 42:837–845CrossRefGoogle Scholar
  24. Helmuth B, Harley CDG, Halpin PM, O’Donnell M, Hofmann GE, Blanchette CA (2002) Climate change and latitudinal patterns of intertidal thermal stress. Science 298:1015–1017CrossRefGoogle Scholar
  25. Helmuth BST, Hofmann G (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol Bull 201:374–384CrossRefGoogle Scholar
  26. Helmuth B, Kingsolver JG, Carrington E (2005) Biophysics, physiological ecology, and climate change: does mechanism matter? Ann Rev Physiol 67:177–201CrossRefGoogle Scholar
  27. Intergovernmental Panel on Climate Change (2007) Climate change 2007: the physical science basis.
  28. Jacques TG, Marshall N, Pilson MEQ (1983) Experimental ecology of the temperate scleractinian coral Astrangia danae. II. Effect of temperature, light intensity and symbiosis with zooxanthellae on metabolic rate and calcification. Mar Biol 76:135–148CrossRefGoogle Scholar
  29. Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1, and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pfl 167:191–194CrossRefGoogle Scholar
  30. Kinzie III RA, Jokiel PL, York R (1984) Effects of light of altered spectral composition on coral zooxanthellae associations and on zooxanthellae in vitro. Mar Biol 78:239–248CrossRefGoogle Scholar
  31. LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134CrossRefGoogle Scholar
  32. Lewis LL, Muller-Parker G (2004) Phylogenetic placement of “zoochlorellae” (Chlorophyta), algal symbiont of the temperate sea anemone Anthopleura elegantissima. Biol Bull 207:87–92CrossRefGoogle Scholar
  33. Littler MM (1980) Southern California rocky intertidal ecosystems: methods, community structure and variability. In: Price JH, Irvine DEG, Farnham WF (eds) The shore environment, Vol 2, Ecosystems. Academic, New York, pp 565–608Google Scholar
  34. Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, New York pp 129–134CrossRefGoogle Scholar
  35. McAuley PJ, Cook CB (1994) Effects of host feeding and dissolved ammonium on cell division and nitrogen status of zooxanthellae in the hydroid Myrionema amboinense. Mar Biol 121:343–348CrossRefGoogle Scholar
  36. McCloskey LR, Aamodt LD, Hazelton WD (1985) A computer-controlled respirometer for monitoring production and respiration of symbiotic organisms in situ. In: Proceedings 5th international coral reef congress, Tahiti 6:137–142Google Scholar
  37. McCloskey LR, Cove TG, Verde EA (1996) Symbiont expulsion from the anemone Anthopleura elegantissima (Brandt) (Cnidaria; Anthozoa). J Exp Mar Biol Ecol 195:173–176CrossRefGoogle Scholar
  38. McCloskey LR, Muscatine L, Wilkerson FP (1994) Daily photosynthesis, respiration, and carbon budgets in a tropical marine jellyfish (Mastigias sp.). Mar Biol 119:13–22CrossRefGoogle Scholar
  39. McCloskey LR, Wethey DS, Porter JW (1978) The measurement and interpretation of photosynthesis and respiration in reef corals. Monogr Oceanogr Methol UNESCO 5:379–396Google Scholar
  40. McFadden CS, Grosberg RK, Cameron BB, Karlton DP, Secord D (1997) Genetic relationships within and between clonal and solitary forms of the sea anemone Anthopleura elegantissima revisited: evidence for the existence of two species. Mar Biol 128:127–139CrossRefGoogle Scholar
  41. McFarland FK, Muller-Parker G (1993) Photosynthesis and retention of zooxanthellae and zoochlorellae within the aeolid nudibranch Aeolidia papillosa. Biol Bull 184:223–229CrossRefGoogle Scholar
  42. Michalek-Wagner K (2001) Seasonal and sex-specific variations in levels of photo-protecting mycosporine-like amino acids (MAAs) in soft corals. Mar Biol 139:651–660CrossRefGoogle Scholar
  43. Minnick MF (1984) Translocation of photosynthates by endosymbiotic Chlorophyceae to the sea anemone Anthopleura elegantissima (Brandt) (Cnidaria, Anthozoa). Master’s thesis, Walla Walla College, WashingtonGoogle Scholar
  44. Muller-Parker G, Davy SK (2001) Temperate and tropical algal–sea anemone symbioses. Invert Biol 120:104–123CrossRefGoogle Scholar
  45. Muller-Parker G, Pierce-Cravens J, Bingham BL (2007) Broad thermal tolerance of the symbiotic dinoflagellate Symbiodinium muscatinei (Dinophyta) in the sea anemone Anthopleura elegantissima (Cnidaria) from northern latitudes. J Phycol 43:25–31CrossRefGoogle Scholar
  46. Muscatine L (1971) Experiments on green algae coexistent with zooxanthellae in sea anemones. Pac Sci 25:13–21Google Scholar
  47. Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611CrossRefGoogle Scholar
  48. Muscatine L, Ferrier-Pages C, Blackburn A, Gates RD, Baghdasarian G, Allemand D (1998) Cell-specific density of symbiotic dinoflagellates in tropical anthozoans. Coral Reefs 17:329–337CrossRefGoogle Scholar
  49. Muscatine L, Wilkerson FP, McCloskey LR (1986) Regulation of population density of symbiotic algae in a tropical marine jellyfish (Mastigias sp.). Mar Ecol Prog Ser 32:279–290CrossRefGoogle Scholar
  50. Nakamura E, Yokohama Y, Tanaka J. (2004) Photosynthetic activity of a temperate coral Acropora pruinosa (Scleractinia, Anthozoa) with symbiotic algae in Japan. Phycol Res 52:38–44Google Scholar
  51. Navarro E, Ortega MM, Madariaga JM (1981) Effect of body size, temperature, and shore level on aquatic and aerial respiration of Actinia equina (L.)(Anthozoa). J Exp Mar Biol Ecol 53:153–162CrossRefGoogle Scholar
  52. Ortega MM, Iglesias JIP, Navarro E (1984) Acclimation to temperature in Actinia equina L.: effects of season and shore level on aquatic oxygen consumption. J Exp Mar Biol Ecol 76:79–87CrossRefGoogle Scholar
  53. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefGoogle Scholar
  54. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon, OxfordGoogle Scholar
  55. Parsons TR, Lalli CM (1988) Comparative oceanic ecology of the plankton communities of the subarctic Atlantic and Pacific oceans. Oceanog Mar Biol Ann Rev 26:317–359Google Scholar
  56. Rivadeneira MM, Fernandez M (2005) Shifts in southern endpoints of distribution in rocky intertidal species along the south-eastern Pacific coast. J Biogeogr 32:203–209CrossRefGoogle Scholar
  57. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60CrossRefGoogle Scholar
  58. Sagarin RD, Barry JP, Gilman SE, Baxter CH (1999) Climate-related change in an intertidal community over short and long term scales. Ecol Monogr 69:465–490CrossRefGoogle Scholar
  59. Saunders BK, Muller-Parker G (1997) The effects of temperature and light on two algal populations in the temperate sea anemone Anthopleura elegantissima (Brandt, 1835). J Exp Mar Biol Ecol 211:213–224CrossRefGoogle Scholar
  60. Savage AM, Goodson MS, Visram S, Trapido-Rosenthal H, Wiedenmann J, Douglas AE (2002) Molecular diversity of symbiotic algae at the latitudinal margins of their distribution: dinoflagellates of the genus Symbiodinium in corals and sea anemones. Mar Ecol Prog Ser 244:17–26CrossRefGoogle Scholar
  61. Sebens KP (1980) The regulation of asexual reproduction and indeterminate body size in the sea anemone Anthopleura elegantissima (Brandt). Biol Bull 158:370–382CrossRefGoogle Scholar
  62. Sebens KP (1982a) Recruitment and habitat selection in the intertidal sea anemones, Anthopleura elegantissima (Brandt) and A. xanthogrammica (Brandt). J Exp Mar Biol Ecol 59:103–124CrossRefGoogle Scholar
  63. Sebens KP (1982b) Asexual reproduction in Anthopleura elegantissima (Anthozoa: Actinaria): seasonality and spatial extent of clones. Ecology 63:434–444CrossRefGoogle Scholar
  64. Sebens KP (1983a) Population dynamics and habitat suitability of the intertidal sea anemones Anthopleura elegantissima and A. xanthogrammica. Ecol Monogr 53:405–433CrossRefGoogle Scholar
  65. Sebens KP (1983b) Morphological variability during longitudinal fission of the intertidal sea anemone, Anthopleura elegantissima (Brandt). Pac Sci 37:121–132Google Scholar
  66. Secord D, 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. Invert Biol 119:139–146CrossRefGoogle Scholar
  67. Secord D, Muller-Parker G (2005) Symbiont distribution along a light gradient within an intertidal cave. Limnol Oceanogr 50:272–278CrossRefGoogle Scholar
  68. Shick JM (1991) A functional biology of sea anemones. Chapman and Hall, UKCrossRefGoogle Scholar
  69. Shick JM, Dykens JA (1984) Photobiology of the symbiotic sea anemone Anthopleura elegantissima: photosynthesis, respiration, and behavior under intertidal conditions. Biol Bull 166:608–619CrossRefGoogle Scholar
  70. Snyder MJ, Rossi S (2004) Stress protein (HSP70 family) expression in intertidal benthic organisms: the example of Anthopleura elegantissima (Cnidaria: Anthozoa). Sci Mar 68:155–162CrossRefGoogle Scholar
  71. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. WH Freeman and Company, New YorkGoogle Scholar
  72. Stimson J (1997) The annual cycle of density of zooxanthellae in the tissues of field and laboratory-held Pocillopora damicornis (Linnaeus). J Exp Mar Biol Ecol 214:35–48CrossRefGoogle Scholar
  73. Stochaj WR, Dunlap WC, Shick JM (1994) Two new UV-absorbing mycosporine-like amino acids from the sea anemone Anthopleura elegantissima and the effects of zooxanthellae and spectral irradiance on chemical composition and content. Mar Biol 118:149–156CrossRefGoogle Scholar
  74. Tomanek L, Helmuth B (2002) Physiological ecology of rocky intertidal organisms: a synergy of concepts. Integ Comp Biol 42:771–775CrossRefGoogle Scholar
  75. Trench RK (1971a) The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates: I The assimilation of photosynthetic products of zooxanthellae by two marine coelenterates. Proc R Soc Lond B 177:225–235CrossRefGoogle Scholar
  76. Trench RK (1971b) The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates: II Liberation of fixed 14C by zooxanthellae in vitro. Proc R Soc Lond B 177:237–250CrossRefGoogle Scholar
  77. Verde EA (1993) The effects of temperature, light, season, and body size on the photosynthesis and respiration of zooxanthellae and zoochlorellae symbiotic within Anthopleura elegantissima (Brandt). Ph.D. dissertation. Florida Institute of Technology, FloridaGoogle Scholar
  78. Verde EA, McCloskey LR (1996a) Carbon budget studies of symbiotic cnidarian anemones—evidence in support of some assumptions. J Exp Mar Biol Ecol 195:161–171CrossRefGoogle Scholar
  79. Verde EA, McCloskey LR (1996b) Photosynthesis and respiration of two species of algal symbionts in the anemone Anthopleura elegantissima (Brandt) (Cnidaria; Anthozoa). J Exp Mar Biol Ecol 195:187–202CrossRefGoogle Scholar
  80. Verde EA, McCloskey LR (1998) Production, respiration, and photophysiology of the mangrove jellyfish Cassiopea xamachana symbiotic with zooxanthellae: effect of jellyfish size and season. Mar Ecol Prog Ser 168:147–162CrossRefGoogle Scholar
  81. Verde EA, McCloskey LR (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 138:447–489CrossRefGoogle Scholar
  82. Verde EA, McCloskey LR (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 141:225–239CrossRefGoogle Scholar
  83. Walther GR Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefGoogle Scholar
  84. Warner ME, Chilcoat GC, McFarland FK, Fitt WK (2002) Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastraea. Mar Biol 141:31–38CrossRefGoogle Scholar
  85. Wilkerson FP, Muller-Parker G, Muscatine L (1983) Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnol Oceanogr 28:1009–1014CrossRefGoogle Scholar
  86. Winer BJ (1971) Statistical principles in experimental design, 2nd edn. McGraw-Hill, New YorkGoogle Scholar
  87. Zamer WE (1986) Physiological energetics of the intertidal sea anemone Anthopleura elegantissima. I. Prey capture, absorption efficiency and growth. Mar Biol 92:299–314CrossRefGoogle Scholar
  88. Zamer WE, Shick JM (1987) Physiological energetics of the intertidal sea anemone Anthopleura elegantissima. II. Energy balance. Mar Biol 93:481–491CrossRefGoogle Scholar
  89. Zamer WE, Shick JM (1989) Physiological energetics of the intertidal sea anemone Anthopleura elegantissima. III. Biochemical composition of body tissues, substrate-specific absorption, and carbon and nitrogen budgets. Oecologia 79:117–127CrossRefGoogle Scholar
  90. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, New JerseyGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Corning School of Ocean Studies Maine Maritime AcademyCastineUSA
  2. 2.Department of BiologyLa Sierra UniversityRiversideUSA

Personalised recommendations