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

Marine Biology

Volumn 152, Issue 4, 2007, Pages 775-792

  Verde, E Alan ^a   McCloskey, L R ^b  

^a MAINE MARITIME ACADEMY   (United States)

^b LA SIERRA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON FIXATION; CLIMATE CHANGE; COMPARATIVE STUDY; GLOBAL CHANGE; INTERTIDAL ENVIRONMENT; MICROHABITAT; PHOTOSYNTHESIS; RESPIRATION; SEASONAL VARIATION; SYMBIOSIS; ZOOXANTHELLA;

NORTH AMERICA; PACIFIC NORTHWEST;

ACTINIARIA; ALGAE; ANEMONE; ANTHOPLEURA ELEGANTISSIMA; DINOPHYCEAE; SYMBIODINIUM; SYMBIODINIUM CALIFORNIUM;

EID: 34548129176     PISSN: 00253162     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00227-007-0737-6     Document Type: Article

References (90)

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 73:551-555
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 43:711-715
3. Bachman S, Muller-Parker G (2007) Viable algae released by the Dermasterias imbricata feeding on the symbiotic sea anemone Anthopleura elegantissima. Mar Biol 150:369-375
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 194:213-232
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 194:233-250
6. Barry JP, Baxter CH, Sagarin RD, Gilman SE (1995) Climate-related, long-term faunal changes in a California rocky intertidal community. Science 267:672-674
7. Bates A (2000) The intertidal distribution of two algal symbionts hosted by Anthopleura xanthogrammica (Brandt 1835). J Exp Mar Biol Ecol 249:249-262
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 117:655-664
9. Bronstein JL (2001) The costs of mutualism. Am Zool 41:825-839
10. Dykens JA, Shick JM (1984) Photobiology of the symbiotic sea anemone, Anthopleura elegantissima: defenses against photodynamic effects and seasonal photoacclimatization. Biol Bull 167:683-697
11. Engebretson HP, Muller-Parker G (1999) Translocation of photosynthetic carbon from two algal symbionts to the sea anemone Anthopleura elegantissima. Biol Bull 197:72-81
12. Fagoonee I, Wilson HB, Hassell MP, Turner JR (1999) The dynamics of zooxanthellae populations: a long-term study in the field. Science 283:843-845
13. Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals. BioScience 43:606-611
14. Falkowski PG, LaRoche J (1991) Acclimation to spectral irradiance in algae. J Phycol 27:8-14
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 45:677-685
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 61:213-232
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 120:599-604
18. Graham DL (1989) Response of algal populations to nutrient conditions in Anthopleura elegantissima (Brandt). Master's thesis, Walla Walla College, Washington
19. Griffiths RJ (1977a) Thermal stress and the biology of Actinia equina L. (Anthozoa). J Exp Mar Biol Ecol 27:141-154
20. Griffiths RJ (1977b) Temperature acclimation in Actinia equina L. (Anthozoa). J Exp Mar Biol Ecol 28:285-292
21. Hand C (1955) The sea anemones of central California. Part II. The endomyarian and mesomyarian anemones. Wasmann J Biol 13:37-99
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 51:487-502
23. Helmuth B (2002) How do we measure the environment? Linking intertidal thermal physiology and ecology through biophysics. Integ Comp Biol 42:837-845
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 298:1015-1017
25. Helmuth BST, Hofmann G (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol Bull 201:374-384
26. Helmuth B, Kingsolver JG, Carrington E (2005) Biophysics, physiological ecology, and climate change: does mechanism matter? Ann Rev Physiol 67:177-201
27. Intergovernmental Panel on Climate Change (2007) Climate change 2007: the physical science basis. http://www.ipcc.ch/
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 76:135-148
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 167:191-194
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 78:239-248
31. LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126-134
32. Lewis LL, Muller-Parker G (2004) Phylogenetic placement of "zoochlorellae" (Chlorophyta), algal symbiont of the temperate sea anemone Anthopleura elegantissima. Biol Bull 207:87-92
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 565-608
34. Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, New York pp 129-134
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 121:343-348
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 6:137-142
37. McCloskey LR, Cove TG, Verde EA (1996) Symbiont expulsion from the anemone Anthopleura elegantissima (Brandt) (Cnidaria; Anthozoa). J Exp Mar Biol Ecol 195:173-176
38. McCloskey LR, Muscatine L, Wilkerson FP (1994) Daily photosynthesis, respiration, and carbon budgets in a tropical marine jellyfish (Mastigias sp.). Mar Biol 119:13-22
39. McCloskey LR, Wethey DS, Porter JW (1978) The measurement and interpretation of photosynthesis and respiration in reef corals. Monogr Oceanogr Methol UNESCO 5:379-396
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 128:127-139
41. McFarland FK, Muller-Parker G (1993) Photosynthesis and retention of zooxanthellae and zoochlorellae within the aeolid nudibranch Aeolidia papillosa. Biol Bull 184:223-229
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 139:651-660
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, Washington
44. Muller-Parker G, Davy SK (2001) Temperate and tropical algal-sea anemone symbioses. Invert Biol 120:104-123
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 43:25-31
46. Muscatine L (1971) Experiments on green algae coexistent with zooxanthellae in sea anemones. Pac Sci 25:13-21
47. Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601-611
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 17:329-337
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 32:279-290
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 52:38-44
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 53:153-162
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 76:79-87
53. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37-42
54. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon, Oxford
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 26:317-359
56. Rivadeneira MM, Fernandez M (2005) Shifts in southern endpoints of distribution in rocky intertidal species along the south-eastern Pacific coast. J Biogeogr 32:203-209
57. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57-60
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 69:465-490
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 211:213-224
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 244:17-26
61. Sebens KP (1980) The regulation of asexual reproduction and indeterminate body size in the sea anemone Anthopleura elegantissima (Brandt). Biol Bull 158:370-382
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 59:103-124
63. Sebens KP (1982b) Asexual reproduction in Anthopleura elegantissima (Anthozoa: Actinaria): seasonality and spatial extent of clones. Ecology 63:434-444
64. Sebens KP (1983a) Population dynamics and habitat suitability of the intertidal sea anemones Anthopleura elegantissima and A. xanthogrammica. Ecol Monogr 53:405-433
65. Sebens KP (1983b) Morphological variability during longitudinal fission of the intertidal sea anemone, Anthopleura elegantissima (Brandt). Pac Sci 37:121-132
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 119:139-146
67. Secord D, Muller-Parker G (2005) Symbiont distribution along a light gradient within an intertidal cave. Limnol Oceanogr 50:272-278
68. Shick JM (1991) A functional biology of sea anemones. Chapman and Hall, UK
69. Shick JM, Dykens JA (1984) Photobiology of the symbiotic sea anemone Anthopleura elegantissima: photosynthesis, respiration, and behavior under intertidal conditions. Biol Bull 166:608-619
70. Snyder MJ, Rossi S (2004) Stress protein (HSP70 family) expression in intertidal benthic organisms: the example of Anthopleura elegantissima (Cnidaria: Anthozoa). Sci Mar 68:155-162
71. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. WH Freeman and Company, New York
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 214:35-48
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 118:149-156
74. Tomanek L, Helmuth B (2002) Physiological ecology of rocky intertidal organisms: a synergy of concepts. Integ Comp Biol 42:771-775
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 177:225-235
76. 14C by zooxanthellae in vitro. Proc R Soc Lond B 177:237-250
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, Florida
78. Verde EA, McCloskey LR (1996a) Carbon budget studies of symbiotic cnidarian anemones-evidence in support of some assumptions. J Exp Mar Biol Ecol 195:161-171
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 195:187-202
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 168:147-162
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 138:447-489
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 141:225-239
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 416:389-395
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 141:31-38
85. Wilkerson FP, Muller-Parker G, Muscatine L (1983) Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnol Oceanogr 28:1009-1014
86. Winer BJ (1971) Statistical principles in experimental design, 2nd edn. McGraw-Hill, New York
87. Zamer WE (1986) Physiological energetics of the intertidal sea anemone Anthopleura elegantissima. I. Prey capture, absorption efficiency and growth. Mar Biol 92:299-314
88. Zamer WE, Shick JM (1987) Physiological energetics of the intertidal sea anemone Anthopleura elegantissima. II. Energy balance. Mar Biol 93:481-491
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 79:117-127
90. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, New Jersey