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Marine Biology

, Volume 156, Issue 12, pp 2493–2503 | Cite as

Effects of photoacclimation on the light niche of corals: a process-based approach

  • Mia O. HoogenboomEmail author
  • Sean R. Connolly
  • Kenneth R. N. Anthony
Original Paper

Abstract

The ecology of photosynthetic organisms is influenced by the need to adjust the photosynthetic apparatus to variable light environments (photoacclimation). In this study, we quantified different components of the photoacclimation process for a reef-building coral (Turbinaria mesenterina, Lamarck, 1816): including, variation in absorption cross-section, size of photosynthetic units, turnover time, chlorophyll content, and colony respiration. We used these calibrations to characterize this species’ light niche, and to determine the sensitivity of the niche boundaries to different processes of photoacclimation. Results showed that the breadth of the light niche was most sensitive to the size of the photosynthetic unit, absorption cross-section, and rates of respiration. Habitats with the highest light availability did not lead to maximal energy acquisition. This was because, although corals acclimated to high light have high rates of photosynthesis per unit chlorophyll, their chlorophyll content was strongly reduced. This suggests that potential energetic benefits that could be achieved through increased light harvesting (i.e., increased chlorophyll content) in high-light habitats are outweighed by costs associated with photoprotection. Such costs appear to place an upper bound on the habitat distributions of coral species. Our approach reveals how the photophysiological processes involved in photoacclimation interact to determine the light niche.

Keywords

Photosynthetic Apparatus Turnover Time Niche Width Unit Surface Area Growth Irradiance 

Notes

Acknowledgments

We thank R. Fox for assistance with fieldwork and staff at James Cook University (JCU) Marine and Aquaculture Research Facilities Unit. This work was funded by the Australian Research Council (ARC) and JCU. This is a contribution from the ARC Centre of Excellence for Coral Reef Studies.

References

  1. Adolf JE, Stoecker DK, Harding LW (2003) Autotrophic growth and photoacclimation in Karlodinium micrum (Dinophyceae) and Storeatula major (Cryptophyceae). J Phycol 39:1101–1108. doi: https://doi.org/10.1111/j.0022-3646.2003.02-086.x CrossRefGoogle Scholar
  2. Anderson JM, Chow WS, Park YI (1995) The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46:129–139. doi: https://doi.org/10.1007/BF00020423 CrossRefGoogle Scholar
  3. Anthony KRN, Hoegh-Guldberg O (2003) Kinetics of photoacclimation in corals. Oecologia 134:23–31. doi: https://doi.org/10.1007/s00442-002-1095-1 CrossRefGoogle Scholar
  4. Anthony KRN, Ridd PV, Orpin AR, Larcombe P, Lough J (2004) Temporal variation of light availability in coastal benthic habitats: effects of clouds, turbidity and tides. Limnol Oceanogr 49:2201–2211CrossRefGoogle Scholar
  5. Anthony KRN, Hoogenboom MO, Connolly SR (2005) Adaptive variation in coral geometry and the optimisation of internal colony light climates. Funct Ecol 19:17–26. doi: https://doi.org/10.1111/j.0269-8463.2005.00925.x CrossRefGoogle Scholar
  6. Babcock RC (1991) Comparative demography of three species of scleractinian corals using age- and size-dependent classifications. Ecol Monogr 61:225–244. doi: https://doi.org/10.2307/2937107 CrossRefGoogle Scholar
  7. Babin M, Morel A, Claustre H, Bricaud A, Kolber Z, Falkowski PG (1996) Nitrogen- and irradiance-dependent variations of the maximum quantum yield of carbon fixation in eutrophic, mesotrophic and oligotrophic marine systems. Deep Sea Res I 43:1241–1272. doi: https://doi.org/10.1016/0967-0637(96)00058-1 CrossRefGoogle Scholar
  8. Bailey S, Walters RG, Jansson S, Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213:794–801. doi: https://doi.org/10.1007/s004250100556 CrossRefGoogle Scholar
  9. Behrenfeld MJ, Maranon E, Siegel DA, Hooker SB (2002) Photoacclimation and nutrient-based model of light-saturated photosynthesis for quantifying oceanic primary production. Mar Ecol Prog Ser 228:103–117. doi: https://doi.org/10.3354/meps228103 CrossRefGoogle Scholar
  10. Chang SS, Prezelin BB, Trench RK (1983) Mechanisms of photoadaptation in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Mar Biol 76:219–229. doi: https://doi.org/10.1007/BF00393021 CrossRefGoogle Scholar
  11. Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626. doi: https://doi.org/10.1146/annurev.pp.43.060192.003123 CrossRefGoogle Scholar
  12. Dove S, Ortiz JC, Enriquez S, Fine M, Fisher P, Iglesias-Prieto R, Thornhill D, Hoegh-Guldberg O (2006) Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnol Oceanogr 51:1149–1158CrossRefGoogle Scholar
  13. Dubinsky Z, Falkowski PG, Wyman K (1986) Light harvesting and utilization by phytoplankton. Plant Cell Physiol 27:1335–1349CrossRefGoogle Scholar
  14. Dustan P (1982) Depth-dependent photoadaptation by zooxanthellae of the reef coral Montastrea annularis. Mar Biol 68:253–264. doi: https://doi.org/10.1007/BF00409592 CrossRefGoogle Scholar
  15. Enriquez S, Mendez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50:1025–1032CrossRefGoogle Scholar
  16. Falkowski PG, Raven JA (1997) Aquatic photosynthesis. Blackwell, OxfordGoogle Scholar
  17. Falkowski PG, Owens TG, Ley AC, Mauzerall DC (1981) Effects of growth irradiance levels on the ratio of reaction centers in two species of marine phytoplankton. Plant Physiol 68:969–973. doi: https://doi.org/10.1104/pp.68.4.969 CrossRefGoogle Scholar
  18. Flameling IA, Kromkamp J (1997) Photoacclimation of Scenedesmus protuberans to fluctuating irradiances simulating vertical mixing. J Plankton Res 19:1011–1024. doi: https://doi.org/10.1093/plankt/19.8.1011 CrossRefGoogle Scholar
  19. Frade PR, Bongaerts P, Winkelhagen AJS, Tonk L, Bak RPM (2008) In situ photobiology of corals over large depth ranges: a multivariate analysis on the roles of environment, host and algal symbiont. Limnol Oceanogr 53:2711–2723CrossRefGoogle Scholar
  20. Gorbunov MY, Kolber ZS, Lesser MP, Falkowski PG (2001) Photosynthesis and photoprotection in symbiotic corals. Limnol Oceanogr 46:75–85CrossRefGoogle Scholar
  21. Gordillo FJL, Jiminez C, Chavarria J, Niell FX (2001) Photosynthetic acclimation to photon irradiance and its relation to chlorophyll fluorescence and carbon assimilation in the halotolerant green alga Dunaliella viridis. Photosynth Res 68:225–235. doi: https://doi.org/10.1023/A:1012969324756 CrossRefGoogle Scholar
  22. Herzig R, Dubinsky Z (1992) Photoacclimation, photosynthesis, and growth in phytoplankton. Isr J Bot 41:199–212Google Scholar
  23. Hoogenboom MO, Anthony KRN, Connolly SR (2006) Energetic cost of photoinhibition in corals. Mar Ecol Prog Ser 313:1–12. doi: https://doi.org/10.3354/meps313001 CrossRefGoogle Scholar
  24. Hoogenboom MO, Connolly SR, Anthony KRN (2008) Interactions between morphological and physiological plasticity optimize energy acquisition in corals. Ecology 89:1144–1154. doi: https://doi.org/10.1890/07-1272.1 CrossRefGoogle Scholar
  25. Houter NC, Pons TL (2005) Gap size effects on photoinhibition in understorey saplings in tropical rainforest. Plant Ecol 179:43–51. doi: https://doi.org/10.1007/s11258-004-5775-2 CrossRefGoogle Scholar
  26. Iglesias-Prieto R, Trench RK (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar Ecol Prog Ser 113:163–175CrossRefGoogle Scholar
  27. Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547CrossRefGoogle Scholar
  28. Jeffery SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194CrossRefGoogle Scholar
  29. Krause GH (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol Plant 74:566–574. doi: https://doi.org/10.1111/j.1399-3054.1988.tb02020.x CrossRefGoogle Scholar
  30. Kuhl M, Cohen Y, Dalsgaard T (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar Ecol Prog Ser 117:159–172. doi: https://doi.org/10.3354/meps117159 CrossRefGoogle Scholar
  31. MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17–38. doi: https://doi.org/10.1046/j.1529-8817.2002.00094.x CrossRefGoogle Scholar
  32. Marra J (1978) Effect of short-term variations in light intensity on photosynthesis of a marine phytoplankter: a laboratory simulation study. Mar Biol 46:191–202. doi: https://doi.org/10.1007/BF00390680 CrossRefGoogle Scholar
  33. Mass T, Einbinder S, Brokovich E, Shashar N, Vago R, Erez J, Dubinsky Z (2007) Photoacclimation of Stylophora pistillata to light extremes: metabolism and calcification. Mar Ecol Prog Ser 334:93–102. doi: https://doi.org/10.3354/meps334093 CrossRefGoogle Scholar
  34. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668. doi: https://doi.org/10.1093/jexbot/51.345.659 CrossRefGoogle Scholar
  35. Murchie EH, Horton P (1997) Acclimation of photosynthesis to irradiance and spectral quality in British plant species: chlorophyll content, photosynthetic capacity and habitat preference. Plant Cell Environ 20:438–448. doi: https://doi.org/10.1046/j.1365-3040.1997.d01-95.x CrossRefGoogle Scholar
  36. 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
  37. Myers J, Graham J-R (1971) The photosynthetic unit in Chlorella measured by repetitive short flashes. Plant Physiol 48:282–286. doi: https://doi.org/10.1104/pp.48.3.282 CrossRefGoogle Scholar
  38. Prezelin BB (1981) Light reactions in photosythesis. In: Platt T (ed) Physiological bases of phytoplankton ecology. Can Bull Fish Aquat Sci 201:1–43Google Scholar
  39. Raps S, Wyman K, Siegelman HW, Falkowski PG (1983) Adaptation of the cyanobacterium Microcystis aeruginosa to light-intensity. Plant Physiol 72:829–832. doi: https://doi.org/10.1104/pp.72.3.829 CrossRefGoogle Scholar
  40. Richardson K, Beardall J, Raven JA (1983) Adaptation of unicellular algae to irradiance: an analysis of strategies. New Phytol 93:157–191. doi: https://doi.org/10.1111/j.1469-8137.1983.tb03422.x CrossRefGoogle Scholar
  41. Robison JD, Warner ME (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J Phycol 42:568–579. doi: https://doi.org/10.1111/j.1529-8817.2006.00232.x CrossRefGoogle Scholar
  42. Rodriguez-Roman A, Hernandez-Pech Z, Thome PE, Enriquez S, Iglesias-Prieto R (2006) Photosynthesis and light utilisation in the Caribbean coral Montastera faveolata recovering from a bleaching event. Limnol Oceanogr 51:2702–2710CrossRefGoogle Scholar
  43. Suggett DJ, Oxborough K, Baker NR, MacIntyre HL, Kana TM, Geider RJ (2003) Fast repetition rate and pulse amplitude modulation chlorophyll-a fluorescence measurements for assessment of photosynthetic electron transport in marine phytoplankton. Eur J Phycol 38:371–384. doi: https://doi.org/10.1080/09670260310001612655 CrossRefGoogle Scholar
  44. Titlyanov EA (1991) The stable level of coral primary production in a wide light range. Hydrobiologia 216/217:383–387. doi: https://doi.org/10.1007/BF00026490 CrossRefGoogle Scholar
  45. Ulstrup KE, Ralph PJ, Larkum AWD, Kuhl M (2006) Intra-colonial variability in light acclimation of zooxanthellae in coral tissues of Pocillopora damicornis. Mar Biol 149:1325–1335. doi: https://doi.org/10.1007/s00227-006-0286-4 CrossRefGoogle Scholar
  46. Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447. doi: https://doi.org/10.1093/jxb/eri060 CrossRefGoogle Scholar
  47. 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 Montastrea. Mar Biol 141:31–38. doi: https://doi.org/10.1007/s00227-002-0807-8 CrossRefGoogle Scholar
  48. Willis BL (1985) Phenotypic plasticity versus phenotypic stability in the reef corals Turbinaria mesenterina and Pavona cactus. In: Proceedings of 5th international coral reef symposium, vol 4, pp 107–112Google Scholar
  49. Wyman KD, Dubinsky Z, Porter JW (1987) Light absorption and utilization among hermatypic corals: a study in Jamaica, West Indies. Mar Biol 96:283–292. doi: https://doi.org/10.1007/BF00427028 CrossRefGoogle Scholar
  50. Zonneveld C (1997) Modeling effects of photoadaptation on the photosynthesis-irradiance curve. J Theor Biol 186:381–388. doi: https://doi.org/10.1006/jtbi.1997.0400 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Mia O. Hoogenboom
    • 1
    • 3
    Email author
  • Sean R. Connolly
    • 1
  • Kenneth R. N. Anthony
    • 2
  1. 1.ARC Centre of Excellence for Coral Reef Studies and School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia
  2. 2.ARC Centre of Excellence for Coral Reef Studies and Centre of Marine StudiesUniversity of QueenslandBrisbaneAustralia
  3. 3.Division of Ecology and Evolutionary BiologyUniversity of GlasgowGlasgowScotland, UK

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