Skip to main content
SpringerLink
Log in

Feeding sustains photosynthetic quantum yield of a scleractinian coral during thermal stress

  • Plant-Animal Interactions - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Thermal resistance of the coral–zooxanthellae symbiosis has been associated with chronic photoinhibition, increased antioxidant activity and protein repair involving high demands of nitrogen and energy. While the relative importance of heterotrophy as a source of nutrients and energy for cnidarian hosts, and as a means of nitrogen acquisition for their zooxanthellae, is well documented, the effect of feeding on the thermal sensitivity of the symbiotic association has been so far overlooked. Here we examine the effect of zooplankton feeding versus starvation on the bleaching susceptibility and photosynthetic activity of photosystem II (PSII) of zooxanthellae in the scleractinian coral Stylophora pistillata in response to thermal stress (daily temperature rises of 2–3°C) over 10 days, employing pulse-amplitude-modulated chlorophyll fluorometry. Fed and starved corals displayed a decrease in daily maximum potential quantum yield (F v/F m) of PSII, effective quantum yield (∆F/F m′) and relative electron transport rates over the course of 10 days. However after 10 days of exposure to elevated temperature, F v/F m of fed corals was still 50–70% higher than F v/F m of starved corals. Starved corals showed strong signs of chronic photoinhibition, which was reflected in a significant decline in nocturnal recovery rates of PSII relative to fed corals. This was paralleled by the progressive inability to dissipate excess excitation energy via non-photochemical quenching (NPQ). After 10 days, NPQ of starved corals had decreased by about 80% relative to fed corals. Feeding treatment had no significant effect on chlorophyll a and c 2 concentrations and zooxanthellae densities, but the mitotic indices were significantly lower in starved than in fed corals. Collectively the results indicate that exogenous food may reduce the photophysiological damage of zooxanthellae that typically leads to bleaching and could therefore play an important role in mediating the thermal resistance of some corals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ambarsari I, Brown BE, Barlow RG, Britton G, Cummings D (1997) Fluctuations in algal chlorophyll and carotenoid pigments during solar bleaching in the coral Goniastrea aspera at Phuket, Thailand. Mar Ecol Prog Ser 159:303–307

    Article  CAS  Google Scholar 

  • Anthony KRN (2006) Enhanced energy status of corals on coastal, high-turbidity reefs. Mer Ecol Prog Ser 319:111–116

    Article  Google Scholar 

  • Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253

    Article  PubMed  Google Scholar 

  • Anthony KRN, Connolly SR, Willis BL (2002) Comparative analysis of energy allocation to tissue and skeletal growth in corals. Limnol Oceanogr 47:1417–1429

    Google Scholar 

  • Anthony RNK, Connolly SR, Hoegh-Guldberg O (2007) Bleaching, energetics, and coral mortality risk: effects of temperature, light and sediment regime. Limnol Oceanogr 52:716–726

    Google Scholar 

  • Brown BE, Suharsono (1990) Damage and recovery of coral reefs affected by El Nino related seawater warming in the Thousand Islands, Indonesia. Coral Reefs 8:163–170

  • Brown BE, Ambarsari I, Warner ME, Fitt WK, Dunne RP, Gibb SW, Cummings DG (1999) Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18:99–105

    Article  Google Scholar 

  • Calow P (1989) Proximate and ultimate responses to stress in biological systems. Biol J Linn Soc 1/2:173–181

    Google Scholar 

  • Clayton WS, Lasker HR (1984) Host feeding regime and zooxanthellal photosynthesis in the anemone, Aiptasia pallida (Verrill). Biol Bull 167:590–600

    Article  CAS  Google Scholar 

  • Cook C, Muller-Parker G, Orlandini CD (1994) Ammonium enhancement of dark carbon fixation and nitrogen limitation in zooxanthellae symbiotic with the reef corals Madracis mirabilis and Montastrea annularis. Mar Biol 118:157–165

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WWIII (2002) Antioxidants in photosynthesis and human nutrition. Science 298:2149–2153

    Article  PubMed  CAS  Google Scholar 

  • Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM (2002) Oxidative stress and seasonal coral bleaching. Free Radic Biol Med 33:533–543

    Article  PubMed  CAS  Google Scholar 

  • Dubinsky Z, Jokiel PL (1994) Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals. Pac Sci 48:313–324

    Google Scholar 

  • Dunn SR, Bythell C, Le Tissier MDA, Burnett WJ, Thomason JC (2002) Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. J Exp Mar Biol Ecol 272:29–53

    Article  Google Scholar 

  • Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and bioenergetics of a symbiotic coral. Bioscience 34:705–709

    Article  CAS  Google Scholar 

  • Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals: ammonium ions and organic materials maintain the density of zooxanthellae. Bioscience 43:606–611

    Article  Google Scholar 

  • Ferrier-Pages C, Allemand D, Gattuso J-P, Jaubert J, Rassoulzadegan R (1998) Microheterotrophy in the zooxanthellate coral Stylophora pistillata: effects of light and ciliate density. Limnol Oceanogr 43:1639–1648

    CAS  Google Scholar 

  • Ferrier-Pages C, Witting J, Tambutte E, Sebens K (2003) Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22:229–240

    Article  Google Scholar 

  • Fitt WK, Cook CB (2001) The effects of feeding or addition of dissolved inorganic nutrients in maintaining the symbiosis between dinoflagellates and a tropical cnidarian. Mar Biol 139:507–517

    Article  Google Scholar 

  • Franklin DJ, Hoegh-Guldberg O, Jones RJ, Berges JA (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Mar Ecol Prog Ser 272:117–130

    Article  Google Scholar 

  • Gardella DJ, Edmunds PJ (1999) The oxygen microenvironment adjacent to the tissue of the scleractinian Dichocoenia stokesii and its effects on symbiont metabolism. Mar Biol 135:289–295

    Article  Google Scholar 

  • Gleeson M, Strong AE (1995) Applying MCSST to coral reef bleaching. Adv Space Res 16:151–154

    Article  Google Scholar 

  • Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189

    Article  PubMed  CAS  Google Scholar 

  • Harland AD, Navarro JC, Spencer-Davies P, Fixter LM (1993) Lipids of some Caribbean and Red Sea corals: total lipid, wax esters, triglycerides and fatty acids. Mar Biol 75:137–149

    Google Scholar 

  • Hawkins AJS (1991) Protein turnover: a functional appraisal. Funct Ecol 5:222–233

    Article  Google Scholar 

  • Hill R, Frankart C, Ralph PJ (2005) Impact of bleaching conditions on the components of non-photochemical quenching in the zooxanthellae of a coral. J Exp Mar Biol Ecol 322:83–92

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O (1988) A Method for determining the surface area of corals. Coral Reefs 7:113–116

    Article  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshwater Res 50:839–866

    Article  Google Scholar 

  • Hoegh-Guldberg O, Jones RJ (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar Ecol Prog Ser 183:73–86

    Article  Google Scholar 

  • Houlbreque F, Tambutte E, Ferrier-Pages C (2003) Effects of zooplankton availability on the rates of photosynthesis, tissue and skeletal growth of the scleractinian coral Stylophora pistillata. J Exp Mar Biol Ecol 296:145–166

    Article  Google Scholar 

  • Houlbreque F, Tambutte E, Allemand D, Ferrier-Pages C (2004) Interactions between feeding, photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata. J Exp Biol 207:1461–1469

    Article  PubMed  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c 1 and c 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanzen Bd 167:191–194

  • Jones RJ, Hoegh-Guldberg O (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dynophyceae) of corals: photoreception, photoinactivation and the relationship to coral bleaching. Plant Cell Environ 24:89–99

    Article  CAS  Google Scholar 

  • Jones RJ, Yellowlees D (1997) Regulation and control of intracellular algae (= zooxanthellae) in hard corals. Proc R Soc Lond Ser B 352:457–468

    Article  Google Scholar 

  • Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230

    Article  CAS  Google Scholar 

  • Jones RJ, Ward S, Amri Y, Hoegh-Guldberg O (2000) Changes in quantum efficiency of photosystem II of symbiotic dinoflagellates of corals after heat stress, and of corals sampled after the 1998 Great Barrier Reef mass bleaching event. Mar Freshwater Res 51:63–71

    Article  Google Scholar 

  • Koehn RK, Bayne BL (1989) Towards a physiological and genetical understanding of the energetics of the stress response. Biol J Linn Soc 37:157–171

    Article  Google Scholar 

  • Levy O, Dubinsky Z, Schneider K, Achituv Y, Zakai D, Gorbunov MY (2004) Diurnal hysteresis in coral photosynthesis. Mar Ecol Prog Ser 268:105–117

    Article  Google Scholar 

  • Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163

    Article  Google Scholar 

  • McAuley P, Cook CB (1994) Effects of host feeding and dissolved ammonium on cell division and nitrogen status of zooxanthellae in the hydroid Myrionema amoinense. Mar Biol 121:343–348

    Article  Google Scholar 

  • Muller-Parker G, McCloskey LR, Hoegh-Guldberg O, McAuley PJ (1994) Effect of ammonium enrichment on animal and algal biomass of the coral Pocillopora daminicornis. Pac Sci 48:273–283

    CAS  Google Scholar 

  • Muscatine L, Falkowski PG, Porter JW, Dubinsky Z (1984) Fate of photosynthetically fixed carbon in light- and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc R Soc Lond Ser B 222:181–202

    CAS  Google Scholar 

  • Ohad I, Kyle DJ, Arntzen J (1984) Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes. J Cell Biol 99:481–485

    Article  PubMed  CAS  Google Scholar 

  • Palardy JE, Grottoli AG, Matthews KA (2005) Effects of upwelling, depth, morphology and polyp size on feeding in three species of Panamanian corals. Mar Ecol Prog Ser 300:79–89

    Article  Google Scholar 

  • Palardy JE, Grottoli AG, Matthews KA (2006) Effect of naturally changing zooplankton concentrations on feeding rates of two coral species in the Eastern Pacific. J Exp Mar Biol Ecol 331:99–107

    Article  Google Scholar 

  • Piniak GA, Lipschultz F, McClelland J (2003) Assimilation and partitioning of prey nitrogen within two anthozoans and their endosymbiotic zooxanthellae. Mar Ecol Prog Ser 262:125–136

    Article  Google Scholar 

  • Richier S, Furla P, Plantivaux A, Merle P-L, Alemand D (2005) Symbiosis-induced adaptation to oxidative stress. J Exp Biol 208:277–285

    Article  PubMed  Google Scholar 

  • Rossi S, Ribes M, Coma R, Gili J-M (2004) Temporal variability in zooplankton prey capture rate of the passive suspension feeder Leptogorgia sarmentosa (Cnidaria: Octocorallia), a case study. Mar Biol 144:89–99

    Article  Google Scholar 

  • Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou G, Govindjee (ed) Chlorophyll fluorescence: a signature of photosynthesis. Kluwer, Dordrecht, pp 279–319

  • Sebens KP, Johnson AS (1991) Effects of water movement on prey capture and distribution of reef corals. Hydrobiology 226:91–101

    Article  Google Scholar 

  • Sebens KP, Vandersall KS, Savina LA, Graham KR (1996) Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in a field enclosure. Mar Biol 127:303–317

    Article  Google Scholar 

  • Sebens KP, Grace SP, Helmuth B, Maney EJ Jr, Miles JS (1998) Water flow and prey capture by three scleractinian corals, Madracis mirabilis, Montastrea cavernosa and Porites porites, in a field enclosure. Mar Biol 131:347–360

    Article  Google Scholar 

  • Sebens KP, Helmuth B, Carrington E, Agius B (2003) Effects of water flow on growth and energetics of the scleractinian coral Agaricia tenuifolia in Belize. Coral Reefs 22:35–47

    Google Scholar 

  • Shick J, Ferrier-Pages C, Grover R, Allemand D (2005) Effects of starvation, ammonium concentration, and photosynthesis on UV-dependent accumulation of mycosporine-like amino acids (MAAs) in the coral Stylophora pistillata. Mar Ecol Progr Ser 295:135–156

    Article  CAS  Google Scholar 

  • Smith DJ, Suggett DJ, Baker NR (2005) Is photoinhibtition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Glob Change Biol 11:1–11

    Article  Google Scholar 

  • Sokal R, Rohlf FJ (1995) Biometry. Freeman, New York

    Google Scholar 

  • Suharsono, Brown BE (1992) Comparative measurements of mitotic index in zooxanthellae from a symbiotic cnidarian subject to temperature increase. J Exp Mar Biol Ecol 158:179–188

  • Szmant-Froelich A (1981) Coral nutrition: comparison of the fate of 14C from ingested labelled brine shrimp and from the uptake of NaH14CO3 by its zooxanthellae. J Exp Mar Biol Ecol 55:133–144

    Article  CAS  Google Scholar 

  • Takahashi S, Nakamura T, Sakamizu M, van Woesik R, Yamasaki H (2004) Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol 45:251–255

    Article  PubMed  CAS  Google Scholar 

  • Titlyanov E, Bil’ K, Fomina I, Titlyanova T, Leletkin V, Eden N, Malkin A, Dubinsky Z (2000) Effects of dissolved ammonium addition and host feeding with Artemia salina on photoacclimation of the hermatypic coral Stylophora pistillata. Mar Biol 137:463–472

    Article  CAS  Google Scholar 

  • Titlyanov EA, Titlyanova TV, Yamazato K, van Woesik R (2001) Photoacclimatation of the hermatypic coral Stylophora pistillata while subject to either starvation or food provisioning. J Exp Mar Biol Ecol 257:163–181

    Article  PubMed  Google Scholar 

  • Underwood A (1997) Experiments in ecology. Their logical design and interpretation using analysis of variances. Cambridge University Press, Cambridge

  • Wang JT, Douglas AE (1999) Essential amino acid synthesis and nitrogen recycling in an alga-invertebrate symbiosis. Mar Biol 135:219–222

    Article  CAS  Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell Environ 19:291–299

    Article  Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012

    Article  PubMed  CAS  Google Scholar 

  • Warner ME, Chilcoat GC, McFarland FK, Fitt WK (2002) Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Carribean reef-building coral Montastrea. Mar Biol 141:31–38

    Article  CAS  Google Scholar 

  • Yakovleva I, Bhagooli R, Takemura A, Hidaka M (2004) Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine. Comp Biochem Physiol B 139:721–730

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank the staff at the University Hasanuddin in Makassar for allowing us to use the facilities. We also thank R. A. Coleman and W. Wosniok for advice on the statistical analyses. This study was carried out as part of the German-Indonesian SPICE Programme (BMBF grant no. 03F0390A).

Author information

Authors and Affiliations

  1. Zentrum für Marine Tropenökologie (ZMT)/Center for Tropical Marine Ecology, Fahrenheitstrasse 6, 28359, Bremen, Germany

    Esther M. Borell & Kai Bischof

Authors
  1. Esther M. Borell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kai Bischof
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Esther M. Borell.

Additional information

Communicated by Craig Osenberg.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Borell, E.M., Bischof, K. Feeding sustains photosynthetic quantum yield of a scleractinian coral during thermal stress. Oecologia 157, 593–601 (2008). https://doi.org/10.1007/s00442-008-1102-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-008-1102-2

Keywords

Search

Navigation