Coral Reefs

, Volume 32, Issue 1, pp 25–33 | Cite as

Using energetic budgets to assess the effects of environmental stress on corals: are we measuring the right things?

Perspective

Abstract

Historically, the response of marine invertebrates to their environment, and environmentally induced stress, has included some measurement of their physiology or metabolism. Eventually, this approach developed into comparative energetics and the construction of energetic budgets. More recently, coral reefs, and scleractinian corals in particular, have suffered significant declines due to climate change-related environmental stress. In addition to a number of physiological, biophysical and molecular measurements to assess “coral health,” there has been increased use of energetic approaches that have included the measurement of specific biochemical constituents (i.e., lipid concentrations) as a proxy for energy available to assess the potential outcomes of environmental stress on corals. In reading these studies, there appears to be some confusion between energy budgets and carbon budgets. Additionally, many assumptions regarding proximate biochemical composition, metabolic fuel preferences and metabolic quotients have been made, all of which are essential to construct accurate energy budgets and to convert elemental composition (i.e., carbon) to energy equivalents. Additionally, models of energetics such as the metabolic theory of ecology or dynamic energy budgets are being applied to coral physiology and include several assumptions that are not appropriate for scleractinian corals. As we assess the independent and interactive effects of multiple stressors on corals, efforts to construct quantitative energetic budgets should be a priority component of realistic multifactor experiments that would then improve the use of models as predictors of outcomes related to the effects of environmental change on corals.

Keywords

Energy budgets Metabolism Carbon budgets Climate change Corals 

Notes

Acknowledgments

The author would like to thank NSF, ONR and NOAA for supporting his work on coral biology, biochemistry and physiology. The manuscript was significantly improved in critical areas by comments from Bill Zamer. A special thank you to Lisa Rodrigues and Andrea Grottoli for access to original data.

References

  1. Achituv Y, Ben-Zion M, Mizrah L (1994) Carbohydrate, lipid, and protein composition of zooxanthellae and animal fraction of the coral Pocillopora damicornis exposed to ammonium enrichment. Pac Sci 48:224–233Google Scholar
  2. Alunno-Bruscia M, Bourlés, Maurer D, Robert C, Mazurié J, Gangnery A, Goulletquer P, Pouvreau S (2011) A single bio-energetics growth and reproduction model for the oyster Crassostrea gigas in six Atlantic ecosystems. J Sea Res 66: 340–348Google Scholar
  3. Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253PubMedCrossRefGoogle Scholar
  4. Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R (2009) Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol 23:359–550CrossRefGoogle Scholar
  5. Banaszak AT, Lesser MP (2009) Effects of solar ultraviolet radiation on coral reef organisms. Photochem Photobiol Sci 8:1276–1294PubMedCrossRefGoogle Scholar
  6. Bayne B, Newell RC (1983) Physiological energetics of marine molluscs. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca, Vol 4. Physiology, Part 1, pp 407–515Google Scholar
  7. Brody S (1945) Bioenergetics and growth. Reinhold Publishing Corp, New York, NY, p 1033Google Scholar
  8. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789CrossRefGoogle Scholar
  9. Coma R, Ribes M, Gili J-M, Zabala M (1998) An energetic approach to the study of life-history traits of two modular colonial benthic invertebrates. Mar Ecol Prog Ser 162:89–103CrossRefGoogle Scholar
  10. Crisp DJ (1971) Energy flow measurements. In: Holme NA, McJntyre AD (eds) Methods for the study of marine benthos. IBP Handbook 16, Blackwell Scientific Publications, 2nd edition, Oxford, pp 284–372Google Scholar
  11. Crisp DJ (1984) Energy flow measurements. In: Holme NA, McJntyre AD (eds) Methods for the study of marine benthos. IBP Handbook 16, Blackwell Scientific Publications, Oxford, pp 284–372Google Scholar
  12. Davies PS (1991) Effect of daylight variation on the energy budgets of shallow-water corals. Mar Biol 108:137–144CrossRefGoogle Scholar
  13. Dykens JA, Shick JM (1982) Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature 297:579–580CrossRefGoogle Scholar
  14. Edmunds PJ, Davies PS (1986) An energy budget for Porites porites (Scleractinia). Mar Biol 92:339–347CrossRefGoogle Scholar
  15. Edmunds PJ, Davies PS (1988) Post-illumination stimulation of respiration rate in the coral Porites porites. Coral Reefs 7:7–9CrossRefGoogle Scholar
  16. Edmunds PJ, Davies PS (1989) An energy budget for Porites porites (Scleractinia), growing in a stressed environment. Coral Reefs 8:37–43CrossRefGoogle Scholar
  17. Edmunds PJ, Gates RD (2003) Has coral bleaching delayed our understanding of fundamental aspects of coral-dinoflagellate symbioses? Bioscience 53:976–980CrossRefGoogle Scholar
  18. Edmunds PJ, Putnam HM, Nisbet RM, Muller EB (2011) Benchmarks in organism performance and their use in comparative analyses. Oecologia 167:379–390PubMedCrossRefGoogle Scholar
  19. Eynaud Y, Nisbet RM, Muller EB (2011) Impact of excess and harmful radiation on energy budgets in scleractinian corals. Ecol Model 222:1315–1322CrossRefGoogle Scholar
  20. Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and the bioenergetics of a symbiotic coral. Bioscience 34:705–709CrossRefGoogle Scholar
  21. Feder ME, Walser J-C (2005) The biological limitations of transcriptomics in elucidating stress and stress responses. J Evol Biol 18:901–910PubMedCrossRefGoogle Scholar
  22. Ferrier MD (1991) Net uptake of dissolve free amino acids by four scleractinian corals. Coral Reefs 10:183–187CrossRefGoogle Scholar
  23. Gates RD, Edmunds PJ (1999) Mechanisms of acclimatization in tropical reef corals. Am Zool 39:30–43Google Scholar
  24. Gattuso J-P, Jaubert J (1988) Computation of metabolic quotients in plant-animal symbiotic units. J Theor Biol 130:205–212CrossRefGoogle Scholar
  25. Gattuso J-P, Jaubert J (1990) Effect of light on oxygen and carbon dioxide fluxes and on metabolic quotients measured in situ in a zooxanthellate coral. Limnol Oceanogr 35:1796–1804CrossRefGoogle Scholar
  26. Gladfelter EH (1985) Metabolism, calcification and carbon budgets. II Organism level studies. Proc 5th Int Coral Reef Congr 4: 527–539Google Scholar
  27. Gnaiger E (1983) Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. In: Gnaiger E, Forstner H (eds) Polorographic oxygen sensors: Aquatic and physiological applications. Springer-Verlag, Berlin and Heidelberg, pp 337–345CrossRefGoogle Scholar
  28. Gnaiger E, Bitterlich G (1984) Proximate biochemical composition and caloric content calculated from elemental CHN analysis: a stoichiometric concept. Oecologia 62:289–298CrossRefGoogle Scholar
  29. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189PubMedCrossRefGoogle Scholar
  30. Grover R, Maguer J-F, Allemand D, Ferrier-Pagés C (2008) Uptake of dissolved free amino acids by the scleractinian coral Stylophora pistillata. J Exp Biol 211:860–865PubMedCrossRefGoogle Scholar
  31. Halldórsson HP, Svavarsson J, Granmo Å (2005) The effect of pollution on scope for growth of the mussel (Mytilus edulis L.) in Iceland. Mar Environ Res 59:47–64PubMedCrossRefGoogle Scholar
  32. Harland AD, Fixter LM, Davies PS, Anderson RA (1992) Effect of light on the total lipid content and storage lipids of the symbiotic sea anemone Anemonia viridis. Mar Biol 112:253–258CrossRefGoogle Scholar
  33. Harland AD, Navarro JC, Davies PS, Fixter LM (1993) Lipids of some Caribbean and Red Sea corals: total lipids, wax esters, triglycerides and fatty acids. Mar Biol 117:113–117CrossRefGoogle Scholar
  34. Hawkins AJS (1985) Relationships between the synthesis and breakdown of protein, dietary absorption and turnovers of nitrogen and carbon in the blue mussel, Mytilus edulis L. Oecologia 66:42–49CrossRefGoogle Scholar
  35. Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, p466Google Scholar
  36. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PJ, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedCrossRefGoogle Scholar
  37. Hofmann GE, Todgham AE (2010) Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annu Rev Physiol 72:127–145PubMedCrossRefGoogle Scholar
  38. Hoogenboom MO, Anthony KRN, Connolly SR (2006) Energetic cost of photoinhibition in corals. Mar Ecol Prog Ser 313:1–12CrossRefGoogle Scholar
  39. Hoogenboom MO, Connolly SR, Anthony KRN (2008) Interactions between morphological and physiological plasticity optimize energy acquisition in corals. Ecology 89:1144–1154PubMedCrossRefGoogle Scholar
  40. Imbs AB, Yakovleva IM (2012) Dynamics of lipid and fatty acid composition of shallow-water corals under thermal stress: an experimental approach. Coral Reefs 31:41–53CrossRefGoogle Scholar
  41. Jokiel PL (2011) The reef coral two compartment proton flux model: a new approach relating tissue-level processes to gross corallum morphology. J Exp Mar Biol Ecol 409:1–12CrossRefGoogle Scholar
  42. Jones AM, Berkelmans R (2011) Tradeoffs to thermal acclimation: energetics and reproduction of a reef coral with heat tolerant Symbiodinium type-D. J Mar Biol 185890Google Scholar
  43. Kleiber M (1975) The fire of life: An introduction to animal energetics. Krieger Publishing Co, Huntington, NY, p 453Google Scholar
  44. Kooijman SALM (1986) Population dynamics on basis of energy budgets. In: Metz JAJ, Diekmann O (eds) The dynamics of physiologically structured populations. Springer-Verlag, pp 266–297Google Scholar
  45. Kühl M, Cohen Y, Dalsgaard T, Jørgensen BB, Revsbech NP (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar Ecol Prog Ser 117:159–172CrossRefGoogle Scholar
  46. Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41:271–283CrossRefGoogle Scholar
  47. Lesser MP (2000) Depth dependent photoacclimatization to solar ultraviolet radiation in the Caribbean coral Montastraea faveolata. Mar Ecol Prog Ser 192:137–151CrossRefGoogle Scholar
  48. Lesser MP (2004) Experimental biology of coral reef ecosystems. J Exp Mar Biol Ecol 300:217–252CrossRefGoogle Scholar
  49. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278PubMedCrossRefGoogle Scholar
  50. Lesser MP (2011) Coral bleaching: Causes and mechanisms. In: Dubinsky Z, Stambler N (eds) Coral reefs: An ecosystem in transition. pp, Springer, pp 405–420CrossRefGoogle Scholar
  51. Lesser MP, Witman JD, Sebens KP (1992) Effects of flow and seston availability on scope for growth of benthic suspension-feeding invertebrates from the Gulf of Maine. Biol Bull 187:319–335CrossRefGoogle Scholar
  52. Lesser MP, Weis VM, Patterson MR, Jokiel PL (1994) Effects of morphology and water motion on carbon delivery and productivity in the reef coral, Pocillopora damicornis (Linnaeus): diffusion barriers, inorganic carbon limitation and biochemical plasticity. J Exp Mar Biol Ecol 178:153–179CrossRefGoogle Scholar
  53. Leuzinger S, Anthony KR, Willis BL (2003) Reproductive energy investment in corals: scaling with module size. Oecologia 136:524–531PubMedCrossRefGoogle Scholar
  54. Lewis S, Lesser MP (1996) Action spectrum for the effects of UV radiation on photosynthesis in the hermatypic coral Pocillopora damicornis. Mar Ecol Prog Ser 134:171–177CrossRefGoogle Scholar
  55. Marsh AG, Leong PKK, Manahan DT (1999) Energy metabolism during embryonic development and larval growth of an Antarctic sea urchin. J Exp Biol 202:2041–2050PubMedGoogle Scholar
  56. Mayfield AB, Hirst MB, Gates RD (2009) Gene expression normalization in a dual-compartment system: a real-time quantitative polymerase chain reaction protocol for symbiotic anthozoans. Mol Ecol Resources 9:462–470CrossRefGoogle Scholar
  57. McCue MN (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol Part A 156:1–18CrossRefGoogle Scholar
  58. Muller EB (2011) Synthesizing units as modeling tool for photosynthesizing organisms with photoinhibition and nutrient limitation. Ecol Model 222:637–644CrossRefGoogle Scholar
  59. Muller EB, Kooijman SALM, Edmunds PJ, Doyle FJ, Nisbet RM (2009) Dynamic energy budgets in syntrophic symbiotic relationships between heterotrophic hosts and autotrophic symbionts. J Theoret Biol 259:44–57CrossRefGoogle Scholar
  60. Muscatine L, McCloskey LR, Marian ME (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611CrossRefGoogle Scholar
  61. Nisbet RM, Jusup M, Klanjscek T, Pecquerie L (2012) Integrating dynamic energy budget (DEB) theory with traditional bioenergetics. J Exp Biol 215:892–902PubMedCrossRefGoogle Scholar
  62. Patterson MR (1992) A mass transfer explanation of metabolic scaling relations in some aquatic invertebrates and algae. Science 255:1421–1423PubMedCrossRefGoogle Scholar
  63. Porter JW, Muscatine L, Dubinsky Z, Falkowski PG (1984) Primary production and photoadaptation in light- and shade- adapted colonies of the symbiotic coral, Stylophora pistillata. Proc Roy Soc Lond 222:161–180CrossRefGoogle Scholar
  64. Porter JW, Fitt WK, Spero HJ, Rogers CS, White MW (1989) Bleaching in reef corals: physiological and stable isotopic responses. Proc Natl Acad Sci USA 86:9342–9346PubMedCrossRefGoogle Scholar
  65. Prosser CL (1991) Comparative animal physiology, Environmental and metabolic physiology 4th ed., Wiley-Blackwell, p592Google Scholar
  66. Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882CrossRefGoogle Scholar
  67. Rodrigues LJ, Grottoli AG, Pease TK (2008) Lipid class composition of bleached and recovering Porites compressa Dana, 1846 and Montipora capitata Dana, 1846 corals from Hawaii. J Exp Mar Biol Ecol 358:136–143CrossRefGoogle Scholar
  68. Sebens KP (1987) Coelenterata. In: Pandian TJ, Vernberg FJ (eds) Animal energetics, vol 1. Academic Press, New York, pp 55–120Google Scholar
  69. 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 22:35–47Google Scholar
  70. Shashar N, Cohen Y, Loya Y (1993) Extreme diel fluctuations of oxygen in diffusive boundary layers surrounding stony corals. Biol Bull 185:455–461CrossRefGoogle Scholar
  71. Shick JM (1991) A functional biology of sea anemones. Chapman and Hall, New York, p 395CrossRefGoogle Scholar
  72. Shick JM, Widdows J, Gnaiger E (1988) Calorimetric studies of behavior, metabolism and energetics of sessile intertidal animals. Am Zool 28:161–181Google Scholar
  73. Shilling FM, Manahan DT (1990) Energetics of early development for the sea urchins Strongylocentrotus pupuratus and Lytechinus pictus and the crustacean Artemia sp. Mar Biol 106:119–127CrossRefGoogle Scholar
  74. Sprung M (1984) Physiological energetics of mussel larvae (Mytilus edulis). I. Shell growth and biomass. Mar Ecol Prog Ser 17:283–293CrossRefGoogle Scholar
  75. Stimson JS (1987) Location, quantity and rate of change in quantity of lipids in tissue of Hawaiian hermatypic corals. Bull Mar Sci 41:889–904Google Scholar
  76. Stumpp M, Wren J, Melzner F, Thorndyke MC, Dupont ST (2011) CO2 induced seawater acidification impacts sea urchin larval development I: elevated metabolic rates decrease scope for growth and induce developmental delay. Comp Biochem Physiol Part A 160:331–340CrossRefGoogle Scholar
  77. Thompson R, Bayne BL (1974) Some relationships between growth, metabolism and food in the mussel, Mytilus edulis. Mar Biol 27:317–326CrossRefGoogle Scholar
  78. van der Meer J (2006) Metabolic theories in ecology. Trends Ecol Evol 21:136–140PubMedCrossRefGoogle Scholar
  79. Warner ME, Lesser MP, Ralph P (2010) Chlorophyll fluorescence in reef building corals. In: Suggett D, Prasil O, Borowitzka M (eds) Chlorophyll a fluorescence in aquatic sciences: Methods and applications. Springer, pp 209–222Google Scholar
  80. Weibel ER, Taylor CR, Hoppeler H (1991) The concept of symmorphosis: a testable hypothesis of structure-function relationship. Proc Natl Acad Sci USA 88:10357–10361PubMedCrossRefGoogle Scholar
  81. Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066PubMedCrossRefGoogle Scholar
  82. Wendt DE (2000) Energetics of larval swimming and metamorphosis in four species of Bugula (Bryozoa). Biol Bull 198:346–356PubMedCrossRefGoogle Scholar
  83. West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276:122–126PubMedCrossRefGoogle Scholar
  84. Widdows J, Bayne BL (1971) Temperature acclimation of Mytilus edulis with reference to its energy budget. J Mar Biol Assoc UK 51:827–843CrossRefGoogle Scholar
  85. Widdows J, Johnson D (1988) Physiological energetics of Mytilus edulis: scope for growth. Mar Ecol Prog Ser 46:113–121CrossRefGoogle Scholar
  86. Yin Y, Ye AJJ, Tan KSW (2009) Autophagy is involved in starvation response and cell death in Blastocyctis. Microbiology 156:665–677PubMedCrossRefGoogle 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. Zamer WE, Van Dorp W (1994) Body size and performance of pathways of carbohydrate metabolism in the sea anemone Metridium senile L. Physiol Zool 67:925–943Google Scholar
  91. Zamer WE, Shick JM, Tapley DW (1989) Protein measurement and energetic considerations: comparisons of biochemical and stoichiometric methods using bovine serum albumin and protein isolated from sea anemones. Limnol Oceanogr 34:256–263CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of Molecular, Cellular and Biomedical SciencesUniversity of New HampshireDurhamUSA

Personalised recommendations