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Oecologia

, Volume 136, Issue 4, pp 524–531 | Cite as

Reproductive energy investment in corals: scaling with module size

  • Sebastian Leuzinger
  • Kenneth R. N. Anthony
  • Bette L. Willis
Ecophysiology

Abstract

In colonial modular organisms, differences in module size and colony growth patterns among species have the potential to impose varying constraints on reproductive investment. Here, we compare reproductive output among seven morphologically different species of spawning reef corals, and analyse the relationship between reproductive output and module (polyp) size. Reproductive output ranged between 132 and 384 J cm−2, with lipid constituting the key indicator of energy investment. Lipid decreased by 85–100%, whereas protein and carbohydrate were relatively invariant between pre- and post-spawning tissues in all species, representing 1–15% and <1%, respectively, of the energy investment to reproductive output. The ratio of energy content in reproductive to somatic tissues (gonadosomatic index, GSI) varied among species from 0.20 (Symphyllia recta) to 1.31 (Acropora tenuis), the latter being the highest value reported for any iteroparous marine invertebrate. Surprisingly, small-polyped species (Acropora, Montipora) had 2- to 6-fold higher GSIs than large-polyped ones (Lobophyllia, Symphyllia). Energy equivalents of tissues increased with the 1.50–1.76 power of polyp diameter for somatic tissues and with the 1.42–1.80 power of polyp diameter for reproductive output. In both cases, increases in energy equivalents with polyp diameter were less than the scaling exponent of 3 predicted for an isometric relationship between tissue volume (or mass) and polyp diameter, indicating significant constraints of space, design or physiological energetics with increasing polyp size. We hypothesise that such constraints have played a key role in the evolution of modularity in cnidarians.

Keywords

Energy investment Reproduction Geometric constraints Biochemistry Scleractinian coral 

Notes

Acknowledgements

We are grateful to Noel Nevers, Sarah Dalesman and Vincent Riviere for assistance in the field and to the staff of Orpheus Island Research Station. We thank Phil Munday, Julian Caley and Andrew Baird for their critical reading and valuable comments. Two anonymous reviewers provided helpful comments that improved the manuscript. The research was supported by grants from the Australian Research Council to K.R.N.A. (A00105071) and to BLW (A 19933007) and a CRC Reef Research Award to S.L. This is contribution number 74 from the Centre for Coral Reef Biodiversity and number 199 from the Coral Ecology Group at James Cook University.

References

  1. Achituv Y, Ben-Zion M, Mizrahi L (1994) Carbohydrate, lipid, and protein composition of zooxanthellae and animal fractions of the coral Pocillopora damicornis exposed to ammonium enrichment. Pac Sci 48:224–233Google Scholar
  2. Anderson JF (1978) Energy content of spider eggs. Oecologia 37:29–58Google Scholar
  3. Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253PubMedGoogle Scholar
  4. Arai T, Kato M, Heyward A, Ikeda Y, T Iizuka T, Maruyama T (1993) Lipid composition of positively buoyant eggs of reef building corals. Coral Reefs 12:71–75Google Scholar
  5. Babcock RC (1991) Comparative demography of three species of scleractinian corals using age- and size-dependent classifications. Ecol Monogr 61:225–244Google Scholar
  6. Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Mar Biol 90:379–394Google Scholar
  7. Ben-David-Zaslow R, Benayahu Y (1999) Temporal variation in lipid, protein and carbohydrate content in the Red Sea soft coral Heteroxenia fuscescens. J Mar Biol Assoc UK 79:1001–1006Google Scholar
  8. Calow P (1978) The evolution of life-cycle strategies in freshwater gastropods. Malacologia 17:351–364Google Scholar
  9. Calow P (1979) The cost of reproduction—a physiological approach. Biol Rev 54:23–40Google Scholar
  10. Calow P (1987) Evolutionary physiological ecology. Cambridge University Press, New YorkGoogle Scholar
  11. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–358Google Scholar
  12. Efron B, Tibshirani RJ (1993) An introduction to the bootstrap. Chapman and Hall, New YorkGoogle Scholar
  13. Fitt K, Howard JS, Halas J, Michael WW, James WP (1993) Recovery of the coral Montastrea annularis in the Florida Keys after the 1987 Caribbean "bleaching event". Coral Reefs 12:57–64Google Scholar
  14. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509Google Scholar
  15. Gnaiger E, Bitterlich G (1984) Proximate biochemical composition and calorific content calculated from elemental CHN analysis: a stochiometric concept. Oecologia 62:289–298Google Scholar
  16. Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194CrossRefGoogle Scholar
  17. Gunderson DR (1997) Trade-off between reproductive effort and adult survival in oviparous and viviparous fishes. Can J Fish Aquat Sci 54:990–998CrossRefGoogle Scholar
  18. Hall VR, Hughes TP (1996) Reproductive strategies of modular animals: comparative studies of reef-building corals. Ecology 77:950–963Google Scholar
  19. Harland AD, Fixter LM, Davies PS, Anderson RA (1991) Distribution of lipids between the zooxanthellae and animal compartment in the symbiotic sea anemone Anemonia viridis: wax esters, triglycerides and fatty acids. Mar Biol 110:13–19Google Scholar
  20. Harland AD, Fixter LM, Davies PS, Anderson RA (1992a) Effect of light on the total lipid content and storage lipids of the symbiotic sea anemone Anemonia viridis. Mar Biol 112:253–258Google Scholar
  21. Harland AD, Davies PS, Fixter LM(1992b) Lipid content of some Caribbean corals in relation to depth and light. Mar Biol 113:357–361Google Scholar
  22. Harrison PL, Wallace CC (1990) Reproduction, dispersal, and recruitment of scleractinian corals. In: Dubinsky Z (ed) Ecosystems of the world, coral reefs. Elsevier, Amsterdam, pp 133–207Google Scholar
  23. Harrison PL, Babcock RC, Bull GD, OliverJK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223:1186–1189Google Scholar
  24. Highsmith RC (1982) Reproduction by fragmentation in corals. Mar Ecol Prog Ser 7:207–226Google Scholar
  25. Hughes TP, Connell J, Ayre D (1992) The evolutionary ecology of corals. Trends Ecol Evol 7:292–295Google Scholar
  26. Lang JC, Chornesky EA (1990) Competition between scleractinian reef corals: a review of mechanisms and effects. In: Dubinsky Z (ed) Ecosystems of the world, coral reefs. Elsevier, Amsterdam, pp 209–252Google Scholar
  27. Maltby L (1999) Studying stress: the importance of organism-level responses. Ecol Appl 9:431–440Google Scholar
  28. Marsh JA (1970) Primary productivity of reef-building calcareous red algae. Ecology 51:255–263Google Scholar
  29. Michaelek-Wagner K, Willis BL (2001) Impacts of bleaching on the soft coral Lobophytum compactum. II. Biochemical changes in adults and their eggs. Coral Reefs 19:240–246Google Scholar
  30. Pearse JS, Pearse VB, Newberry AT (1989) Telling sex from growth: dissolving Maynard-Smith's paradox. Bull Mar Sci 45:433–446Google Scholar
  31. Sakai K (1998) Effect of colony size, polyp size, and budding mode on egg production in a colonial coral. Biol Bull 195:319–325Google Scholar
  32. Schaffer WM (1983) The application of optimal control theory to the general life history problem. Am Nat 121:418–431CrossRefGoogle Scholar
  33. Sebens KP (1981) The allometry of feeding, energetics, and body size in three sea anemone species. Biol Bull 161:152–171Google Scholar
  34. Sebens KP (1987) The ecology of indeterminate growth in animals. Annu Rev Ecol Syst 18:371–407CrossRefGoogle Scholar
  35. Shine R, Schwarzkopf L (1992) The evolution of reproductive effort in lizards and snakes. Evolution 46:62–75Google Scholar
  36. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  37. 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
  38. Stobart B, Babcock RC, Willis BL (1992) Biannual spawning of three species of scleractinian coral from the Great Barrier Reef. Proc 7th Int Coral Reef Symp 1:494–499Google Scholar
  39. Szmant-Froelich A, Pilson MEQ (1980) The Effects of feeding frequency and symbiosis with zooxanthellae on the biochemical composition of Astrangia danae. J Exp Mar Biol Ecol 48:85–98Google Scholar
  40. Van Den Berghe EP (1992) Parental care and the cost of reproduction in a Mediterranean fish. Behav Ecol Sociobiol 30:373–378Google Scholar
  41. Veron JEN (1986) Corals of Australia and the Indo-Pacific, 2nd edn. University of Hawaii Press, HonoluluGoogle Scholar
  42. Ward S (1995a) Two patterns of energy allocation for growth, reproduction and lipid storage in the scleractinian coral Pocillopora damicornis. Coral Reefs 14:87–90Google Scholar
  43. Ward S (1995b) The effect of damage on the growth, reproduction and storage of lipids in the scleractinian coral Pocillopora damicornis (Linnaeus). J Exp Mar Biol Ecol 187:193–206CrossRefGoogle Scholar
  44. Williams GC (1975) Sex and evolution. Princeton University Press, New JerseyGoogle Scholar
  45. Willis BL, Babcock RC, Harrison PL, Oliver JK, Wallace CC (1985) Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984. Proceedings of the 5th Int Coral Reef Symposium, pp 343–348Google Scholar
  46. Yamashiro H, Oku H, Higa H, Chinen I, Sakai K (1999) Composition of lipids, fatty acids and sterols in Okinawan corals. Comp Biochem Physiol B. 122:397–407Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Sebastian Leuzinger
    • 1
  • Kenneth R. N. Anthony
    • 1
    • 2
  • Bette L. Willis
    • 1
  1. 1.School of Marine Biology and AquacultureJames Cook UniversityTownsvilleAustralia
  2. 2.Centre for Coral Reef BiodiversityJames Cook UniversityTownsvilleAustralia

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