Coral Reefs

, Volume 32, Issue 1, pp 137–152 | Cite as

Are all eggs created equal? A case study from the Hawaiian reef-building coral Montipora capitata

  • Jacqueline L. Padilla-Gamiño
  • Robert R. Bidigare
  • Daniel J. Barshis
  • Ada Alamaru
  • Laetitia Hédouin
  • Xavier Hernández-Pech
  • Frederique Kandel
  • Sherril Leon Soon
  • Melissa S. Roth
  • Lisa J. Rodrigues
  • Andrea G. Grottoli
  • Claudia Portocarrero
  • Stephanie A. Wagenhauser
  • Fenina Buttler
  • Ruth D. Gates


Parental effects have been largely unexplored in marine organisms and may play a significant role in dictating the phenotypic range of traits in coral offspring, influencing their ability to survive environmental challenges. This study explored parental effects and life-stage differences in the Hawaiian reef-building coral Montipora capitata from different environments by examining the biochemical composition of mature coral colonies and their eggs. Our results indicate that there are large biochemical differences between adults and eggs, with the latter containing higher concentration of lipids (mostly wax esters), ubiquitinated proteins (which may indicate high turnover rate of proteins) and antioxidants (e.g., manganese superoxide dismutase). Adults displayed high phenotypic plasticity, with corals from a high-light environment having more wax esters, lighter tissue δ13C signatures and higher Symbiodinium densities than adults from the low-light environment who had higher content of accessory pigments. A green-algal pigment (α-carotene) and powerful antioxidant was present in eggs; it is unclear whether this pigment is acquired from heterotrophic food sources or from endolithic green algae living in the adult coral skeletons. Despite the broad phenotypic plasticity displayed by adults, parental investment in the context of provisioning of energy reserves and antioxidant defense was the same in eggs from the different sites. Such equality in investment maximizes the capacity of all embryos and larvae to cope with challenging conditions associated with floating at the surface and to disperse successfully until an appropriate habitat for settlement is found.


Biochemical phenotype Coral eggs Coral reproduction Egg provisioning Gamete variation Maternal effects Spawner 



Special thanks to M. Sales, J. Cozo, R. Gabriel, G. Carter, M. Hagedorn, P. Duarte-Quiroga, K. Stender and the wonderful volunteers who helped to collect samples during the spawning events. Thanks to R. Briggs, S. Christensen and Y. Matsui for their invaluable technical support and to K. Ruttenberg for laboratory space. Thanks to M. Gorbunov, R. Kinzie and anonymous reviewers for their helpful comments. JLPG was supported by the Mexican National Council for Science and Technology (CONACyT), the World Bank Coral Reef Targeted Research program and the Center for Microbial Oceanography: Research and Education (C-MORE). The research was funded by the National Science Foundation (OCE-0752604 to RDG and OIA-0554657 administered by the University of Hawai’i, OCE-0542415 to AGG) and the Pauley Foundation. This is HIMB contribution number 1519, SOEST contribution number 8753 and 2007 Pauley Summer Program Contribution number 8.

Supplementary material

338_2012_957_MOESM1_ESM.docx (13 kb)
Supplementary material 1 (DOCX 13 kb)
338_2012_957_MOESM2_ESM.eps (449 kb)
Appendix I. Linear regression representing the relationship between the number of egg–sperm bundles and their respective ash-free dry weight (mg) in Montipora capitata (EPS 449 kb)
338_2012_957_MOESM3_ESM.eps (249 kb)
Appendix II. (a) δ15N and (b) N:P ratios in adults and eggs of Montipora caitata. Mean ± SE (EPS 248 kb)


  1. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image Processing with Image. J. Biophotonics International 11:36–42Google Scholar
  2. Abrego D, Ulstrup KE, Willis BL, van Oppen MJH (2008) Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc B-Biol Sci 275:2273–2282CrossRefGoogle Scholar
  3. Alamaru A, Yam R, Shemesh A, Loya Y (2009a) Trophic biology of Stylophora pistillata larvae: evidence from stable isotope analysis. Mar Ecol Prog Ser 383:85–94CrossRefGoogle Scholar
  4. Alamaru A, Loya Y, Brokovich E, Yam R, Shemesh A (2009b) Carbon and nitrogen utilization in two species of Red Sea corals along a depth gradient: Insights from stable isotope analysis of total organic material and lipids. Geochim Cosmochim Acta 73:5333–5342CrossRefGoogle Scholar
  5. Arai T, Kato M, Heyward A, Ikeda Y, Iizuka T, Maruyama T (1993) Lipid-composition of positively buoyant eggs of reef building corals. Coral Reefs 12:71–75CrossRefGoogle Scholar
  6. Badyaev AV, Uller T (2009) Parental effects in ecology and evolution: mechanisms, processes and implications. Proc R Soc B-Biol Sci 364:1169–1177Google Scholar
  7. Barshis DJ, Stillman JH, Gates RD, Toonen RJ, Smith LW, Birkeland C (2010) Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity? Mol Ecol 19:1705–1720PubMedCrossRefGoogle Scholar
  8. Bidigare RR, Van Heukelem L, Trees CC (2005) Analysis of algal pigments by high-performance liquid chromatography. In: Andersen R (ed) Algal culturing techniques. Academic Press, London, pp 327–345Google Scholar
  9. Bodin N, Le Loc’h F, Hily C (2007) Effect of lipid removal on carbon and nitrogen stable isotope ratios in crustacean tissues. J Exp Mar Biol Ecol 341:168–175CrossRefGoogle Scholar
  10. Cantin NE, van Oppen MJH, Willis BL, Mieog JC, Negri AP (2009) Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28:405–414CrossRefGoogle Scholar
  11. DeNiro MJ, Epstein S (1977) Mechanisms of carbon isotope fractionation associated with lipid synthesis. Science 197:261–263PubMedCrossRefGoogle Scholar
  12. Donelson JM, Munday PL, McCormick MI (2009) Parental effects on offspring life histories: when are they important? Biol Lett 5:262–265PubMedCrossRefGoogle Scholar
  13. Epel D, Hemela K, Shick M, Patton C (1999) Development in the floating world: Defenses of eggs and embryos against damage from UV radiation. Am Zool 39:271–278Google Scholar
  14. Figueiredo J, Baird AH, Cohen MF, Flot JF, Kamiki T, Meziane T, Tsuchiya M, Yamasaki H (2012) Ontogenetic change in the lipid and fatty acid composition of scleractinian coral larvae. Coral Reefs 31:613–619CrossRefGoogle Scholar
  15. Fine M, Loya Y (2002) Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc R Soc B-Biol Sci 269:1205–1210CrossRefGoogle Scholar
  16. Fine M, Meroz-Fine E, Hoegh-Guldberg O (2005) Tolerance of endolithic algae to elevated temperature and light in the coral Montipora monasteriata from the southern Great Barrier Reef. J Exp Biol 208:75–81PubMedCrossRefGoogle Scholar
  17. Gaither MR, Rowan R (2010) Zooxanthellar symbiosis in planula larvae of the coral Pocillopora damicornis. J Exp Mar Biol Ecol 386:45–53PubMedCrossRefGoogle Scholar
  18. Ginzburg LR (1998) Inertial growth: population dynamics based on maternal effects. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, Oxford, U.K., pp 42–53Google Scholar
  19. Govindjee Wong D, Prezelin BB, Sweeney BM (1979) Chlorophyll a fluorescence of Gonyaulax polyedra grown on a light-dark cycle and after transfer to constant light. Photochem Photobiol 30:405–411PubMedCrossRefGoogle Scholar
  20. Grasshoff K, Ehrhardt M, Kremling K (eds) (1983) Methods of seawater analysis. Verlag-Chemie, WeinheimGoogle Scholar
  21. Grottoli AG, Wellington GM (1999) Effect of light and zooplankton on skeletal delta C-13 values in the eastern Pacific corals Pavona clavus and Pavona gigantea. Coral Reefs 18:29–41CrossRefGoogle Scholar
  22. Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar Biol 145:621–631CrossRefGoogle Scholar
  23. Halliwell B, Gutteridge J (1999) Free radicals in biology and medicine. Oxford University Press, OxfordGoogle Scholar
  24. Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci USA 104:1745–1750PubMedCrossRefGoogle Scholar
  25. Harii S, Nadaoka K, Yamamoto M, Iwao K (2007) Temporal changes in settlement, lipid content and lipid composition of larvae of the spawning hermatypic coral Acropora tenuis. Mar Ecol Prog Ser 346:89–96CrossRefGoogle Scholar
  26. Harii S, Yamamoto M, Hoegh-Guldberg O (2010) The relative contribution of dinoflagellate photosynthesis and stored lipids to the survivorship of symbiotic larvae of the reef-building corals. Mar Biol 157:1215–1224CrossRefGoogle Scholar
  27. Hirose M, Kinzie RA, Hidaka M (2001) Timing and process of entry of zooxanthellae into oocytes of hermatypic corals. Coral Reefs 20:273–280CrossRefGoogle Scholar
  28. Hodgson G (1985) Abundance and distribution of planktonic coral larvae in Kaneohe bay, Oahu. Hawaii. Mar Ecol Prog Ser 26:61–71CrossRefGoogle Scholar
  29. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, 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
  30. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933PubMedCrossRefGoogle Scholar
  31. Hughes AD, Grottoli AG, Pease TK, Matsui Y (2010) Acquisition and assimilation of carbon in non-bleached and bleached corals. Mar Ecol-Prog Ser 420:91–101CrossRefGoogle Scholar
  32. Jacobs MW, Podolsky RD (2010) Variety is the spice of life histories: Comparison of intraspecific variability in marine invertebrates. Integr Comp Biol 50:630–642PubMedCrossRefGoogle Scholar
  33. Jeffrey SW (1968) Pigment composition of Siphonales algae in the brain coral Favia. Biol Bull 135:141–148CrossRefGoogle Scholar
  34. Jeffrey SW (1976) The occurrence of chlorophyll c1 and c2 in algae. J Phycol 12:349–354Google Scholar
  35. Jokiel PH, Lesser MP, Ondrusek ME (1997) UV-absorbing compounds in the coral Pocillopora damicornis: Interactive effects of UV radiation, photosynthetically active radiation, and water flow. Limnol Oceanogr 42:1468–1473CrossRefGoogle Scholar
  36. Kolinski SP (2004) Sexual reproduction and the early life history of Montipora capitata in Kane’ohe Bay, O’ahu, Hawai’i. Ph.D. thesis, University of Hawaii at Manoa, p 152Google Scholar
  37. Lee RF, Hagen W, Kattner G (2006) Lipid storage in marine zooplankton. Mar Ecol Prog Ser 307:273–306CrossRefGoogle Scholar
  38. Lesser MP (2006) Oxidative stress in marine environments: Biochemistry and physiological ecology. Annu Rev Physiol 68:253–278PubMedCrossRefGoogle Scholar
  39. Lesser MP, Stochaj WR, Tapley DW, Shick JM (1990) Bleaching in coral-reef anthozoans - Effects of irradiance, ultraviolet-radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8:225–232CrossRefGoogle Scholar
  40. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494PubMedCrossRefGoogle Scholar
  41. Lough JM (2008) 10th anniversary review: a changing climate for coral reefs. J Environ Monit 10:21–29PubMedCrossRefGoogle Scholar
  42. Magnusson SH, Fine M, Kuhl M (2007) Light microclimate of endolithic phototrophs in the scleractinian corals Montipora monasteriata and Porites cylindrica. Mar Ecol Prog Ser 332:119–128CrossRefGoogle Scholar
  43. Maragos JE (1972) A study of the ecology of Hawaiian reef corals. Dissertation, University of Hawaii, Ph.DGoogle Scholar
  44. Markey KL, Baird AH, Humphrey C, Negri AP (2007) Insecticides and a fungicide affect multiple coral life stages. Mar Ecol Prog Ser 330:127–137CrossRefGoogle Scholar
  45. Marquis CP, Baird AH, de Nys R, Holmstrom C, Koziumi N (2005) An evaluation of the antimicrobial properties of the eggs of 11 species of scleractinian corals. Coral Reefs 24:248–253CrossRefGoogle Scholar
  46. Marshall DJ, Allen RM, Crean AJ (2008) The ecological and evolutionary importance of maternal effects in the sea. Oceanogr Mar Biol Annu Rev 46:203–250CrossRefGoogle Scholar
  47. Michalek-Wagner K, Willis BL (2001) Impacts of bleaching on the soft coral Lobophytum compactum. II. Biochemical changes in adults and their eggs. Coral Reefs 19:240–246CrossRefGoogle Scholar
  48. Monaghan EJ, Ruttenberg KC (1999) Dissolved organic phosphorus in the coastal ocean: Reassessment of available methods and seasonal phosphorus profiles from the Eel River Shelf. Limnol Oceanogr 44:1702–1714CrossRefGoogle Scholar
  49. Moran AL, McAlister JS (2009) Egg size as a life history character of marine invertebrates: Is it all it’s cracked up to be? Biol Bull 216:226–242PubMedGoogle Scholar
  50. Mousseau TA, Fox CW (1998) Maternal effects as adaptations. Oxford University Press, New YorkGoogle Scholar
  51. Nesa B, Baird AH, Harii S, Yakovleva I, Hidaka M (2012) Algal symbionts increase DNA damage in coral planulae exposed to sunlight. Zool Stud 51:12–17Google Scholar
  52. Niyogi KK, Bjorkman O, Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci USA 94:14162–14167PubMedCrossRefGoogle Scholar
  53. Padilla-Gamiño JL, Gates RD (2012) Spawning dynamics in the Hawaiian reef building coral Montipora capitata. Mar Ecol Prog Ser 449:145–160CrossRefGoogle Scholar
  54. Padilla-Gamiño JL, Pochon X, Bird C, Concepcion GT, Gates RD (2012) From parent to gamete: Vertical transmission of Symbiodinium (Dinophyceae) ITS2 Sequence Assemblages in the reef building coral Montipora capitata. PLoS ONE 7(6):e38440. doi: 10.1371/journal.pone.0038440 PubMedCrossRefGoogle Scholar
  55. Palardy JE, Rodrigues LJ, Grottoli AG (2008) The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths. J Exp Mar Biol Ecol 367:180–188CrossRefGoogle Scholar
  56. Palmer CV, Modi CK, Mydlarz LD (2009) Coral fluorescent proteins as antioxidants. PLoS ONE 4(10):e7298. doi: 10.1371/journal.pone.0007298 PubMedCrossRefGoogle Scholar
  57. Papina M, Meziane T, van Woesik R (2003) Symbiotic zooxanthellae provide the host-coral Montipora digitata with polyunsaturated fatty acids. Comp Biochem Phys B 135:533–537CrossRefGoogle Scholar
  58. Pickart CM, Summers RG, Shim H, Kasperek EM (1991) Dynamics of ubiquitin pools in developing sea-urchin embryos Dev Grow Differ 33:587–598CrossRefGoogle Scholar
  59. Rinkevich B (1989) The contribution of photosynthetic products to coral reproduction. Mar Biol 101:259–263CrossRefGoogle Scholar
  60. Rodrigues LJ, Grottoli AG (2006) Calcification rate and the stable carbon, oxygen, and nitrogen isotopes in the skeleton, host tissue, and zooxanthellae of bleached and recovering Hawaiian corals. Geochim Cosmochim Acta 70:2781–2789CrossRefGoogle Scholar
  61. Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882CrossRefGoogle Scholar
  62. Rodrigues LJ, Grottoli AG, Lesser MP (2008) Long-term changes in the chlorophyll fluorescence of bleached and recovering corals from Hawaii. J Exp Biol 211:2502–2509PubMedCrossRefGoogle Scholar
  63. Rowan R (2004) Coral bleaching—Thermal adaptation in reef coral symbionts. Nature 430:742–742PubMedCrossRefGoogle Scholar
  64. Schlichter D, Zscharnack B, Krisch H (1995) Transfer of photoassimilates from endolithic algae to coral tissue. Naturwissenschaften 82:561–564CrossRefGoogle Scholar
  65. Silversand C, Haux C (1997) Improved high-performance liquid chromatographic method for the separation and quantification of lipid classes: application to fish lipids. J Chromatogr B 703:7–14CrossRefGoogle Scholar
  66. Stat M, Morris E, Gates RD (2008) Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci USA 105:9256–9261PubMedCrossRefGoogle Scholar
  67. Sultan SE (1996) Phenotypic plasticity for offspring traits in Polygonum persicaria. Ecology 77:1791–1807CrossRefGoogle Scholar
  68. Veron JEN (2000) Corals of the world. Sea Challengers, Townsville, AustraliaGoogle Scholar
  69. Wade MJ (1998) The evolutionary genetics of maternal effects. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, Oxford, UK, pp 5–21Google Scholar
  70. Wallace CC (1985) Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus Acropora. Mar Biol 88:217–233CrossRefGoogle Scholar
  71. Wellington GM, Fitt WK (2003) Influence of UV radiation on the survival of larvae from broadcast-spawning reef corals. Mar Biol 143:1185–1192CrossRefGoogle Scholar
  72. Wulff RD (1986) Seed size variation in Desmodium paniculatum. 2. Effects on seedling growth and physiological performance. J Ecol 74:99–114CrossRefGoogle Scholar
  73. Yakovleva IM, Baird AH, Yamamoto HH, Bhagooli R, Nonaka M, Hidaka M (2009) Algal symbionts increase oxidative damage and death in coral larvae at high temperatures. Mar Ecol Prog Ser 378:105–112CrossRefGoogle Scholar
  74. Zhukova NV, Titlyanov EA (2003) Fatty acid variations in symbiotic dinoflagellates from Okinawan corals. Phytochem 62:191–195CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Jacqueline L. Padilla-Gamiño
    • 1
    • 2
    • 11
  • Robert R. Bidigare
    • 1
    • 2
  • Daniel J. Barshis
    • 1
    • 3
  • Ada Alamaru
    • 4
  • Laetitia Hédouin
    • 1
    • 5
  • Xavier Hernández-Pech
    • 6
  • Frederique Kandel
    • 1
  • Sherril Leon Soon
    • 1
    • 2
  • Melissa S. Roth
    • 7
    • 8
  • Lisa J. Rodrigues
    • 9
  • Andrea G. Grottoli
    • 10
  • Claudia Portocarrero
    • 1
  • Stephanie A. Wagenhauser
    • 1
  • Fenina Buttler
    • 2
  • Ruth D. Gates
    • 1
  1. 1.Hawaii Institute of Marine BiologyUniversity of HawaiiKaneoheUSA
  2. 2.Department of OceanographyUniversity of HawaiiHonoluluUSA
  3. 3.Hopkins Marine StationStanford UniversityPacific GroveUSA
  4. 4.Department of ZoologyTel Aviv UniversityTel AvivIsrael
  5. 5.USR 3278 CNRS-EPHE-CRIOBE, Laboratoire d’excellence “CORAIL”Université de PerpignanPerpignan CedexFrance
  6. 6.ICMyLUniversidad Nacional Autónoma de MéxicoPuerto MorelosMexico
  7. 7.Physical Biosciences DivisionLawrence Berkeley National LaboratoryBerkeleyUSA
  8. 8.Department of Plant and Microbial BiologyUC BerkeleyBerkeleyUSA
  9. 9.Department of Geography and EnvironmentVillanova UniversityVillanovaUSA
  10. 10.School of Earth SciencesOhio State UniversityColumbusUSA
  11. 11.Ecology, Evolution and Marine BiologyUC Santa BarbaraSanta BarbaraUSA

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