Coral color and depth drive symbiosis ecology of Montipora capitata in Kāne‘ohe Bay, O‘ahu, Hawai‘i

Abstract

Scleractinian corals form symbioses with diverse photosynthetic dinoflagellates (genus Symbiodinium) that confer varying levels of performance and stress tolerance to their hosts. Variation in thermal stress susceptibility (i.e., bleaching) among conspecific corals is linked to variability in symbiont community composition, yet factors driving heterogeneous symbiont associations within a population are poorly understood. To investigate potential drivers, we characterized Symbiodinium communities in Montipora capitata (N = 707 colonies) across the biophysical regions, reef types, and depth range of Kāne‘ohe Bay (Hawai‘i, USA), where this dominant reef-builder associates with Symbiodinium spp. in clade C (C31) and/or D (S. glynnii), and occurs as brown and orange color morphs. The distribution of these traits was primarily influenced by depth: orange, D-dominated colonies were more prevalent in shallow, high light environments (< 2 m), whereas brown, C-dominated colonies were more prevalent with increasing depth and light attenuation. Though either color morph could be dominated by either symbiont, brown colonies were almost exclusively C-dominated, while orange colonies were more likely to be D-dominated above 4.3 m, and C-dominated below, revealing a significant interaction between color morph and symbiosis ecology. The distribution of orange, D-dominated colonies extended deeper on patch reefs, where light penetrates deeper, compared to the more turbid, fringing reefs, further supporting light as the driver of these patterns. This work reveals that symbiont community variability may arise either from holobiont phenotypic plasticity or differential survival across light gradients, with implications for predicting coral bleaching responses and informing management applications such as selective breeding of robust corals.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Notes

  1. 1.

    Formerly referred to as ITS2 type D1-4-6 (sensu LaJeunesse et al. 2010) and mistakenly characterized in Hawai‘i as D1a by LaJeunesse et al. (2004a, b) (see Wham et al. 2017).

References

  1. Bahr KD, Bruno J, Jokiel PL, Toonen RJ (2015) The unnatural history of Kane’ohe Bay: coral reef resilience in the face of centuries of anthropogenic impacts. PeerJ 3:e950

    Article  PubMed  PubMed Central  Google Scholar 

  2. Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst 40:551–571

    Article  Google Scholar 

  3. Baker AC (2001) Ecosystems: reef corals bleach to survive change. Nature 411:765–766

    Article  PubMed  CAS  Google Scholar 

  4. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

    Article  Google Scholar 

  5. Baker DM, Andras JP, Jordán-Garza AG, Fogel ML (2013) Nitrate competition in a coral symbiosis varies with temperature among Symbiodinium clades. ISME J 7:1248–1251

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193

    Article  Google Scholar 

  7. Bongaerts P, Carmichael M, Hay KB, Tonk L, Frade PR, Hoegh-guldberg O (2015) Prevalent endosymbiont zonation shapes the depth distributions of scleractinian coral species. Proc R Soc Open Sci 2:1–11

    Google Scholar 

  8. 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 28:405–414

    Article  Google Scholar 

  9. Chen CA, Wang JT, Fang LS, Yang YW (2005) Fluctuating algal symbiont communities in Acropora palifera (Scleractinia: acroporidae) from Taiwan. Mar Ecol Prog Ser 295:113–121

    Article  Google Scholar 

  10. Cooper TF, Ulstrup KE, Dandan SS, Heyward AJ, Kühl M, Muirhead A, O’Leary RA, Ziersen BEF, van Oppen MJH (2011) Niche specialization of reef-building corals in the mesophotic zone: metabolic trade-offs between divergent Symbiodinium types. Proc R Soc B 278:1840–1850

    Article  PubMed  Google Scholar 

  11. Cunning R (2016) Data for: patterns of bleaching and recovery of Montipora capitata in Kāne‘ohe Bay, Hawai‘i, USA (version 1.0). Zenodo. http://doi.org/10.5281/zenodo.53231

  12. Cunning R, Baker AC (2013) Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Change 3:259–262

    Article  Google Scholar 

  13. Cunning R, Silverstein RN, Baker AC (2015) Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change. Proc R Soc B 282:20141725

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Cunning R, Ritson-Williams R, Gates RD (2016) Patterns of bleaching and recovery of Montipora capitata in Kāne‘ohe Bay, Hawai‘i, USA. Mar Ecol Prog Ser 551:131–139

    Article  CAS  Google Scholar 

  15. D’Angelo C, Denzel A, Vogt A, Matz MV, Oswald F, Salih A, Nienhaus GU, Wiedenmann J (2008) Blue light regulation of host pigment in reef-building corals. Mar Ecol Prog Ser 364:97–106

    Article  CAS  Google Scholar 

  16. DeSalvo MK, Estrada A, Sunagawa S, Medina M (2012) Transcriptomic responses to darkness stress point to common coral bleaching mechanisms. Coral Reefs 31:215–228

    Article  Google Scholar 

  17. Ezzat L, Maoz F, Maguer JF, Grover R, Ferrier-Pagès C (2017) Carbon and nitrogren acquisition in shallow and deep holobionts of the Scleractinian coral S. pistillata. Front Mar Sci 4:102

    Article  Google Scholar 

  18. Frade PR, Englebert N, Faria J, Visser PM, Bak RPM (2008a) Distribution and photobiology of Symbiodinium types in different light environments for three colour morphs of the coral Madracis pharensis: is there more to it than total irradiance? Coral Reefs 27:913–925

    Article  Google Scholar 

  19. Frade PR, de Jonghe F, Vermuelen F, van Bleuswuk J, Bak RPM (2008b) Variation in symbiont distribution between closely related coral species over large depth ranges. Mol Ecol 17:691–703

    Article  PubMed  CAS  Google Scholar 

  20. Gittins JR, D’Angelo C, Oswald F, Edwards RJ, Wiedenmann J (2015) Fluorescent protein-mediated colour polymorphism in reef corals: multicopy genes extend the adaptation/acclimatization potential to variable light environments. Mol Ecol 24:453–465

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Glynn PW, Maté JL, Baker AC, Calderón MO (2001) Coral bleaching and mortality in Panama and Ecuador during the 1997–1998 El Niño-Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bull Mar Sci 69:79–109

    Google Scholar 

  22. Grigg RW (1965) Ecological studies of black corals in Hawaii. Pac Sci 19:244–259

    Google Scholar 

  23. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Knowlton N (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  PubMed  CAS  Google Scholar 

  24. Iglesias-Prieto R, Beltrá NVH, Lajeunesse TC, Reyes-Bonilla H, Thomé PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc B 271:1757–1763

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Innis T, Cunning R (2018) Data for: Coral color and depth drive symbiosis ecology of Montipora capitata in Kāne‘ohe Bay, O‘ahu, Hawai‘i (Version v1.0.0). Zenodo. https://doi.org/10.5281/zenodo.1172180

  26. Jacobson EC (2005) Light attenuation in a nearshore coral reef ecosystem. Master’s thesis, University of Hawaii at Manoa, Honolulu, HI

  27. Jokiel PL, Coles SL (1977) Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar Biol 43:201–208

    Article  Google Scholar 

  28. Jones AM, Berkelmans R, Van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc B 275:1359–1365

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Kelmanson IV, Matz MV (2003) Molecular basis and evolutionary origins of color diversity in great star coral Montastraea cavernosa (Scleractinia: Faviida). Mol Biol Evol 20:1125–1133

    Article  PubMed  CAS  Google Scholar 

  30. LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown BE, Obura DO, Hoegh-Guldberg O, Fitt WK (2010) Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37:785–800

    Article  Google Scholar 

  31. LaJeunesse TC, Thornhill DJ, Cox EF, Stanton F, Fitt WK, Schmidt GW (2004a) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596–603

    Google Scholar 

  32. LaJeunesse TC, Thornhill DJ (2011) Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolution through psbA non-coding region genotyping. PLoS One 6:e29013

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, Schmidt GW (2004b) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596–603

    Google Scholar 

  34. Little AF, van Oppen M, Willis BL (2004) Flexibility in algal endosymbiosis: shapes growth in reef corals. Science 304:1492–1494

    Article  PubMed  CAS  Google Scholar 

  35. Lowe RJ, Falter JL, Monismith SG, Atkinson MJ (2009) Wave-driven circulation of a coastal reef-lagoon system. J Phys Oceanogr 39:873–893

    Article  Google Scholar 

  36. Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460

    Article  Google Scholar 

  37. Oswald F, Schmitt F, Leutenegger A, Ivanchenko S, D’Angelo C, Salih A, Matz MV (2007) Contributions of host and symbiont pigments to the coloration of reef corals. FEBS J 274:1102–1122

    Article  PubMed  CAS  Google Scholar 

  38. 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:e38440

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Pettay DT, Wham DC, Smith RT, Iglesias-Prieto R, LaJeunesse TC (2015) Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella. Proc Natl Acad Sci USA 112:7513–7518

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai‘i. Mol Phylogenet Evol 56:492–497

    Article  PubMed  CAS  Google Scholar 

  41. Poland DM, Coffroth MA (2016) Trans-generational specificity within a cnidarian–algal symbiosis. Coral Reefs 36:119–129

    Article  Google Scholar 

  42. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://R-project.org/

  43. Ritson-Williams R, Gates RD (2016a) Kaneohe Bay seawater temperature data 2014 and 2015. Zenodo. https://doi.org/10.5281/zenodo.53226

    Article  Google Scholar 

  44. Ritson-Williams R, Gates RD (2016b) Kaneohe Bay light data 2014 and 2015. Zenodo. https://doi.org/10.5281/zenodo.53227

    Article  Google Scholar 

  45. Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742

    Article  PubMed  CAS  Google Scholar 

  46. Rowan R, Knowlton N, Paine RT (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci USA 92:2850–2853

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269

    Article  PubMed  CAS  Google Scholar 

  48. Salih A, Larkum A, Cox G, Kühl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853

    Article  PubMed  CAS  Google Scholar 

  49. Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S (2007) Niche partitioning of closely related symbiotic dinoflagellates. Mol Ecol 16:3721–3733

    Article  PubMed  CAS  Google Scholar 

  50. Shore-Maggio A, Runyon CM, Ushijima B, Aeby GS, Callahan SM (2015) Differences in bacterial community structure in two color morphs of the Hawaiian reef coral Montipora capitata. Appl Env Microbiol 81:7312–7318

    Article  CAS  Google Scholar 

  51. Silverstein RN, Correa AMS, Baker AC (2012) Specificity is rarely absolute in coral-algal symbiosis: implications for coral response to climate change. Proc R Soc B 279:2609–2618

    Article  PubMed  PubMed Central  Google Scholar 

  52. Smith SV, Kimmerer WJ, Laws EA, Brock RE, Walsh TW (1981) Kaneohe Bay Sewage Diversion Experiment: perspectives on ecosystem responses to nutritional perturbation. Pac Sci 35:279–395

    CAS  Google Scholar 

  53. Stat M, Bird CE, Pochon X, Chasqui L, Chauka LJ, Concepcion GT, Logan D, Takabayashi M, Toonen RJ, Gates RD (2011) Variation in Symbiodinium ITS2 sequence assemblages among coral colonies. PLoS One 6:e15854

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Takabayashi M, Hoegh-Guldberg O (1995) Ecological and physiological differences between two colour morphs of the coral Pocillopora damicornis. Mar Biol 123:705–714

    Article  Google Scholar 

  55. Thornhill DJ, Fitt WK, Schmidt GW (2006) Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25:515–519

    Article  Google Scholar 

  56. Todd P, Sidle R, Chou L (2002) Plastic corals from Singapore: 2. Coral reefs 21:407–408

    Google Scholar 

  57. Toller WW, Rowan R, Knowlton N (2001) Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol Bull 201:360–373

    Article  PubMed  CAS  Google Scholar 

  58. van Oppen MJH, Oliver JK, Putnam HM, Gates RD (2015) Building coral reef resilience through assisted evolution. Proc Natl Acad Sci USA 112:2307–2313

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Wham DC, Ning G, LaJeunesse TC (2017) Symbiodinium glynnii sp. nov., a species of stress-tolerant symbiotic dinoflagellates from pocilloporid and montiporid corals in the Pacific Ocean. Phycologia 56:396–409

    Article  Google Scholar 

  60. Yuyama I, Harii S, Hidaka M (2012) Algal symbiont type affects gene expression in juveniles of the coral Acropora tenuis exposed to thermal stress. Mar Env Res 76:41–47

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank J. Levy, D. Fant and A. Wen for field assistance and the Hawai‘i Department of Aquatic Resources for authorizing coral sample collection (SAP 2016-69 and SAP 2016-55). TI thanks M. Patterson, J. Grabowski and L. Magee for mentorship. RC was supported by NSF PRFB #1400787. CW and RRW were partially funded by Environmental Protection Agency (EPA) STAR Fellowships #FP-91779401-1 and #FP-917660. The views expressed in this publication have not been reviewed or endorsed by the EPA and are solely those of the authors.

Author information

Affiliations

Authors

Corresponding author

Correspondence to R. Cunning.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Topic Editor Dr. Simon Davy

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Innis, T., Cunning, R., Ritson-Williams, R. et al. Coral color and depth drive symbiosis ecology of Montipora capitata in Kāne‘ohe Bay, O‘ahu, Hawai‘i. Coral Reefs 37, 423–430 (2018). https://doi.org/10.1007/s00338-018-1667-0

Download citation

Keywords

  • Symbiodinium
  • Symbiosis
  • Coral pigment
  • Polymorphism