Advertisement

Coral Reefs

, Volume 38, Issue 2, pp 359–371 | Cite as

Symbiosis and host morphological variation: Symbiodiniaceae photosynthesis in the octocoral Briareum asbestinum at ambient and elevated temperatures

  • Blake D. Ramsby
  • Tamar L. GouletEmail author
Report

Abstract

Intra-species morphological variation may occur in sessile organisms, such as corals, living in different habitats. Conversely, the octocoral Briareum asbestinum exhibits both encrusting and upright branching morphologies at the same shallow water habitat, enabling studying physiological differences uncoupled from habitat variation due to depth or reef location. We investigated the mutualism between endosymbiotic dinoflagellate algae, Breviolum spp. (previously clade B Symbiodinium), and these B. asbestinum morphologies at ambient and elevated temperatures. Based on msh1 gene sequences, the host morphologies were genetically similar although they differed in protein content, polyp expansion behavior, and associated Breviolum (B19 for encrusting and B21 for branching B. asbestinum). Due to colony orientation, polyps in encrusting B. asbestinum experienced irradiance levels nearly three times higher than polyps in the branching morph, which probably contributed to the lower photochemical and light absorption efficiencies of the Breviolum in encrusting fragments. The light-limited portion of photosynthesis–irradiance curves and the intracellular chlorophyll concentrations, however, indicated that Breviolum in both morphologies were acclimated to similar internal irradiances. Encrusting B. asbestinum exhibited higher Breviolum density, areal chlorophyll a, and greater photosynthetic rates cm−2 compared to branching B. asbestinum. Notably, elevated temperature did not cause bleaching in either morphology, as Breviolum and chlorophyll densities did not differ significantly from ambient temperature, although the two morphologies adjusted some of the measured parameters, indicating coping with the stressor. In the face of continued ocean warming, the high thermal tolerance of octocorals may reinforce the shift of Caribbean reefs from scleractinian coral to octocoral dominance.

Keywords

Caribbean Coral Climate change Zooxanthellae Symbiodinium Breviolum 

Notes

Acknowledgements

We thank the staff, scientists, particularly Dr. R. Iglesias-Prieto, and students at the Unidad Académica de Sistemas Arrecifales, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México for their assistance and M. McCauley and K.P. Shirur for help in the field. Funding for this work was provided by the Explorer’s Club to BDR and by the National Science Foundation under Grant No. IOS 0747205 to TLG. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

338_2019_1782_MOESM1_ESM.docx (17 kb)
Supplementary material 1 (DOCX 16 kb)

References

  1. Bayer FM (1961) The shallow-water Octocorallia of the West Indian region. Studies on the Fauna of Curaçao and other Caribbean Islands 12(1):1–373Google Scholar
  2. Bilewitch JP, Coates KA, Currie DC, Trapido-Rosenthal HG (2010) Molecular and morphological variation supports monotypy of the octocoral Briareum Blainville, 1830 (Octocorallia: Alcyonacea) in the Western Atlantic. Proc Biol Soc Wash 123:93–112CrossRefGoogle Scholar
  3. Brazeau DA, Harvell CD (1994) Genetic structure of local populations and divergence between growth forms in a clonal invertebrate, the Caribbean octocoral Briareum asbestinum. Mar Biol 119:53–60CrossRefGoogle Scholar
  4. Brown BE (1997) Coral bleaching - causes and consequences. Coral Reefs 16:S129-S138CrossRefGoogle Scholar
  5. Bruno JF, Edmunds PJ (1997) Clonal variation for phenotypic plasticity in the coral Madracis mirabilis. Ecology 78:2177–2190CrossRefGoogle Scholar
  6. Dubé CE, Boissin E, Maynard JA, Planes S (2017) Fire coral clones demonstrate phenotypic plasticity among reef habitats. Mol Ecol 26:3860–3869CrossRefGoogle Scholar
  7. Falkowski PG, Dubinsky Z (1981) Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature 289:172–174CrossRefGoogle Scholar
  8. Finney JC, Pettay DT, Sampayo EM, Warner ME, Oxenford HA, LaJeunesse TC (2010) The relative significance of host–habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microb Ecol 60:250–263CrossRefGoogle Scholar
  9. 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 27:913–925CrossRefGoogle Scholar
  10. Frade PR, Bongaerts P, Winkelhagen AJS, Tonk L, Bak RPM (2008b) In situ photobiology of corals over large depth ranges: a multivariate analysis on the roles of environment, host, and algal symbiont. Limnol Oceanogr 53:2711–2723CrossRefGoogle Scholar
  11. France SC, Hoover LL (2002) DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia 471:149–155CrossRefGoogle Scholar
  12. Fujiki T, Taguchi S (2002) Variability in chlorophyll a specific absorption coefficient in marine phytoplankton as a function of cell size and irradiance. J Plank Res 24:859–874CrossRefGoogle Scholar
  13. Fujioka Y (1999) Mass destruction of the hermatypic corals during a bleaching event in Ishigaki Island, southwestern Japan. Galaxea, JCRS 1:41–50CrossRefGoogle Scholar
  14. Goulet TL, Coffroth MA (2004) The genetic identity of dinoflagellate symbionts in Caribbean octocorals. Coral Reefs 23:465–472Google Scholar
  15. Goulet TL, Shirur KP, Ramsby BD, Iglesias-Prieto R (2017) The effects of elevated seawater temperatures on Caribbean gorgonian corals and their algal symbionts, Symbiodinium spp. PLoS ONE 12:e0171032CrossRefGoogle Scholar
  16. Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, McGinley M, Baumann J, Matsui Y (2014) The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob Change Biol 20:3823–3833CrossRefGoogle Scholar
  17. Gutierrez-Rodriguez C, Barbeitos MS, Sánchez JA, Lasker HR (2009) Phylogeography and morphological variation of the branching octocoral Pseudopterogorgia elisabethae. Mol Phylogen Evol 50:1–15CrossRefGoogle Scholar
  18. Hannes AR, Barbeitos MS, Coffroth MA (2009) Stability of symbiotic dinoflagellate type in the octocoral Briareum asbestinum. Mar Ecol Prog Ser 391:65–72CrossRefGoogle Scholar
  19. Harvell CD, Kim K, Quirolo C, Weir J, Smith GW (2001) Coral bleaching and disease: contributors to 1998 mass mortality in Briareum asbestinum (Octocorallia, Gorgonacea). Hydrobiologia 460:97–104CrossRefGoogle Scholar
  20. Helmuth B, Sebens KP (1993) The influence of colony morphology and orientation to flow on particle capture by the scleractinian coral Agaricia agaricites (Linnaeus). J Exp Mar Biol Ecol 165:251–278CrossRefGoogle Scholar
  21. Hoogenboom MO, Connolly SR, Anthony KRN (2008) Interactions between morphological and physiological plasticity optimize energy acquisition in corals. Ecology 89:1144–1154CrossRefGoogle Scholar
  22. Hunter RL, LaJeunesse TC, Santos SR (2007) Structure and evolution of the rDNA internal transcribed spacer (ITS) region 2 in the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J Phycol 43:120–128CrossRefGoogle Scholar
  23. Iglesias-Prieto R, Beltran VH, 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 Lond B 271:1757–1763CrossRefGoogle Scholar
  24. Jones A, Berkelmans R (2012) The photokinetics of thermo-tolerance in Symbiodinium. Mar Ecol 33:490–498CrossRefGoogle Scholar
  25. Kaniewska P, Anthony KRN, Hoegh-Guldberg O (2008) Variation in colony geometry modulates internal light levels in branching corals, Acropora humilis and Stylophora pistillata. Mar Biol 155:649–660CrossRefGoogle Scholar
  26. Kaniewska P, Anthony KRN, Sampayo EM, Campbell PR, Hoegh-Guldberg O (2014) Implications of geometric plasticity for maximizing photosynthesis in branching corals. Mar Biol 161:313–328CrossRefGoogle Scholar
  27. Kaniewska P, Magnusson SH, Anthony KRN, Reef R, Kühl M, Hoegh-Guldberg O (2011) Importance of macro- versus microstructure in modulating light levels inside coral colonies. J Phycol 47:846–860CrossRefGoogle Scholar
  28. LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880CrossRefGoogle Scholar
  29. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400CrossRefGoogle Scholar
  30. LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134CrossRefGoogle Scholar
  31. LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580CrossRefGoogle Scholar
  32. Lasker HR (2005) Gorgonian mortality during a thermal event in the Bahamas. Bull Mar Sci 76:155–162Google Scholar
  33. Lasker HR, Peters EC, Coffroth MA (1984) Bleaching of reef coelenterates in the San Blas Islands, Panama. Coral Reefs 3:183–190CrossRefGoogle Scholar
  34. Lesser MP, Shick JM (1989) Effects of irradiance and ultraviolet radiation on photoadaptation in the zooxanthellae of Aiptasia pallida: primary production, photoinhibition, and enzymic defenses against oxygen toxicity. Mar Biol 102:243–255CrossRefGoogle Scholar
  35. 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
  36. Levy O, Dubinsky Z, Achituv Y (2003) Photobehavior of stony corals: responses to light spectra and intensity. J Exp Biol 206:4041–4049CrossRefGoogle Scholar
  37. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131CrossRefGoogle Scholar
  38. Marsh JJA (1970) Primary productivity of reef-building calcareous red algae. Ecology 51:255–263CrossRefGoogle Scholar
  39. McCauley M, Banaszak AT, Goulet TL (2018) Species traits dictate seasonal-dependent responses of octocoral–algal symbioses to elevated temperature and ultraviolet radiation. Coral Reefs 37:901–917CrossRefGoogle Scholar
  40. McClanahan TR, Weil E, Cortés J, Baird AH, Ateweberhan M (2009) Consequences of coral bleaching for sessile reef organisms. In: van Oppen MJH, Lough JM (eds) Coral Bleaching: Patterns, Processes, Causes and Consequences. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 121–138CrossRefGoogle Scholar
  41. Middlebrook R, Hoegh-Guldberg O, Leggat W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J Exp Biol 211:1050–1056CrossRefGoogle Scholar
  42. Muscatine L, Cernichiari E (1969) Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol Bull 137:506–523CrossRefGoogle Scholar
  43. Oakley CA, Davy SK (2018) Cell Biology of Coral Bleaching. In: van Oppen MJH, Lough JM (eds) Coral Bleaching: Patterns, Processes, Causes and Consequences. Springer International Publishing, Cham, pp 189–211CrossRefGoogle Scholar
  44. Oakley CA, Durand E, Wilkinson SP, Peng L, Weis VM, Grossman AR, Davy SK (2017) Thermal shock induces host proteostasis disruption and endoplasmic reticulum stress in the model symbiotic cnidarian Aiptasia. J Proteome Res 16:2121–2134CrossRefGoogle Scholar
  45. Odum HT, Odum EP (1955) Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecol Monogr 25:291–320CrossRefGoogle Scholar
  46. 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:e38440CrossRefGoogle Scholar
  47. Pinzon JH, LaJeunesse TC (2011) Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Mol Ecol 20:311–325CrossRefGoogle Scholar
  48. Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701Google Scholar
  49. Prada C, Hellberg ME (2013) Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral. Proc Natl Acad Sci USA 110:3961–3966CrossRefGoogle Scholar
  50. Prada C, Schizas N, Yoshioka P (2008) Phenotypic plasticity or speciation? A case from a clonal marine organism. BMC Evol Biol 8:47CrossRefGoogle Scholar
  51. Prada C, Weil E, Yoshioka P (2010) Octocoral bleaching during unusual thermal stress. Coral Reefs 29:41–45CrossRefGoogle Scholar
  52. Prada C, McIlroy SE, Beltrán DM, Valint DJ, Ford SA, Hellberg ME, Coffroth MA (2014) Cryptic diversity hides host and habitat specialization In a gorgonian-algal symbiosis. Mol Ecol 23:3330–3340CrossRefGoogle Scholar
  53. Ramsby BD, Shirur KP, Iglesias-Prieto R, Goulet TL (2014) Symbiodinium photosynthesis in Caribbean octocorals. PLoS ONE 9:e106419CrossRefGoogle Scholar
  54. Rodríguez-Martínez RE, Ruíz-Rentería F, van Tussenbroek B, Barba-Santos G, Escalante-Mancera E, Jordán-Garza G, Jordán-Dahlgren E (2010) Environmental state and tendencies of the Puerto Morelos CARICOMP site, Mexico. Rev Biol Trop 58 Suppl 3:23–43Google Scholar
  55. Rodríguez-Román A, Hernandez-Pech X, Thomé PE, Enríquez S, Iglesias-Prieto R (2006) Photosynthesis and light utilization in the Caribbean coral Montastraea faveolata recovering from a bleaching event. Limnol Oceanogr 51:2702–2710CrossRefGoogle Scholar
  56. Rossi S, Schubert N, Brown D, Soares MdO, Grosso V, Rangel-Huerta E, Maldonado E (2018) Linking host morphology and symbiont performance in octocorals. Sci Rep 8:12823CrossRefGoogle Scholar
  57. Sánchez JA, Wirshing HH (2005) A field key to the identification of tropical western Atlantic zooxanthellate octocorals (Octocorallia: Cnidaria). Carib J Sci 41:508–522Google Scholar
  58. Sánchez JA, Mcfadden CS, France SC, Lasker HR (2003) Molecular phylogenetic analyses of shallow-water Caribbean octocorals. Mar Biol 142:975–987CrossRefGoogle Scholar
  59. Scheufen T, Iglesias-Prieto R, Enríquez S (2017) Changes in the number of symbionts and Symbiodinium cell pigmentation modulate differentially coral light absorption and photosynthetic performance. Front Mar Sci 4:309CrossRefGoogle Scholar
  60. Sebens KP (1984) Water flow and coral colony size: interhabitat comparisons of the octocoral Alcyonium siderium. Proc Natl Acad Sci USA 81:5473–5477CrossRefGoogle Scholar
  61. Shirur KP, Ramsby BD, Iglesias-Prieto R, Goulet TL (2014) Biochemical composition of Caribbean gorgonians: Implications for gorgonian — Symbiodinium symbiosis and ecology. J Exp Mar Biol Ecol 461:275–285CrossRefGoogle Scholar
  62. Smith H, Epstein H, Torda G (2017) The molecular basis of differential morphology and bleaching thresholds in two morphs of the coral Pocillopora acuta. Sci Rep 7:10066CrossRefGoogle Scholar
  63. Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83:315–337CrossRefGoogle Scholar
  64. van Woesik R, Sakai K, Ganase A, Loya Y (2011) Revisiting the winners and the losers a decade after coral bleaching. Mar Ecol Prog Ser 434:67–76CrossRefGoogle Scholar
  65. van Woesik R, Irikawa A, Anzai R, Nakamura T (2012) Effects of coral colony morphologies on mass transfer and susceptibility to thermal stress. Coral Reefs 31:633–639CrossRefGoogle Scholar
  66. Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012CrossRefGoogle Scholar
  67. Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066CrossRefGoogle Scholar
  68. West JM (1997) Plasticity in the sclerites of a gorgonian coral: tests of water motion, light level, and damage cues. Biol Bull 192:279–289CrossRefGoogle Scholar
  69. West JM, Harvell CD, Walls AM (1993) Morphological plasticity in a gorgonian coral (Briareum asbestinum) over a depth cline. Mar Ecol Prog Ser 94:61–69CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiologyUniversity of MississippiUniversityUSA
  2. 2.College of Science and EngineeringJames Cook UniversityTownsvilleAustralia

Personalised recommendations