Limits to physiological plasticity of the coral Pocillopora verrucosa from the central Red Sea

Coral Reefs

Volumn 33, Issue 4, 2014, Pages 1115-1129

  Ziegler, Maren ^a,b   Roder, Cornelia M ^c   Büchel, Claudia ^a   Voolstra, Christian R ^c  

^a GOETHE UNIVERSITY   (Germany)

^b BIODIVERSITY AND CLIMATE RESEARCH CENTRE BIK F   (Germany)

^c KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

Coral reef; Metabolic plasticity; Pocillopora verrucosa; Red Sea; Transplants

Indexed keywords

EID: 84939886236     PISSN: 07224028     EISSN: 14320975     Source Type: Journal    
DOI: 10.1007/s00338-014-1192-8     Document Type: Article

References (73)

1. Alamaru A, Loya Y, Brokovich E, Yam R, Shemesh A (2009) 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 73:5333–5342
2. Anthony KRN (1999) Coral suspension feeding on fine particulate matter. J Exp Mar Biol Ecol 232:85–106
3. Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253
4. Auld JR, Agrawal AA, Relyea RA (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc Lond B Biol Sci 277:503–511
5. Bachar A, Achituv Y, Pasternak Z, Dubinsky Z (2007) Autotrophy versus heterotrophy: the origin of carbon determines its fate in a symbiotic sea anemone. J Exp Mar Biol Ecol 349:295–298
6. Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc R Soc Lond B Biol Sci 273:2305–2312
7. Bongaerts P, Riginos C, Hay K, van Oppen M, Hoegh-Guldberg O, Dove S (2011) Adaptive divergence in a scleractinian coral: physiological adaptation of Seriatoporahystrix to shallow and deep reef habitats. BMC Evol Biol 11:303
8. Brown BE (1997) Adaptations of reef corals to physical environmental stress. Adv Mar Biol 31:221–299
9. Brown BE, Ambarsari I, Warner ME, Fitt WK, Dunne RP, Gibb SW, Cummings DG (1999) Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18:99–105
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 28:405–414
11. Clarke K, Gorley R (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth
12. Clayton WS, Lasker HR (1982) Effects of light and dark treatments on feeding by the reef coral Pocilloporadamicornis (Linnaeus). J Exp Mar Biol Ecol 63:269–279
13. Coleman AW, Suarez A, Goff LJ (1994) Molecular delineation of species and syngens in volvocacean green algae (Chlorophyta). J Phycol 30:80–90
14. Cooper TF, Lai M, Ulstrup KE, Saunders SM, Flematti GR, Radford B, van Oppen MJH (2011a) Symbiodinium genotypic and environmental controls on lipids in reef building corals. PLoS One 6:e20434
15. Cooper TF, Ulstrup KE, Dandan SS, Heyward AJ, Kuhl M, Muirhead A, O’Leary RA, Ziersen BEF, Van Oppen MJH (2011b) Niche specialization of reef-building corals in the mesophotic zone: metabolic trade-offs between divergent Symbiodinium types. Proc R Soc Lond B Biol Sci 278:1840–1850
16. Cooper TF, Berkelmans R, Ulstrup KE, Weeks S, Radford B, Jones AM, Doyle J, Canto M, O’Leary RA, van Oppen MJH (2011c) Environmental factors controlling the distribution of Symbiodinium harboured by the coral Acroporamillepora on the Great Barrier Reef. PLoS One 6:e25536
17. DeSalvo MK, Sunagawa S, Fisher PL, Voolstra CR, Iglesias-Prieto R, Medina M (2010) Coral host transcriptomic states are correlated with Symbiodinium genotypes. Mol Ecol 19:1174–1186
18. DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. TREE 13:77–81
19. English S, Wilkinson C, Baker V (1997) Survey manual for tropical marine resources. Australian Institute of Marine Science, Townsville, Australia
20. Falkowski PG, Dubinsky Z (1981) Light-shade adaptation of Stylophorapistillata, a hermatypic coral from the Gulf of Eilat. Nature 289:172–174
21. Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and the bioenergetics of a symbiotic coral. Bioscience 34:705–709
22. Ferrier-Pagès C, Witting J, Tambutté E, Sebens KP (2003) Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophorapistillata. Coral Reefs 22:229–240
23. Ferrier-Pagès C, Allemand D, Gattuso JP, Jaubert J, Rassoulzadegan R (1998) Microheterotrophy in the zooxanthellate coral Stylophorapistillata: effects of light and ciliate density. Limnol Oceanogr 43:1639–1648
24. Frade PR, Bongaerts P, Winkelhagen AJS, Tonk L, Bak RPM (2008a) In situ photobiology of corals over large depth ranges: a multivariate analysis on the roles of environment, host, and algal symbiont. Limnol Oceanogr 53:2711–2723
25. Frade PR, De Jongh F, Vermeulen F, Van Bleijswijk J, Bak RPM (2008b) Variation in symbiont distribution between closely related coral species over large depth ranges. Mol Ecol 17:691–703
26. Franklin E, Stat M, Pochon X, Putnam H, Gates R (2012) GeoSymbio: a hybrid, cloud-based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium–host symbioses. Mol Ecol Resour 12:369–373
27. Gates RD, Edmunds PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. Amer Zool 39:30–43
28. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189
29. Hiller RG, Wrench PM, Gooley AP, Shoebridge G, Breton J (1993) The major intrinsic light-harvesting protein of Amphidinium: characterization and relation to other light-harvesting proteins. Photochem Photobiol 57:125–131
30. Hofmann E, Wrench PM, Sharples FP, Hiller RG, Welte W, Diederichs K (1996) Structural basis of light harvesting by carotenoids: peridinin-chlorophyll-protein from Amphidiniumcarterae. Science 272:1788–1791
31. Hoogenboom M, Rodolfo-Metalpa R, Ferrier-Pages C (2010) Co-variation between autotrophy and heterotrophy in the Mediterranean coral Cladocoracaespitosa. J Exp Biol 213:2399–2409
32. Iglesias-Prieto R, Trench RK (1997) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll-protein complexes to different photon-flux densities. Mar Biol 130:23–33
33. Iglesias-Prieto R, Beltran VH, LaJeunesse TC, Reyes-Bonilla H, Thome PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc Lond B Biol Sci 271:1757–1763
34. Jeffrey SW, Haxo FT (1968) Photosynthetic pigments of symbiotic dinoflagellates (zooxanthellae) from corals and clams. Biol Bull 135:149–165
35. 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194
36. 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 Lond B Biol Sci 275:1359–1365
37. Kinzie RA, Jokiel PL, York R (1984) Effects of light of altered spectral composition on coral zooxanthellae associations and on zooxanthellae in vitro. Mar Biol 78:239–248
38. Kowalewska G, Szymczak M (2001) Influence of selected abiotic factors on the decomposition of chlorophylls. Oceanologia 43:315–328
39. Krämer WE, Schrameyer V, Hill R, Ralph PJ, Bischof K (2013) PSII activity and pigment dynamics of Symbiodinium in two Indo-Pacific corals exposed to short-term high-light stress. Mar Biol 160:563–577
40. LaJeunesse TC (2001) Investigating the biodiversity, ecology and phylogeny of endosymbionticdinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880
41. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400
42. LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleuraelegantissima (Brandt). Biol Bull 199:126–134
43. LaJeunesse TC, Bonilla HR, Warner ME, Wills M, Schmidt GW, Fitt WK (2008) Specificity and stability in high latitude eastern Pacific coral-algal symbioses. Limnol Oceanogr 53:719–727
44. LaJeunesse TC, Smith R, Walther M, Pinzon J, Pettay DT, McGinley M, Aschaffenburg M, Medina-Rosas P, Cupul-Magana AL, Perez AL, Reyes-Bonilla H, Warner ME (2010) Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proc R Soc Lond B Biol Sci 277:2925–2934
45. Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Biol Ecol 375:1–8
46. Lesser MP, Slattery M, Stat M, Ojimi M, Gates RD, Grottoli A (2010) Photoacclimatization by the coral Montastraeacavernosa in the mesophotic zone: light, food, and genetics. Ecology 91:990–1003
47. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in Algal Endosymbioses Shapes Growth in Reef Corals. Science 304:1492–1494
48. Lowry O, Rosebrough N, Farr A, Randall R (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
49. McCloskey LR, Muscatine L (1984) Production and respiration in the Red Sea coral Stylophorapistillata as a function of depth. Proc R Soc Lond B Biol Sci 222:215–230
50. McGinley MP, Aschaffenburg MD, Pettay DT, Smith RT, LaJeunesse TC, Warner ME (2012) Symbiodinium spp. in colonies of eastern Pacific Pocillopora spp. are highly stable despite the prevalence of low-abundance background populations. Mar Ecol Prog Ser 462:1–7
51. Monismith SG (2007) Hydrodynamics of coral reefs. Annu Rev Fluid Mech 39:37–55
52. Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Ecosystems of the world, coral reefs. Elsevier, Amsterdam, pp 75–87
53. Muscatine L, Porter JW, Kaplan IR (1989) Resource partitioning by reef corals as determined from stable isotope composition. Mar Biol 100:185–193
54. 15N) isotopic composition of symbiotic scleractinian corals. PLoS One 8:e81247
55. Oku H, Yamashiro H, Onaga K, Sakai K, Iwasaki H (2003) Seasonal changes in the content and composition of lipids in the coral Goniastreaaspera. Coral Reefs 22:83–85
56. Padilla-Gamiño JL, Hanson KM, Stat M, Gates RD (2012) Phenotypic plasticity of the coral Poritesrus: acclimatization responses to a turbid environment. J Exp Mar Biol Ecol 434–435:71–80
57. Palardy JE, Grottoli AG, Matthews KA (2005) Effects of upwelling, depth, morphology and polyp size on feeding in three species of Panamanian corals. Mar Ecol Prog Ser 300:79–89
58. Palardy JE, Grottoli AG, Matthews KA (2006) Effect of naturally changing zooplankton concentrations on feeding rates of two coral species in the Eastern Pacific. J Exp Mar Biol Ecol 331:99–107
59. 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 367:180–188
60. Papagiannakis E, van Stokkum IHM, Fey H, Büchel C, van Grondelle R (2005) Spectroscopic characterization of the excitation energy transfer in the fucoxanthin-chlorophyll protein of diatoms. Photosynth Res 86:241–250
61. Patton JS, Abraham S, Benson AA (1977) Lipogenesis in the intact coral Pocilloporacapitata and its isolated zooxanthellae: evidence for a light-driven carbon cycle between symbiont and host. Mar Biol 44:235–247
62. Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701
63. Pochon X, Putnam HM, Burki F, Gates RD (2012) Identifying and characterizing alternative molecular markers for the symbiotic and free-living dinoflagellategenus Symbiodinium. PLoS One 7:e29816
64. Ralph PJ, Gademann R, Larkum AWD, Schreiber U (1999) In situ underwater measurements of photosynthetic activity of coral zooxanthellae and other reef dwelling dinoflagelateendosymbionts. Mar Ecol Prog Ser 180:139–147
65. Roder C, Fillinger L, Jantzen C, Schmidt GM, Khokiattiwong S, Richter C (2010) Trophic response of corals to large amplitude internal waves. Mar Ecol Prog Ser 412:113–128
66. Roder C, Jantzen C, Schmidt GM, Kattner G, Phongsuwan N, Richter C (2011) Metabolic plasticity of the corals Poriteslutea and Diploastreaheliopora exposed to large amplitude internal waves. Coral Reefs 30:57–69
67. Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882
68. Swart PK, Saied A, Lamb K (2005) Temporal and spatial variation in the delta N-15 and delta C-13 of coral tissue and zooxanthellae in Montastraeafaveolata collected from the Florida reef tract. Limnol Oceanogr 50:1049–1058
69. Thornhill DJ, Xiang Y, Fitt WK, Santos SR (2009) Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominantCaribbean corals. PLoS One 4:e6262
70. Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83:315–337
71. van Oppen MJH, Bongaerts P, Underwood JN, Peplow LM, Cooper TF (2011) The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia. Mol Ecol 20:1647–1660
72. Veal CJ, Carmi M, Fine M, Hoegh-Guldberg O (2010) Increasing the accuracy of surface area estimation using single wax dipping of coral fragments. Coral Reefs 29:893–897
73. Wellington GM (1982) An experimental analysis of the effects of light and zooplankton on coral zonation. Oecologia 52:311–320