Acropora recruits harbor "rare" Symbiodinium in the environmental pool

Coral Reefs

Volumn 32, Issue 2, 2013, Pages 355-366

  Yamashita, H ^a   Suzuki, G ^a   Hayashibara, T ^a   Koike, K ^b  

^a FISHERIES RESEARCH AGENCY   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Acropora; Recruits; Symbiodinium; Symbiont acquisition; Symbiosis

Indexed keywords

ABUNDANCE; ADULT; ALGAL BLOOM; CLADISTICS; CORAL; DINOFLAGELLATE; POPULATION DENSITY; RECRUITMENT (POPULATION DYNAMICS); SURVIVAL; SYMBIONT;

ACROPORA; ALGAE; ANTHOZOA; DINOPHYCEAE; SYMBIODINIUM;

EID: 84877073852     PISSN: 07224028     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00338-012-0980-2     Document Type: Article

References (63)

1. Abrego D, van Oppen MJH, Willis BL (2009a) Highly infectious symbiont dominates initial uptake in coral juveniles. Mol Ecol 18: 3518-3531.
2. Abrego D, van Oppen MJH, Willis BL (2009b) Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny. Mol Ecol 18: 3532-3543.
3. Adams LM, Cumbo VR, Takabayashi M (2009) Exposure to sediment enhances primary acquisition of Symbiodinium by asymbiotic coral larvae. Mar Ecol Prog Ser 377: 149-156.
4. 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.
5. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34: 661-689.
6. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals' adaptive response to climate change. Nature 430: 741.
7. Bhagooli R, Hidaka M (2004) Release of zooxanthellae with intact photosynthetic activity by the coral Galaxeafascicularis in response to high temperature stress. Mar Biol 145: 329-337.
8. Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16: 129-138.
9. Carlos AA, Baillie BK, Maruyama T (2000) Diversity of dinoflagellate symbionts (zooxanthellae) in a host individual. Mar Ecol Prog Ser 195: 93-100.
10. Chen CA, Yang YW, Wei NV, Tsai WS, Fang LS (2005) Symbiont diversity in the scleractinian corals from tropical reefs and non-reef communities in Taiwan. Coral Reefs 24: 11-22.
11. Coffroth MA, Lewis CF, Santos SR, Weaver JL (2006) Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Curr Biol 16: R985-R987.
12. Correa AMS, McDonald MD, Baker AC (2009) Development of clade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detecting clade D symbionts in Caribbean corals. Mar Biol 156: 2403-2411.
13. 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.
14. Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and the bioenergetics of a symbiotic coral. Bioscience 34: 705-709.
15. Fitt WK (1985) Chemosensory responses of the symbiotic dinoflagellate Symbiodiniummicroadriaticum (Dinophyceae). J Phycol 21: 62-67.
16. Gómez-Cabrera MdC, Ortiz JC, Loh WKW, Ward S, Hoegh-Guldberg O (2008) Acquisition of symbiotic dinoflagellates (Symbiodinium) by juveniles of the coral Acropora longicyathus. Coral Reefs 27: 219-226.
17. Harii S, Tasuda N, Rodriguez-Lanetty M, Irie T, Hidaka M (2009) Onset of symbiosis and distribution patterns of symbiotic dinoflagellates in the larvae of scleractinian corals. Mar Biol 156: 1203-1212.
18. Hayashibara T, Iwao K, Omori M (2004) Induction and control of spawning in Okinawan staghorn corals. Coral Reefs 23: 406-409.
19. Hollingsworth LL, Kinzie RA III, Lewis TD, Krupp DA, Leong J-AC (2005) Phototaxis of motile zooxanthellae to green light may facilitate symbiont capture by coral larvae. Coral Reefs 24: 523.
20. Iglesias-Prieto R, Beltrán VH, LaJeunesse TC, Reyes-Bonilla H, Thomé PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals of the eastern Pacific. Proc R Soc Lond B 271: 1757-1763.
21. Ishikura M, Hagiwara K, Takishita K, Haga M, Iwai K, Maruyama T (2004) Isolation of new Symbiodinium strains from Tridacnid giant clam (Tridacna crocea) and sea slug (Pteraeolida ianthina) using culture medium containing giant clam tissue homogenate. Mar Biotechnol 6: 378-385.
22. Jimbo M, Yamashita H, Koike K, Sakai R, Kamiya H (2010) Effects of lectin in the scleractinian coral Ctenactis echinata on symbiotic zooxanthellae. Fish Sci 76: 355-363.
23. 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.
24. Kinzie RA, Takayama M, Santos SR, Coffroth MA (2001) The adaptive bleaching hypothesis: experimental tests of critical assumptions. Biol Bull 200: 51-58.
25. Koike K, Jimbo M, Sakai R, Kaeriyama M, Muramoto K, Ogata T, Maruyama T, Kamiya H (2004) Octocoral chemical signaling selects and controls dinoflagellate symbionts. Biol Bull 207: 80-86.
26. Koike K, Yamashita H, Oh-Uchi A, Tamaki M, Hayashibara T (2007) A quantitative real-time PCR method for monitoring Symbiodinium in the water column. Galaxea 9: 1-12.
27. 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: 866-880.
28. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141: 387-400.
29. LaJeunesse TC, Bhagooli R, Hidaka M, Done T, deVantier L, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004) Closely related Symbiodinium spp. differ in relative dominance within coral reef host communities across environmental, latitudinal, and biogeographic gradients. Mar Ecol Prog Ser 284: 147-161.
30. Lien Y-T, Nakano Y, Plathong S, Fukami H, Wang J-T, Chen CA (2007) Occurrence of the putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlying coral communities. Coral Reefs 26: 35-44.
31. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304: 1492-1494.
32. Littman RA, van Oppen MJH, Willis BL (2008) Methods for sampling free-living Symbiodinium (zooxanthellae) and their distribution and abundance at Lizard Island (Great Barrier Reef). J Exp Mar Biol Ecol 364: 48-53.
33. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4: 122-131.
34. Manning MM, Gates RD (2008) Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef. Limnol Oceanogr 53: 1853-1861.
35. Mieog JC, van Oppen MJH, Cantin NE, Stam WT, Olsen JL (2007) Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs 26: 449-457.
36. Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Coral reefs: Ecosystems of the world. Elsevier, New York, pp 75-87.
37. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Mol Phylogenet Evol 56: 492-497.
38. Pochon X, Pawlowski J, Zanietti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139: 1069-1078.
39. Pochon X, Stat M, Takabayashi M, Chasqui L, Chauka LJ, Logan DDK, Gates RD (2010) Comparison of endosymbiotic and free-living Symbiodinium (Dinophyceae) diversity a Hawaiian reef environment. J Phycol 46: 53-65.
40. Rodriguez-Lanetty M, Krupp DA, Weis M (2004) Distinct ITS types of Symbiodinium in Clade C correlate with cnidarian/dinoflagellate specificity during onset of symbiosis. Mar Ecol Prog Ser 275: 97-102.
41. Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs. J Phycol 34: 407-417.
42. Rowan R (2004) Thermal adaptations in reef coral symbionts. Nature 430: 742.
43. Rowan R, Powers DA (1991) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251: 1348-1351.
44. 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.
45. Sampayo EM, Ridgwat T, Bongaerts P, Hoegh-Guldberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci USA 105: 10444-10449.
46. Santos SR, Taylor DJ, Kinzie RA, Hidaka M, Sakai K, Coffroth MA (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol 23: 97-111.
47. Savage AM, Goodson MS, Visram S, Trapido RH, Wiedenmann J, Douglas AE (2002) Molecular diversity of symbiotic algae at the latitudinal margins of their distribution: dinoflagellates of the genus Symbiodinium in corals and anemones. Mar Ecol Prog Ser 244: 17-26.
48. Suzuki G, Hayashibara T, Shirayama Y, Fukami H (2008) Evidence of species-specific habitat selectivity of Acropora corals based on identification of new recruits by two molecular markers. Mar Ecol Prog Ser 355: 149-159.
49. Suzuki G, Kai S, Yamashita H, Suzuki K, Iehisa Y, Hayashibara T (2011) Narrower grid structure of artificial reef enhances initial survival of in situ settled coral. Mar Pollut Bull 62: 2803-2812.
50. Suzuki G, Arakaki S, Kai S, Hayashibara T (2012a) Habitat differentiation in the early life stage of simultaneously mass-spawning corals. Coral Reefs 31: 535-545.
51. Suzuki G, Arakaki S, Suzuki K, Iehisa Y, Hayashibara T (2012b) What is the optimal density of larval seeding in Acropora corals? Fish Sci 78: 801-808.
52. Takabayashi M, Santos SR, Cook CB (2004) Mitochondrial DNA phylogeny of the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J Phycol 40: 160-164.
53. Takishita K, Ishikura M, Koike K, Maruyama T (2003) Comparison of phylogenies based on nuclear-encoded SSU rDNA and plastid-encoded psbA in the symbiotic dinoflagellate genus Symbiodinium. Phycologia 42: 285-291.
54. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Häggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101: 13531-13535.
55. Toller WW, Rowan R, Knowlton N (2001) Zooxanthellae of the Montastraeaannularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biol Bull 201: 348-359.
56. Trench RK (1987) Dinoflagellates in non-parasitic symbioses. In: Taylor FJR (ed) The biology of the dinoflagellates. Blackwell, Oxford, pp 530-570.
57. van Oppen MJH, Palstra FP, Piquet A-T, Miller DJ (2001) Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc R Soc Lond B 268: 1759-1767.
58. Wilcox TP (1998) Large-subunit ribosomal RNA systematics of symbiotic dinoflagellates: Morphology does not recapitulate phylogeny. Mol Phylogenet Evol 10: 436-448.
59. Wood-Charlson EM, Hollingsworth LL, Krupp DA, Weis VM (2006) Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell Microbiol 8: 1985-1993.
60. Yamashita H, Koike K Genetic identity of free-living Symbiodinium obtained over a broad latitudinal range in the Japanese coast. Phycol Res. doi: 10. 1111/pre. 12004 (in press).
61. Yamashita H, Suzuki G, Hayashibara T, Koike K (2011) Do corals select zooxanthellae by alternative discharge? Mar Biol 158: 87-100.
62. Yuyama I, Hayakawa H, Endo H, Iwao K, Takeyama H, Maruyama T, Watanabe T (2005) Identification of symbiotically expressed coral mRNAs using a model infection system. Biochem Biophys Res Commun 336: 793-798.
63. Yuyama I, Harii S, Hidaka M (2011) Algal symbiont type affects gene expression in juveniles of the coral Acroporatenuis exposed to thermal stress. Mar Environ Res 76: 41-47.