The promiscuous larvae: Flexibility in the establishment of symbiosis in corals

Coral Reefs

Volumn 32, Issue 1, 2013, Pages 111-120

  Cumbo, V R ^a   Baird, A H ^a   van Oppen, M J H ^a,b  

^a JAMES COOK UNIVERSITY   (Australia)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

Author keywords

Climate change; Coral reefs; Free living Symbiodinium; Sediment; Symbiosis

Indexed keywords

CLIMATE CHANGE; CORAL REEF; DINOFLAGELLATE; ENDOSYMBIONT; LARVA; SYMBIOSIS;

AUSTRALIA; CORAL SEA; GREAT BARRIER REEF; PACIFIC OCEAN; QUEENSLAND;

EID: 84874803626     PISSN: 07224028     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00338-012-0951-7     Document Type: Article

References (58)

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. Babcock RC, Heyward AJ (1986) Larval development of certain gamete spawning scleractinian corals. Coral Reefs 5: 111-116.
5. Baird AH, Cumbo VR, Leggat W, Rodriguez-Lanetty M (2007) Fidelity and flexibility in coral symbioses. Mar Ecol Prog Ser 347: 307-309.
6. 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.
7. Baird AH, Bhagooli R, Nonaka M, Yakovleva I, Yamamoto HH, Hidaka M, Yamasaki H (2010) Environmental controls on the establishment and development of algal symbiosis in corals. Proc 11th Int Coral Reef Symp 5: 108-112.
8. Baker AC (1999) Symbiosis ecology of reef-building corals. Ph. D. thesis, University of Miami, p 120.
9. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34: 661-689.
10. Bay LK, Cumbo VR, Abrego D, Kool JT, Ainsworth TD, Willis BL (2011) Infection dynamics vary between symbiont types and cell surface treatments during establishment of endosymbiosis of coral larvae. Diversity 3: 356-374.
11. Berkelmans R (2002) Time-integrated thermal bleaching thresholds of reefs and their variation on the Great Barrier Reef. Mar Ecol Prog Ser 229: 73-82.
12. 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, B 273: 2305-2312.
13. Chang SS, Prezelin BB, Trench RK (1983) Mechanism of photoadaptation in 3 strains of the symbiotic dinoflagellate Symbiodinium-microadriaticum. Mar Biol 76: 219-229.
14. 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.
15. Correa AMS, McDonald DM, 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.
16. Cumbo VC (2012) The establishment of symbiosis in corals. Ph. D. thesis, James Cook University, p 198.
17. Douglas AE (1994) Symbiotic interactions. Oxford University Press, New York.
18. Dunn SR, Weis VM (2009) Apoptosis as a post-phagocytic winnowing mechanism in a coral-dinoflagellate mutualism. Environ Microbiol 11: 268-276.
19. Fabricius KE, Mieog JC, Colin PL, Idip D, van Oppen MJH (2004) Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol Ecol 13: 2445-2458.
20. Gomez-Cabrera MD, Ortiz J, Loh W, Ward S, Hoegh-Guldberg O (2008) Acquisition of symbiotic dinoflagellates (Symbiodinium) by juveniles of the coral Acropora longicyathus. Coral Reefs 27: 219-226.
21. Goulet TL (2006) Most corals may not change their symbionts. Mar Ecol Prog Ser 321: 1-7.
22. Harii S, Yasuda 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.
23. Harrison PL, Wallace CC (1990) Reproduction dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Ecosystems of the world: Coral reefs. Elsevier, Amsterdam, pp 133-207.
24. Hirose M, Reimer JD, Hidaka M, Suda S (2008) Phylogenetic analyses of potentially free-living Symbiodinium spp. isolated from coral reef sand in Okinawa. Japan. Mar Biol 155: 105-112.
25. Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Climate Change 2: 116-120.
26. 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.
27. Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: The host as a habitat. Am Nat 162: S51-S62.
28. LaJeunesse TC (2005) "Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the miocene-pliocene transition. Mol Biol Evol 22: 570-581.
29. LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanogr 48: 2046-2054.
30. LaJeunesse TC, Bhagooli R, Hidaka M, DeVantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284: 147-161.
31. 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.
32. Manning MM, Gates RD (2008) Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef. Limnol Oceanogr 53: 1853-1861.
33. 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.
34. Mieog JC, van Oppen MJH, Berkelmans R, Stam WT, Olsen JL (2009a) Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR. Mol Ecol Resources 9: 74-82.
35. Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJH (2009b) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS ONE 4: e6364.
36. Muscatine L, Porter JW (1977) Reef corals - mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27: 454-460.
37. Nishikawa A, Katoh M, Sakai K (2003) Larval settlement rates and gene flow of broadcast-spawning (Acropora tenuis) and planula-brooding (Stylophora pistillata) corals. Mar Ecol Prog Ser 256: 87-97.
38. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Mol Phylogenet Evol 56: 492-497.
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 in a Hawaiian reef environment. J Phycol 46: 53-65.
40. Porto I, Granados C, Restrepo JC, Sánchez JA (2008) Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean reefs. PLoS ONE 3: e2160.
41. Rodriguez-Lanetty M, Loh W, Carter D, Hoegh-Guldberg O (2001) Latitudinal variability in symbiont specificity within the widespread scleractinian coral Plesiastrea versipora. Mar Biol 138: 1175-1181.
42. Rodriguez-Lanetty M, Krupp DA, Weis VM (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.
43. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci USA 92: 2850-2853.
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. Schoenberg DA, Trench RK (1980) Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. III. Specificity and infectivity of Symbiodinium microadriaticum. Proc R Soc, B 207: 445-460.
46. Schwarz JA, Krupp DA, Weis VM (1999) Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. Biol Bull 196: 70-79.
47. Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts-Symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8: 23-43.
48. Takabayashi M, Adams LM, Pochon X, Gates RD (2012) Genetic diversity of free-living Symbiodinium in surface water and sediment of Hawai'i and Florida. Coral Reefs 31: 157-167.
49. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Haggblom 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.
50. 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.
51. Ulstrup KE, van Oppen MJH (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol Ecol 12: 3477-3484.
52. van Oppen MJH (2001) In vitro establishment of symbiosis in Acropora millepora planulae. Coral Reefs 20: 200.
53. van Oppen MJH, Palstra FP, Piquet AM-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, B 268: 1759-1767.
54. van Oppen MJH, Mahiny AJ, Done TJ (2005) Geographic distribution of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24: 482-487.
55. Venera-Ponton DE, Diaz-Pulido G, Rodriguez-Lanetty M, Hoegh-Guldberg O (2010) Presence of Symbiodinium spp. in macroalgal microhabitats from the southern Great Barrier Reef. Coral Reefs 29: 1049-1060.
56. Wilkinson DM, Sherratt TN (2001) Horizontally acquired mutualisms, an unsolved problem in ecology? Oikos 92: 377-384.
57. Yacobovitch T, Benayahu Y, Weis VM (2004) Motility of zooxanthellae isolated from the Red Sea soft coral Heteroxenia fuscescens (Cnidaria). J Exp Mar Biol Ecol 298: 35-48.
58. 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: 105-112.