The ecology and phylogeny of cyanobacterial symbionts in sponges

Marine Ecology

Volumn 29, Issue 2, 2008, Pages 178-192

  Usher, Kayley M ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Cyanobacteria; Cyanosponges; Sponges; Symbiosis; Transmission

Indexed keywords

BIOGEOGRAPHY; CYANOBACTERIUM; GEOGRAPHICAL DISTRIBUTION; HOST SPECIFICITY; HOST-SYMBIONT INTERACTION; PHYLOGENY; SPONGE; SYMBIOSIS;

CYANOBACTERIA; OSCILLATORIA SPONGELIAE; SYNECHOCOCCUS; SYNECHOCOCCUS SPONGIARUM;

EID: 45249120852     PISSN: 01739565     EISSN: 14390485     Source Type: Journal    
DOI: 10.1111/j.1439-0485.2008.00245.x     Document Type: Review

References (113)

1. Becerro M.A., Turon X., Uriz M.J., Templado J. (2003) Can a sponge feeder be a herbivore? Tylodina perversa (Gastropoda) feeding on Aplysina aerophoba (Demospongiae). Biological Journal of the Linnaean Society, 78, 429-438.
2. Belda-Baillie C.A., Baillie B.K., Maruyama T. (2002) Specificity of a model cnidarian-dinoflagellate symbiosis. Biological Bulletin, 202, 74-85.
3. Bennett A., Bogorad L. (1973) Complementary chromatic adaptation in a filamentous blue-green alga. Journal of Cell Biology, 58, 419-435.
4. Berthold R.J., Borowitzka M.A., Mackay M.A. (1982) The ultrastructure of Oscillatoria spongeliae, the blue-green algal endosymbiont of the sponge Dysidea herbacea. Phycologia, 21, 327-335.
5. Bewley C.A., Holland N.D., Faulkner D.J. (1996) Two classes of metabolites from Theonella swinhoei are localised in distinct populations of bacterial symbionts. Experientia, 52, 716-722.
6. Borowitzka M.A., Hinde R. (1999) Sponges symbiotic with algae or cyanobacteria in coral reefs. In: Shamsudin L., Shazili N.A.M., Saadon M.N., Borowitzka M.A. (Eds), Assessment and Monitoring of Marine Systems. Aspirasi Teras Sdn. Bhd., Terengganu, Malaysia: 7-17.
7. Borowitzka M.A., Hinde R., Pironet F. (1989) Carbon fixation by the sponge Dysidea herbacea and its endosymbiont Oscillatoria spongeliae. In: Choat J.H., Barnes D.J., Borowitzka M.A., Coll J.C., Davies P.J., Flood P., Hatcher B.G., Hopley D., Hutchings P.A., Kinsey D., Orme G.R., Pichon M., Sale P.F., Sammarco P.W., Wallace C.C., Wilkinson C.R., Wolanski E., Bellwood O. (Eds), Proceedings of the 6th International Coral Reef Symposium, Townsville: 151-156.
8. Brunskill G.J. (2004) New Guinea and its coastal seas, a testable model of wet tropical coastal processes: An introduction to project topics. Continental Shelf Research, 24, 2273-2295.
9. Cerrano C., Magnino G., Sarà A., Bavestrello G., Gaino E. (2001) Necrosis in a population of Petrosia ficiformis (Porifera, Demospongiae) in relation with environmental stress. Italian Journal of Zoology, 68, 131-136.
10. Cheshire A.C., Wilkinson C.R., Seddon S., Westphalen G. (1997) Bathymetric and seasonal changes in photosynthesis and respiration of the phototrophic sponge Phyllospongia lamellosa in comparison with respiration by the heterotrophic sponge Ianthella basta on Davies Reef, Great Barrier Reef. Marine and Freshwater Research, 48, 589-599.
11. Cohen F.M. (2002) What are bacterial species? Annual Review of Microbiology, 56, 457-487.
12. Cowen R. (1983) Algal symbiosis and its recognition in the fossil record. In: Tevesz M.J.S., McCall P.L. (Eds), Biotic Interactions in Recent and Fossil Benthic Communities. Plenum Press, New York: 431-478.
13. Cox G.C., Hiller R.G., Larkum A.W.D. (1985) An unusual cyanophyte, containing phycourobilin and symbiotic with ascidians and sponges. Marine Biology, 89, 149-163.
14. Davy S.K., Turner J.R., Lucas I.A.N. (1997) The nature of temperate anthozoan - dinoflagellate symbioses. Proceedings of the 8th International Coral Reef Symposium Panama, Vol. 2, 1307-1312.
15. Debelius H. (1996) Voracious carnivores. In: Peyer B. (Ed.), Nudibranchs and Sea Snails Indo-Pacific Field Guide. IKAN-Unterwasserarchiv, Frankfurt: P. 321.
16. Diaz M.C. (1996) Molecular and ecological studies of sponge-microbial associations. Ph.D. thesis, University of California, Santa Cruz.
17. Diaz M.C. (1997) Molecular detection and characterization of specific bacterial groups associated with tropical sponges. Proceedings of the 8th International Coral Reef Symposium, Panama, Vol. 2, 1399-1402.
18. Diaz M.C. (1999) Perspectives on sponge-cyanobacterial symbioses. Memoirs of the Queensland Museum, 44, 154.
19. Diaz M.C., Ward B.B. (1997) Sponge-mediated nitrification in tropical benthic communities. Marine Ecology Progress Series, 156, 97-107.
20. Diaz M.C., Thacker R.W., Rützler K., Piantoni C. (2007) Two new haplosclerid sponges from Caribbean Panama with symbiotic filamentous cyanobacteria, and an overview of sponge-cyanobacteria associations. In: Custódio M.R., Lôbo-Hajdu G., Hajdu E., Muricy G. (Eds), Porifera Research: Biodiversity, Innovation and Sustainability, Rio de Janeiro, Museu Nacional: 31-39 - 2007. Série Livros 28, Museu, Rio de Janeiro: 31-39.
21. Douglas A.E. (1998) Host benefit and the evolution of specialization in symbiosis. Heredity, 81, 599-603.
22. Erwin P.M., Thacker R.W. (2007) Incidence and identity of photosynthetic symbionts in Caribbean coral reef sponge assemblages. Journal of the Marine Biological Association of the United Kingdom, 87, 1683-1692.
23. Fabricius K.E., Klumpp D.W. (1995) Widespread mixotrophy in reef-inhabiting soft corals: The influence of depth, and colony expansion and contraction on photosynthesis. Marine Ecology Progress Series, 125, 195-204.
24. Fahnenstiel G.L., Carrick H.J., Iturriaga R. (1991) Physiological characteristics and food-web dynamics of Synechococcus in Lakes Huron and Michigan. Limnology and Oceanography, 36, 219-234.
25. Feldmann J. (1933) Sur Quelques cyanophycées vivant dans le tissu des éponges de Banyuls. Archives de Zoologie Expérimentale et Générale, 75, 331-404.
26. Flatt P.M., Gautschi J.T., Thacker R.W., Musafija-Girt M., Crews P., Gerwick W.H. (2005) Identification of the cellular site of polychlorinated peptide biosynthesis in the marine sponge Dysidea (Lamellodysidea) herbacea and symbiotic cyanobacterium Oscillatoria spongeliae by CARD-FISH analysis. Marine Biology, 147, 761-774.
27. Flowers A.E., Garson M.J., Webb R.I., Dumdei E.J., Charan R.D. (1998) Cellular origin of chlorinated diketopiperazines in the dictyoceratid sponge Dysidea herbacea (Keller). Cell Tissue Research, 292, 597-607.
28. Fromont J., Garson M. (1999) Sponge bleaching on the West and East coasts of Australia. Coral Reefs, 18, 340.
29. Furnas M., Crosbie N.D. (1999) In situ growth dynamics of the photosynthetic prokaryotic picoplankters Synechococcus and Prochlorococcus. In: Charpy L., Larkum A.W.D. (Eds), Marine Cyanobacteria. Bulletin de l'Institut Oceanographique de Monaco, 19, 387-417.
30. Glover H.E. (1985) The physiology and ecology of the marine cyanobacterial genus Synechococcus. Advances in Aquatic Microbiology, 3, 49-107.
31. Golubic S., Le Campion-Alsumard T., Campbell S.E. (1999) Diversity of marine cyanobacteria. In: Charpy L., Larkum A.W.D. (Eds), Marine Cyanobacteria. Bulletin de l'Institut Oceanographique de Monaco, 19, 53-76.
32. Gómez R., Erpenbeck D., Richelle-Maurer E., Van Dijk T., Woldringh C.L., Van Soest R.W.M. (2004) Affinities of the Aphanocapsa feldmanni - like cyanobacteria from the marine sponge Xestospongia muta based on genetic and morphological analysis. In: Pansini M., Pronzato R., Bavestrello G., Manconi R. (Eds), Sponge Science in the New Millennium. Bollettino dei Musei e degli Istituti Biologici dell'Università di Genova, 68, 335-347.
33. Hentschel U., Hopke J., Horn M., Friedrich A.B., Wagner M., Hacker J., Moore B.S. (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Applied and Environmental Microbiology, 68, 4431-4440.
34. Hinde R., Pironet F., Borowitzka M.A. (1994) Isolation of Oscillatoria spongeliae, the filamentous cyanobacterial symbiont of the marine sponge Dysidea herbacea. Marine Biology, 119, 99-104.
35. Honda D., Yokota A., Sugiyama J. (1999) Detection of seven major evolutionary lineages in cyanobacteria based on the 16S rRNA gene sequence analysis with new sequences of five marine Synechococcus strains. Journal of Molecular Evolution, 48, 723-739.
36. Joshua S., Mullineaux C.W. (2004) Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiology Preview, 135, 1-8.
37. Lan R., Reeves P.R. (2001) When does a clone deserve a name? A perspective on bacterial species based on population genetics. Trends in Microbiology, 9, 419-424.
38. Larkum A.W.D., Cox G.C., Hiller R.G., Parry D.L., Dibbayawan T.P. (1987) Filamentous cyanophytes containing phycourobilin and in symbiosis with sponges and an ascidian of coral reefs. Marine Biology, 95, 1-13.
39. Larkum A.W.D., Cox G.C., Dibbayawan T.P. (1988) Prokaryotic algal symbionts of coral reef sponges. Proceedings of the 6th International Coral Reef Symposium, 3, 163-169.
40. Lesser M.P., Farrell J.H. (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs, 23, 367-377.
41. Lewin R.A. (1975) A marine Synechococcus (Cyanophyta, Chroococcales) epizoic on ascidians. Phycologia, 14, 153-160.
42. Lewin R.A. (2002) Prochlorophyta - a matter of class distinctions. Photosynthesis Research, 73, 59-61.
43. Litvaitis M.K. (2002) A molecular test of cyanobacterial phylogeny, inferences from constraint analyses. Hydrobiologia, 468, 135-145.
44. Maldonado M., Young C.M. (1998) Limits on the bathymetric distribution of keratose sponges, a field test in deep water. Marine Ecology Progress Series, 174, 123-139.
45. Miki W., Otaki N., Yokoyama A., Kusumi T. (1996) Possible origin of zeaxanthin in the marine sponge, Reniera japonica. Experientia, 52, 93-96.
46. Moore L.R., Chisholm S.W. (1999) Photophysiology of the marine cyanobacterium Prochlorococcus: Ecotypic differences among cultured isolates. Limnology and Oceanography, 44, 628-638.
47. Münchhoff J., Hirose E., Maruyama T., Sunairi M., Burns B.P., Neilan B.A. (2007) Host specificity and phylogeography of the prochlorophyte Prochloron sp., an obligate symbiont in didemnid ascidians. Environmental Microbiology, 9, 890-899.
48. Murray R.G.E., Brenner D.J., Colwel R.R., De Vos P., Goodfellow M., Grimont P.A.D., Pfennig N., Stackebrandt E., Zavarzin G.A. (1990) Report of the ad hoc committee on approaches to taxonomy within the Proteobacteria. International Journal of Systematic Bacteriology, 40, 213-215.
49. Oren M., Steindler L., Ilan M. (2005) Transmission, plasticity and the molecular identification of cyanobacterial symbionts in the Red Sea sponge Diacarnus erythraenus. Marine Biology, 148, 35-41.
50. Parry D.L. (1986) Prochloron on the sponge Aplysilla sp. Bulletin of Marine Science, 38, 388-390.
51. Partensky F., Blanchot J., Vaulot D. (1999) Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters, a review. In: Charpy L., Larkum A.W.D. (Eds), Marine Cyanobacteria. Bulletin de l'Institut Oceanographique de Monaco, 19, 457-475.
52. Plantivaux A., Furla P., Zoccola D., Garello G., Forcioli D., Richier S., Merle P.-L., Tambutté E., Tambutté S., Allemand D. (2004) Molecular characterization of two CuZn-superoxide dismutases in a sea anemone. Free Radical Biology and Medicine, 37, 1170-1181.
53. Rasmussen U., Johansson C. (2002) Diversity and specificity in cyanobacterial symbioses. In: Osborne B. (Ed.), Biology and Environment, Vol. 102B. Proceedings of the Royal Irish Academy 2000. Criterion Press, Dublin: 53-55.
54. Raven J.A. (2002) The evolution of cyanobacteria symbioses. In: Osborne B. (Ed.), Biology and Environment, Vol. 102. Proceedings of the Royal Irish Academy 2000. Criterion Press, Dublin: 3-6.
55. Regoli F., Cerrano C., Chierici E., Bompadre S., Bavestrello G. (2000) Susceptibility to oxidative stress of the Mediterranean demosponge Petrosia ficiformis, role of endosymbionts and solar irradiance. Marine Biology, 137, 453-461.
56. Ridley C.P., Bergquist P.R., Harper K.M., Faulkner D.J., Hooper J.N.A., Haygood M.G. (2005a) Speciation and biosynthetic variation in four dictyoceratid sponges and their cyanobacterial symbiont, Oscillatoria spongeliae. Chemistry and Biology, 12, 397-406.
57. Ridley C.P., Faulkner D.J., Haygood M.G. (2005b) Investigation of Oscillatoria spongeliae - dominated bacterial communities in four Dictyoceratid sponges. Applied and Environmental Microbiology, 71, 7366-7375.
58. Roberts D.E., Cummins S.P., Davis A.R., Pangway C. (1999) Evidence for symbiotic algae in sponges from temperate coastal reefs in New South Wales, Australia. Memoirs of the Queensland Museum, 44, 493-497.
59. Roberts D.E., Davis A.R., Cummins S.P. (2006) Experimental manipulation of shade, silt, nutrients and salinity on the temperate reef sponge Cymbastela concentrica. Marine Ecology Progress Series, 307, 143-154.
60. Rodriguez-Lanetty M., Krupp D.A., Weis V.M. (2004) Distinct ITS types of Symbiodinium in Clade C correlate with cnidarian/dinoflagellate specificity during onset of symbiosis. Marine Ecology Progress Series, 275, 97-102.
61. 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.
62. Rützler K. (1981) An unusual bluegreen alga symbiotic with two new species of Ulosa (Porifera, Hymeniacidonidae) from Carrie Bow Cay, Belize. P.S.Z.N.: Marine Ecology, 2, 35-50.
63. Rützler: K. (1990) Associations between Caribbean sponges and photosynthetic organisms. In: Rützler K. (Ed.), New Perspectives in Sponge Biology. Smithsonian Institute Press, Washington, DC: 455-466.
64. Rützler K., Muzik K. (1993) Terpios hoshinota, a new cyanobacteriosponge threatening Pacific reefs. Scientia Marina, 57, 395-403.
65. Sarà M., Bavestrello G., Cattaneo-Vietti R., Cerrano C. (1998) Endosymbiosis in sponges, relevance for epigenesis and evolution. Symbiosis, 25, 57-70.
66. Scalera Liaci L., Sciscioli M., Matarrese A. (1971) La riproduzione sessuale di alcuni Tetractinomorpha (Porifera). Atti della Società Peloritana di Scienze Fisiche Matematiche e Naturali, 17, 235-245.
67. Scalera Liaci L., Sciscioli M., Matarrese A. (1973) Raffronto tra il comportamento sessuale di alcune Ceractinomorpha. Rivista di Biologia, 66, 135-153.
68. Schwarz J.A., Krupp D.A., Weis V.M. (1999) Late larval development and onset of symbiosis in the Scleractinian coral Fungia scutaria. Biological Bulletin, 196, 70-79.
69. Sears B.B. (1980) Elimination of plastids during spermatogenesis and fertilization in the plant kingdom. Plasmid, 4, 233-255.
70. Seddon S., Cheshire A.C., Wilkinson C.R. (1993) Photophysiology and acclimation of the coral reef sponge Cymbastela concentrica across a depth gradient. Proceedings of the 7th International Coral Reef Symposium, 2, 847-852.
71. Shimada A., Yano N., Kanai S., Lewin R.A., Maruyama T. (2003) Molecular phylogenetic relationship between two symbiotic photo-oxygenic prokaryotes, Prochloron sp. and Synechocystis trididemni. Phycologia, 42, 193-197.
72. Stackebrandt E., Goebel B.M. (1994) Taxonomic note: A place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. International Journal of Systematic Bacteriology, 44, 846-849.
73. Steindler L., Huchon D., Avni A., Ilan M. (2005) 16S rRNA phylogeny of sponge-associated cyanobacteria. Applied and Environmental Microbiology, 71, 4127-4131.
74. Taylor D.L. (1973) Algal symbionts of invertebrates. Annual Review of Microbiology, 27, 171-187.
75. Taylor M.W., Schupp P.J., de Nys R., Kjelleberg S., Steinberg P.D. (2005) Biogeography of bacteria associated with the marine Sponge Cymbastela concentrica. Environmental Microbiology, 7, 419-433.
76. Taylor M.W., Radax R., Steger D., Wagner M. (2007) Sponge-associated microorganisms: Evolution, ecology, and biotechnological potential. Microbiology and Molecular Biology Reviews, 71, 295-347.
77. Thacker R.W. (2005) Impacts of shading on sponge-cyanobacteria symbioses: A comparison between host-specific and generalist associations. Integrated Comparative Biology, 45, 369-376.
78. Thacker R.W., Starnes S. (2003) Host specificity of the symbiotic cyanobacterium Oscillatoria spongeliae in marine sponges, Dysidea spp. Marine Biology, 142, 643-648.
79. Thacker R.W., Diaz M.C., Rützler K., Erwin P.M., Kimble S.J.A., Pierce M.J., Dillard S.L. (2007) Phylogenetic relationships among the filamentous cyanobacterial symbionts of Caribbean sponges and a comparison of photosynthetic production between sponges hosting filamentous and unicellular cyanobacteria. In: Custódio M.R., Lôbo-Hajdu G., Hajdu E., Muricy G. (Eds), Porifera Research: Biodiversity, Innovation and Sustainability - 2007, Série Livros 28. Museu Nacional, Rio de Janeiro: 621-626.
80. Turner S. (1997) Molecular systematics of oxygenic photosynthetic bacteria. Plant Systematics and Evolution, 11, 13-52.
81. Unson M.D., Faulkner D.J. (1993) Cyanobacterial symbiont biosynthesis of chlorinated metabolites from Dysidea herbacea (Porifera). Experientia, 49, 349-353.
82. Unson M.D., Holland N.D., Faulkner D.J. (1994) A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue. Marine Biology, 119, 1-11.
83. Urbach E., Robertson D.L., Chisholm S.W. (1992) Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature, 355, 267-270.
84. Urbach E., Scanlan D.J., Distel D.L., Waterbury J.B., Chisholm S.W. (1998) Rapid diversification of marine picophytoplankton with dissimilar light-harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (Cyanobacteria). Journal of Molecular Evolution, 46, 188-201.
85. Usher K.M., Kuo J., Fromont J., Sutton D. (2001) Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia, 461, 15-23.
86. Usher K.M., Fromont J., Sutton D.C., Toze S. (2004a) The biogeography and phylogeny of unicellular cyanobacterial symbionts in selected sponges from Australia and the Mediterranean. Microbial Ecology, 48, 167-177.
87. Usher K.M., Toze S., Fromont J., Kuo J., Sutton D.C. (2004b) A new species of cyanobacterial symbiont from the marine sponge Chondrilla nucula. Symbiosis, 36, 183-192.
88. Usher K.M., Sutton D.C., Toze S., Kuo J., Fromont J. (2005) Inter-generational transmission of microbial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Marine and Freshwater Research, 56, 125-131.
89. Usher K.M., Kuo J., Fromont J., Toze S., Sutton D.C. (2006) Comparative morphology of five species of symbiotic and non-symbiotic coccoid cyanobacteria. European Journal of Phycology, 41, 179-188.
90. Vacelet J. (1971) Étude en microscopie électronique de l'association entre une cyanophycée chroococcale et une éponge du genre Verongia. Journal Microscopie, 12, 363-380.
91. Verde E.A., McCloskey L.R. (1996) Photosynthesis and respiration of two species of algal symbionts in the anemone Anthopluera elegantissima (Brandt) (Cnidaria, Anthozoa). Journal of Experimental Marine Biology and Ecology, 195, 187-202.
92. Vicente V.P. (1990) Overgrowth activity by the encrusting sponge Chondrilla nucula on a coral reef in Puerto Rico. Proceedings of the 3rd International Sponge Symposium. In: Rützler K. (Ed.), New Perspectives in Sponge Biology. Smithsonian Institution Press, Washington, DC, 436-442.
93. Vicente V.P. (1990) Response of sponges with autotrophic endosymbionts during the coral-bleaching episode in Puerto Rico. Coral Reefs, 8, 199-202.
94. Ward B.B. (2005) Molecular approaches to marine microbial ecology and the marine nitrogen cycle. Annual Review of Earth and Planetary Science, 33, 301-333.
95. Ward D.M., Ferris M.J., Nold S.C., Bateson M.M. (1998) A natural view of microbial biodiversity within hot spring cyanobacterial mat communities. Microbiology and Molecular Biology Reviews, 62, 1353-1370.
96. Waterbury J.B., Rippka R. (1989) Subsection 1. Order Chroococcales Wettstein 1924, emend. Rippka et.al., 1979. In: Staley J.T., Bryant M.P., Pfennig N., Holt J.G. (Eds), Bergey's Manual of Systematic Bacteriology, Vol. 3. Williams and Wilkins, Baltimore: 1728-1746.
97. Wayne L.G., Brenner D.J., Colwell R.R., Grimont P.A.D., Kandler O., Krichevsky M.I., Moore L.H., Moore W.E.C., Murray R.E.C., Stackebrandt E., Starr M.P., Truper H.G. (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. International Journal of Systematic Bacteriology, 37, 463-464.
98. Webb V.L., Maas E.W. (2002) Sequence analysis of 16S rRNA gene of cyanobacteria associated with the marine sponge Mycale (Carmia) hentscheli. FEMS Microbiology Letters, 207, 43-47.
99. Webster N.S., Hill R.T. (2001) The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by an α-proteobacterium. Marine Biology, 138, 843-851.
100. Wilkinson C.R. (1978) Microbial associations in sponges. III. Ultrastructure of the in situ associations in coral reef sponges. Marine Biology, 49, 177-185.
101. Wilkinson C.R. (1979) Nutrient translocation from symbiotic cyanobacteria to coral reef sponges. In: Lévi C., Boury-Esnault N. (Eds), Biologie des Spongiarires, Vol. 291. Colloques du Centre National Recherche Scientifique, Paris: 373-380.
102. Wilkinson C.R. (1983) Net primary productivity in coral reef sponges. Science, 219, 410-412.
103. Wilkinson C.R. (1984) Immunological evidence for the Precambrian origin of bacterial symbiosis in marine sponges. Proceedings of the Royal Society of London. Series B, 220, 509-517.
104. Wilkinson C.R. (1987a) Significance of microbial symbionts in sponge evolution and ecology. Symbiosis, 4, 135-146.
105. Wilkinson C.R. (1987b) Productivity and abundance of large sponge populations on Flinders Reef flats, Coral Sea. Coral Reefs, 5, 183-188.
106. Wilkinson C.R. (1987c) Interocean differences in size and nutrition of coral reef sponge populations. Science, 236, 1654-1657.
107. Wilkinson C.R. (1992) Symbiotic interactions between marine sponges and algae. In: Reisser W. (Ed.), Algae and Symbiosis, Plants, Animals, Fungi, Viruses. Interactions Explored. Biopress LTD, Bristol: 112-151.
108. Wilkinson C.R., Cheshire A.C. (1988) Growth rate of Jamaican coral reef sponges after Hurricane Allen. Biological Bulletin, 175, 175-179.
109. Wilkinson C.R., Cheshire A.C. (1990) Comparisons of sponge populations across the Barrier Reefs of Australia and Belize: Evidence for higher productivity in the Caribbean. Marine Ecology Progress Series, 67, 285-294.
110. Wilkinson C.R., Fay P. (1979) Nitrogen fixation in coral reef sponges with symbiotic cyanbacteria. Nature, 279, 527-529.
111. Wilkinson C.R., Trott L.A. (1985) Light as a factor determining the distribution of sponges across the central Great Barrier Reef. Proceedings of the 5th International Coral Reef Congress, 5, 125-130.
112. Wilkinson C.R., Vacelet J. (1979) Transplantation of marine sponges to different conditions of light and current. Journal of Experimental Marine Biology and Ecology, 37, 91-104.
113. Wyman M., Fay P. (1986) Underwater light climate and the growth and pigmentation of planktonic blue-green algae (Cyanobacteria) I. The influence of light quality. Proceedings of the Royal Society of London. Series B, 227, 367-380.