Unseen players shape benthic competition on coral reefs

Trends in Microbiology

Volumn 20, Issue 12, 2012, Pages 621-628

  Barott, Katie L ^a   Rohwer, Forest L ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

3DAM; Allelochemistry; Bacteria; Coral; Crustose coralline algae; DDAM; Holobiont; Macroalgae; Organic matter; Phage; Turf algae

Indexed keywords

CHLOROPHYLL A; DISSOLVED ORGANIC MATTER;

BENTHOS; CORAL REEF; GEOMETRY; HERBIVORY; HYDROPHILICITY; HYDROPHOBICITY; INTRASPECIFIC COMPETITION; MACROALGA; METAMORPHOSIS; MICROBIAL COMMUNITY; NONHUMAN; PHOTOSYNTHESIS; PRIORITY JOURNAL; REVIEW; WATER FLOW;

ANIMALS; ANTHOZOA; BACTERIA; BIOTA; CORAL REEFS; MICROBIAL INTERACTIONS; ORGANIC CHEMICALS; POPULATION DYNAMICS; SEAWATER; SEAWEED; VIRUSES;

ALGAE; ANTHOZOA;

EID: 84869496636     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2012.08.004     Document Type: Review

References (98)

1. Lang J.C., Chornesky E.A. Competition between scleractinian reef corals: a review of mechanisms and effects. Ecosyst. World 1990, 25:209-252.
2. Hughes T.P., et al. Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr. Biol. 2007, 17:360-365.
3. McCook L.J. Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 1999, 18:357-367.
4. Sandin S.A., et al. Baselines and degradation of coral reefs in the northern Line Islands. PLoS ONE 2008, 3:e1548.
5. Burkepile D.E., Hay M.E. Herbivore vs. nutrient control or marine primary producers: context-dependent effects. Ecology 2006, 87:3128-3139.
6. Vermeij M.J.A., et al. The effects of nutrient enrichment and herbivore abundance on the ability of turf algae to overgrow coral in the Caribbean. PLoS ONE 2010, 5:e14312.
7. Smith J.E., et al. The effects of top-down versus bottom-up control on benthic coral reef community structure. Oecologia 2010, 163:497-507.
8. Littler M.M., et al. Harmful algae on tropical coral reefs: bottom-up eutrophication and top-down herbivory. Harmful Algae 2006, 5:565-585.
9. Burkepile D., Hay M. Nutrient versus herbivore control of macroalgal community development and coral growth on a Caribbean reef. Mar. Ecol. Prog. Ser. 2009, 389:71-84.
10. Sotka E.E., Hay M.E. Effects of herbivores, nutrient enrichment, and their interactions on macroalgal proliferation and coral growth. Coral Reefs 2009, 28:555-568.
11. Jompa J., McCook L.J. The effects of nutrients and herbivory on competition between a hard coral (Porites cylindrica) and a brown alga (Lobophora variegata). Limnol. Oceanogr. 2002, 47:527-534.
12. Jompa J., McCook L.J. Effects of competition and herbivory on interactions between a hard coral and a brown alga. J. Exp. Mar. Biol. Ecol. 2002, 271:25-39.
13. Lirman D. Competition between macroalgae and corals: effects of herbivore exclusion and increased algal biomass on coral survivorship and growth. Coral Reefs 2001, 19:392-399.
14. Adey W. Coral reefs: algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. J. Phycol. 1998, 34:393-406.
15. Negri A.P., et al. Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar. Ecol. Prog. Ser. 2001, 223:121-131.
16. Price N. Habitat selection, facilitation, and biotic settlement cues affect distribution and performance of coral recruits in French Polynesia. Oecologia 2010, 163:747-758.
17. Arnold S.N., Steneck R.S. Settling into an increasingly hostile world: the rapidly closing 'recruitment window' for corals. PLoS ONE 2011, 6:e28681.
18. Vermeij M.J.A., et al. Crustose coralline algae can suppress macroalgal growth and recruitment on Hawaiian coral reefs. Mar. Ecol. Prog. Ser. 2011, 422:1-7.
19. Barott K., et al. Hyperspectral and physiological analyses of coral-algal interactions. PLoS ONE 2009, 4:e8043.
20. Barott K.L., et al. Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae. Proc. R. Soc. B: Biol. Sci. 2012, 279:1655-1664.
21. McCook L. Competition between corals and algal turfs along a gradient of terrestrial influence in the nearshore central Great Barrier Reef. Coral Reefs 2001, 19:419-425.
22. Chadwick N.E., Morrow K.M. Competition among sessile organisms on coral reefs. Coral Reefs: An Ecosystem in Transition 2011, 347-371. Springer. Z. Dubinsky, N. Stambler (Eds.).
23. River G.F., Edmunds P.J. Mechanisms of interaction between macroalgae and scleractinians on a coral reef in Jamaica. J. Exp. Mar. Biol. Ecol. 2001, 261:159-172.
24. Titlyanov E.A., et al. Interaction between benthic algae (Lyngbya bouillonii, Dictyota dichotoma) and scleractinian coral Porites lutea in direct contact. J. Exp. Mar. Biol. Ecol. 2007, 342:282-291.
25. Rasher D.B., Hay M.E. Chemically rich seaweeds poison corals when not controlled by herbivores. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:9683-9688.
26. Smith J.E., et al. Indirect effects of algae on coral: Algae-mediated, microbe-induced coral mortality. Ecol. Lett. 2006, 9:835-845.
27. Tanner J.E. Competition between scleractinian corals and macroalgae: an experimental investigation of coral growth, survival and reproduction. J. Exp. Mar. Biol. Ecol. 1995, 190:151-168.
28. Foster N., et al. Competitive effects of macroalgae on the fecundity of the reef-building coral Montastraea annularis. Mar. Ecol. Prog. Ser. 2008, 367:143-152.
29. Birrell C.L., et al. Effects of benthic algae on the replenishment of corals and the implications for the resilience of coral reefs. Oceanogr. Mar. Biol. Annu. Rev. 2008, 46:25-64.
30. Arnold S.N., et al. Running the gauntlet: inhibitory effects of algal turfs on the processes of coral recruitment. Mar. Ecol. Prog. Ser. 2010, 414:91-105.
31. Birrell C.L., et al. Effects of algal turfs and sediment on coral settlement. Mar. Pollut. Bull. 2005, 51:408-414.
32. Box S.J., Mumby P.J. Effect of macroalgal competition on growth and survival of juvenile Caribbean corals. Mar. Ecol. Prog. Ser. 2007, 342:139-149.
33. Jompa J., McCook L.J. Coral-algal competition: macroalgae with different properties have different effects on corals. Mar. Ecol. Prog. Ser. 2003, 258:87-95.
34. Fricke A., et al. Succession patterns in algal turf vegetation on a Caribbean coral reef. Bot. Mar. 2011, 54:111-126.
35. Barott K.L., et al. Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ. Microbiol. 2011, 13:1192-1204.
36. Quan-Young L.I., Espinoza-Avalos J. Reduction of zooxanthellae density, chlorophyll a concentration, and tissue thickness of the coral Montastraea faveolata (Scleractinia) when competing with mixed turf algae. Limnol. Oceanogr. 2006, 51:1159-1166.
37. Haas A., et al. Seasonal monitoring of coral-algae interactions in fringing reefs of the Gulf of Aqaba, Northern Red Sea. Coral Reefs 2010, 29:93-103.
38. Wangpraseurt D., et al. In situ oxygen dynamics in coral-algal interactions. PLoS ONE 2012, 7:e31192.
39. Haas A., et al. Effect of inorganic and organic nutrient addition on coral-algae assemblages from the Northern Red Sea. J. Exp. Mar. Biol. Ecol. 2009, 380:99-105.
40. Linares C., et al. Effects of turf algae on recruitment and juvenile survival of gorgonian corals. Mar. Ecol. Prog. Ser. 2012, 452:81-88.
41. Barott K.L., et al. Natural history of coral-algae competition across a gradient of human activity in the Line Islands. Mar. Ecol. Prog. Ser. 2012, 460:1-12.
42. Nugues M.M., et al. Coral defense against macroalgae: differential effects of mesenterial filaments on the green alga Halimeda opuntia. Mar. Ecol. Prog. Ser. 2004, 278:103-114.
43. Nugues M.M., et al. Algal contact as a trigger for coral disease. Ecol. Lett. 2004, 7:919-923.
44. Bourne D.G., et al. Microbial disease and the coral holobiont. Trends Microbiol. 2009, 17:554-562.
45. Sutherland K.P., et al. Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar. Ecol. Prog. Ser. 2004, 266:265-272.
46. Dinsdale E.A., et al. Microbial ecology of four coral atolls in the Northern Line Islands. PLoS ONE 2008, 3:e1584.
47. Raymundo L.J., et al. Functionally diverse reef-fish communities ameliorate coral disease. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17067-17070.
48. Dinsdale E.A., Rohwer F. Fish or germs? Microbial dynamics associated with changing trophic structures on coral reefs. Coral Reefs: An Ecosystem in Transition 2011, 231-240. Springer. Z. Dubinsky, N. Stambler (Eds.).
49. Haas A.F., et al. Effects of coral reef benthic primary producers on dissolved organic carbon and microbial activity. PLoS ONE 2011, 6:e27973.
50. 2 availability. Mar. Ecol. Prog. Ser. 2010, 411:61-71.
51. Kline D.I., et al. Role of elevated organic carbon levels and microbial activity in coral mortality. Mar. Ecol. Prog. Ser. 2006, 314:119-125.
52. Kuntz N.M., et al. Pathologies and mortality rates caused by organic carbon and nutrient stressors in three Caribbean coral species. Mar. Ecol. Prog. Ser. 2005, 294:173-180.
53. Vermeij M.J.A., et al. Survival and settlement success of coral planulae: independent and synergistic effects of macroalgae and microbes. Oecologia 2009, 159:325-336.
54. Rasher D.B., et al. Macroalgal terpenes function as allelopathic agents against reef corals. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:17726-17731.
55. Paul V.J., et al. Chemically mediated interactions between macroalgae Dictyota spp. and multiple life-history stages of the coral Porites astreoides. Mar. Ecol. Prog. Ser. 2011, 426:161-170.
56. Morrow K.M., et al. Allelochemicals produced by Caribbean macroalgae and cyanobacteria have species-specific effects on reef coral microorganisms. Coral Reefs 2011, 30:309-320.
57. Koehl M.A.R., Hadfield M.G. Hydrodynamics of larval settlement from a larva's point of view. Integr. Comp. Biol. 2010, 50:539-551.
58. Shashar N., et al. Hydromechanical boundary layers over a coral reef. J. Exp. Mar. Biol. Ecol. 1996, 199:17-28.
59. Azam F. Microbial control of oceanic carbon flux: the plot thickens. Science 1998, 280:694-696.
60. Williams S.L., Carpenter R.C. Effects of unidirectional and oscillatory water flow on nitrogen fixation (acetylene reduction) in coral reef algal turfs, Kaneohe Bay, Hawaii. J. Exp. Mar. Biol. Ecol. 1998, 226:293-316.
61. Patterson M.R., et al. In situ measurements of flow effects on primary production and dark respiration in reef corals. Limnol. Oceanogr. 1991, 36:936-948.
62. Lesser M.P., et al. Effects of morphology and water motion on carbon delivery and productivity in the reef coral, Pocillopora damicornis (Linnaeus): diffusion barriers, inorganic carbon limitation, and biochemical plasticity. J. Exp. Mar. Biol. Ecol. 1994, 178:153-179.
63. Marhaver, K.L. et al. (2012) Janzen-Connell effects in a broadcast-spawning Caribbean coral: distance-dependent survival of larvae and settlers. Ecology, doi:10.1890/12-0985.1.
64. Frias-Lopez J., et al. Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl. Environ. Microbiol. 2002, 68:2214.
65. Pandolfi J.M. Response of Pleistocene coral reefs to environmental change over long temporal scales. Am. Zool. 1999, 39:113-130.
66. Knowlton N., et al. Coral reef biodiversity. Life in the World's Oceans: Diversity, Distribution, and Abundance 2010, 65-77. Wiley-Blackwell. A. McIntyre (Ed.).
67. Knowlton N., Jackson J.B.C. Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol. 2008, 6:e54.
68. Lachnit T., et al. Specific epibacterial communities on macroalgae: phylogeny matters more than habitat. Aquat. Biol. 2009, 5:181-186.
69. Knowlton N., Rohwer F. Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am. Nat. 2003, 162:S51-S62.
70. Toller W., et al. Genetic evidence for a protozoan (phylum Apicomplexa) associated with corals of the Montastraea annularis species complex. Coral Reefs 2002, 21:143-146.
71. Burke C., et al. Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J. 2011, 5:590-600.
72. Kvennefors E.C.E., et al. Bacterial communities of two ubiquitous Great Barrier Reef corals reveals both site- and species-specificity of common bacterial associates. PLoS ONE 2010, 5:e10401.
73. Rohwer F., et al. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 2002, 243:1-10.
74. Klaus J.S., et al. Bacterial communities inhabiting the healthy tissues of two Caribbean reef corals: interspecific and spatial variation. Coral Reefs 2005, 24:129-137.
75. Chen C.-P., et al. The dynamics of microbial partnerships in the coral Isopora palifera. ISME J. 2011, 5:728-740.
76. Hong M.-J., et al. Influence of species specificity and other factors on bacteria associated with the coral Stylophora pistillata in Taiwan. Appl. Environ. Microbiol. 2009, 75:7797-7806.
77. Staufenberger T., et al. Phylogenetic analysis of bacteria associated with Laminaria saccharina. FEMS Microbiol. Ecol. 2008, 64:65-77.
78. Sweet M., et al. Dynamics of bacterial community development in the reef coral Acropora muricata following experimental antibiotic treatment. Coral Reefs 2011, 31:1121-1133.
79. Bourne D., et al. Changes in coral-associated microbial communities during a bleaching event. ISME J. 2007, 2:350-363.
80. Daniels C.A., et al. Spatial heterogeneity of bacterial communities in the mucus of Montastraea annularis. Mar. Ecol. Prog. Ser. 2011, 426:29-40.
81. Sweet M., et al. Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 2011, 30:39-52.
82. Ritchie K.B. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 2006, 322:1-14.
83. Shnit-Orland M., Kushmaro A. Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol. Ecol. 2009, 67:371-380.
84. Rypien K.L., et al. Antagonistic interactions among coral-associated bacteria. Environ. Microbiol. 2010, 12:28-39.
85. Egan S., et al. Phylogenetic relationship and antifouling activity of bacterial epiphytes from the marine alga Ulva lactuca. Brief report. Environ. Microbiol. 2000, 2:343-347.
86. Nakanishi K., et al. Bacteria that induce morphogenesis in Ulva pertusa (Chlorophyta) grown under axenic conditions. J. Phycol. 2008, 32:479-482.
87. Johnson C.R., Sutton D.C. Bacteria on the surface of crustose coralline algae induce metamorphosis of the crown-of-thorns starfish Acanthaster planci. Mar. Biol. 1994, 120:305-310.
88. Lesser M., et al. Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar. Ecol. Prog. Ser. 2007, 346:143-152.
89. Raina J.B., et al. Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl. Environ. Microbiol. 2009, 75:3492.
90. Mao-Jones J., et al. How microbial community composition regulates coral disease development. PLoS Biol. 2010, 8:e1000345.
91. Reshef L., et al. The coral probiotic hypothesis. Environ. Microbiol. 2006, 8:2068-2073.
92. Thurber R.V., et al. Metagenomic analysis of stressed coral holobionts. Environ. Microbiol. 2009, 11:2148-2163.
93. Case R.J., et al. Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga. Environ. Microbiol. 2011, 13:529-537.
94. Thurber V., et al. Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:18413.
95. Ainsworth T., Hoegh-Guldberg O. Bacterial communities closely associated with coral tissues vary under experimental and natural reef conditions and thermal stress. Aquat. Biol. 2009, 4:289-296.
96. Campbell A.H., et al. Climate change and disease: bleaching of a chemically defended seaweed. Global Change Biol. 2011, 17:2958-2970.
97. Meron D., et al. The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J. 2011, 5:51-60.
98. Webster N.S., et al. Elevated seawater temperature causes a microbial shift on crustose coralline algae with implications for the recruitment of coral larvae. ISME J. 2010, 5:759-770.