Simultaneous top‐down and bottom‐up forces control macroalgal blooms on coral reefs (Reply to the comment by Hughes et al.)

. 1996. Demographic approaches to community dynamics: A coral reef example. Ecology 77: 2256–2260. , B. D. KELLER, J. B. C. JACKSON, AND M. J. BOYLE. 1985. Mass mortality of the echinoid Diadema antillarum in Jamaica. Bull. Mar. Sci. 36: 377–384. , D. C. REED, AND M. J. BOYLE. 1987. Herbivory on coral reefs: Community structure following mass-mortality of sea urchins. J. Exp. Mar. Biol. Ecol. 113: 39–59. JANSSON, M., H. OLSSON, AND K. PATTERSON. 1988. Phosphatases: Origin, characteristics and function in lakes. Hydrobiologia 170: 157–175. LAPOINTE, B. E. 1997. Nutrient thresholds for eutrophication and macroalgal blooms on coral reefs in Jamaica and southeast Florida. Limnol. Oceanogr. 42: 1119–1131. LEE, T. N., M. E. CLARKE, E. WILLIAMS, A. M. SZMANT, AND T. BERGER. 1994. Evolution of the Tortugas Gyre and its influence on recruitment in the Florida Keys. Bull. Mar. Sci. 54: 621– 646. LEICHTER, J. J., S. R. WING, S. L. MILLER, AND M. W. DENNY. 1996. Pulsed delivery of subthermocline water to Conch Reef, Florida Keys by internal tidal bores. Limnol. Oceanogr. 41: 1490–1501. LESSIOS, H. A. 1988. Mass mortality of Diadema antillarum in the Caribbean: What have we learned? Annu. Rev. Ecol. Syst. 19: 371–393. LEWIS, S. 1986. The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol. Monogr. 56: 183–200. LIDDELL, W. D., AND S. L. OHLHORST. 1986. Changes in the benthic community composition following the mass morality of Diadema antillarum at Jamaica. J. Exp. Mar. Biol. Ecol. 95: 271– 278. , AND . 1992. Ten years of distribution and change on a Jamaican fringing reef. Proc. 7th Int. Coral Reef Symp., Guam 1: 144–150. MCFARLANE, A. H. 1991. The mariculture potential of Gracilaria species (Rhodophyta) in Jamaican nitrate-enriched back-reef habitats: Growth, nutrient uptake and elemental composition. Ms. thesis, Univ. of Miami. MILLHAM, N. P., AND B. L. HOWES. 1994. Nutrient balance of a shallow coastal embayment: I. Patterns of groundwater discharge. Mar. Ecol. Prog. Ser. 112: 155–167. MORRISON, D. 1988. Comparing fish and urchin grazing in shallow and deeper coral reef algal communities. Ecology 69: 1367– 1382. MUNRO, J. L. 1983. Caribbean coral reef fisheries. ICLARM Stud. Rev. 7: 1–276. OGDEN, J. C., R. A. BROWN, AND N. SALESKY. 1973. Grazing by the echinoid Diadema antillarum. Formation of halos around West-Indian patch reefs. Science 182: 715–717. SAMMARCO, P. W., J. S. LEVINTON, AND J. C. OGDEN. 1974. Grazing and control of coral reef community structure by Diadema antillarum Philippi (Echinodermata: Echinoidea): A preliminary study. J. Mar. Res. 32: 47–53. STENECK, R. S. 1988. Herbivory on coral reefs: A synthesis. Proc. 6th Int. Coral Reef Symp. 1: 37–49. . 1993. Is herbivore loss more damaging to reefs than hurricanes? Case studies from two Caribbean reef systems (1978– 1988), p. 220–226. In R. Ginsburg [ed.], Proceedings of a colloquium on global aspects of coral reefs: Health, hazards and history. Univ. of Miami. SZMANT, A. M. 1997. Nutrient effects on coral reefs: A hypothesis on the importance of topographic and trophic complexity on nutrient dynamics. Proc. 8th Int. Coral Reef Symp. 2: 1527– 1532. , AND A. FORRESTER. 1996. Water column and sediment nitrogen and phosphorus distribution patterns in the Florida Keys, and potential relationships to past and present coral reef development. Coral Reefs 15: 21–41. VAN DEN HOEK, C., A. M. BREEMAN, R. P. M. BAK, AND G. VAN BUURT. 1978. The distribution of algae, corals and gorgonians in relation to depth, light attenuation, water movement and grazing pressure in the fringing coral reef of Curacao, Netherlands Antilles. Aquat. Bot. 5: 1–46. WOODLEY, J. D. 1999. Diadema exerts top-down control of macroalgae on Jamaican coral reefs. Coral Reefs 18: In press.

[1]  M. Littler,et al.  Models of tropical reef biogenesis: the contribution of algae , 1984 .

[2]  C. Wilkinson,et al.  Effects of fish grazing and damselfish territoriality on coral reef algae. II. Nitrogen fixation , 1983 .

[3]  T. Hughes Catastrophes, Phase Shifts, and Large-Scale Degradation of a Caribbean Coral Reef , 1994, Science.

[4]  J. Kremer,et al.  Episodic nutrient supply to a Kelp forest ecosystem in Southern California , 1984 .

[5]  C. D’Elia,et al.  NUTRITIONAL STUDIES OF TWO RED ALGAE. I. GROWT RATE AS A FUNCTION OF NITROGEN SOURCE AND CONCENTRATION 1 , 1978 .

[6]  S. Lewis The Role of Herbivorous Fishes in the Organization of a Caribbean Reef Community , 1986 .

[7]  M. Furnas,et al.  Shelf-scale nitrogen and phosphorus budgets in the central Great Barrier Reef (16-19oS) , 1997 .

[8]  G. Likens,et al.  Technical Report: Human Alteration of the Global Nitrogen Cycle: Sources and Consequences , 1997 .

[9]  P. Bell,et al.  Eutrophication and coral reefs—some examples in the Great Barrier Reef lagoon , 1992 .

[10]  T. Goreau Bleaching and reef community change in Jamaica: 1951-1991 , 1992 .

[11]  S. V. Smith,et al.  C:N:P ratios of benthic marine plants1 , 1983 .

[12]  W. J. Mattson,et al.  Herbivory in relation to plant nitrogen content , 1980 .

[13]  P. Mccormick,et al.  Periphyton-Water Quality Relationships along a Nutrient Gradient in the Northern Florida Everglades , 1996, Journal of the North American Benthological Society.

[14]  Steven L. Miller,et al.  Algal blooms on coral reefs: What are the causes? , 1999 .

[15]  James W. Porter,et al.  Nitrate-Rich Groundwater Inputs To Discovery Bay, Jamaica - A Significant Source Of N To Local Coral Reefs , 1981 .

[16]  Mark W. Denny,et al.  Pulsed delivery of subthermocline water to Conch Reef (Florida Keys) by internal tidal bores , 1996 .

[17]  B. Lapointe Macroalgal production and nutrient relations in oligotrophic areas of Florida Bay , 1989 .

[18]  B. Lapointe,et al.  Experimental outdoor studies with Ulva fasciata Delile. I. Interaction of light and nitrogen on nutrient uptake, growth, and biochemical composition , 1981 .

[19]  B. Hatcher,et al.  Coral reef ecosystems: how much greater is the whole than the sum of the parts? , 1997, Coral Reefs.

[20]  R. Carpenter Mass mortality of a Caribbean sea urchin: Immediate effects on community metabolism and other herbivores. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[21]  H. Lessios,et al.  MASS MORTALITY OF DIADEMA ANTILLARUM IN THE CARIBBEAN: What Have We Learned? , 1988 .

[22]  J. Stimson,et al.  Nitrogen-limited growth in the coral reef chlorophyte Dictyosphaeriacavernosa, and the effect of exposure to sediment-derived nitrogen on growth , 1996 .

[23]  B. Lapointe,et al.  Modification of benthic community structure by natural eutrophication: the Belize barrier reef , 1993 .

[24]  P. Sammarco Effects of fish grazing and damselfish territoriality on coral reef algae. 1. Algal community structure , 1983 .

[25]  Charles S. Yentsch,et al.  A bridge between ocean optics and microbial ecology , 1989 .

[26]  Stephen V. Smith,et al.  Dissolved nutrients of a high-latitude coral reef, Houtman Abrolhos Islands, Western Australia , 1984 .