Abstract
We conducted a 20-week manipulative field experiment on shallow forereefs of the Florida Keys to assess the separate and interactive effects of herbivory and nutrient enrichment on the development of macroalgal communities and the fitness of the corals Porites porites and Siderastrea siderea. Excluding large herbivorous fishes produced macrophyte blooms both with and without nutrient enrichment. In contrast, there were no direct effects of nutrient enrichment. There were, however, small, but significant, interactive effects of herbivory and enrichment on macroalgal cover. Following nutrient enrichment, total macroalgae and the common seaweeds Dictyota spp. were suppressed in the presence, but not in the absence, of large herbivorous fishes—suggesting that fishes were selectively feeding on nutrient-enriched macrophytes. Access by large herbivores prevented algal overgrowth of corals, but these large fishes also directly grazed both corals. Excluding fishes did not alter survivorship of either coral species, but did decrease parrotfish grazing scars on both corals and increased the net growth of P. porites. Nutrient additions had no direct effects on the survivorship of corals, but there was a trend (P = 0.097) for nutrients to stimulate the growth of P. porites. The preponderance of experiments available to date indicates that loss of key herbivores is a major factor driving macroalgal blooms on coral reefs; anthropogenic nutrient pollution generally plays a more minor role.
References
Aronson RB, Precht WF (2001) Evolutionary paleoecology of Caribbean coral reefs. In: Allmon WD, Bottjer DJ (eds) Evolutionary paleoecology: the ecological context of macroevolutionary change. Columbia University Press, New York, pp 171–234
Aronson RB, Precht WF (2006) Conservation, precaution, and Caribbean reefs. Coral Reefs 25:441–450
Aronson R, Macintyre I, Precht W, Murdoch T, Wapnick C (2002) The expanding scale of species turnover events on coral reefs in Belize. Ecol Monogr 72:233–249
Atkinson M (1988) Are coral reefs nutrient-limited? Proc 6th Int Coral Reef Symp 6:157–166
Baums IB, Miller MW, Szmant AM (2003) Ecology of a corallivorous gastropod, Coralliophila abbreviata, on two scleractinian hosts. 1. Population structure of snails and corals. Mar Biol 142:1083–1091
Beach KS, Walters LJ, Borgeas HB (2006) Irradiance and nutrient limitation of Dictyota spp. populations on Conch Reef, Florida Keys, USA. J Exp Mar Biol Ecol 329:101–112
Belliveau SA, Paul VJ (2002) Effects of herbivory and nutrients on the early colonization of crustose coralline and fleshy algae. Mar Ecol Prog Ser 232:105–114
Bellwood D, Choat J (1990) A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. Environ Biol Fish 28:189–214
Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833
Birrell CL, McCook LJ, Willis BL, Diaz-Pulido GA (2008) Effects of benthic algae on the replenishment of corals and the implications for the resilience of coral reefs. Oceanogr Mar Biol 46:25–63
Boyer K, Fong P, Armitage A, Cohen R (2004) Elevated nutrient content of tropical macroalgae increases rates of herbivory in coral, seagrass, and mangrove habitats. Coral Reefs 23:530–538
Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139
Burkepile DE, Hay ME (2008) Herbivore species richness and feeding complementarity affect community structure and function: the case for Caribbean reefs. Proc Natl Acad Sci USA 105:16201–16206
Burkepile DE, Hay ME (in press) Nutrient vs. herbivore control of macroalgal community development and coral growth on a Caribbean coral reef. Mar Ecol Prog Ser
Carpenter RC (1986) Partitioning herbivory and its effects on coral reef algal communities. Ecol Appl 56:345–363
Carpenter R, Edmunds P (2006) Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals. Ecol Lett 9:271–280
Cruz-Rivera E, Hay ME (2003) Prey nutritional quality interacts with chemical defenses to affect consumer feeding and fitness. Ecol Monogr 73:483–506
Delgado O, Lapointe BE (1994) Nutrient-limited productivity of calcareous versus fleshy macroalgae in a eutrophic, carbonate-rich tropical marine environment. Coral Reefs 13:151–159
Diaz-Pulido G, McCook L (2003) Relative roles of herbivory and nutrients in the recruitment of coral-reef seaweeds. Ecology 84:2026–2033
Dodge RE (1984) Coral calcification rates by the buoyant technique: effects of alizarin staining. J Exp Mar Biol Ecol 75:217–232
Edmunds PJ, Carpenter RC (2001) Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef. Proc Natl Acad Sci USA 98:5067–5071
Fong P, Smith TB, Wartian MJ (2006) Epiphytic cyanobacteria maintain shifts to macroalgal dominance on coral reefs following ENSO disturbance. Ecology 87:1162–1168
Furman BT, Heck KL (2008) Effects of nutrient enrichment and grazers on coral reefs: an experimental assessment. Mar Ecol Prog Ser 363:89–101
Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960
Gardner TA, Cote IM, Gill AB, Grant A, Watkinson AR (2005) Hurricanes and Caribbean coral reefs: impacts, recovery patterns and role in long-term decline. Ecology 86:174–184
Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425
Harborne AR, Mumby PJ, Kappel CV, Dahlgren CP, Micheli F, Holmes KE, Sanchirico JN, Broad K, Elliott IA, Brumbaugh DR (2008) Reserve effects and natural variation in coral reef communities J Appl Ecol 45:1010–1018
Hay ME (1984) Patterns of fish and urchin grazing on Caribbean coral reefs: are previous results typical? Ecology 65:446–454
Hay ME (1997) The ecology and evolution of seaweed–herbivore interactions on coral reefs. Coral Reefs 16:S67–S76
Hay ME, Taylor PR (1985) Competition between herbivorous fish and urchins on Caribbean reefs. Oecologia 65:591–598
Hay ME, Parker J, Burkepile D, Caudill C, Wilson A, Hallinan Z, Chequer A (2004) Mutualisms and aquatic community structure: the enemy of my enemy is my friend. Annual Review of Ecology Evolution and Systematics 35:175–197
Heck KL, Valentine JF (2007) The primacy of top-down effects in shallow benthic ecosystems. Estuaries and Coasts 30:371–381
Heck KL, Valentine JF, Pennock JR, Spitzer PM (2006) Effects of nutrient enrichment and grazing on shoalgrass Halodule wrightii and its epiphytes: results of a field experiment. Mar Ecol Prog Ser 326:145–156
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547
Hughes TP, Szmant AM, Steneck RS, Carpenter RC, Miller SL (1999) Algal blooms on coral reefs: what are the causes? Limnol Oceanogr 44:1583–1586
Hughes TP, Rodrigues MJ, Bellwood D, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365
Jackson JBC (2008) Ecological extinction and evolution in a brave new ocean. Proc Natl Acad Sci USA 105:11458–11465
Jackson JBC, Kirby MX, Berger WH, Bjorndal K, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandsson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638
Jompa J, McCook LJ (2002) The effects of nutrients and herbivory on competition between a hard coral (Porites cylindrica) and a brown alga (Lobophora variegata). Limnol Oceanogr 47:527–534
Knowlton N (1992) Thresholds and multiple stable states in coral reef community dynamics. Am Zool 32:674–682
Lapointe BE (1997) Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida. Limnol Oceanogr 42:1119–1131
Lapointe BE, Barile PJ, Yentsch C, Littler MM, Littler DS, Kakuk B (2004) The relative importance of nutrient enrichment and herbivory on macroalgal communities near Norman’s Pond Cay, Exumas Cays, Bahamas: a “natural” enrichment experiment. J Exp Mar Biol Ecol 298:275–301
Lapointe BE, Barile PJ, Littler MM, Littler DS (2005) Macroalgal blooms on southeast Florida coral reefs II. Cross-shelf discrimination of nitrogen sources indicates widespread assimilation of sewage nitrogen. Harmful Algae 4:1106–1122
Larned S (1998) Nitrogen- versus phosphorus-limited growth and sources of nutrients for coral reef macroalgae. Mar Biol 132:409–421
Larned S, Atkinson M (1997) Effects of water velocity on NH4 and PO4 uptake and nutrient-limited growth in the macroalga Dictyosphaeria cavernosa. Mar Ecol Prog Ser 157:295–302
Leichter JJ, Wing SR, Miller SL, Denny MW (1996) Pulsed delivery of subthermocline water to Conch Reef (Florida Keys) by internal tidal bores. Limnol Oceanogr 41:1490–1501
Leichter JJ, Stewart HL, Miller SL (2003) Episodic nutrient transport to Florida coral reefs. Limnol Oceanogr 48:1394–1407
Lesser MP (2004) Experimental biology of coral reef ecosystems. J Exp Mar Biol Ecol 300:217–252
Lessios HA (1988) Mass mortality of Diadema antillarum in the Caribbean—what have we learned. Annu Rev Ecol Syst 19:371–393
Lewis SM (1986) The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol Appl 56:183–200
Littler MM, Littler DS (1984) Models of tropical reef biogenesis: the contribution of algae. Progress in Phycological Research 3:323–364
Littler MM, Taylor P, Littler DS (1989) Complex interactions in the control of coral zonation on a Caribbean reef flat. Oecologia 80:331–340
Littler MM, Littler DS, Brooks BL (2006a) Harmful algae on tropical coral reefs: bottom-up eutrophication and top-down herbivory. Harmful Algae 5:565–585
Littler MM, Littler DS, Brooks BL, Lapointe BE (2006b) Nutrient manipulation methods for coral reef studies: a critical review and experimental field data. J Exp Mar Biol Ecol 336:242–253
Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161
McClanahan TR, Cokos BA, Sala E (2002) Algal growth and species composition under experimental control of herbivory, phosphorus and coral abundance in Glovers Reef, Belize. Mar Pollut Bull 44:441–451
McClanahan TR, Sala E, Stickels PA, Cokos BA, Baker AC, Starger CJ, Jones SH (2003) Interaction between nutrients and herbivory in controlling algal communities and coral condition on Glover’s Reef, Belize. Mar Ecol Progr Ser 261:135–147
McClanahan T, Carreiro-Silva M, DiLorenzo M (2007) Effect of nitrogen, phosphorous, and their interaction on coral reef algal succession in Glover’s Reef, Belize. Mar Pollut Bull 54:1947–1957
McCook LJ (1999) Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18:357–367
McCook LJ, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400–417
Miller MW (1998) Coral/seaweed competition and the control of reef community structure within and between latitudes. Oceanogr Mar Biol Annu Rev 36:65–96
Miller MW, Hay ME (1996) Coral-seaweed-grazer-nutrient interactions on temperate reefs. Ecol Monogr 66:323–344
Miller MW, Hay ME (1998) Effects of fish predation and seaweed competition on the survival and growth of corals. Oecologia 113:231–238
Miller MW, Hay ME, Miller SL, Malone D, Sotka EE, Szmant AM (1999) Effects of nutrients versus herbivores on reef algae: a new method for manipulating nutrients on coral reefs. Limnol Oceanogr 44:1847–1861
Millero FJ, Feistel R, Wright DG, McDougall TJ (2008) The composition of standard seawater and the definition of the reference-composition salinity scale. Deep Sea Res I 55:50–72
Mumby PJ, Steneck RS (2008) Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends Ecol Evol 23:555–563
Mumby PJ, Dahlgren CP, Harborne AR, Kappel CV, Micheli F, Brumbaugh DR, Holmes KE, Mendes JM, Broad K, Sanchirico JN, Buch K, Box S, Stoffle RW, Gill AB (2006) Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98–101
Mumby PJ, Hastings A, Edwards H (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98–101
Randall JE (1961) Overgrazing of algae by herbivorous marine fishes. Ecology 42:812
Richardson LL (1998) Coral diseases: what is really known? Trends Ecol Evol 13:438–443
Rogers CS (1990) Responses of coral reefs and reef organisms to sedimentation. Mar Ecol Prog Ser 62:185–202
Rotjan RD, Lewis SM (2005) Selective predation by parrotfishes on the reef coral Porites astreoides. Mar Ecol Prog Ser 305:193–201
Rougerie F, Wauthy B (1993) The endo-upwelling concept: from geothermal convection to reef construction. Coral Reefs 12:19–30
Russell BD, Connell SD (2007) Response of grazers to sudden nutrient pulses in oligotrophic versus eutrophic conditions. Mar Ecol Prog Ser 349:73–80
Smith VH, Tilman GD, Nekola JC (1999) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ Pollut 100:179–196
Smith JE, Smith CM, Hunter CL (2001) An experimental analysis of the effects of herbivory and nutrient enrichment on benthic community dynamics on a Hawaiian reef. Coral Reefs 19:332–342
Smith JE, Smith CM, Vroom PS, Beach KL, Miller SL (2004) Nutrient and growth dynamics of Halimeda tuna on Conch Reef, Florida Keys: possible influence of internal tides on nutrient status and physiology. Limnol Oceanogr 49:1923–1936
Stachowicz JJ, Hay ME (1999) Mutualism and coral persistence: the role of herbivore resistance to algal chemical defense. Ecology 80:2085–2101
Stephenson W, Searles RB (1960) Experimental studies on the ecology of intertidal environments at Heron Island. I. Exclusion of fish from beach rock. Aust J Mar Freshw Res 11:241–267
Szmant AM (2002) Nutrient enrichment on coral reefs: is it a major cause of coral reef decline? Estuaries 25:743–766
Szmant A, Forrester A (1996) Water column and sediment nitrogen and phosphorus distribution patterns in the Florida Keys, USA. Coral Reefs 15:21–41
Thacker RW, Ginsburg DW, Paul VJ (2001) Effects of herbivore exclusion and nutrient enrichment on coral reef macroalgae and cyanobacteria. Coral Reefs 19:318–329
Worm B, Reusch TBH, Lotze HK (2000) In situ nutrient enrichment: methods for marine benthic ecology. Int Rev Hydrobiol 85:359–375
Acknowledgements
This research was supported by the Teasley Endowment to Georgia Tech with supplemental support from the University of North Carolina, Wilmington National Undersea Research Center (to MEH) and NSF grant OCE-0550245 (to ES). We thank S. Bullard, G. Cetrulo, E.H. Hay, K. Hay, A. Hollebone, and C. Kicklighter for help with field work. This represents Grice Publication number 343.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Ecology Editor Prof. Peter Mumby
Rights and permissions
About this article
Cite this article
Sotka, E.E., Hay, M.E. Effects of herbivores, nutrient enrichment, and their interactions on macroalgal proliferation and coral growth. Coral Reefs 28, 555–568 (2009). https://doi.org/10.1007/s00338-009-0529-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-009-0529-1