Skip to main content

Advertisement

SpringerLink
Log in

Effects of herbivory, nutrients, and reef protection on algal proliferation and coral growth on a tropical reef

  • Community ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Maintaining coral reef resilience against increasing anthropogenic disturbance is critical for effective reef management. Resilience is partially determined by how processes, such as herbivory and nutrient supply, affect coral recovery versus macroalgal proliferation following disturbances. However, the relative effects of herbivory versus nutrient enrichment on algal proliferation remain debated. Here, we manipulated herbivory and nutrients on a coral-dominated reef protected from fishing, and on an adjacent macroalgal-dominated reef subject to fishing and riverine discharge, over 152 days. On both reefs, herbivore exclusion increased total and upright macroalgal cover by 9–46 times, upright macroalgal biomass by 23–84 times, and cyanobacteria cover by 0–27 times, but decreased cover of encrusting coralline algae by 46–100% and short turf algae by 14–39%. In contrast, nutrient enrichment had no effect on algal proliferation, but suppressed cover of total macroalgae (by 33–42%) and cyanobacteria (by 71% on the protected reef) when herbivores were excluded. Herbivore exclusion, but not nutrient enrichment, also increased sediment accumulation, suggesting a strong link between herbivory, macroalgal growth, and sediment retention. Growth rates of the corals Porites cylindrica and Acropora millepora were 30–35% greater on the protected versus fished reef, but nutrient and herbivore manipulations within a site did not affect coral growth. Cumulatively, these data suggest that herbivory rather than eutrophication plays the dominant role in mediating macroalgal proliferation, that macroalgae trap sediments that may further suppress herbivory and enhance macroalgal dominance, and that corals are relatively resistant to damage from some macroalgae but are significantly impacted by ambient reef condition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

MPA:

Marine protected area

Non-MPA:

Non-marine protected area

CCA:

Crustose coralline algae

RDM:

Relative dominance model

References

  • Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bellwood DR, Fulton CJ (2008) Sediment-mediated suppression of herbivory on coral reefs: decreasing resilience to rising sea levels and climate change? Limnol Oceanogr 53:2695–2701

    Article  Google Scholar 

  • Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827–833

    Article  PubMed  CAS  Google Scholar 

  • Birrell CL, McCook LJ, Willis BL (2005) Effects of algal turfs and sediment on coral settlement. Mar Poll Bull 51:408–414

    Article  CAS  Google Scholar 

  • 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 Annu Rev 46:25–63

    Article  Google Scholar 

  • Bruno JF, Petes LE, Harvell CD, Hettinger A (2003) Nutrient enrichment can increase the severity of coral diseases. Ecol Lett 6:1056–1061

    Article  Google Scholar 

  • Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biology 5:e124

    Article  CAS  Google Scholar 

  • Burkepile DE, Hay ME (2006) Herbivore versus nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139

    Article  PubMed  Google Scholar 

  • Burkepile DE, Hay ME (2008) Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proc Natl Acad Sci USA 105:16201–16206

    Article  PubMed  CAS  Google Scholar 

  • Burkepile DE, Hay ME (2009) Nutrient versus herbivore control of macroalgal community development and coral growth on a Caribbean reef. Mar Ecol Prog Ser 389:71–84

    Article  Google Scholar 

  • Burkepile DE, Hay ME (2010) Impact of herbivore identity on algal succession and coral growth on a Caribbean reef. PLoS One 5:e8963

    Article  PubMed  Google Scholar 

  • Carilli JE, Norris RD, Black BA, Walsh SM, McField M (2009) Local stressors reduce coral resilience to bleaching. PLoS One 4:e6324

    Article  PubMed  Google Scholar 

  • Cheal A, MacNeil M, Cripps E, Emslie M, Jonker M, Schaffelke B, Sweatman H (2010) Coral–macroalgal phase shifts or reef resilience: links with diversity and functional roles of herbivorous fishes on the Great Barrier Reef. Coral Reefs 29:1005–1015

    Article  Google Scholar 

  • Diaz-Pulido G, McCook LJ (2003) Relative roles of herbivory and nutrients in the recruitment of coral-reef seaweeds. Ecology 84:2026–2033

    Article  Google Scholar 

  • Elmhirst T, Connolly SR, Hughes TP (2009) Connectivity, regime shifts and the resilience of coral reefs. Coral Reefs 28:949–957

    Article  Google Scholar 

  • Folke C, Carpenter S, Walker B, Scheffer M, Elmqvist T, Gunderson L, Holling CS (2004) Regime shifts, resilience, and biodiversity in ecosystem management. Annu Rev Ecol Evol Syst 35:557–581

    Article  Google Scholar 

  • Harvell D, Jordan-Dahlgren E, Merkel S, Rosenberg E, Raymundo L, Smith G, Weil E, Willis B (2007) Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20:172–195

    Article  Google Scholar 

  • Hauri C, Fabricius KE, Schaffelke B, Humphrey C (2010) Chemical and physical environmental conditions underneath mat- and canopy-forming macroalgae, and their effects on understorey corals. PLoS One 5:e12685

    Article  PubMed  Google Scholar 

  • Heck KL, Valentine JF (2007) The primacy of top-down effects in shallow benthic ecosystems. Estuar Coasts 30:371–381

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hoey AS, Bellwood DR (2011) Suppression of herbivory by macroalgal density: a critical feedback on coral reefs? Ecol Lett 14:267–273

    Article  PubMed  Google Scholar 

  • Houk P, Musburger C, Wiles P (2010) Water quality and herbivory interactively drive coral-reef recovery patterns in American Samoa. PLoS One 5:e13913

    Article  PubMed  Google Scholar 

  • Hughes TP (1994) Catastrophes, phase-shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551

    Article  PubMed  CAS  Google Scholar 

  • Hughes TP, Szmant AM, Steneck RS, Carpenter R, Miller S (1999) Algal blooms on coral reefs: what are the causes? Limnol Oceanogr 44:1583–1586

    Article  CAS  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  PubMed  CAS  Google Scholar 

  • Hughes TP, Rodrigues MJ, Bellwood DR, 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

    Article  PubMed  CAS  Google Scholar 

  • Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642

    Article  PubMed  Google Scholar 

  • Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson 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 293:629–637

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Knowlton N, Jackson JBC (2008) Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol 6:e54

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lapointe BE, Barile PJ, Yentsch CS, 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

    Article  Google Scholar 

  • Lewis SM (1986) The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol Monogr 56:183–200

    Article  Google Scholar 

  • Littler MM, Littler DS (1984) Models of tropical reef biogenesis: the contribution of algae. In: Round FE, Chapman DJ (eds) Progress in phycological research. Biopress, Bristol, pp 323–364

    Google Scholar 

  • Littler MM, Littler DS, Brooks BL, Lapointe BE (2006a) Nutrient manipulation methods for coral reef studies: a critical review and experimental field data. J Exp Mar Biol Ecol 336:242–253

    Article  Google Scholar 

  • Littler MM, Littler DS, Brooks BL (2006b) Harmful algae on tropical coral reefs: bottom-up eutrophication and top-down herbivory. Harmful Algae 5:565–585

    Article  Google Scholar 

  • 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 Prog Ser 261:135–147

    Article  Google Scholar 

  • McCook LJ (1996) Effects of herbivores and water quality on Sargassum distribution on the central great barrier reef: cross-shelf transplants. Mar Ecol Prog Ser 139:179–192

    Article  Google Scholar 

  • Miller MW, Hay ME (1998) Effects of fish predation and seaweed competition on the survival and growth of corals. Oecologia 113:231–238

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Montoya JP (2008) Nitrogen stable isotopes in marine environments. In: Capone DG, Carpenter EJ, Mulholland MR, Bronk DA (eds) Nitrogen in the marine environment. Academic, London, pp 1277–1302

    Chapter  Google Scholar 

  • Mumby PJ, Harborne AR (2010) Marine reserves enhance the recovery of corals on Caribbean reefs. PLoS One 5:e8657

    Article  PubMed  Google Scholar 

  • Mumby PJ, Steneck RS (2008) Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends Ecol Evol 23:555–563

    Article  PubMed  Google Scholar 

  • Mumby PJ, Hastings A, Edwards HJ (2007a) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98–101

    Article  PubMed  CAS  Google Scholar 

  • Mumby PJ, Harborne AR, Williams J, Kappel CV, Brumbaugh DR, Micheli F, Holmes KE, Dahlgren CP, Paris CB, Blackwell PG (2007b) Trophic cascade facilitates coral recruitment in a marine reserve. Proc Natl Acad Sci USA 104:8362–8367

    Article  PubMed  CAS  Google Scholar 

  • Nugues MM, Roberts CM (2003) Coral mortality and interaction with algae in relation to sedimentation. Coral Reefs 22:507–516

    Article  Google Scholar 

  • Rasher DB, Hay ME (2010) Chemically rich seaweeds poison corals when not controlled by herbivores. Proc Natl Acad Sci USA 107:9683–9688

    Article  PubMed  CAS  Google Scholar 

  • Rasher DB, Stout EP, Engel S, Kubanek J, Hay ME (2011) Macroalgal terpenes function as allelopathic agents against reef corals. Proc Natl Acad Sci USA. doi:10.1073/pnas.1108628108

  • Raymundo LJ, Halford AR, Maypa AP, Kerr AM (2009) Functionally diverse reef-fish communities ameliorate coral disease. Proc Natl Acad Sci USA 106:17067–17070

    Google Scholar 

  • Selig ER, Bruno JF (2010) A global analysis of the effectiveness of marine protected areas in preventing coral loss. PLoS One 5:e9278

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Smith JE, Morrigan S, Edwards RA, Obura D, Pantos O, Sala E, Sandin SA, Smriga S, Hatay M, Rohwer FL (2006) Indirect effects of algae on coral: algae-mediated, microbe-induced mortality. Ecol Lett 9:835–845

    Article  PubMed  Google Scholar 

  • Smith JE, Hunter CL, Smith CM (2010) The effects of top-down versus bottom-up control on benthic coral reef community structure. Oecologia 163:497–507

    Article  PubMed  Google Scholar 

  • Sotka EE, Hay ME (2009) Effects of herbivores, nutrient enrichment, and their interactions on macroalgal proliferation and coral growth. Coral Reefs 28:555–568

    Article  Google Scholar 

  • Stamski RE, Field ME (2006) Characterization of sediment trapped by macroalgae on a Hawaiian reef flat. Estuar Coast Shelf Sci 66:211–216

    Article  Google Scholar 

  • Steneck RS (1988) Herbivory on coral reefs: a synthesis. Proceedings of 6th International Coral Reef Symposium 1:37–49

  • Steneck RS (1997) Crustose corallines, other algal functional groups, herbivores and sediment: complex interactions along reef productivity gradients. Proceedings of 8th International Coral Reef Symposium 1:695–700

  • 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

    Article  Google Scholar 

  • Umezawa Y, Miyajima T, Yamamuro M, Kayanne H, Koike I (2002) Fine-scale mapping of land-derived nitrogen in coral reefs by delta N-15 in macroalgae. Limnol Oceanogr 47:1405–1416

    Article  Google Scholar 

  • Umezawa Y, Miyajima T, Tanaka Y, Koike I (2007) Variation in internal delta N-15 and delta C-13 distributions and their bulk values in the brown macroalga Padina australis growing in subtropical oligotrophic waters. J Phycol 43:437–448

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Fijian government and Korolevu-i-wai district elders for research permissions. T. Andras and C. Dell provided valuable laboratory assistance. Support was provided by research grants from the National Institutes of Health (U01-TW007401) and the National Science Foundation (OCE 0929119), a National Science Foundation Integrative Graduate Education and Research Traineeship grant (DGE-0114400), and the Teasley Endowment to the Georgia Institute of Technology. The experiments reported here comply with the current laws of the country in which the experiments were performed.

Conflict of interest

The authors declare no conflict of interest with the organizations that funded this research.

Author information

Authors and Affiliations

  1. School of Biology, Georgia Institute of Technology, Atlanta, GA, 30332, USA

    Douglas B. Rasher, Sebastian Engel, Joseph P. Montoya & Mark E. Hay

  2. Reef Explorer Fiji, PO Box 183, Korolevu, Fiji

    Victor Bonito

  3. Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK

    Gareth J. Fraser

Authors
  1. Douglas B. Rasher
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sebastian Engel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Victor Bonito
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gareth J. Fraser
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joseph P. Montoya
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mark E. Hay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark E. Hay.

Additional information

Communicated by Geoffrey Trussell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rasher, D.B., Engel, S., Bonito, V. et al. Effects of herbivory, nutrients, and reef protection on algal proliferation and coral growth on a tropical reef. Oecologia 169, 187–198 (2012). https://doi.org/10.1007/s00442-011-2174-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-2174-y

Keywords

Search

Navigation