Skip to main content

Advertisement

Log in

Reduced density of the herbivorous urchin Diadema antillarum inside a Caribbean marine reserve linked to increased predation pressure by fishes

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Disease has dramatically reduced populations of the herbivorous urchin Diadema antillarum Philippi on Caribbean reefs, contributing to an increased abundance of macroalgae and reduction of coral cover. Therefore, recovery of D. antillarum populations is critically important, but densities are still low on many reefs. Among the many potential factors limiting these densities, the focus of this study is on predation pressure by fishes. Marine reserves provide opportunities to examine large-scale manipulations of predator–prey interactions and, therefore, D. antillarum densities were compared inside and outside a reserve in The Bahamas (Exuma Cays Land and Sea Park; ECLSP). Urchins and their fish predators were surveyed at nine sites inside and outside the ECLSP. Because of lower fishing effort, the total biomass of urchin predators, weighted by their dietary preferences for urchins, was significantly higher inside the ECLSP. Furthermore, fish community structure was significantly different inside the Park because of the increased biomass of the majority of species. No urchins were seen inside the ECLSP and this was significantly lower than the density of 0.04 urchin m−2 outside the Park. Regression analysis indicated that the relationship between the biomass of urchin predators and the proportion of transects containing urchins was non-linear, suggesting that small increases in fish biomass dramatically reduce urchin abundances. The link between lower density of urchins and higher density of their predators inside the ECLSP is strengthened by discounting five alternative primary mechanisms (variations in macroalgal cover, larval supply, environmental setting, density of other urchin species and abundance of predators not surveyed). Caribbean marine reserves have an important conservation role, but increased fish predation appears to reduce densities of D. antillarum. Urchins currently have limited functional significance on Bahamian reefs, but any future recovery of D. antillarum is likely to be limited in reserves, with potentially important ecological consequences.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

References

  • Bak RPM (1985) Recruitment patterns and mass mortalities in the sea urchin Diadema antillarum. Proc 5th Int Coral Reef Congr 5: 267–272

    Google Scholar 

  • Bauer JC (1980) Observations on geographical variations in population density of the echinoid Diadema antillarum within the western North Atlantic. Bull Mar Sci 30:509–515

    Google Scholar 

  • Bechtel JD, Gayle P, Kaufman L (2006) The return of Diadema antillarum to Discovery Bay: patterns of distribution and abundance. Proc 10th Int Coral Reef Symp: 367–375

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

    Article  PubMed  CAS  Google Scholar 

  • Bohnsack JA, Harper DE (1988) Length–weight relationships of selected marine reef fishes from the southeastern United States and the Caribbean. NOAA Technical Memorandum NMFS-SEFC-215

  • Box SJ, Mumby PJ (2007) Effect of macroalgal competition on growth and survival of juvenile Caribbean corals. Mar Ecol Prog Ser 342:139–149

    Article  Google Scholar 

  • Brown-Saracino J, Peckol P, Curran HA, Robbart ML (2007) Spatial variation in sea urchins, fish predators, and bioerosion rates on coral reefs of Belize. Coral Reefs 26:71–78

    Article  Google Scholar 

  • Carpenter RC (1990a) Mass mortality of Diadema antillarum. I. Long-term effects on sea urchin population-dynamics and coral reef algal communities. Mar Biol 104:67–77

    Article  Google Scholar 

  • Carpenter RC (1990b) Mass mortality of Diadema antillarum. II. Effects on population densities and grazing intensity of parrotfishes and surgeonfishes. Mar Biol 104:79–86

    Article  Google Scholar 

  • Carpenter RC, Edmunds PJ (2006) Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals. Ecol Lett 9:268–277

    Google Scholar 

  • Chiappone M, Sullivan Sealey KM (2000) Marine reserve design criteria and measures of success: lessons learned from the Exuma Cays Land and Sea Park, Bahamas. Bull Mar Sci 66:691–705

    Google Scholar 

  • Chiappone M, Swanson DW, Miller SL (2002) Density, spatial distribution and size structure of sea urchins in Florida Keys coral reef and hard-bottom habitats. Mar Ecol Prog Ser 235:117–126

    Article  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960

    Article  PubMed  CAS  Google Scholar 

  • Garrison VH, Rogers CS, Beets J, Friedlander AM (2004) The habitats exploited and the species trapped in a Caribbean island trap fishery. Environ Biol Fish 71:247–260

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hay ME (1984) Patterns of fish and urchin grazing on Caribbean coral reefs: are previous results typical? Ecology 65:446–454

    Article  Google Scholar 

  • Hoffman SG, Robertson DR (1983) Foraging and reproduction of two Caribbean reef toadfishes (Batrachoididae). Bull Mar Sci 33:919–927

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Karlson RH, Levitan DR (1990) Recruitment-limitation in open populations of Diadema antillarum: an evaluation. Oecologia 82:40–44

    Article  Google Scholar 

  • Kramer PA (2003) Synthesis of coral reef health indicators for the western Atlantic: results of the AGRRA program (1997–2000). Atoll Res Bull 496:1–57

    Google Scholar 

  • Lee SC (2006) Habitat complexity and consumer-mediated positive feedbacks on a Caribbean coral reef. Oikos 112:442–447

    Article  Google Scholar 

  • Lessios HA (1988) Mass mortality of Diadema antillarum in the Caribbean: what have we learned? Annu Rev Ecol Syst 19:371–393

    Google Scholar 

  • Lessios HA (1995) Diadema antillarum 10 years after mass mortality: still rare, despite help from a competitor. Proc R Soc Lond Ser B Biol Sci 259:331–337

    Article  Google Scholar 

  • Levitan DR (1989) Density-dependent size regulation in Diadema antillarum: effects on fecundity and survivorship. Ecology 70:1414–1424

    Article  Google Scholar 

  • Levitan DR (1992) Community structure in times past: influence of human fishing pressure on algal-urchin interactions. Ecology 73:1597–1605

    Article  Google Scholar 

  • McClanahan TR (1999) Predation and the control of the sea urchin Echinometra viridis and fleshy algae in the patch reefs of Glovers Reef, Belize. Ecosystems 2:511–523

    Article  Google Scholar 

  • McClanahan TR, Shafir SH (1990) Causes and consequences of sea urchin abundance and diversity in Kenyan coral reef lagoons. Oecologia 83:362–370

    Google Scholar 

  • McClanahan TR, Muthiga NA, Kamukuru AT, Machano H, Kiambo RW (1999) The effects of marine parks and fishing on coral reefs of northern Tanzania. Biol Conserv 89:161–182

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Mora C, Andréfouët S, Costello MJ, Kranenburg C, Rollo A, Veron J, Gaston KJ, Myers RA (2006) Coral reefs and the global network of marine protected areas. Science 312:1750–1751

    Article  PubMed  CAS  Google Scholar 

  • Morrison D (1988) Comparing fish and urchin grazing in shallow and deeper coral reef algal communities. Ecology 69:1367–1382

    Article  Google Scholar 

  • Mumby PJ, Clarke KR, Harborne AR (1996) Weighting species abundance estimates for marine resource assessment. Aquat Conserv: Mar Freshw Ecosyst 6:115–120

    Article  Google Scholar 

  • Mumby PJ, Edwards AJ, Arias-González JE, Lindeman KC, Blackwell PG, Gall A, Gorczynska MI, Harborne AR, Pescod CL, Renken H, Wabnitz CCC, Llewellyn G (2004) Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature 427:533–536

    Article  PubMed  CAS  Google Scholar 

  • Mumby PJ, Hedley JD, Zychaluk K, Harborne AR, Blackwell PG (2006a) Revisiting the catastrophic die-off of the urchin Diadema antillarum on Caribbean coral reefs: fresh insights on resilience from a simulation model. Ecol Model 196:131–148

    Article  Google Scholar 

  • 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 (2006b) Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98–101

    Article  PubMed  CAS  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 

  • Mumby PJ, Broad K, Brumbaugh DR, Dahlgren CP, Harborne AR, Hastings A, Holmes KE, Kappel CV, Micheli F, Sanchirico JN (2008) Coral reef habitats as surrogates of species, ecological functions, and ecosystem services. Conserv Biol 22:941–951

    Article  PubMed  Google Scholar 

  • Nugues MM, Bak RPM (2006) Differential competitive abilities between Caribbean coral species and a brown alga: a year of experiments and a long-term perspective. Mar Ecol Prog Ser 315:75–86

    Article  Google Scholar 

  • Ogden JC, Lobel PS (1978) The role of herbivorous fishes and urchins in coral reef communities. Environ Biol Fish 3:49–63

    Article  Google Scholar 

  • Pinnegar JK, Polunin NVC, Francour P, Badalamenti F, Chemello R, Harmelin-Vivien ML, Hereu B, Milazzo M, Zabala M, D’Anna G, Pipitone C (2000) Trophic cascades in benthic marine ecosystems: lessons for fisheries and protected-area management. Environ Conserv 27:179–200

    Article  Google Scholar 

  • Randall JE (1967) Food habitats of reef fishes of the West Indies. Stud Trop Oceanogr 5:665–847

    Google Scholar 

  • Randall JE, Schroeder RE, Starck WA (1964) Notes on the biology of the echinoid Diadema antillarum. Caribb J Sci 4:421–433

    Google Scholar 

  • Ray C (ed) (1958) Report of the Exuma Cays Park Project (revised edition of 1961). Submitted to the Government of the Bahamas, Nassau

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

Download references

Acknowledgements

This study was funded by the Khaled bin Sultan Living Oceans Foundation. We thank the Bahamas Department of Marine Resources, Ian Fair, Bruce Purdy, and the crew of the Pirates Lady for fieldwork support. We are very grateful to Jim Lindsey for help with gnlm. The editorial staff and four anonymous reviewers significantly improved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. R. Harborne.

Additional information

Communicated by Environment Editor Prof. Rob van Woesik

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material (DOC 941 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harborne, A.R., Renaud, P.G., Tyler, E.H.M. et al. Reduced density of the herbivorous urchin Diadema antillarum inside a Caribbean marine reserve linked to increased predation pressure by fishes. Coral Reefs 28, 783–791 (2009). https://doi.org/10.1007/s00338-009-0516-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-009-0516-6

Keywords

Navigation