Hostname: page-component-77c89778f8-5wvtr Total loading time: 0 Render date: 2024-07-20T13:47:02.097Z Has data issue: false hasContentIssue false

Higher population densities of the sea urchin Diadema antillarum linked to wave sheltered areas in north Puerto Rico Archipelago

Published online by Cambridge University Press:  20 June 2014

Ruber Rodríguez-Barreras*
Affiliation:
Department of Biology, University of Puerto Rico, Río Piedras, PO Box 23360 San Juan, Puerto Rico 00931-3360
María E. Pérez
Affiliation:
Department of Mathematics, and Center of Applied Tropical and Conservation, University of Puerto Rico, Río Piedras, PO Box 23355 San Juan, Puerto Rico 00931-335
Alex E. Mercado-Molina
Affiliation:
Department of Biology, University of Puerto Rico, Río Piedras, PO Box 23360 San Juan, Puerto Rico 00931-3360
Stacey M. Williams
Affiliation:
Institute for Social-Ecological Research, PO Box 3151, Lajas, Puerto Rico 00667
Alberto M. Sabat
Affiliation:
Department of Biology, University of Puerto Rico, Río Piedras, PO Box 23360 San Juan, Puerto Rico 00931-3360
*
Correspondence should be addressed to: R. Rodríguez-Barreras, Department of Biology, University of Puerto Rico, Rio Piedras, PO Box 23360 San Juan, Puerto Rico 00931-3360 email: ruber.rodriguez@outlook.com

Abstract

The long-spined sea urchin Diadema antillarum has been the focus of multiple studies since the mass mortality event in the 1980s. The recovery of this key herbivore in the wider Caribbean is essential for the well-being of coral reefs. This study examined the population density and structure of D. antillarum at seven northern fringing reefs of Puerto Rico between 2011 and 2013. The total mean density of the sea urchins in northern Puerto Rico was 0.9 ±0.3 ind m−2. Densities of D. antillarum significantly differed among sites, but not temporally. Differences in mean sizes were significant among sites and seasons. Areas with higher densities of D. antillarum showed lower cover of non-calcareous algae. Wave exposure was correlated with the abundance of the sea urchin. This study indicates that the observed abundance of D. antillarum has not yet returned to pre-mortality levels. However, densities showed some degree of recovery when compared with previous studies, enabling at least some degree of control on fleshy macroalgae communities. No significant changes in density occurred between 2011 and 2013, and sites with higher densities were generally located in leeward areas. The low relative abundance of small size individuals points towards recruitment limitation as an explanation for the limited recovery of D. antillarum.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alvarez-Filip, L., Dulvy, N.K., Gill, J.A., Cote, I.M. and Watkinson, A.R. (2009) Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. Proceedings of the Royal Society, B 276, 30193025.Google Scholar
Bak, R.P.M., Carpay, M.J.E. and Ruyter van Steveninck, E.D. (1984) Densities of the sea urchin Diadema antillarum before and after mass mortalities on the coral reefs of Curacao. Marine Ecology 17, 105108.CrossRefGoogle Scholar
Bauer, J.C. (1980) Observations of geographical variations in population density of the echinoid Diadema antillarum within the Western North Atlantic. Bulletin of Marine Science 30, 509515.Google Scholar
Bellwood, D.R., Hughes, T.P., Folke, C. and Nystrom, M. (2004) Confronting the coral reef crisis. Nature 429, 827833.Google Scholar
Bythell, J.C., Gladfelter, E.H. and Bythell, M. (1993) Chronic and catastrophic natural mortality of three common Caribbean reef corals. Coral Reefs 12, 143152.CrossRefGoogle Scholar
Bythell, J.C., Hillis-Starr, Z.M. and Rogers, C.S. (2000) Local variability but landscape stability in coral reef communities following repeated hurricane impacts. Marine Ecology Progress Series 204, 93100.Google Scholar
Box, G.E.P. and Cox, D.R. (1964) An analysis of transformations (with discussion). Journal of the Royal Statistical Society, B 26, 211252.Google Scholar
Brown-Saracino, J., Peckol, P., Curran, H.A. and Robbart, M.L. (2007) Spatial variation in sea urchins, fish predators, and bioerosion rates on coral reefs of Belize. Coral Reefs 26, 7178.Google Scholar
Butman, C.A. (1987) Larval settlement of soft sediment in vertebrates: the spatial scales of pattern explained by active habitat selection and the emerging role of hydrodynamical processes. Oceanography and Marine Biology: an Annual Review 25, 113165.Google Scholar
Carpenter, R.C. and Edmunds, P.J. (2006) Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals. Ecology Letters 9, 271280.Google Scholar
Chiappone, M., Rutten, L.M., Swanson, D.W. and Miller, S.L. (2008) Population status of the urchin Diadema antillarum in the Florida Keys 25 years after the Caribbean mass mortality. In Proceedings of the 11th International Coral Reef Symposium, Fort Lauderdale, Florida, 7–11 July, pp. 706–710.Google Scholar
Chollett, I., Mumby, P.J., Müller-Karger, F. E. and Hu, C. (2012) Physical environments of the Caribbean Sea. Limnology and Oceanography 57, 12331244.CrossRefGoogle Scholar
Clemente, S. and Hernández, J.C. (2008) Influence of wave exposure and habitat complexity in determining spatial variation of the sea urchin Diadema aff. antillarum Echinoidea: Diadematidae) populations and macroalgal cover (Canary Islands–Eastern Atlantic Ocean). Biología Tropical 56, 229254.Google Scholar
Craft, L.L. (1975) Aspects of the biology of the crab Percnon gibbesi (Milne Edwards) and its commensal association with the sea urchin Diadema antillarum Phillipi. MSc thesis. University of Puerto Rico.Google Scholar
De'ath, G., Fabricius, K.E., Sweatman, H. and Puotinen, M. (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences of the United States of America 109, 1799517999.CrossRefGoogle ScholarPubMed
Debrot, A.O. and Nagelkerken, I. (2006) Recovery of the long-spined sea urchin Diadema antillarum in Curacao (Netherlands Antilles) linked to lagoonal and wave sheltered shallow rocky habitats. Bulletin of Marine Science 79, 415424.Google Scholar
Edmunds, P.J. and Carpenter, R.C. (2001) Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean Reef. Proceedings of the National Academy of Sciences of the United States of America 98, 50675071.Google Scholar
Fabricius, K.F. (2011) Factors determining the resilience of coral reefs to eutrophication: a review and conceptual model. In Dubinsky, Z. and Stambleredts, N. (eds) Ecosystems in transition. Coral reefs. Dordrecht, The Netherlands: Springer, pp. 493505.CrossRefGoogle Scholar
Gardner, T.A., Côté, I.M., Gill, J.A., Grant, A. and Watkinson, A.R. (2003) Long-term region-wide declines in Caribbean corals. Science 301, 958960.Google Scholar
Harborne, A.R., Renaud, P.G. and Tyler, E.H. (2009) Reduced density of the herbivorous urchin Diadema antillarum inside a Caribbean marine reserve linked to increased predation pressure by fishes. Coral Reefs 28, 783791.Google Scholar
Hay, M.E. and Fenical, W. (1988) Marine plant–herbivore interactions: the ecology of chemical defense. Annual Review of Ecology and Systematics 19, 111145.Google Scholar
Hernández, J.C., Clemente, S., Sangil, C. and Brito, A. (2008) The key role of the sea urchin Diadema aff. antillarum in controlling macroalgae assemblages throughout the Canary Islands (eastern subtropical Atlantic): a spatio-temporal approach. Marine Environmental Research 66, 259270.Google Scholar
Hughes, T.P., Keller, B.D., Jackson, J.B. and Boyle, M.J. (1985) Mass mortality of the Echinoid Diadema antillarum Philippi in Jamaica. Bulletin of Marine Science 36, 377–84.Google Scholar
Hughes, T.P. (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reefs. Science 9, 15471551.Google Scholar
Hughes, T.P., Graham, N.A.J., Jackson, J.B.C., Mumby, P.J. and Steneck, R.S. (2010) Rising to the challenge of sustaining coral reef resilience. Trends in Ecology and Evolution 25, 633642.Google Scholar
Hunte, W., Côté, I. and Tomascik, T. (1986) On the dynamics of the mass mortality of Diadema antillarum in Barbados. Coral Reefs 4, 135139.Google Scholar
Hunte, W. and Younglao, D. (1988) Recruitment and population recovery of Diadema antillarum (Echinodermata; Echinoidea) in Barbados. Marine Ecology Progress Series 45, 109119.Google Scholar
Hunter, I.G. (1977) Sediment production by Diadema antillarum on a Barbados fringing reef. In Proceedings of the Third International Coral Reef Symposium, Miami, Florida: Rosenstiel School, University of Miami, May, Volume 2, pp. 105–110.Google Scholar
Idjadi, J.A., Haring, R.N. and Precht, W.F. (2010) Recovery of the sea urchin Diadema antillarum promotes scleractinian coral growth and survivorship on shallow Jamaican reefs. Marine Ecology Progress Series 403, 91100.Google Scholar
Karlson, R.H. and Levitan, D.R. (1990) Recruitment-limitation in open populations of Diadema antillarum: an evaluation. Oecologia 82, 4044.CrossRefGoogle ScholarPubMed
Knowlton, N. (2001) Sea urchin recovery from mass mortality: new hope for Caribbean coral reefs? Proceedings of the National Academy of Sciences of the United States of America 98, 48224824.Google Scholar
Kohler, K.E., and Gill, S.M. (2006) Coral Point Count with Excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Computers and Geosciences 32, 12591269.Google Scholar
Kramer, P.A., Kramer, P.R. and Ginsburg, R.N. (2003) Assessment of the Andros island reef system, Bahamas (Part 1: Stony corals and algae). Atoll Research Bulletin 496, 77100.Google Scholar
Lacey, E., Fourqurean, J.W. and Collado-Videz, L. (2013) Increased algal dominance despite presence of Diadema antillarum populations on a Caribbean coral reef. Bulletin of Marine Science 89, 603620.Google Scholar
Leber, K., Lorenzen, K., Main, K.M.M. and Vaughan, D. (2008) Developing restoration methods to aid in recovery of a key herbivore Diadema antillarum on Florida coral reefs. Mote Technical Report 1295, 26 pp.Google Scholar
Lessios, H.A. (1981) Reproductive periodicity of the echinoids Diadema and Echinometra on the two coasts of Panama. Journal of Experimental Marine Biology and Ecology 50, 4761.Google Scholar
Lessios, H.A, Cubit, J.D., Robertson, D.R., Shulman, M.J., Parker, M.R., Garrity, S.D. and Levings, S.C. (1984) Mass mortality of Diadema antillarum on the Caribbean coast of Panama. Coral Reefs 3, 173182.Google Scholar
Lessios, H.A. (2005) Diadema antillarum populations in Panama twenty years following mass mortality. Coral Reefs 24, 125127.Google Scholar
Levitan, D., Edmunds, P.J. and Levitan, K.E. (2014) What makes a species common? No evidence of density-dependent recruitment or mortality of the sea urchin Diadema antillarum after the 1983–1984 mass mortality. Oecologia 175, 117128.CrossRefGoogle ScholarPubMed
Liddell, W.D. and Ohlhorst, S.L. (1986) Changes in benthic community composition following the mass mortality of Diadema at Jamaica. Journal of Experimental Marine Biology and Ecology 95, 271278.Google Scholar
Littler, M.M., Littler, D.S. and Titlyanov, E.A. (1991) Comparisons of N-limited and P-limited productivity between high granitic islands versus low carbonate atolls in the Seychelles archipelago. A test of the relative-dominance paradigm. Coral Reefs 10, 199209.CrossRefGoogle Scholar
Lugo-Ascorbe, M.A. (2004) Population status of the black sea urchin Diadema antillarum (Philippi) in La Parguera, Puerto Rico, 20 years after the mass mortality event. MSc thesis. Department of Marine Sciences, University of Puerto Rico.Google Scholar
Martín-Blanco, F., González-Sansón, G., Pina-Amargós, F. and Clero-Alonso, L. (2010) Abundance, distribution and size structure of Diadema antillarum (Echinodermata: Diadematidae) in South Eastern Cuban coral reefs. Biología Tropical 58, 663676.Google Scholar
Martín-Blanco, F., Clero-Alonso, F., González Sansón, G. and Pina-Amargós, F. (2011). Influence of Diadema antillarum populations (Echinodermata: Diadematidae) on algal community structure in Jardines de la Reina, Cuba. Biología Tropical 59, 11491163.Google Scholar
Miller, R.J., Adams, A.J., Ogden, N.B., Ogden, J.C. and Ebersole, J.P. (2003) Diadema antillarum 17 years after mass mortality: is recovery beginning on St Croix? Coral Reefs 22, 181187.Google Scholar
Miller, R.J., Adams, A.J., Ebersole, J.P. and Ruiz, E. (2007) Evidence for positive density-dependent effects in recovering Diadema antillarum populations. Journal of Experimental Marine Biology and Ecology 349, 215222.Google Scholar
Myhre, S. and Acevedo-Gutiérrez, A. (2007) Recovery of sea urchin Diadema antillarum populations is correlated to increased coral and reduced macroalgal cover. Marine Ecology and Progress Series 329, 205210.CrossRefGoogle Scholar
NOAA Coral Reef Watch (2000) NOAA Coral Reef Watch Operational 50-km Satellite Coral Bleaching Degree Heating Weeks Product, Jan. 1 2001–Dec. 31 2011. Silver Spring, MD: NOAA Coral Reef Watch. Available at: http://coralreefwatch.noaa.gov/satellite/hdf/index.php (accessed 22 April 2014).Google Scholar
Noriega, N., Pauls, S. and Mónaco, C. (2006) Abundancia de Diadema antillarum (Echinodermata: Echinoidea) en las costas de Venezuela. Biología Tropical 54, 793802.Google Scholar
Pennington, J.T. (1985) The ecology of fertilization of echinoid eggs: the consequence of sperm dilution, adult aggregation, and synchronous spawning. Biological Bulletin. Marine Biological Laboratory, Woods Hole 169, 417430.Google Scholar
Pinheiro, J., Bates, D. and DebRoy, S. (2013) nlme: linear and nonlinear mixed effects models. R package version 3.1-111. Vienna: R Foundation for Statistical Computing.Google Scholar
Phinney, J.T., Muller-Karger, F., Dustan, P. and Sobel, J. (2001) Using remote sensing to reassess the mass mortality of Diadema antillarum 1983–1984. Conservation Biology 15, 885–881.Google Scholar
R Core Team (2013) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
Rivera, J.A. and Vicente, V.P. (1976) Diadema antillarum (Philippi): enhancement of coral species in Thalassia beds. Proceedings of the Association of Island Marine Laboratories of the Caribbean 12, 18.Google Scholar
Rodríguez, A., Hernández, J.C., Clemente, S. and Coppard, S.E. (2013) A new species of Diadema (Echinodermata: Echinoidea: Diadematidae) from the eastern Atlantic Ocean and a neotype designation of Diadema antillarum (Philippi, 1845). Zootaxa 3636, 144170.Google Scholar
Rogers, A. and Lorenzen, K. (2008) Recovery of Diadema antillarum and the potential for active rebuilding measures: modelling population dynamics. In Proceedings of the 11th International Coral Reef Symposium. Fort Lauderdale, FL, 7–11 July, pp. 956–960.Google Scholar
Ruiz-Ramos, D.V., Hernández-Delgado, E.A. and Schizas, N.V. (2011) Population status of the long-spined urchin Diadema antillarum in Puerto Rico 20 years after a mass mortality event. Bulletin of Marine Science 87, 113127.Google Scholar
Sammarco, P.W., Levinton, J.S. and Ogden, J.C. (1974) Grazing and control of coral reef community structure by Diadea antillarum. Philippi (Echinodermata: Echinoidea): a preliminary study. Journal of Marine Research 32, 4753.Google Scholar
Sammarco, P.W. (1982) Effects of grazing by Diadema antillarum Philippi (Echinodermata: Echinoidea) on algal diversity and community structure. Journal of Experimental Marine Biology and Ecology 65, 83105.Google Scholar
Sellers, J.A., Casey, L.O., Burge, E.J. and Koepfler, E.T. (2009) Population growth and distribution of Diadema antillarum at Discovery Bay, Jamaica. The Open Marine Biology Journal 3, 105111.Google Scholar
Soto-Santiago, F.J. and Irizarry-Soto, E. (2013) The sea urchin Diadema antillarum (Echinodermata, Equinoidea), algal cover and juvenile coral densities in La Parguera, Puerto Rico. Cuadernos de Investigación, UNED 5, 3339.Google Scholar
Steiner, S.C. and Williams, S.M. (2006) A recent increase in the abundance of the echinoid Diadema antillarum in Dominica (Lesser Antilles): 2001–2005. Biología Tropical 54, 97103.Google Scholar
Steneck, R.S. (1988) Herbivory on coral reefs: a synthesis. In Proceedings of the sixth International Coral Reef Symposium, Australia, Volume 1, 8–12 August, pp. 37–49.Google Scholar
Tuya, F., Martin, J.A., and Luque, A. (2004) Patterns of nocturnal movement of the long-spined sea urchin Diadema antillarum (Philippi) in Gran Canaria. Helgoland Marine Research 58, 2631.Google Scholar
Tuya, F., Ortega-Borges, L., Del Rosario-Pinilla, A.B. and Haroun, R.J. (2006) Spatio-temporal variability in a key herbivore, the long-spined black sea urchin (Diadema antillarum, Echinodermata: Echinoidea) in the Canary Islands. Journal of the Marine Biological Association of the United Kingdom 86, 791797.Google Scholar
Tuya, F., Cisneros-Aguirre, J., Ortega-Borges, L. and Haroun, R.J. (2007) Bathymetric segregation of sea urchins on reefs of the Canarian Archipelago: role of flow-induced forces. Estuarine, Coastal and Shelf Science 73, 481488.Google Scholar
USGS (United States Geological Survey) (1996) Atlas of ground-water resources in Puerto Rico and the U.S. Virgin Islands. In Veve, T.D. and Taggart, B.E. (eds) Water resources investigation report, 94–4198. Reston, VA: USGS, 151 pp.Google Scholar
Valdez, M.F. and Villalobos, C.R. (1978) Distribución espacial, correlación con el substrato y grado de agregación de Diadema antillarum Philippi (Echinodermata: Echinoidea). Biología Tropical 26, 237245.Google Scholar
Venables, W.N. and Ripley, B.D. (2002) Modern applied statistics with S. 4th editionNew York: Springer, 495 pp.Google Scholar
Vicente, V.P. (1987) The ecology of the encrusting demosponge Chondrilla nucula (Schmidt) in a coral reef community in Puerto Rico. PhD thesis. Department of Marine Sciences, University of Puerto Rico.Google Scholar
Vicente, V.P. and Goenaga, C. (1984) Mortandades masivas del erizo de mar Diadema antillarum (Philippi) en Puerto Rico. Centro para Estudios Energéticos y Ambientales, Div. Ecología Marina, University of Puerto Rico. Reporte CEER-M-195, 30 pp.Google Scholar
Weil, E., Torres, J.L. and Ashton, M. (2005) Population characteristics of the sea urchin Diadema antillarum in La Parguera, Puerto Rico, 17 years after the mass mortality event. Biología Tropical 53, 219231.Google Scholar
Williams, I.D. and Polunin, N.V.C. (2001) Large-scale associations between macroalgal cover and grazer biomass on mid-depth reefs in the Caribbean. Coral Reefs 19, 358366.CrossRefGoogle Scholar
Williams, S.M., García-Sais, J.R. and Capella, J. (2009) Temporal variation of early larval stages of the long-spined sea urchin Diadema antillarum in La Parguera, Puerto Rico. Caribbean Journal of Science 45, 110117.Google Scholar
Williams, S.M., Benavides-Serrato, M., García-Arrarás, J.E., Hernández-Delgado, E.A. and Rodríguez-Barreras, R. (2013) Review of echinoderm research in Puerto Rico, with the focus on biological and ecological aspects. In Alvarado-Barrientos, J.J. and Solis-Marin, F.A. (eds) Echinoderm research and diversity in Latin America. New York: Springer, pp. 437469.Google Scholar
Zar, J.H. (2010) Biostatistical analysis. 5th edition. Upper Saddle River, NJ: Prentice-Hall, 944 pp.Google Scholar