The Great Diadema antillarum Die-Off: 30 Years Later

Annual Review of Marine Science

Volumn 8, Issue , 2016, Pages 267-283

  Lessios, H A ^a  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

Author keywords

Algae; Coral reef; Mortality; Population recovery; Recruitment

Indexed keywords

ALGAE; GALLIUM ALLOYS; MAMMALS; PHASE SHIFT; PHASE SHIFTERS; POPULATION DYNAMICS; RECOVERY; REEFS;

CORAL RECRUITMENT; CORAL REEF; MASS MORTALITY; MORTALITY; POPULATION DENSITIES; RECRUITMENT; SEA URCHIN; SHALLOW WATERS;

POPULATION STATISTICS;

ALGA; CORAL REEF; GROWTH RATE; HERBIVORY; MORTALITY; POPULATION DENSITY; RECRUITMENT (POPULATION DYNAMICS); SURVIVORSHIP;

BERMUDA; CARIBBEAN COAST [COLOMBIA]; COLOMBIA; FLORIDA [UNITED STATES]; UNITED STATES;

ALGAE; ANTHOZOA; DIADEMA ANTILLARUM; ECHINOIDEA;

ANIMAL; CORAL REEF; ECOSYSTEM; GROWTH, DEVELOPMENT AND AGING; HISTORY; MARINE BIOLOGY; POPULATION DENSITY; SEA URCHIN;

ANIMALS; CORAL REEFS; ECOSYSTEM; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; MARINE BIOLOGY; POPULATION DENSITY; SEA URCHINS;

EID: 84954304488     PISSN: 19411405     EISSN: 19410611     Source Type: Journal    
DOI: 10.1146/annurev-marine-122414-033857     Document Type: Article

References (132)

1. Andres NG, Witman JD. 1995. Trends in community structure on a Jamaican reef. Mar. Ecol. Prog. Ser. 118:305-10
2. Aronson RB, Heck KL Jr, Valentine JF. 2001. Measuring predation with tethering experiments. Mar. Ecol. Prog. Ser. 214:311-12
3. Aronson RB, Precht WF. 2000. Herbivory and algal dynamics on the coral reef at Discovery Bay, Jamaica. Limnol. Oceanogr. 45:251-55
4. Attrill MJ, Kelmo F. 2007. Opportunistic responses of Diadema antillarum (Echinodermata: Echinoidea) populations following the 1997-98 El Niño event in Bahia, Brazil. Estuar. Coast. Shelf Sci. 73:243-48
5. Attrill MJ, Kelmo F, Jones MB. 2004. Impact of the 1997-98 El Niño event on the coral reef-associated echinoderm assemblage from northern Bahia, northeastern Brazil. Clim. Res. 26:151-58
6. Bak RPM. 1985. Recruitment patterns and mass mortalities in the sea urchin Diadema antillarum. InProceedings of the 5th International Coral Reef Congress, Tahiti, 27 May-1 June 1985, Vol. 5: Miscellaneous Papers, ed. M Harmelin Vivien, B Salvat, pp. 267-72. Moorea, Fr. Polyn. : Antenne Museum-EPHE
7. Bak RPM, Carpay MJE, de Ruyter van Steveninck ED. 1984. Densities of the sea urchin Diadema antillarum before and after mass mortalities on the coral reefs of Curacao. Mar. Ecol. Prog. Ser. 17:105-8
8. Bauer JC. 1980. Observations on geographical variations in population density of the echinoid Diadema antillarum within theWestern North Atlantic. Bull. Mar. Sci. 30:509-15
9. Beck G, Miller R, Ebersole J. 2008. Significance of immune responses in Diadema antillarum to Caribbeanwide mass mortality. In Proceedings of the 11th International Coral Reef Symposium, Fort Lauderdale, Florida, 7-11 July 2008, Vol. 1, ed. BM Riegl, RE Dodge, pp. 224-28. Fort Lauderdale, FL: Nova Southeast. Univ.
10. Beck G, Miller R, Ebersole J. 2014. Mass mortality and slow recovery of Diadema antillarum: Could compromised immunity be a factor? Mar. Biol. 161:1001-13
11. Bologna PA, Webb-Wilson L, Connelly P, Saunders JE. 2012. A new baseline for Diadema antillarum, Echinometra viridis, E. lucunter, and Eucidaris tribuloides populations within the Cayos Cochinos MPA, Honduras. Gulf Caribb. Res. 24:1-5
12. Burge CA, Eakin MC, Friedman CS, Froelich B, Hershberger PK, et al. 2014. Climate change influences on marine infectious diseases: implications for management and society. Annu. Rev. Mar. Sci. 6:249-77
13. Carpenter RC. 1981. Grazing by Diadema antillarum (Philippi) and its effects on the benthic algal community. J. Mar. Res. 39:749-65
14. Carpenter RC. 1984. Predator and population density control of homing behavior in the Caribbean echinoid Diadema antillarum. Mar. Biol. 82:101-8
15. Carpenter RC. 1985. Sea urchin mass mortality: effects on reef algal abundance, species composition, and metabolism and other coral reef herbivores. In Proceedings of the 5th International Coral Reef Congress, Tahiti, 27 May-1 June 1985, Vol. 4: Symposia and Seminars, ed. C Gabrie, B Salvat, pp. 53-60. Moorea, Fr. Polyn. : Antenne Museum-EPHE
16. Carpenter RC. 1986. Partitioning herbivory and its effects on coral-reef algal communities. Ecol. Monogr. 56:345-63
17. Carpenter RC. 1988. Mass-mortality of a Caribbean sea urchin: immediate effects on community metabolism and other herbivores. PNAS 85:511-14
18. Carpenter RC. 1990. Mass mortality of Diadema antillarum I. Long-term effects on sea urchin population dynamics and coral reef algal communities. Mar. Biol. 104:67-77
19. Carpenter RC. 1997. Invertebrate predators and grazers. In Life and Death of Coral Reefs, ed. C Birkeland, pp. 198-248. New York: Chapman & Hall
20. Carpenter RC, Edmunds PJ. 2006. Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals. Ecol. Lett. 9:268-77
21. Chiappone M, Rutten L, Miller S, Swanson D. 2013. Recent trends (1999-2011) in population density and size of the echinoid Diadema antillarum in the Florida Keys. Fla. Sci. 76:23-35
22. Clemente S, Lorenzo-Morales J, Mendoza JC, Lopez C, Sangil C, et al. 2014. Sea urchin Diadema africanum mass mortality in the subtropical eastern Atlantic: role of waterborne bacteria in a warming ocean. Mar. Ecol. Prog. Ser. 506:1-14
23. Cote IM, PrechtWF, Aronson RB, Gardner TA. 2013. Is Jamaica a good model for understanding Caribbean coral reef dynamics? Mar. Pollut. Bull. 76:28-31
24. Courchamp F, Clutton-Brock T, Grenfell B. 1999. Inverse density dependence and the Allee effect. Trends Ecol. Evol. 14:405-10
25. de Ruyter van Steveninck ED, Bak RPM. 1986. Changes in abundance of coral reef bottom components related to mass mortality of the sea urchin Diadema antillarum. Mar. Ecol. Prog. Ser. 34:87-94
26. Debrot AO, Nagelkerken I. 2006. Recovery of the long-spined sea urchin Diadema antillarum in Curacao (Netherlands Antilles) linked to lagoonal andwave sheltered shallow rocky habitats. Bull. Mar. Sci. 79:415-24
27. Donovan SK. 2005. The fossil record of Diadema in the Caribbean. Coral Reefs 24:603-5
28. Dulvy NK, Sadovy Y, Reynolds JD. 2003. Extinction vulnerability in marine populations. Fish Fish. 4:25-64
29. Eckert GL. 1998. Larval development, growth and morphology of the sea urchin Diadema antillarum. Bull. Mar. Sci. 63:443-51
30. Edmunds PJ, Bruno JF. 1996. The importance of sampling scale in ecology: kilometer-wide variation in coral reef communities. Mar. Ecol. Prog. Ser. 143:165-71
31. Edmunds PJ, Carpenter RC. 2001. Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef. PNAS 98:5067-71
32. Entrambasaguas L, Perez-Ruzafa A, Garcia-Charton JA, Stobart B, Bacallado JJ. 2008. Abundance, spatial distribution and habitat relationships of echinoderms in the Cabo Verde Archipelago (eastern Atlantic). Mar. Freshw. Res. 59:477-88
33. Fonseca AC. 2003. A rapid assessment at Cahuita National Park, Costa Rica, 1999 (part 1: stony corals and algae). Atoll Res. Bull. 496:248-57
34. Fonseca AC, Salas E, Cortés J. 2006. Monitoreo del arrecife coralinoMeager Shoal, Parque Nacional Cahuita, Costa Rica (sitio CARICOMP). Rev. Biol. Trop. 54:755-63
35. Forcucci D. 1994. Population density, recruitment and 1991 mortality event of Diadema antillarum in the Florida Keys. Bull. Mar. Sci. 54:917-28
36. Furman B, Heck KL. 2009. Differential impacts of echinoid grazers on coral recruitment. Bull. Mar. Sci. 85:121-32
37. Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR. 2003. Long-term region-wide declines in Caribbean corals. Science 301:958-60
38. Glynn PW. 1984. Widespread coral mortality and the 1982-83 El Niño warming event. Environ. Conserv. 11:133-46
39. González-Gaviria FT, Garca-Urueña R. 2011. Estado actual de las poblaciones del erizo negro Diadema antillarum Philippi (Echinoidea: Diadematidae) en el Parque Nacional Natural Tayrona y playa Blanca, Santa Marta, Caribe Colombiano. Bol. Investig. Mar. Costeras 40:401-17
40. Haley MP, Solandt JL. 2001. Population fluctuations of the sea urchins Diadema antillarum and Tripneustes ventricosus at Discovery Bay, Jamaica: A case of biological succession? Caribb. J. Sci. 37:239-45
41. Harborne AR, Renaud PG, TylerEHM, Mumby PJ. 2009. Reduced density of the herbivorous urchin Diadema antillarum inside a Caribbean marine reserve linked to increased predation pressure by fishes. Coral Reefs 28:783-91
42. Harvell CD, Aronson R, Baron N, Connell J, Dobson A, et al. 2004. The rising tide of ocean diseases: unsolved problems and research priorities. Front. Ecol. Environ. 2:375-82
43. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, et al. 1999. Emerging marine diseases: climate links and anthropogenic factors. Science 285:1505-10
44. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, et al. 2002. Climate warming and disease risks for terrestrial and marine biota. Science 296:2158-62
45. Hay ME. 1984. Patterns of fish and urchin grazing on Caribbean coral reefs: Are previous results typical? Ecology 65:446-54
46. HayME, Taylor PR. 1985. Competition between herbivorous fishes and urchins on Caribbean reefs. Oecologia 65:591-98
47. Hernández JC, Clemente S, Sangil C, 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. Mar. Environ. Res. 66:259-70
48. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, et al. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318:1737-42
49. Hughes TP. 1994. Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547-51
50. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, et al. 2003. Climate change, human impacts, and the resilience of coral reefs. Science 301:929-33
51. Hughes TP, Connell J. 1999. Multiple stressors on coral reefs: A long-term perspective. Limnol. Oceanogr. 44:932-40
52. Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS. 2010. Rising to the challenge of sustaining coral reef resilience. Trends Ecol. Evol. 25:633-42
53. Hughes TP, Keller BD, Jackson JBC, Boyle MJ. 1985. Mass mortality of the echinoid Diadema antillarum Philippi in Jamaica. Bull. Mar. Sci. 36:377-84
54. Hughes TP, Reed DC, Boyle MJ. 1987. Herbivory on coral reefs: community structure following mass mortalities of sea urchins. J. Exp. Mar. Biol. Ecol. 113:39-59
55. Hughes TP, Szmant AM, Steneck R, Carpenter R, Miller S. 1999. Algal blooms on coral reefs: What are the causes? Limnol. Oceanogr. 44:1583-86
56. HunteW, Cote I, Tomascik T. 1986. Onthe dynamics of themassmortality of Diadema antillarum in Barbados. Coral Reefs 4:135-39
57. Hunte W, Younglao D. 1988. Recruitment and population recovery of Diadema antillarum (Echinodermata, Echinoidea) in Barbados. Mar. Ecol. Prog. Ser. 45:109-19
58. Hunter IG. 1977. Sediment production by Diadema antillarum on a Barbados fringing reef. In Proceedings of the 3rd International Coral Reef Symposium, Vol. 2: Geology, ed. DL Taylor, pp. 111-19. Coral Gables, FL: Univ. Miami Rosenstiel Sch. Mar. Atmos. Sci.
59. Idjadi J, Haring R, Precht W. 2010. Recovery of the sea urchin Diadema antillarum promotes scleractinian coral growth and survivorship on shallow Jamaican reefs. Mar. Ecol. Prog. Ser. 403:91-100
60. Jackson JBC. 1997. Reefs since Columbus. In Proceedings of the 8th International Coral Reef Symposium, Vol. 1, ed. HA Lessios, IG Macintyre, pp. 97-106. Panama City, Panama: Smithson. Trop. Res. Inst.
61. Jackson JBC. 2008. Ecological extinction and evolution in the brave new ocean. PNAS 105:11458-65
62. Jackson JBC, Kirby MX, BergerWH, Bjorndal KA, Botsford LW, et al. 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629-37
63. Karlson RH, Levitan DR. 1990. Recruitment-limitation in open populations of Diadema antillarum: An evaluation. Oecologia 82:40-44
64. Kramer PA. 2003. Synthesis of coral reef health indicators for the Western Atlantic: results of the AGRRA program (1997-2000). Atoll Res. Bull. 496:1-58
65. Lafferty KD, Harvell CD, Conrad JM, Friedman CS, Kent ML, et al. 2015. Infectious diseases affect marine fisheries and aquaculture economics. Annu. Rev. Mar. Sci. 7:471-96
66. Lafferty KD, Porter JW, Ford SE. 2004. Are diseases increasing in the ocean? Annu. Rev. Ecol. Evol. Syst. 35:31-54
67. Lapointe BE. 1997. Nutrient thresholds for eutrophication and macroalgal blooms on coral reefs in Jamaica and southeast Florida. Limnol. Oceanogr. 42:1119-31
68. Lessios HA. 1981. Reproductive periodicity of the echinoids Diadema and Echinometra on the two coasts of Panama. J. Exp. Mar. Biol. Ecol. 50:47-61
69. Lessios HA. 1984. Possible prezygotic reproductive isolation in sea urchins separated by the Isthmus of Panama. Evolution 38:1144-48
70. Lessios HA. 1988a. Mass mortality of Diadema antillarum in the Caribbean: What have we learned? Annu. Rev. Ecol. Syst. 19:371-93
71. Lessios HA. 1988b. Population dynamics of Diadema antillarum (Echinodermata: Echinoidea) following mass mortality in Panama. Mar. Biol. 99:515-26
72. Lessios HA. 1991. Presence and absence of monthly reproductive rhythms among 8 Caribbean echinoids off the coast of Panama. J. Exp. Mar. Biol. Ecol. 153:27-47
73. Lessios HA. 1995. Diadema antillarum 10 years after mass mortality: still rare, despite help from a competitor. Proc. R. Soc. B 259:331-37
74. Lessios HA. 1996. Methods of quantifying abundance of marine organisms. In Methods and Techniques of Underwater Research: Proceedings of the American Academy of Underwater Sciences 1996 Scientific Diving Symposium, ed. MA Lang, CC Baldwin, pp. 149-57. Washington, DC: Smithson. Inst.
75. Lessios HA. 1998. Shallow water echinoids of Cayos Cochinos, Honduras. Rev. Biol. Trop. 46:95-101
76. Lessios HA. 2001. Molecular phylogeny of Diadema: systematic implications. In Echinoderms 2000: Proceedings of the 10th International Echinoderm Conference, ed. MBarker, pp. 487-95. Lisse, Neth. : Swets&Zeitinger
77. Lessios HA. 2005. Diadema antillarum populations in Panama twenty years following mass mortality. Coral Reefs 24:125-27
78. Lessios HA, Cubit JD, Robertson DR, Shulman MJ, Parker MR, et al. 1984a. Mass mortality of Diadema antillarum on the Caribbean coast of Panama. Coral Reefs 3:173-82
79. LessiosHA, Garrido MJ, Kessing BD. 2001a. Demographic history of Diadema antillarum, a keystone herbivore on Caribbean reefs. Proc. R. Soc. B 268:2347-53
80. Lessios HA, Kessing BD, Pearse JS. 2001b. Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55:955-75
81. Lessios HA, Robertson DR, Cubit JD. 1984b. Spread of Diadema mass mortality through the Caribbean. Science 226:335-37
82. Levitan DR. 1988a. Algal-urchin biomass responses following mass mortality of Diadema antillarum Philippi at Saint John, U. S. Virgin Islands. J. Exp. Mar. Biol. Ecol. 119:167-78
83. Levitan DR. 1988b. Asynchronous spawning and aggregative behavior in the sea urchin Diadema antillarum (Philippi). In Echinoderm Biology, ed. RD Burke, PV Mladenov, P Lambert, RL Parsley, pp. 181-86. Rotterdam, Neth. : A. A. Balkema
84. Levitan DR. 1988c. Density-dependent size regulation and negative growth in the sea urchin Diadema antillarum Philippi. Oecologia 76:627-29
85. Levitan DR. 1989. Density-dependent size regulation in Diadema antillarum: effects on fecundity and survivorship. Ecology 70:1414-24
86. Levitan DR. 1991. Influence of body size and population density on fertilization success and reproductive output in a free-spawning invertebrate. Biol. Bull. 181:261-68
87. Levitan DR. 1992. Community structure in times past: influence of human fishing pressure on algal urchin interactions. Ecology 73:1597-605
88. Levitan DR, Edmunds PJ, Levitan KE. 2014. What makes a species common? No evidence of densitydependent recruitment or mortality of the sea urchin Diadema antillarum after the 1983-1984 mass mortality. Oecologia 175:117-28
89. Levitan DR, McGovern TM. 2005. The Allee effect in the sea. In Marine Conservation Biology: The Science of Maintaining the Sea's Biodiversity, ed. EA Norse, LB Crowder, pp. 47-57. Washington, DC: Island
90. Lewis SM, Wainwright PC. 1985. Herbivore abundance and grazing intensity on a Caribbean coral reef. J. Exp. Mar. Biol. Ecol. 87:215-28
91. LiddelWD, Ohlhorst SL. 1986. Changes in benthic community composition following the mass mortality of Diadema at Jamaica. J. Exp. Mar. Biol. Ecol. 95:271-78
92. Lugo MA. 2004. Population status of the black sea urchin Diadema antillarum (Phillipi) in La Parguera, Puerto Rico, 20 years after the mass mortality event. MS Thesis, Univ. Puerto Rico, Mayag üez
93. Macintyre IG, Glynn PW, Hinds F. 2005. Evidence of the role of Diadema antillarum in the promotion of coral settlement and survivorship. Coral Reefs 24:273
94. Martin-Blanco F, Gonzalez-Sanson G, Pina-Amargosi F, Clero-Alonso L. 2010. Abundance, distribution and size structure of Diadema antillarum (Echinodermata: Diadematidae) in South Eastern Cuban coral reefs. Rev. Biol. Trop. 58:663-76
95. McClanahan TR, Muthiga NA. 1998. An ecological shift in a remote coral atoll of Belize over 25 years. Environ. Conserv. 25:122-30
96. McGeheeMA. 2008. Changes in the coral reef community of southwest Puerto Rico 1995 to 2005. Caribb. J. Sci. 44:345-54
97. Miller M, Kramer K, Williams S, Johnston L, Szmant A. 2009. Assessment of current rates of Diadema antillarum larval settlement. Coral Reefs 28:511-15
98. Miller RJ, Adams AJ, Ebersole JP, Ruiz E. 2007. Evidence for positive density-dependent effects in recovering Diadema antillarum populations. J. Exp. Mar. Biol. Ecol. 349:215-22
99. Miller RJ, Adams AJ, Ogden NB, Ogden JC, Ebersole JP. 2003. Diadema antillarum 17 years after mass mortality: Is recovery beginning on St. Croix? Coral Reefs 22:181-87
100. Moses CM, Bonem RM. 2001. Recent population dynamics of Diadema antillarum and Tripneustes ventricosus along the north coast of Jamaica, W. I. Bull. Mar. Sci. 68:327-36
101. Mumby PJ, Hastings A, Edwards HJ. 2007. Thresholds and the resilience of Caribbean coral reefs. Nature 450:98-101
102. Murillo MM, Cortes J. 1984. Alta mortalidad en la poblacion del erizo del Mar Diadema antillarum (Echinodermata, Echinoidea), en el Parque nacional Cahuita, Limon, Costa Rica. Rev. Biol. Trop. 32:515-18
103. Myhre S, Acevedo-Gutierrez A. 2006. Recovery of sea urchin Diadema antillarum populations is correlated to increased coral and reduced macroalgal cover. Mar. Ecol. Prog. Ser. 329:205-10
104. Noriega N, Pauls SM, del Monaco C. 2006. Abundance of Diadema antillarum (Echinodermata: Echinoidea) in the coasts of Venezuela. Rev. Biol. Trop. 54:793-802
105. Ogden JC. 1976. Some aspects of herbivore-plant relationships on Caribbean reefs and seagrass beds. Aquat. Bot. 2:103-16
106. Ogden JC, Brown RA, Salesky N. 1973. Grazing by the echinoid Diadema antillarum: formation of halos aroundWest Indian patch reefs. Science 182:715-17
107. Paddack MJ, Reynolds JD, Aguilar C, Appeldoorn RS, Beets J, et al. 2009. Recent region-wide declines in Caribbean reef fish abundance. Curr. Biol. 19:590-95
108. Reinthal PN, Kensley B, Lewis SM. 1984. Dietary shifts in the queen triggerfish, Balistes vetula, in the absence of its primary food item, Diadema antillarum. Mar. Ecol. 5:191-95
109. Robertson DR. 1987. Responses of two coral reef toadfishes (Batrachodidae) to the demise of their primary prey, the sea urchin Diadema antillarum. Copeia 1987:637-42
110. Robertson DR. 1991. Increases in surgeonfish populations after mass mortality of the sea urchin Diadema antillarum in Panama indicate food limitation. Mar. Biol. 111:437-44
111. Rodrguez A, Hernández JC, Clemente S, Coppard SE. 2013. A new species of Diadema (Echinodermata: Echinoidea: Diadematidae) from the eastern Atlantic Ocean and a neotype designation of Diadema antillarum (Philippi, 1845). Zootaxa 3636:144-70
112. Rodrguez-Barreras R, Pérez ME, Mercado-Molina AE, Williams SM, Sabat AM. 2014. Higher population densities of the sea urchin Diadema antillarum linked to wave sheltered areas in north Puerto Rico Archipelago. J. Mar. Biol. Assoc. UK 94:1661-69
113. Ruiz-Ramos DV, Hernández-Delgado EA, Schizas NV. 2011. Population status of the long-spined urchin Diadema antillarum in Puerto Rico 20 years after a mass mortality event. Bull. Mar. Sci. 87:113-27
114. Sammarco PW. 1982a. Echinoid grazing as a structuring force in coral communities:whole reef manipulations. J. Exp. Mar. Biol. Ecol. 61:31-55
115. Sammarco PW. 1982b. Effects of grazing by Diadema antillarum Philippi (Echinodermata: Echinoidea) on algal diversity and community structure. J. Exp. Mar. Biol. Ecol. 65:83-105
116. Schutte VGW, Selig ER, Bruno JF. 2010. Regional spatio-temporal trends in Caribbean coral reef benthic communities. Mar. Ecol. Prog. Ser. 402:115-22
117. Scoffin TP, Stearn CW, Boucher D, Frydl P, Hawkins CM, et al. 1980. Calcium carbonate budget of a fringing reef on the west coast of Barbados. Part II. Erosion, sediments and internal structure. Bull. Mar. Sci. 30:475-508
118. Sellers AJ, Casey LO, Burge EJ, Koepfler ET. 2009. Population growth and distribution of Diadema antillarum at Discovery Bay, Jamaica. Open Mar. Biol. J. 3:105-11
119. Shinn EA, Griffin DW, Seba DB. 2003. Atmospheric transport of mold spores in clouds of desert dust. Arch. Environ. Health 58:498-504
120. Shinn EA, SmithGW, Prospero JM, Betzer P, Hayes ML, et al. 2000. African dust and the demise of Caribbean coral reefs. Geophys. Res. Lett. 27:3029-31
121. Shulman MJ, Robertson DR. 1996. Changes in the coral reefs of San Blas, Caribbean Panama: 1983 to 1990. Coral Reefs 15:231-36
122. Soto-Santiago FJ, Irizarry-Soto E. 2013. The sea urchin Diadema antillarum (Echinodermata, Equinoidea), algal cover and juvenile coral densities in La Parguera, Puerto Rico. Cuad. Investig. UNED 5:33-40
123. Steiner SCC, Williams SM. 2006. The density and size distribution of Diadema antillarum in Dominica (Lesser Antilles): 2001-2004. Mar. Biol. 149:1071-78
124. Vermeij MJA, Debrot AO, van der Hal N, Bakker J, Bak RPM. 2010. Increased recruitment rates indicate recovering populations of the sea urchin Diadema antillarum in Curaçao. Bull. Mar. Sci. 86:719-25
125. Weil E, Losada F, Bone D. 1984. Spatial variations in density and size of the echinoid Diadema antillarum Philippi on some Venezuelan coral reefs. Bijdr. Dierkd. 54:73-82
126. Weil E, Torres JL, Ashton M. 2005. Population characteristics of the sea urchin Diadema antillarum in La Parguera, Puerto Rico, 17 years after the mass mortality event. Rev. Biol. Trop. 53:219-31
127. Williams ID, Polunin NVC. 2001. Large-scale associations between macroalgal cover and grazer biomass on mid-depth reefs in the Caribbean. Coral Reefs 19:358-66
128. Williams SM, Benavides-Serrato M, Garca-Arrarás JE, Hernández-Delgado EA, Rodrguez-BarrerasR. 2013. Review of echinoderm research in Puerto Rico, with the focus on biological and ecological aspects. In Echinoderm Research and Diversity in Latin America, ed. JJ Alvarado, FA Sols-Martn, pp. 437-69. New York: Springer
129. Williams SM, Garcia-Sais JR, Capella J. 2009. Temporal variation of early larval stages of the long-spined sea urchin Diadema antillarum in La Parguera, Puerto Rico. Caribb. J. Sci. 45:110-17
130. Williams SM, Garcia-Sais JR, Yoshioka PM. 2011. Spatial variation of Diadema antillarum settlement in La Parguera, Puerto Rico. Bull. Mar. Sci. 87:531-40
131. Woodley JD, Gayle PMH, Judd N. 1999. Sea-urchins exert top-down control of macroalgae on Jamaican coral reefs (2). Coral Reefs 18:193
132. Zea S. 1998. Biotic changes in the reef complex of San Andres Island (southwestern Caribbean Sea, Colombia) occurring over nearly three decades. Atoll Res. Bull. 456:1-30