Benthic and fish population monitoring associated with a marine protected area in the nearshore waters of Grenada, Eastern Caribbean
Robert Anderson1*, Clare Morrall2*, Steve Nimrod2, Robert Balza1, Craig Berg3*, Jonathan Jossart1
*Dirección para correspondencia Abstract ]]>
Annual benthic and fish population surveys were completed at five locations in the nearshore waters along Grenada´s southwest coast during 2008-2010. Two survey sites are located in a newly launched Marine Protected Area (MPA). Photo Quadrat (PQ) and Point Line Intercept (PLI) surveys were used to determine substrate cover. Algae was the primary live cover increasing significantly from 45.9% in 2008 to 52.7% in 2010 (PLI). Algae was also predominant (61.0%-59.3%) in the PQ surveys although ]]>
Chromis spp. dominated the survey sites at 65.2% in 2008 ]]>
]]>
Palabras clave: cobertura bentónica, coral, peces de arrecife, monitoreo, Grenada, Caribe Oriental. The island nation of Grenada is part of the Eastern Caribbean region recently classified as being at ]]>
et al. 2008). Of the 160 km2 of reef area in Grenada 41% were listed as having a high-risk threat index and 40% were listed as very high (Burke & Maidens 2004). The primary contributors to this rating were coastal development and fishing pressure.
Coral communities ]]>
et al. 2011, Walsh 2011). In an analysis of the Grenadian demersal fish catch and fishing effort from 1986 to 1993, Jeffrey (2000) found that the number of boats employed in the demersal fishery off the west coast of Grenada increased by 200% however the catch declined by nearly 75% during this seven year period. Local overfishing often targets large herbivorous species reducing these fish stocks thus contributing to increased abundance of macroalgae on coral ]]>
et al. 2005, Arnold 2007, Birrell et al. 2008, Mora 2008).
Introduction of excess nutrients to coral reef systems from coastal development further enhances overgrowth of algae (Lapointe et al.1997) ]]>
et al. 2009). These local stressors weaken a coral community’s resilience (Hughes 1994, Hughes et al. 2003, Gardner et al. 2003, Wilkinson 2008) making it more vulnerable to global climate change and increased storm activities (Goldenberg et al. 2001, Eakin et al. 2010, ]]>
et al. 2010). Grenada has been impacted by two major hurricanes in the past decade: Ivan in September 2004 and Emily in July 2005. Major storms such as these can result in devastating effects on reefs breaking down the basic structure and dislodging corals leaving leveled areas of rubble (Woodley et al. 1981).
Many countries have ]]>
A development plan for Grenada’s National Protected Areas System identified the need for external assistance in research and monitoring of Grenada’s protected areas (Mac Leod 2007). Initial surveys at nine sites off the southwest coast of ]]>
et al. 2008). This 2008-2010 study builds on the initial survey and establishes a foundation upon which the effectiveness of the Moliniere-Beausejour MPA management techniques may be evaluated.
]]>
Study Area: Five sites ranging in depth from 5.2m-12.2m, located along Grenada’s southwest coast were established in 2008. Similar reefs both inside and outside the MPA that are frequently used by the dive industry were selected. Dragon Bay (12° 5’6.00”N 61°45’45.36”W) and Flamingo Bay (12° 5’30.36”N 61°45’30.60”W) are in MPAs, while Northern Exposure Shallow (12° 1’57.30”N 61°46’14.28”W), Northern Exposure Deep (12° 2’22.14”N ]]>
Materials and Methods
]]>
The substrate composition of Grenada’s southwest coast was surveyed with the Photo Quadrat (PQ) and Point Line Intercept (PLI) methods. The PQ method allows for careful identification of substrate types from a digital photograph. Although identification of substrate types is not always optimal based on digital photos this approach allowed more intense scrutiny of the substrate since time is not a factor in the sampling process. In addition using Coral Point Count with Excel extensions (CPCe) v.3.6 ]]>
Diadema antillarum, abundance occurring within a twometer wide ]]>
Divers completed fish data collections along each transect in ten minutes. ]]>
Sixty photo quadrats from each transect were processed using Coral Point Count with Excel extensions (CPCe) v.3.6 (Kohler & Gill 2006). A Canon EOS Digital Rebel XTI camera in an Ikelite underwater housing was used to take a picture at every half-meter mark. Attached to the underwater housing was a tube with a calibrated scale used to maintain a consistent distance (60cm) from the substrate and to assist with scaling in the CPCe software program. The images were uploaded into the CPCe software program, and a ]]>
et al. (2009) found that whether nine or ninety-nine points were used in a1m2 area, the difference for large categories was not significant. Thus for the 400 cm2
area in this study 8 points were deemed sufficient. Also, a Sony HDR-SR8 video camera in an Amphibico underwater housing was used to take video of each location to record a broader perspective of the survey sites.
For both the PLI and PQ data a repeated measure analysis of variance (ANOVAR) using transects as the ]]>
]]>
To identify interactions between the MPA and non-protected area from 2008 to 2010 a two-way ANOVAR was used. This was only done for the PLI data, because the PQ data had an insufficient sample size. In order to effectively make this comparison the same sample size needed to be used for the MPA and non-protected area. This was accomplished by selecting two of the three non-protected locations, Quarter Wreck and Northern Exposure Shallow. The above criteria for assessing normality, sphericity, and significance were used. When an interaction was found to be significant a follow up ]]>
Results
Substrate (PLI): Algae was the dominant substrate cover found at all locations off Grenada’s southwest coast (Fig. 1). Algae increased significantly from 45.9% (SE=1.7; n=35) in 2008 to 52.7% (1.4; 35) in 2010 (ANOVAR, F=7.431, p=0.001). Comparison of major algal groups (macroalgae, turf and coralline) showed that macroalgae consistently ]]>
1 & 2).
Algal cover in the MPA ranged from 46.3% (3.9; 12) to 51.4% (3.5; 12) over the three years, while in the non-protected area it ranged from 44.0% (3.2; 12) to 50.3% (2.2; 12); ]]>
Table 3). Yet the different types of algae experienced significant interaction. Turf algae did have a significant interaction (Two-way ANOVAR, F=6.738, p=0.005), but the follow up tests showed no significant differences between the MPA and non-protected area. Coralline algae also exhibited a significant interaction (Two-way ANOVAR, F=17.752, p=0.000), and for 2010 the 32.4% (3.3; 12) found in the non-protected area was significantly greater than the 18.2% (3.6; 12) in the MPA. Macroalgae did not exhibit any significant interaction ]]>
Table 4).
The hard coral cover did not vary significantly from year to year ranging from 16.5% (1.0; 35) to 15.4% (1.3; 35) (Fig. 1) (ANOVAR, F=0.531, p=0.591) (Fig. 1). However the ]]>
5 & 6).
Hard coral cover ranged from 15.2% (2.2; 12) to 19.9% (4.3; 12) in ]]>
Table 3). Although hard coral did not differ significantly (Two-way ANOVAR, F=0.072, p=0.931) in overall percent between the MPA and non-protected area encrusting coral did have a significant interaction between time and location (Two-way ANOVAR, F=7.049, p=0.004). Yet in follow up analyses no significant differences between the MPA and non-protected area was found. Massive (Two-way ANOVAR, F=3.555, p=0.046) and branching ]]>
Table 7).
While hard coral cover remained stable, gorgonian cover significantly dropped from 3.7% (0.4; 32) and 4.0% (0.6; 32) in 2008 and 2009 to 1.8% (0.3; 32) in 2010 (ANOVAR, F=19.609, p=0.000). ]]>
Other significant changes in the substrate were seen in the sponge and non-living categories. Sponge cover saw a sudden decrease from 4.6% (0.8; 35) in 2008 to 2.2% (0.4; 35) in 2009, but recovered to 4.9% (0.8; 35) in 2010 (ANOVAR, F=6.212, p=0.005). Also non-living substrate significantly decreased from 25.2% (1.7; 35) and 21.9% (1.9; 35) in 2008 and 2009 to 14.2% (1.3; 35) in 2010 (ANOVAR, F=14.745, p=0.000) (Fig. 1).
Further comparisons of percent cover in the MPA to non-protected areas revealed that gorgonian cover did have a significant interaction (Two-way ANOVAR, F=13.005, p=0.000). Additional tests of gorgonian cover in the MPA and non-protected areas showed no significant difference among years. Sponge cover also exhibited a significant interaction (Two-way ANOVAR, F=8.654, p=0.002). The sponge cover in the MPA was not significantly different from the ]]>
Table 3).
Substrate (Photo Quadrat): Algae, the dominant substrate cover, ranging from 61.0% (1.5; 19) in 2008, 59.9% (1.9; 19) in 2009 and 59.3% (1.8, 19) in 2010 showed no significant annual differences ]]>
Fig. 2). Although the percent cover of algae did not change across years, the type of algae observed did. Macroalgae which occurred more frequently than other types of algae increased significantly in 2010. Turf algae dipped significantly in 2009 and coralline algae decreased significantly in 2010 (Table 1 & 2).
]]>
Percent hard coral cover remained stable across years ranging from 11.4% (0.7; 18) to 12.0% (1.1; 18) (ANOVAR, F=0.037, p=0.964). Of the three hard coral forms recorded branching coral occurred most frequently with no significant annual variation (Table 3 & 4). Cyanobacteria which was not recorded over the three year sampling period with the PLI method was similar in percent cover to hard coral ranging from 14.7% (1.5; 19) to 11.9% (1.7; 19) (ANOVAR, F=1.314, p=0.277). Percent sponge cover did ]]>
Fig. 2).
Fish: A total of 62 fish species were observed at the five sampling locations from 2008 to 2010 (Table 8). The major groups of fish analyzed included
Chromis spp., damselfishes, parrotfishes, surgeonfishes, and wrasse. Chromis spp. were separated from the damselfishes because of their large number. Diversity indices were quite high and similar across all sites (Table 9).
Relative abundance of all but one ]]>
Chromis spp., the largest group observed, showed a downward trend going from 65.2% (3.5; 34) to 49.8% (4.2; 34); however the difference was not significant (ANOVAR, F=3.611, p=0.032). Damselfishes ranged from 11.1% (1.7; 32) to 15.5% (1.7; 32) (ANOVAR, F=3.531, p=0.035) and parrotfishes from 10.1% (1.6; 36) to 6.4% (0.7; 36) (ANOVAR, F=1.732, p=0.184) (
Fig. 3). Surgeonfishes also remained stable between 0.9% (0.1; 31) and 1.3% (0.2; 31) (ANOVAR, F=0.146, p=0.864). Wrasse however showed a significant increase from 7.3% (1.0; 35) to 15.5% (2.1; 35) (ANOVAR, F=7.341, p=0.001) (Fig. 3). ]]>
In comparing the MPA to the non-protected area, a significant interaction between time and location was observed for the chromis, which ranged from 47.8% (6.8; 12) to 77.1% (3.7; 12) in the MPA and 42.0% (6.4; 12) to 45.8% (6.7; 12) in the non-protected area (Two-way ANOVAR, F=6.303, p=0.007). Additional tests revealed that percent chromis ]]>
Table 11). During 2008 the wrasse were significantly higher in the non-protected area at 11.9% (1.9; 12), whereas the MPA only had 3.5% (1.1; 12) wrasse (Table 10). None of the ]]>
Table 11).
The density of fishes on the other hand did show significant differences for most groups over the years of the study. Chromis spp. decreased significantly from 669.3 fish/100
m2 (180.5; 30) to 286.6 fish/100m2 (78.3; 30) (ANOVAR, F=9.215, p=0.000). Damselfishes density also significantly decreased from 70.3 fish/100m2 (3.7; 34) in ]]>
m2 (2.7; 34) in 2009 (Bonferroni, p=0.000) and 55.3 fish/100m2 (5.2; 34) in 2010 (Bonferroni, p=0.015) (ANOVAR, F=17.994, p=0.000). The density of parrotfishes significantly decreased from 39.5 fish/100
m2 (3.2; 30) and 39.7 fish/100m2 (4.2; 30) in 2008 and 2009 to 26.3 fish/100m2 (4.5; 30) in 2010 (ANOVAR, F=10.786, p=0.000). Wrasse density however showed an increase from 37.6 fish/100
m2 (4.6; 34) and 30.2 fish/100m2 (3.5; 34) in 2008 and 2009 to 68.6 fish/100m2 (15.4) in 2010 but the change was not significant (ANOVAR, F=3.525, p=0.035). The density of surgeonfishes did not significantly change, however it showed a downward trend going from 6.3 ]]>
m2 (0.8; 25) in 2008 to 5.9 fish/100m2 (1.4; 25) in 2009, and finally to 4.5 fish/100m2 (0.5; 25) in 2010 (ANOVAR, F=1.859, p=0.179) (Fig. 4). The only fish group that experienced a significant ]]>
Table 11). Damselfish in 2010 were significantly higher in the non-protected area at 54.9% (3.5; 11), while only 36.8% (4.8; 12) were observed in the MPA (ANOVA, F=9.600, p=0.005) (Table 12).
The observed fish ]]>
Combined Diadema antillarum density for Grenada’s southwest coast exhibited a significant downward trend ]]>
m2 (0.5; 36) in 2008, to 1.9 urchins/100m2 (0.5; 36) in 2009 and to only 0.2 urchins/100m2 (0.1; 36) in 2010 (ANOVAR, F=6.078, p=0.004). It should be noted even after log transformation the data did not fulfill the assumption of normality, however sphericity ]]>
Discussion
Data collected during three annual surveys indicates benthic cover in the nearshore waters off the ]]>
et al. 2008, Wilkinson 2008, Mumby 2009, Walsh 2011). Algae has been the dominant substrate cover on Caribbean reefs since a major ecological phase shift occurred in the 1980s. Overfishing, hurricane damage and a disease-induced die-off of
D. antillarum have been proposed as major factors in this shift (Hughes 1994, Gardner et al. 2003).
Low densities of D. antillarum in Grenadian nearshore waters may be one of the key factors in the high algal component of this benthic community. The mean
D. antillarum density found in 2x30m belt transects off the coast of Grenada during this study ranged from 0.002/m2 to 0.031/m2 which is much lower than the 4.25/m2 densities measured in 2003 by Carpenter ]]>
m2 they found associated with reefs of six countries around the Caribbean. Based on general surveys across a spectrum of western Atlantic reefs between 1998-2000 Kramer (2003) reported mean D. antillarum densities of 0.029/m2. Newman
et al. (2006) found mean densities of 0.019/m2 at similar depths in the western and northern Caribbean. In both studies fleshy macroalgae generally dominated the reef benthic communities where these low D. antillarum densities occurred.
Given the importance ]]>
D. antillarum in the coral reef community reestablishment of D. antillarum may have potential as a management tool to enhance coral growth in algal dominated systems. This potential became apparent when a phase shift reversal was noted on Jamaica’s north coast. Coral cover increased from 23% in 1995 to 54% in 2004 with higher growth rates of juvenile corals and higher densities of small juvenile recruits in “dense urchin zones” (Idjadi et al. 2006, 2010, Bechtel et al. ]]>
D. antillarum on coral recovery sparked introductions of additional D. antillarum into Grenada’s MPA from adjacent populations in 2011 (Nimrod personal communication). These relocations will hopefully result in significant increases in local populations of D. antillarum that will reduce macroalgae and facilitate an increase in coral ]]>
Understanding the composition of Grenada’s southwest coastal nearshore fish community will also inform existing and future fisheries management practices. Heavy fishing pressure has been identified as one of the key factors in transformation of coral reefs to algal dominated systems (Hawkins & Roberts 2003). Fishing methods in Grenada include beach seining, trap nets, hand lines and spearing. Target species are mainly carnivores ]]>
et al. (2010) ]]>
et al. (2011) divides herbivorous fishes into roving herbivores or “foragers” (parrotfish Scarus spp. and surgeonfish Acanthurus spp.) and “farmers” (territorial damselfish Stegastes spp.) in order to evaluate their potential influence on algal succession and ]]>
et al. 2011). In Grenada’s nearshore fish community herbivores were dominated by parrotfishes (Scaridae) at 70.2% followed by territorial damselfish fish (Pomacentrus spp., Stegastes spp., Microspathodon spp.) at 17.9% and ]]>
Acanthurus spp.) at 11.5%. Thus “farmers” comprised only 17.9% in the Grenadian nearshore herbivorous fish community while “foragers” made up 82.1%. It is understandable therefore that turf algae comprised such a small portion of the algal community and fleshy macroalgae made up the majority. Arnold (2007) demonstrated that grazing by scrapers such as parrotfish and urchins facilitate coral recruitment more than territorial damselfishes that maintain low levels of turf algae. Since the species composition of herbivores in ]]>
In addition to low ]]>
et al. (2009) described the importance of taking into consideration the complex interaction of herbivory, nutrient levels and stochastic events in understanding existing conditions and developing management strategies for coral reef communities. Lapointe et al. (1997) argued that nutrient input from ]]>
et al. (2008a) saw a shift from dominance by a few large top predator fish species to dominance by small lower trophic level consumers, primarily planktivores, in areas of increasing human populations. The dominance of planktivores (primarily Chromis spp.) ]]>
et al. 2009). ]]>
The three years of monitoring at permanent transects in this study provide a basis for future trend analysis and evaluation of management practices. Hughes et al. (2010) advocates long term monitoring of important taxonomic groups as well as identification of mechanisms and feedbacks in order to detect indicators of phase shifts. He also encourages agencies involved in research and management of reefs to take a proactive integrative approach through education of ]]>
This study establishes a baseline ]]>
Agaricia and Porites rather than framework builders such as Acropora and Montastrea. These framework builders that formerly dominated reefs in the Caribbean are essential to surviving the destructive forces of major storms. The ]]>
Agaricia and Porites. Given the importance of framework builders to the resilience of coral reef communities identification of coral species will be added to the monitoring program to better understand the coral community.
The similarity between the MPA and ]]>
In addition to focusing on local environments it is important to connect these studies to broader ecosystem wide analyses. Ogden (2010) encourages moving toward an ]]>
D. antillarum die-off, wide spread white band disease and the annual plume of discharge from Venezuela’s Orinoco River. Efforts are ongoing to strengthen connections of this ongoing monitoring effort to the network of Caribbean marine laboratories and provide information that will assist regional management. ]]>
Acknowledgements
Funding for this project was provided by the Fischer Family Foundation and Mr. Gary Stimac and is greatly appreciated. A special thanks to Jacob Krause for playing a major role in developing this program. Thanks are also offered to Jillian Groeschel, Kyle ]]>
References ]]>
Arnold, S.N. 2007. Running the gauntlet to coral recruitment through a sequence of local multiscale processes. MSc Thesis, Univ. Maine, Orono, Maine, USA. [ Links ]
Bascompte, J., C.J. Melian & E. Sala. 2005. Interaction strength combinations and the overfishing of a marine food web. Proc. Natl. Acad. Sci. USA 102: 5443-5447. [ Links ]
Bechtel, J.D., P. Gayle & L. Kaufman. 2006. The return of Diadema antillarum to Discovery Bay: patterns of distribution and abundance. Proc. 10th Int. Coral Reef Symp., Okinawa 1: 367-375. [ Links ]
Birrell, C.L., L. J. McCook, B.L. Willis & G.A. DiazPulido. 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. [ Links ]
Bouchon, C., P. Portillo, Y. Bouchon-Navaro, M. Louis, P. Hoetjes, K. De Meyer, D. Macrae, H. Armstrong, V. Datadin, S. Harding, J. Mallela, R. Parkinson, J. van Bochove, S. Wynne, D. Lirman, J. Herlan, A. Baker, L. Collado, S. Nimrod, J. Mitchell, C. Morrall, C. Isaac. 2008. Chapter 19. Status of coral reefs of the Lesser Antilles: The French West Indies, The Netherlands Antilles, Anguilla, Grenada, Trinidad and Tobago, p. 265-279 In: Wilkinson, C. (Ed.). Status of coral reefs of the world 2008. Global Coral Reef Monitoring and Reef and Rainforest Research Centre, Townsville, Australia. [ Links ]
Burke, L. & J. Maidens. 2004. Reefs at Risk in the Caribbean. World Resources Institute, Washington D.C., USA. [ Links ]
Burke, L., K. Reytar, M. Spalding & A. Perry. 2011. Reefs at Risk Revisited. World Resource Institute, Washington, D.C., USA. [ Links ]
Burkepile, D.E. & M.E. Hay. 2010. Impact of herbivore identity on algal succession and coral growth on a Caribbean reef. PLoS ONE 5: e8963. [ Links ]
Carpenter, R.C. & P.J. Edmunds. 2006. Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals. Ecol. Lett. 9: 268-277. [ Links ]
Ceccarelli, D.M., G.P. Jones & L.J. McCook. 2011. Interactions between herbivorous fish guilds and their influence on algal succession on a coastal coral reef. J. Exp. Mar. Biol. Ecol. 399: 60-67. [ Links ]
Crosby, M.P. & E. S. Reese. 1996. A manual for monitoring coral reefs with indicator species: butterfly fishes as indicators of change on the Indo-Pacific reefs, Office of Ocean and Coastal Resource Management, NOAA, Silver Spring, Maryland, USA. [ Links ]
Dumas, P., A. Bertaud, C. Peignon, M. Leopold & D. Pelletier. 2009. A “quick and clean” photographic method for the description of coral reef habitats. J. Exp. Mar. Biol. Ecol. 368:161-168. [ Links ]
Eakin, C.M., J.A. Morgan, S.F. Heron, T.B. Smith, G. Liu, L. Alvarez-Filip, B. Baca, E. Bartels, C. Bastidas, C. Bouchon, M. Brandt, A. Bruckner, L. Bunkley-Williams, A. Cameron, B.D. Causey, M. Chiappone, T.R.L. Christensen, M.J.C. Crabbe, O. Day, E. de la Guardia, G. Díaz-Pulido, D. DiResta, D.L. Gil-Agudelo, D. Gilliam, R. Ginsburg, S. Gore, H.M. Guzman, J.C. Hendee, E.A. Hernández-Delgado, E. Husain, C.F.G. Jeffrey, R.J. Jones, E. Jordán-Dahlgren, L. Kaufman, D.I. Kline, P. Kramer, J.C. Lang, D. Lirman, J. Mallela, C. Manfrino, J.P. Maréchal, K. Marks, J. Mihaly, W.J. Miller, E.M. Mueller, E. Muller, C.A. Orozco-Toro, H.A. Oxenford, D. Ponce-Taylor, N. Quinn, K.B. Ritchie, S. Rodríguez, A. Ramírez, S. Romano, J.F. Samhouri, J.A. Sánchez, G.P. Schmahl, B. Shank, W.J. Skirving, S.C.C. Steiner, E. Villamizar, S.M. Walsh, C. Walter, E. Weil, E. H. Williams, K. W. Roberson & Y. Yusuf. 2010. Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005. PLoS ONE 5: e13969. [ Links ]
Finlay, J. 2000. Grenada: National Biodiversity Strategy and Action Plan: Assessment and Analysis of Fisheries Marine and Coastal Areas, Consultants Report. United Nations Development Programme; Global Environmental Facility. Project No.: GRN/98/ G31/A/1G/99. [ Links ]
Gardner, T.A., I.M. Côté, J.A. Gill, A. Grant & A.R. Watkinson. 2003. Long term region-wide declines in Caribbean corals. Science 301: 958-960. [ Links ]
Goldenberg, S.B., C.W. Landsea, A.M. Mestas-Nuñez & W.M. Gray. 2001. The recent increase in Atlantic hurricane activity: causes and implications. Science 293: 474-479. [ Links ]
Hughes, T.P. 1994. Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265: 1547-1551. [ Links ]
Hughes, T.P., A.H. Baird, D.R. Bellwood, M. Card, S.R. Connolly, C. Folke, R. Grosberg, O. Hoegh-Guldberg, J.B.C. Jackson, J. Kleypas, J.M. Lough, P. Marshall, M. Nystrom, S.R. Palumbi, J. M. Pandolfi, B. Rosen & J. Roughgarden. 2003. Climate change, human impacts, and the resilience of coral reefs. Science 301: 929-933. [ Links ]
Hughes, T.P., N. Graham, J.B.C. Jackson, P.J. Mumby & R.S. Steneck. 2010. Rising to the challenge of sustaining coral reef resilience. Trends Ecol. Evol. 25: 633-642. [ Links ]
Idjadi, J.A., S.C. Lee, J.F. Bruno, W.F. Precht, L. Allen-Requa & P.J. Edmunds. 2006. Rapid phase shift reversal on a Jamaican coral reef. Coral Reefs 25:65-68. [ Links ]
Idjadi, J.A., R.N. Haring & W.F. Precht. 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. [ Links ]
Jeffrey, C.F.G. 2000. Annual, coastal and seasonal variation in Grenadian demersal fisheries (1986-1993) and implications for management. Bull. Mar. Sci. 66: 305-319. [ Links ] Kohler, K.E. & S.M. Gill. 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. Comput. Geosci. 32: 1259-1269. [ Links ]
Kramer, P.A. 2003. Synthesis of coral reef health indicators for the western Atlantic: results of the AGRRA program (1997-2000). Atoll. Res. Bull. 496: 1- 57. [ Links ]
Lapointe, B.E., M.M. Littler & D.S. Littler. 1997. Macroalgal overgrowth of fringing coral reefs at Discovery Bay, Jamaica: bottom-up versus top-down control. Proc. 8th Int. Coral Reef Symp., Panama. 927-932. [ Links ]
Littler, M.M., D.S. Littler & B.L. Brooks. 2009. Herbivory, nutrients, stochastic events, and relative dominances of benthic indicator groups on coral reefs: a review and recommendations. Proc. Mar. Sci. Network Symp., Washington, DC, USA. Smithsonian Contr. Mar. Sci. 38: 401-414. [ Links ]
Mora, C. 2008. A clear human footprint in the coral reefs of the Caribbean. Proc. Royal Soc. B. 275: 767-773. [ Links ]
Mumby, P.J. 2009. Phase shifts and the stability of macroalgal communities on Caribbean coral reefs. Coral Reefs 28: 761-773. [ Links ]
Newman, M.J.H., G.A. Paredes, E. Sala & J.B.C. Jackson. 2006. Structure of Caribbean coral reef communities across a large gradient of fish biomass. Ecol. Lett. 9: 1216-1227. [ Links ]
Ogden, J. 2010. Marine spatial planning (MSP): A first step to ecosystem-based management (EBM) in the wider Caribbean. Rev. Biol. Trop. 58 (Suppl. 3): 71-79. [ Links ]
Sandin, S.A., J.E. Smith, E.E. DeMartini, E.A. Dinsdale, S.D. Donner, A.M. Friedlander, T. Konotchick, M. Malay, J.E. Maragos, D. Obura, O. Pantos, G. Paulay, M. Richie, F. Rohwer, R.E. Schroeder, S. Walsh, J.B.C. Jackson, N. Knowlton & E. Sala. 2008. Baselines and degradation of coral reefs in the Northern Line Islands. PLoS ONE 3: e1548. [ Links ]
Sokal, R.R. and J.F. Rohlf. 1995. Biometry. 3rd ed. W.H. Freeman, New York. [ Links ]
Toller, W., A.O. Debrot, M.J.A. Vermeij & P. C. Hoetjes. 2010. Reef fishes of Saba Bank, Netherlands Antilles: assemblage structure across a gradient of habitat types. PLoS ONE 5: e9207. [ Links ]
Walsh, S.M. 2011. Ecosystem-scale effects of nutrients and fishing on coral reefs. Mar. Biol. 2011: 1-13. [ Links ]
Wilkinson, C. 2008. Status of Coral Reefs of the World: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville, Australia. [ Links ]
*Correspondencia: Robert Anderson: Wisconsin Lutheran College, 8800 W. Bluemound Rd., Milwaukee, WI 53226, USA; banderson@wlc.edu. Clare Morrall: St. George’s University, P.O. BOX 7, St. George’s, Grenada, West Indies; cmorrall@sgu.edu. Steve Nimrod: St. George’s University, P.O. BOX 7, St. George’s, Grenada, West Indies; snimrod@sgu.edu. Robert Balza: Wisconsin Lutheran College, 8800 W. Bluemound Rd., Milwaukee, WI 53226, USA; rob.balza@wlc.edu. ]]>
Craig Berg: Milwaukee County Zoo, 10001 W Bluemound Road, Milwaukee, WI 53226, USA; craig.berg@milwcnty.com. Jonathan Jossart: Wisconsin Lutheran College, 8800 W. Bluemound Rd., Milwaukee, WI 53226, USA; jossart1@gmail.com.