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BULLETIN OF MARINE SCIENCE, 84(3): 295–306, 2009

CORAL REEF PAPER

IMPACT OF HURRICANES EMILY AND WILMA ON THE CORAL COMMUNITY OF COZUMEL ISLAND, MEXICO Lorenzo Álvarez-Filip, Marinés Millet-Encalada, and Héctor Reyes-Bonilla ABSTRACT

In 2005, the Mexican Caribbean was impacted by two powerful hurricanes: Emily (July) and Wilma (October). This study assessed the immediate damage caused by these events on the coral community in the Marine Protected Area of Cozumel. Six reefs were evaluated during three time periods: before the hurricanes, after Emily, and after Wilma. In each reef, six transects were surveyed to determine the cover of corals. The results indicate a cumulative decline of 56% in live coral cover after both hurricanes had struck. At the generic level, chi-square statistics revealed a uniform reduction in the percent cover of the different coral genera. Standard ecological indices indicated no major modifications in community structure; however, the taxonomic distinctness and ordination analysis revealed a directional change to an increasingly more homogeneous composition of species after each impact. The present study reveals a significant decrease in live coral cover and gradual modifications in composition of assemblages after the hurricanes, but paradoxically, there were no major modifications in community structure.

Worldwide, tropical reefs are suffering a significant decline in coral cover as a result of local and global-scale disturbances. In the Caribbean Sea, hurricanes and tropical storms have historically played an important role shaping reef communities (Hughes and Connell, 1999). These events can modify the structure (Blanchon, 1997) and function (Harmelin-Vivien, 1994) of the reef ecosystems in a short period of time. The ecological changes and the time period needed for recovery after the impact of a hurricane are quite variable, as they depend on, among other factors, the intensity of the disturbance, the previous condition of the reef, and the level of connectivity of the damaged area (Hughes and Connell, 1999). Because of the complexity and number of variables involved, the direction of succession and time required for reefs to return to their pre-disturbance state are quite unpredictable, and in general, the process is poorly understood (Woodley et al., 1981; Hughes and Connell, 1999). In addition to natural disturbances, Caribbean reef degradation seems to be greatly influenced by human activities (Mora, 2008), disease, loss of functional groups, and the rise in ocean temperature (Hughes, 1994; Bruno et al., 2007; Hoegh-Guldberg et al., 2007). These factors may intensify the damages caused by natural phenomena, as seen in the increase in frequency and intensity of hurricanes and tropical storms as a consequence of increase in sea temperature (Webster et al., 2005). Thus, understanding the patterns of damage and subsequent recovery of reef communities after natural impacts is increasingly relevant in the context of human-perturbed ecosystems. During 2005, the western Caribbean was hit by Hurricanes Emily and Wilma, two of the strongest hurricanes recorded in the region. Emily reached the northern Yucatán Peninsula on 17 July, with sustained maximum winds of 260 km hr–1, and a few months later (October 21), Wilma affected the same area, moving very slowly (5 km hr–1) in a north-northwest direction, with sustained winds of 220 km hr–1 and gusts of more than 300 km hr–1. Wilma was one of the most intense hurricanes recorded Bulletin of Marine Science

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in the Atlantic Ocean, with the lowest atmospheric pressure ever registered in the Northern Hemisphere (882 mbar; NHC, 2005). Both storms impacted Cozumel Island: the eye of Hurricane Emily passed within 5 km southeast of the southern tip of Cozumel, and Hurricane Wilma (with an eye diameter of 63 km) passed directly over the island (Álvarez-Filip and Gil, 2006). The structure and composition of Cozumel reefs was originally described in the 1980s (Fenner, 1988; Jordán-Dahlgren, 1988; Muckelbauer, 1990), and since then these ecosystems have been considered among the healthiest in México and among the best preserved in the western Caribbean (Arriaga-Carrera et al., 1998). Their extensive coral cover and complex architecture allows them to harbor a great diversity of marine species, including fish, mollusks, polychaetes, and sponges (Ochoa-Rivera et al., 2000; Zea and Weil, 2003; Jordán-Dahlgren and Rodríguez-Martínez, 2003). There are few human perturbations to the reef system; nevertheless, the effects of Emily and Wilma were considerable. They were briefly outlined by Álvarez-Filip and Gil (2006), but a detailed description of the changes in coral community structure and composition is still needed. Here we describe and evaluate the level of damage that the two hurricanes caused to the coral communities inside the national park, where the best preserved reefs of the island are located. Materials and Methods Study Area.—Cozumel (Fig. 1) is located 22 km off the east coast of the Yucatán Peninsula in Mexico. It is an elongated continental island 46 km long and 16 km wide, with its main axis in a north-south direction. The area is influenced by the continuous south-to-north flow of the Yucatán Current, which moves through the channel, reaching 3 or 4 kts in the summer, and by the presence of temporal and tide-induced coastal countercurrents, which reach a maximum speed of 2 kts (Chávez et al., 2003). During the year, sea surface temperature fluctuates between 23° and 30 °C with an average of 27.5 °C and salinity averages 34.5 (WOA, 2005). The island is occasionally affected by hurricanes in summer and fall (June to November), with August and September experiencing the most intense activity. The southwestern coast of the island has been under official protection since 1980; it was first declared a refuge for flora and fauna, and later was recategorized as a marine park, with an area of 11,987 ha (Anonymous, 1998). The Parque Nacional Arrecifes de Cozumel (PNAC), its official name, extends from the north end of Paraíso reef (20°35´22˝N, 86°43´46˝W) to the southernmost tip of the island, and then continues north as far as Punta Chiqueros on the island’s windward side (20°16´11˝N, 86°59´26˝W; Fig. 1). Field Work.—Data for this study were obtained through a biannual monitoring program conducted in spring and autumn by PNAC as part of the Mesoamerican Barrier Reef System monitoring program (Almada-Villela et al., 2003). To evaluate the status of the reefs before and after the hurricanes, six linear barrier reefs were visited on the west side of the PNAC: Paraiso, Chankanaab, Yucab, Paso del Cedral, Palancar, and Colombia (Fig. 1). Three surveys were carried out: (1) before the hurricanes (May 10 to June 8, 2005); (2) one week after Hurricane Emily (July 25 to August 8, 2005); and (3) three weeks after Hurricane Wilma (14–23 November, 2005). At each site, four to six 30-m transects were randomly located between 10 and 15 m depth on the top of the frontal reefs and parallel to the coast (n = 108 for the study). The sites were georeferenced to ensure that the surveyed area (~1000 m2) was the same for each survey. To evaluate coral abundance, we used the point intercept method which records the percentage of benthic components in 30-m line transects, with identification of coral genus or species every 25 cm along the transect (120 points per transect).

ÁLVAREZ-FILIP ET AL.: HURRICANE IMPACTS ON COZUMEL REEFS

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Figure 1. Geographical location of the study sites. PA-Paraíso, CHA-Chankana´ab, YU-Yucab, PC-Paso del Cedral, PAL-Palancar, COL-Colombia. Continuous line delimits the Parque Nacional Arrecifes de Cozumel. Data Analysis.—Richness and abundance were directly calculated from field data, and cover was then used to calculate the following ecological indices: Shannon-Wiener diversity (H´ log e), Pielou evenness (J´), and taxonomic distinctness (Δ*) (Krebs, 1999; Clarke and Warwick, 2001). Although the use of Δ* in the analysis of coral ecosystems is still limited (Brown et al., 2002), the index has been successfully applied in aquatic communities and has considerable potential for environmental assessment and conservation (Graham et al., 2006). Oneway ANOVA was used to analyze transect data and detect statistically significant differences among periods (before the hurricanes, after Emily, and after Wilma). Kolmogorov-Smirnov and Levene tests were used to determine if the data were normal and homoscedastic, and when ANOVA assumptions were not met, the non-parametric Kruskal-Wallis analysis was used to make comparisons. When the null hypothesis was rejected, the Tukey and Nemenyi test (non parametric) were applied to determine which periods differed (before hurricanes, after Emily, and after Wilma; Zar, 1999). Changes in coral community composition were assessed using non-metric multidimensional scaling (nMDS), based on a similarity matrix of all transects constructed with Euclidian distance (Clarke and Warwick, 2001). Finally, the goodness-of-fit tests (χ2) were used to show if relative abundance of individual coral genera varied between successive periods. In this case, the expected values of coral cover per genus after each hurricane were calculated as if their coral losses were proportional to the average loss of the entire community.

Results General Observations.—A total of 15 genera and 23 species of coral were found in the surveys (Table 1). Live coral cover in Cozumel was 24.4 ± 1.4% (mean ± SE) in May 2005. After the impact of Hurricane Emily, reef coral cover decreased to 17.7 ±

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Table 1. Mean cover (± SE) of all coral species registered on Cozumel reefs in each period. Acropora cervicornis (Lamarck, 1816) Agaricia agaricites (Linnaeus, 1758) Agaricia lamarcki Milne-Edwards and Haime, 1851 Agaricia tenuifolia Dana, 1846 Colpophyllia natans (Houttuyn, 1772) Dendrogyra cylindrus Ehrenberg, 1834 Diploria clivosa (Ellis and Solander, 1786) Diploria labrinthiformis (Linnaeus, 1758) Diploria strigosa (Dana, 1846) Eusmilia fastigiata (Pallas, 1766) Isophyllastrea rigida (Dana, 1846) Madracis decactis (Lyman, 1859) Meandrina meandrites (Linnaeus, 1758) Millepora alcicornis Linnaeus, 1758 Montastraea annularis (Ellis and Solander, 1786) Montastraea cavernosa (Linnaeus, 1767) Montastraea faveolata (Ellis and Solander, 1786) Mycetophyllia lamarckiana Milne-Edwards and Haime, 1848 Porites astreoides Lesueur, 1816 Porites porites (Pallas, 1766) Siderastrea radians (Pallas, 1766) Siderastrea siderea (Ellis and Solander, 1786) Stephanocoenia michelini Milne-Edwards and Haime, 1848

Before – 6.08 (0.67) 0.15 (0.08) 3.12 (0.66) – – 0.09 (0.05) 0.03 (0.03) 0.25 (0.13) 0.68 (0.13) 0.09 (0.05) – 0.40 (0.16) 0.15 (0.06) 0.52 (0.30) 1.14 (0.24) 1.42 (0.44) 0.09 (0.05) 1.45 (0.23) 7.99 (1.26) 0.03 (0.03) 1.67 (0.28) 0.06 (0.04)

Emily 0.03 (0.03) 4.95 (0.36) 0.03 (0.03) 2.02 (0.49) 0.05 (0.04) – 0.10 (0.05) 0.08 (0.04) 0.03 (0.03) 0.43 (0.11) 0.05 (0.04) 0.18 (0.06) 0.23 (0.08) 0.15 (0.06) 1.79 (0.41) 1.19 (0.20) – 0.08 (0.04) 1.69 (0.22) 2.42 (0.49) – 1.69 (0.24) 0.13 (0.05)

Wilma – 3.92 (0.42) – 0.13 (0.09) 0.08 (0.08) 0.03 (0.03) – 0.03 (0.03) 0.03 (0.03) 0.24 (0.07) 0.08 (0.04) 0.03 (0.03) 0.35 (0.12) 0.19 (0.07) 0.51 (0.20) 0.94 (0.17) 0.48 (0.21) 0.05 (0.04) 1.29 (0.24) 0.54 (0.17) – 1.61 (0.21) 0.13 (0.06)

0.9% (mean ± SE), and after Wilma, coral cover diminished to a low of 10.8 ± 0.6% (mean ± SE; Fig. 2). This represented a reduction of 27% in coral cover from May to July, and a total reduction of 56% between May and November. The Kruskal-Wallis and the posteriori tests showed significant differences in coral cover between each of the three sampling periods (H2,108 = 49.53, P < 0.001; Fig. 2). Community Structure.—The mean number of coral species decreased significantly after Hurricane Wilma (F2,90 = 10.54, P < 0.01; Fig. 3A). Although the ShannonWiener diversity index (H´) appeared to decrease after Hurricane Wilma, this was not significant (F2,90 = 2.90, P = 0.059; Fig. 3B). Similarly, evenness (J´) appeared to increase after each disturbance, but this was not significant (F2,90 = 2.37, P =0.098; Fig. 3C). Taxonomic distinctness (Δ*) increased significantly after Wilma (F2,90 = 3.36, P = 0.039; Fig. 3D). The nMDS indicated a directional change in coral community composition. Records from before the hurricane season (May) were widespread and did not show a clustered arrangement in the ordination, indicating distinct differences among the surveyed sites (Fig. 4). After the passage of Hurricane Emily, there was a small decrease in the dispersion of the points (homogenization in the relative abundance of the species). After the passage of Hurricane Wilma, points were clustered tightly, a pattern distinct from that of the previous survey periods. These results demonstrate that the succession of hurricanes in 2005 caused a homogenization of coral community structure at Cozumel (Fig. 4).


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Figure 2. Live coral cover (mean ± SE) at Cozumel during each of the analyzed periods: Before = before hurricane season (May 2005); Emily = after Hurricane Emily (July 2005); Wilma = after Hurricane Wilma (October 2005).

Figure 3. Average values of community structure indices (mean ± SE) before the hurricane season, after Hurricane Emily (July, 2005), and after Hurricane Wilma (October, 2005): (A) species richness (S); (B) Shannon-Wiener diversity (H´); (C) Pielou evenness (J´); and (D) taxonomic distinctness (Δ*).

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Figure 4. Two-dimensional nonmetric-MDS based on standardized Euclidian distance showing the coral community composition in 108 transects during the three surveyed periods. Before = before hurricane season (May 2005); Emily = after Hurricane Emily (July 2005); Wilma = after Hurricane Wilma (October 2005).

Cover Coral at Genus Level.—In May of 2005, Agaricia and Porites were the dominant coral genera, each with a mean absolute cover of > 9%; together, these genera represented 74% of the total relative cover in the park. Next in abundance were Montastraea and Siderastrea with 2.8 ± 0.4% (mean ± SE) and 1.7 ± 0.2% (mean ± SE) absolute cover, respectively, while nine other genera had < 1% cover (Fig. 5). After Emily, total live coral cover decreased by almost one third, although the rank order of the seven most common coral genera was almost the same in relation to May 2005. Porites was much more affected than Agaricia, as its abundance was reduced by nearly 50% after the first hurricane. After Wilma, Agaricia had lost over 50% of its original cover, while Porites had lost about 80% of its cover. By November, the order of dominant species had changed, with Porites becoming the third most common genus, after Agaricia and Montastraea. In the case of Montastraea, cover was relatively stable between May and July–August 2005 and then decreased from ~3% to ~2% after Wilma in October (Fig. 5). Although live coral cover decreased significantly after each hurricane (Fig. 2), the goodness of fit test demonstrated that there were no significant differences in relative abundances of the complete set of genera between subsequent periods (May to Emily: χ2 = 1.63, df = 13, P = 0.990; Emily to Wilma: χ2 = 1.36, df = 14, P = 0.990); indicating that hurricane-induced damage occurred uniformly across most coral genera. However, Agaricia and Porites were noticeably more affected than other genera (Table 2). Total coral cover by poritids was 2% and 1% less than expected after Emily and Wilma, respectively, and cover by agaricids was 0.25% lower than expected. At the same time, Montastraea and Siderastrea were the most resistant genera, as their total abundance was higher than expected after both events. Discussion Hurricanes have significant immediate impacts on coral reefs, changing community structures by affecting recruitment, predation, and competition (Nyström and


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Figure 5. Coral cover (mean ± SE) for the different genera recorded in the periods (A) before hurricanes; (B) after Hurricane Emily; and (C) after Hurricane Wilma.

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Table 2. Differences between observed and expected frequencies of coral cover after hurricanes impact, according to the goodness-of-fit test (χ2). Acropora Agaricia Colpophyllia Dendrogyra Diploria Eusmilia Isophyllastrea Madracis Meandrina Millepora Montastraea Mycetophyllia Porites Siderastrea Stephanocoenia

Emily 0.01 0.50 0.06 0.00 0.01 0.01 0.01 0.16 −0.08 −0.05 1.05 0.02 −2.13 0.39 0.07

Wilma 0.01 −0.22 0.01 0.02 0.11 −0.04 0.04 −0.08 0.20 0.10 0.21 0.01 −0.95 0.55 0.04

Folke, 2001). These disturbances also contribute to the dynamic character of coral reefs and enhance the maintenance of ecosystem functioning in resilient systems (Carpenter et al., 2001; McClanahan et al., 2002). Gardner et al. (2005) reported that coral cover in the Caribbean was reduced by 17%, on average in the year following a hurricane, and they did not find evidence of reef recovery in the first 8 yrs after the disturbance. In the present study, the lost of coral cover (i.e., 56% in < 5 mo) was much greater than that predicted by the metanalyses carried out by Gardner and collaborators, possibly due to the strength of the two hurricanes that struck the island. For the Caribbean basin, few studies have reported such dramatic declines as that reported here. Woodley et al. (1981) demonstrated that Hurricane Allen destroyed 99% of Acropora corals, 23% of the foliaceous and encrusting Agaricia corals, and only 9% of the massive Monstastraea colonies. While Mah and Stearn (1986) reported a decline from 33% to approximately 10% coral cover in Barbados reefs, which represented 70% total loss of cover, they indicated that Porites porites was the most affected species. However, both studies were describing shallower reefs than those reported here. In the only previous study that addressed the impact of a tropical storm in Cozumel, a decline from 26.5% to 15.6% was observed in average coral cover after Hurricane Gilbert in 1988 (Fenner, 1991). Gilbert, therefore, had a more destructive effect than either of the separate effects of Emily and Wilma (Fig. 2). However, the overall damage to coral cover caused by the combined effect of both 2005 hurricanes is one of the most severe caused by tropical Caribbean storms over a short period of time. In the present study, coral cover before the passage of the hurricanes (May, 2005) was about 25%. Between Hurricane Gilbert in 1988 and Emily in 2005, Cozumel did not experience any strong hurricane impacts (Hurricane Roxana struck the area in 1995 but without severe consequences). This suggests that the time needed for recovery of coral cover from hurricanes, without the influence of major anthropogenic stressors (e.g., coastal development, fisheries), may be less than two decades.


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The effects of hurricanes on coral reef diversity are complex and sometimes contradictory (Rogers et al., 1983). The intermediate disturbance hypothesis (Connell, 1978) predicts that intermediate intensities of disturbance produce the highest diversity and high intensity disturbances produce lower levels of diversity (Rogers, 1993; Hacker and Gaines, 1997). The pattern of decrease in the number of species following a high magnitude disturbance appears to apply to coral diversity in Cozumel reefs, caused principally by the intense impact of Hurricane Wilma. However, in this study, the diversity and evenness indices did not show significant changes after perturbations as they did in other studies (Rogers et al., 1983). Taxonomic distinctness, a reliable index for detecting variations in community organization after a disturbance (Warwick and Clarke, 1998), did show an increase in the distance of the taxonomic hierarchies among coral species after the passage of Hurricane Wilma. Because the identity of the species recorded in the study did not vary greatly among surveys (Table 1), the increase in value of the index is associated with a homogenization of relative abundance among higher taxa (genera or families), as suggested by Warwick and Clarke (2001). In our case, some of the dominant species, in particular Agaricia and Porites spp. had their numbers depleted, while at the same time, the cover of other genera such as Siderastrea and Montastraea, did not vary much. These findings illustrate that the hurricanes caused a restructuring of the relative abundances of coral at higher taxonomic levels, but did not affect qualitative species composition. It seems that the mechanism how Δ* increased at Cozumel was a combination of a lowered coral cover of the dominant species with a concomitant rise in relative abundance of the subordinate ones. Ordination analysis (nMDS) of the spatial pattern in community structure showed a unidirectional decrease in variance after the hurricanes, especially after Wilma. Other studies (e.g., Bythell et al., 1993; Brown et al., 2002) documented breakdowns in multivariate patterns of coral communities due to local/regional disturbances. Bythell et al. (1993) found shifts in the community structure detected by nMDS dissimilarity measures but not by the Shannon diversity statistic (H´), similar to our results. Branching and foliose corals, such as some Porites and Agaricia species, suffered the greatest damage from the 2005 hurricanes, coinciding with the general view that branching corals are more susceptible to hurricane damage than massive species (Woodley et al., 1981; Lugo et al., 2000). According to Fenner (1991), Porites porites forma furcata, Agaricia tenuifolia, and Madracis mirabilis, were the Cozumel species most affected by Hurricane Gilbert. Before the 2005 hurricane season, the former two species were widely abundant in the reefs; however, M. mirabilis was fairly uncommon during our reef surveys as well as elsewhere on the west coast of the PNAC (PNAC, unpubl. data). This empirical observation needs to be studied further; however, it suggests that while overall coral cover can recover after a disturbance, species composition may change over the long term. The abrasion, erosion, fracture, and death caused by Hurricane Wilma exposed large amounts of substratum, thereby greatly increasing the surface available for recruitment and growth of sessile organisms. Branching corals may play a critical role in the reestablishment of coral communities after destruction by being rapid colonizers (Fenner, 1991; Bythell et al., 1993; Hughes and Connell, 1999). Disturbances that have intensities low enough to leave significant amounts of branching corals may allow reefs to recover rapidly, as reported previously (Stoddart, 1974; Fenner,

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1991; Jordán-Dahlgren, 1992). Such destructive disturbances have damaging effects on corals over short time scales, yet are predicted to prevent competitive exclusion of species and help to maintain typical diversity of coral reef community structure (Connell, 1978). Due to the decrease of dominant corals in Cozumel, the coral community had a more homogeneous composition after the hurricanes. However, there were no significant differences among genera. Agaricia was the most abundant genus in all three surveys, but after Wilma, Porites and Montastraea shifted places in rank abundance. These findings are consistent with simulation models (Andres and Rodenhouse, 1993), that demonstrated that due to high numbers of larval recruits and high individual growth rates, Agaricia agaricites displayed the highest resilience following storms of various frequencies and intensities. Coral reefs are subject to many types of stressors simultaneously, and the influence of these stressors are likely synergistic rather than additive (Hughes and Connell, 1999). In the past three decades, Caribbean reefs have suffered a massive live coral cover decline (Gardner et al., 2003) and shifts from coral-dominated to fleshy algaedominated ecosystems (Jackson, 1991; Hughes, 1994). Contrary to those reports, for almost 20 yrs, Cozumel reefs have been relatively healthy and have showed their capability to recover from disturbance and to cope with the increase in coastal uses. However, more intensive and frequent physical disturbances, combined with the dramatic increase of urbanization and tourist development projected for the island and elsewhere in the Mexican Caribbean, could potentially overwhelm the natural resilience of Cozumel’s coral reefs (Nyström and Folke, 2001; Bellwood et al., 2004; Adger et al., 2005). Acknowledgments We thank G. Nava, O. Olingard, and the staff of the Parque Nacional Arrecifes de Cozumel (PNAC) for their invaluable help during the surveys. This project was partially funded by the PNAC, the project SEMARNAT-2004-C01-00108 (to H.R.B.) and the CONACYT (171864) and SEP scholarships to L.A-F. The manuscript was improved through the comments of two anonymous reviewers and S. Palminteri kindly proofread the English version.

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