*Dirección para correspondencia:

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Abstract

Populations of the common sea fan (Gorgonia ventalina) were decimated by an aspergillosis outbreak throughout the Caribbean two decades ago. Since then, aspergillosis has been considered as the principal cause of mortality in sea fans. However, prevalence and presumably incidence of this disease have been declining in the Caribbean since the mid 1990s. Incidence indicates new ]]>

Key words: Gorgonia ventalina, disease, prevalence, mortality, Caribbean, sea fans.
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Resumen

Las poblaciones de abanicos de mar (Gorgonia ventalina) fueron diezmadas por una epidemia de aspergilosis que afectó gran parte del Caribe, hace más de dos décadas. Desde entonces, a la aspergilosis se le ha considerado ]]>

Palabras clave: Gorgonia ventalina, aspergilosis, prevalencia, mortalidad, abanicos de mar, Caribe.

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Mass mortality of sea fans, especially of Gorgonia ventalina (Linnaeus, 1758) populations, occurred throughout of the Caribbean during the 1980s-1990s (Guzmán & Cortés 1984, Garzón-Ferreira & Zea 1992, Nagelkerken et al. 1997). Since then, the ]]> et al. 2006, Mullen et al. 2006, Toledo-Hernández et al. 2007); and the  identification for the causative agent(s) of this disease (Smith et al. 1996, Toledo-Hernández et al. 2008, ]]> et al. 2010). Most studies of sea fans around the Caribbean have shown aspergillosis as an important cause of colony mortality (Kim & Harvell 2004, Mullen et al. 2006, Nugues & Nagelkerken 2006). However, given that prevalence and presumably incidence have been declining in the Caribbean since the mid 1990s (Kim & Harvell 2004, Bruno et al. 2011), other causes of mortality such as detachment, fracture of the ]]> et al. 1981, Yoshioka & Yoshioka 1991). In fact, disease can be better understood as interacting with other causes of colony mortality (Toledo et al. 2008), with their relative contribution varying spatially and temporally with habitat. For example, areas with high wave energy such shallow areas in the fore reef should experience high mortality due to detachment (Birkeland 1974).

The demography of gorgonians is strongly size-dependent. Sites subjected to horizontal bedload movement can experience high mortality of small colonies due to smothering by sediments (Yoshioka & Yoshioka 1989, Yoshioka 1994). High mortality of small sea fan colonies can also be expected in sites with high disease incidence, since disease mainly kills small colonies (Toledo-Hernández et al. 2009). ]]>

In this study, we followed 448 colonies for one year to evaluate differences in disease incidence and prevalence, and in factors causing mortality across these reefs, ]]>

]]> Materials and methods

Study sites: The study was carried out at six reefs in Puerto Rico: Culebrita (CB), Vieques (VI), Humacao (HU), Icacos (IK), Piñeros (IP) and Jobos (JO) (Fig. 1) between September 2006 and September 2007. The study sites can be classified as ]]> et al. 2001). Most reefs had moderate water transparency, with the exception of JO which showed poor water quality with high sedimentation and low transparency.

Sea fan monitoring: Three transects ]]> G. ventalina was numbered with an aluminum tag nailed near its base, photographed and its height measured to the nearest cm. Transects were monitored at six months intervals. The health status of each colony was recorded by examination of the photographs. We defined healthy colonies as those with no lesions, purple spots or overgrowth of fouling organisms. Diseased colonies were defined as those with an active disease lesion as described for aspergillosis: a necrotic area surrounded by a purple halo (Petes et al. 2003). Colonies with purple spots were those with no necrotic tissue, and having few or numerous small purple spots. Fouled colonies were those showing fouling organisms such as algae or fire corals colonizing the blade. Predated colonies were those showing predation marks by Cyphoma gibbossum. Colonies were also divided into three height classes: small (<20cm), médium (20-50cm), and large (50-90cm). Differences in colony density and size (height) among reefs ]]>

Incidence and prevalence of disease: Incidence indicates new cases of disease in previously healthy colonies, while prevalence indicates percent of diseased colonies at a ]]> et al. ]]> et al. 2002, Mullen et al. 2006), we also analyzed prevalence of diseased colonies adding colonies with purple spots in order to compare prevalence levels with the previous literature.

Mortality of sea fans: Mortality was categorized as caused by: (1) disease when 100% of the colony area ]]> Millepora spp.), or other fouling organisms. Chi square analyses were used to test for differences in the causes of mortality among sites and size classes.

Results

A total of 448 colonies of G. ventalina were tagged in the studied reefs. Colony density differed among reefs (Kruskal-Wallis test, H=23.47, p=0.0003, Fig. 2), with Icacos (IK) showing the highest density (6 colonies m^-2±16.25 SE), while, Humacao (1.53 colonies m^-2±0.66 SE), and ]]> -2±2.60 SE) the lowest. Median colony height differed significantly among reefs, (Kruskal-Wallis test, H=233.079, p<0.001), with Icacos being dominated by small colonies (<20cm), and Humacao and Culebrita by large ones (Fig. 3). A posteriory test for colony height showed Icacos as significantly different from the other reefs, except Vieques; it also showed that Humacao and Culebrita differed significantly from Icacos and Vieques. ]]>

Prevalence and Incidence of disease: Healthy sea fans were the most common state at all reefs (Table 1).  Colonies with aspergillosis and purple spots were observed at similar proportions (Table 2). Injuries caused by predation and overgrowth by Millepora were rarely observed. No significant ]]> Table 2). Disease prevalence (strict definition) varied between 0%-32%. However, this variability was not significantly different (repeated measure ANOVA, prevalence by reef: df=5, F=0.90, p=0.51; by time: df=2, F=1.39, p=0.26; interaction time-reef: df=10, F=1.26, p=0.30). The same tendency was observed among size clases (χ²=3.72, df=2, p=0.15). If colonies with purple spots are pooled with diseased colonies, prevalence increases from 3.45%-32.7% ( Table 3). Although, this difference in prevalence was not significant among sites, it was significant among size classes (Table 2). The incidence of lesions characterized as aspergillosis was very low, with only eight new cases between the first and second census, and five between the second and third census (Table 4).

Mortality: 74 of 448 colonies (16.5%) died during the study period.  Probability of death varied among reefs (χ²=39.8, df=5, p<0.001) and  among size classes (χ²=22.1, df=2, p<0.001). Icacos experienced the highest mortality (29%) and Piñeros the least (0%). Small fans experienced proportionally higher mortality than the medium and large colonies. The main cause of mortality at all reefs was detachment, followed by disease lesions and overgrowth ( Table 5). The proportion of detachment varied significantly among reefs (χ²=35.4, df=5, p<0.001). Icacos experienced twice the expected number of detached colonies, while Jobos and Humacao showed the least. Significant differences were also found in the proportion of detached colonies among sizes (χ²=12.5, df=2, p=0.002). Small colonies detached proportionally more. Probability of detachment did not vary with the health state of the colony (χ²=3.56, ]]>

Discussion

Incidence and prevalence of aspergillosis: Measuring incidence and prevalence are important to ]]>

In our case, incidence of aspergillosis was very low among sites and through time. Thereby, we can infer that infection rate of aspergillosis was very low and no epizootic was occurring in these reefs. The low prevalence observed supports this inference. Prevalence was similar over time at each reef, with no spatial or temporal variation. In fact, there is a general ]]> et al. 2011). In the Caribbean, reports suggest geographical variability in the prevalence of aspergillosis. Prevalence of 8.4-22% has been reported for the Florida Keys (Kim & Harvell 2004), and in Venezuela and Bermuda of 10% 12.5% (Weil 2004). However, higher prevalences have been reported in Curacao with 52% (Nugues & Nagelkerken 2006), the Florida Keys with 42-58% (Jolles et al. 2002, Kim et al. 2006), and Yucatan ]]> et al. 2006). It is possible that part of the variation among these studies is explained by differences in the definition of disease. Tumors, purple spots and colonized tissue can be included within the definition (Petes et al. 2003, Nagelkerken et al. 1997) and sometimes what is considered as diseased colony is not defined. When we pooled colonies with purple spots with diseased ones, prevalence increased dramatically for most of ]]> et al. 2008).

Anthropogenic stressors such as elevated temperatures, high sedimentation rates, or low water quality can compromise the immune response of sea fan colonies and make them ]]> et al. 2003, Ward et al. 2007). Given that these factors can exhibit local differences, they may affect infection rate and virulence which may result in spatial variation in disease incidence or prevalence (Kim & Harvell 2004, Mullen et al. 2006, Nugues & Nagelkerken 2007, Ward et al. 2007). In Eastern Puerto Rico, low prevalence and incidence ]]> et al. 2011). However, temporal and spatial variability was found in Western Puerto Rico (La Parguera, Flynn & ]]> et al. 2010) maybe more important than anthropogenic stressors in determining disease ]]>

Effect of density and size structure of sea fans on disease: There are several studies that suggest disease prevalence is density dependent, because neighboring colonies can be more susceptible to infection (Nagelkerken et al. 1997, Jolles et al. 2002). However, our results do not support the conclusion ]]>

The observed spatial variability in sea fan abundance and size structure can be explained by the ]]>

Our results also suggest that spatial differences in size structure and density may be related to abiotic factors at the reef scale. Such as, although good water quality ]]>

Mortality in sea fans: Detachment was the main cause of mortality in sea fans in the studied reefs. Death of colonies by disease or injuries was rare. This is consistent with the low prevalence of disease found in the study sites. Detachment is considered one of the main causes of mortality in most species of gorgonians (Birkeland 1974, Yoshioka & Yoshioka 1991, Toledo-Hernández et al. 2009), and wave action is considered as the principal cause of detachment (Yoshioka & Yoshioka 1989). It also tends to be restricted to shallow water and exposed zones (Whale ]]>
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Health status did not affect the probability of detachment, but colony size did: small colonies were more susceptible. This result is consistent with Toledo-Hernández et al. (2009), who found high mortality in small sea fans especially healthy ones by detachment. Large colonies were less affected by detachment contrary to expectation. They should be more likely to detach due to increase in the drag-force resistance ]]> et al. 2003). In our study, the lower probability of detachment observed in large colonies could be explained by size refuge hypothesis. Sites with less energy (currents, waves), may promote growth to a large size; while sites with high energy will promote growth to a relatively smaller size. In general, sea fans are adapted to withstand high energy due to wave action or currents and they are mainly observed in the crest of the reefs. Another explanation, might be small scale variability in reef quality related to protection from high energy. In a reef with ]]>

In conclusion, sea fans populations from Eastern Puerto Rico are not currently affected by an epizootic. It ]]>
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Acknowledgments

This study was supported by grants from UPR Sea Grant (NOAA award NA16RG2278, project R-92-1-04 and NOAA award NA16RG2278, project R-R-92-2-08), NOAA-CRES program, NIH-SCORE Grant #S06GM08102, and NSF-CREST. Anabella Zuluaga-Montero thanks the ]]>
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*Correspondencia a: Anabella Zuluaga-Montero & Alberto M. Sabat: Department of Biology, University of Puerto Rico - Río Piedras, PO Box 23360, San Juan, Puerto Rico 00931-3360 USA; abzuluaga@gmail.com, amsabat@gmail.com
1. Department of Biology, University of Puerto Rico - Río Piedras, PO Box 23360, San Juan, Puerto Rico 00931-3360 USA; abzuluaga@gmail.com, amsabat@gmail.com

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