<I>Cenchritis Muricatus</I>

BULLETIN OF MARINE SCIENCE, 84(3): 307–313, 2009

E fFECTS of disturbance on Cenchritis muricatus (beaded periwinkle) populations on small islands in the Bahamas

Jonah Piovia-Scott

ABSTRACT D isturbance can have multiple impacts on shoreline gastropods. This study compares populations of a common supralittoral snail on islands in exposed and protected areas; the former are subject to much more disturbance from wave action and storm surges. Cenchritis muricatus (Linnaeus, 1758) density was six times higher on protected islands than on exposed islands, representing 2.5 times more biomass. Contrary to expectation, individuals were larger on exposed islands than on protected islands (mean lengths were 26.1 mm and 20.0 mm, respectively); this difference was primarily explained by a significant negative relationship between body size and density coupled with the fact that exposed islands had lower densities. I suggest that periodic large disturbances and oceanographic processes associated with dispersal limit the abundance of C. muricatus on exposed islands, and that larger sizes on exposed islands were probably due to enhanced growth caused by reduced intraspecific competition.

D isturbance can have profound impacts on ecological communities (Sousa, 1984; Pickett and White, 1985). These impacts have been particularly well-studied in shoreline ecosystems where disturbance, usually in the form of wave action, affects a wide variety of taxa (Dayton, 1971; Paine and Levin, 1981; Underwood, 1999; Walker et al., 2008). Gastropods are a common component of most shoreline ecosystems, and disturbance can affect gastropods both directly, by inhibiting settlement (Crisp, 1955; Sousa, 1979; Bushek, 1988; Pawlik and Butman, 1993) or dislodging individuals from the substrate (Boulding and van Alstyne, 1993; Trussell, 1997), and indirectly, by removing predators (Menge and Sutherland, 1976; Menge, 1978), competitors (Steffani and Branch, 2003a,b), or facilitators (Underwood, 1999). These direct and indirect effects can lead to either increased (Underwood and McFadyen, 1983; Brown and Quinn, 1988) or decreased (Menge and Sutherland, 1976; Boulding and van Al- styne, 1993) abundance in exposed sites. In contrast, there is a relatively consistent tendency for conspecific individuals to be smaller at exposed sites than at protected sites (e.g., Emson and Faller-Fritsch, 1976; Etter, 1989; Richardson and Brown, 1990; Trussell, 1997), a pattern usually attributed to increased susceptibility to dislodge- ment with size (Denny et al., 1985; Trussell et al., 1993) or changes in foraging behavior that limit growth rate at exposed sites (Etter, 1996). This study examined the effects of disturbance on the abundance, size, and biomass of a common supralittoral gastropod by surveying populations on exposed and protected islands. The Exuma Cays in the central Bahamas (Fig. 1A) represent an ideal system for studying the effects of disturbance. Small islands in close physical proximity experience very different disturbance regimes. Islands located in “creek” areas are sheltered from high wind and wave action, whereas islands outside of these sheltered areas are not. Exposed islands are also more affected by periodic large storms (Spiller et al., 1998), and the eyes of four hurricanes have passed within 130 km of the study sites in

Figure 1. Map of the study location in (A) Exuma Cays, the Bahamas indicating protected islands P and exposed islands E, (B) near Staniel Cay and (C) Great Exuma. the decade prior to this study (Hurricanes Lili 1996, Floyd 1999, Michelle 2001, and Frances 2004). The littorinid snail Cenchritis muricatus (Linnaeus, 1758) is the most abundant supralittoral gastropod on small islands in the Exuma Cays (pers. obs.). Cenchritis muricatus is common throughout the Caribbean, South Florida, and the Bahamas (Clench and Abbott, 1942; Abbott, 1954; Trussell, 1997), where it is distributed from the waterline up to at least 3.6 m in vertical height and 28 m in horizontal distance from the water’s edge (Lang et al., 1998; Emson et al., 2002). Organisms in this supralittoral fringe habitat are thought to be regulated chiefly by abiotic factors (Vermeij, 1972a; Lang et al., 1998). I explored the effect of disturbance on C. muricatus by examining its abundance, size, and biomass on exposed and protected islands at two study sites in the Exuma Cays.

Materials and Methods

Study System.—This study was conducted in the Exuma island chain in the central Baha- mas (Fig. 1A) in September and October 2005. I surveyed 16 small islands (480–3033 m2) for C. muricatus, which inhabited all parts of each island. Eight islands were located near Staniel Cay, five of these were in “creek” areas protected on both sides by larger islands and three were on the exposed west side of the island chain (Fig. 1B). One of the exposed islands was a narrow peninsula of a slightly larger island. The remaining eight islands were located 100 km to the southwest, near Great Exuma. Four of these were on the exposed south side of the island while the other four were in a protected harbor on the north side (Fig. 1C). Sampling.—I surveyed C. muricatus populations on each island by counting and measur- ing all C. muricatus in circular plots with an area of 0.1963 m2 (0.25 m radius). Between 25 and 50 plots were distributed systematically on each study island using transects. First, I es- poviacotti -s : effect of disturbance on beaded periwinkles 309 tablished a primary transect across the longest axis of the island, beginning and ending at the high water line; I then established secondary transects perpendicular to the primary transect at regular intervals. Sampling plots were established at 2 m intervals along the secondary transects, starting 1 m from the high water line. I adjusted the spacing between secondary transects in order to sample a similar number of plots on each island. Cenchritis muricatus density was calculated as the mean number of individuals per plot on each island. Body size was measured as the length along the longest axis of the shell; I used the average length of sampled individuals on an island for analyses. The relative biomass of each individual was the cube of the height, which is proportional to the dry tissue mass (Borkowski, 1974); I calculated biomass as the mean relative biomass per plot on each island. Analysis.—Differences between exposed and protected islands in C. muricatus density, mean length, and biomass were analyzed using ANOVA, with exposure and study site as predictors. Protected islands and exposed islands did not differ in mean area (t-test:P = 0.77) or mean perimeter-to-area ratio (t-test: P = 0.63). I analyzed the effect of density on size using linear regression. All models were consistent with assumptions of homogeneity of variances and normality of residuals. Analyses were conducted using PROC GLM in SAS v 8.0 (SAS Institute, 1999).

Results

The number of snails counted and measured per island ranged from 2 to 432. There were significant differences inC. muricatus density, average length, and biomass between exposed and protected islands. Protected islands had six times more individuals per plot than exposed islands (ANOVA: F1,13 = 5.95, P = 0.030; Fig. 2A). Average C. muricatus length was greater on exposed islands (26.1 mm) than on protected islands (20.0 mm) (ANOVA: F1,13 = 11.65, P = 0.005; Fig. 2B). Average biomass per plot was 2.5 times larger on protected islands (ANOVA: F1,13 = 6.97, P = 0.020; Fig. 2C).

There was a negative relationship between mean shell length and mean density (F1,14 = 38.36, P < 0.001; Fig. 3). This pattern was also evident on protected islands alone

(F1,7 = 33.46, P < 0.001), but was not significant on exposed islands (F1,5 = 4.56, P = 0.086), although the trend was in the same direction.

Discussion

Cenchritis muricatus had higher densities and higher biomass on protected islands than on exposed islands, indicating that exposure to disturbance limits snail density and biomass. Individuals on exposed islands were larger than those on protected

Figure 2. Cenchritis muricatus on protected (n = 9) and exposed (n = 7) islands: (A) Mean (± SE) number of individuals per plot, (B) mean (± SE) shell length of all measured individuals on an island, and (C) mean (± SE) biomass per plot. 310 BULLETIN OF MARINE SCIENCE, VOL. 84, NO. 3, 2009

Figure 3. Mean Cenchritis muricatus shell length and mean density per plot on protected (closed symbols) and exposed (open symbols) islands. Squares represent islands near Staniel Cay and circles represent islands near Great Exuma. Linear regression line is shown (R2 = 0.73). islands, but this effect may be explained primarily by the fact that these islands had lower densities. Since exposed islands have lower densities but larger individuals, the difference in biomass between protected and exposed islands is not as great as the difference in density. Four processes could contribute to the observed differences in C. muricatus density, size, and biomass between exposed and protected islands: (1) removal by disturbance, (2) recruitment limitation, (3) intraspecific competition, and (4) predation. Interspecific competition is unlikely to be important, as C. muricatus is the only mollusc that regularly occurs over 1 m inland from the high water line on the study islands (pers. obs.). While other processes, such as parasitism, could be important, I do not have sufficient evidence to address them here. Exposed islands experience higher levels of erosive wind and wave action in the supralittoral zone (L. Yang, University of California-Davis, pers. comm.) and tend to be more affected by periodic large storms (Spiller et al., 1998). These large storms cre- ate high wave action and storm surges, and their combined effects can scour exposed shoreline habitats. This sort of mechanical disturbance may reduce C. muricatus abundance by dislodging individuals from the substrate and washing them off an island. Previous studies have found that, under normal conditions, areas with higher wave action do not have lower C. muricatus abundances than areas with lower wave action (Minton and Gochfeld, 2001). However, a dramatic decline in C. muricatus abundance was observed following a hurricane that struck the Exuma Cays in 1995 (Emson et al., 2002). Thus, it is likely that differences in C. muricatus are not due to chronic wind and wave action but rather to major storm disturbance. Recruitment limitation, although not measured in this study, could account for lower C. muricatus densities on exposed islands. Differences in recruitment between poviacotti -s : effect of disturbance on beaded periwinkles 311

exposed and protected islands could be due to differences in the availability or delivery of larvae (Porri et al., 2006). The availability of larvae is expected to be higher in protected areas due to a greater density of spawning individuals coupled with greater potential for the retention of locally produced larvae (Swearer et al., 2002). Larval retention will occur to the extent that protected creek areas are hydrographi- cally isolated from surrounding waters (McQuaid and Phillips, 2006). Furthermore, higher wave action at exposed sites has the potential to decrease the rate of attach- ment of larvae to the substrate by creating more turbulence (Crisp, 1955; Levin, 1983; Bushek, 1988; Pawlik and Butman, 1993). While the reduced abundance of C. muricatus on exposed islands is consistent with expectations, the larger size of periwinkles on exposed islands is not. Hydrodynamic forces, including those associated with large storms, tend to remove gastropods with larger shells (Denny et al., 1985; Etter, 1989; Trussell, 1997). While some individuals may protect themselves from these forces in rock crevices or other shelters, significant portions of the population are exposed to wave action (Lang et al., 1998, pers. obs.). Thus, if disturbance causes higher mortality on exposed islands by dislodging individuals, as hypothesized above, mean size is expected to be smaller, not larger. The tight relationship between density and average size suggests that intraspecific competition may play an important role in the size structure of C. muricatus populations. Lower densities on exposed islands may lead to higher resource availability, which could in turn cause snails to grow faster (Petraitis, 2002) and attain larger sizes. Exposed sites may also provide greater feeding opportunity (Clench and Ab- bott, 1942), which could enhance growth rates. However, the relationship between density and size also holds true among only protected islands, indicating that density plays an important role in determining size structure even on islands where feeding opportunities are expected to be similar. Thus, low conspecific density clearly plays a role in allowing individuals on exposed island to grow larger, and enhanced feeding opportunities may contribute to the larger sizes attained on exposed islands. Predation also has the potential to decrease densities on exposed islands. However, predation by crabs, which are often important predators of littorines, tends to be more intense at protected sites than at exposed sites (Menge and Sutherland, 1976; Menge, 1978; Trussell, 1997). This would lead to lower densities at protected sites, the opposite of what was observed in this study. Thus, predation is unlikely to be involved in generating the observed patterns of C. muricatus density. In summary, abiotic factors are generally thought to be more important deter- minants of population characteristics in the supralittoral fringe than biotic factors (Vermeij, 1972b; Lang et al., 1998). While periodic large disturbances and oceanographic processes associated with dispersal may limit the abundance of C. muricatus on exposed islands, the tight relationship between abundance and average size suggests that intraspecific competition may also play an important role in structuring populations of this species.

Acknowledgments

I thank D. Spiller for support in the planning and conduct of the research and the prepara- tion of this manuscript, the Bahamas Ministry of Agriculture and Fisheries for permission to conduct the research, the UC Davis Center for Population Biology for funding, and A. Wright, L. Yang, K. Aquilino, T. W. Schoener, and two anonymous reviewers for helpful comments. 312 BULLETIN OF MARINE SCIENCE, VOL. 84, NO. 3, 2009

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Date Submitted: 14 July, 2008. Date Accepted: 20 March, 2009. Available Online: 6 April, 2009.

Address: Center for Population Biology, University of California, One Shields Avenue, Davis, California 95616. E-mail: .

&lt;I&gt;Cenchritis Muricatus&lt;/I&gt;

<I>Cenchritis Muricatus</I>