<I>Sphaeroma Terebrans</I>

BULLETIN OF MARINE SCIENCE, 76(1): 27–46, 2005

THE DISTRIBUTION AND ABUNDANCE OF SPHAEROMA TEREBRANS, A WOOD-BORING ISOPOD OF RED MANGROVE (RHIZOPHORA MANGLE) HABITAT WITHIN TAMPA BAY

R. Allen Brooks and Susan S. Bell

ABSTRACT This study was conducted to determine the distribution, abundance, and demog- raphy of a wood boring isopod, Sphaeroma terebrans Bate, 1866, within the prop roots of the red mangrove, Rhizophora mangle L., in eight sites within Tampa Bay, Florida. Sphaeroma terebrans in Tampa Bay displayed reproductive activity year- round and bay-wide synchrony in their density pattern. On average approximately 60% (range: 25%–86%) of the intertidal aerial roots surveyed were occupied by S. terebrans. Although infestation levels by S. terebrans in Tampa Bay were similar to that of more tropical regions, the distribution of S. terebrans was not continuous throughout the study sites. A substantially higher occurrence and density of S. terebrans was found in the northern compared to more southern study sites within the Bay. Additionally, some seemingly suitable areas of the bay (i.e., Pinellas Point, Skyway, Fort Desoto) were actually unoccupied on some dates. Although sites differed in the frequency with which roots were attacked, the density of burrows and isopods in an occupied root was similar, with most attacked roots containing 3–5 burrows. The results of a transplantation experiment indicated that neither abiotic factors nor substrate quality limit the burrowing capabilities or survival of adult S. terebrans in the areas where they are absent. Instead, dispersal limitation, linked with diﬀerential juvenile survival, most likely controls isopod distribution and abundance within Tampa Bay.

Sphaeroma terebrans (Bate, 1866), a wood boring isopod, is distributed worldwide in tropical mangroves (Estevez, 1978). Arguably, S. terebrans is not native to North and South America but was introduced from the Indo-Pacific when isopods bored into the hull of wooden shipping vessels (Carlton, 1994). Regionally, within North America, geographical surveys indicate that S. terebrans is distributed continuous- ly along both the east and west coast of Florida but, curiously, is not found in the Florida Keys (Conover and Reid, 1975; Rice et al., 1990). The isopod is found farther south, however, in the tropics of Central and South America (Ellison and Farnsworth, 1990). Local within-stand occupation by S. terebrans has been noted to be patchy with seemingly habitable areas unoccupied (Estevez, 1978). Abiotic differences in salinity, water temperature, dissolved oxygen, suspended solids, and flow have all been suggested to potentially influence the distribution of S. terebrans (Conover and Reid, 1975; Estevez, 1978; Barkati and Tirmizi, 1990). Ellison and Farnsworth (1990) and Ellison et al. (1996), also found that root fouling by sponges and colonial ascidians can impact isopod distribution. Sphaeroma terebrans exploits habitat created by mangrove prop roots and, in Florida, bores almost exclusively into unattached aerial roots of the red mangrove, Rhizophora mangle L. Once constructed, the burrow is used for 1) protection from both abiotic (exposure, desiccation) and biotic factors (Estevez, 1978); 2) filter-feeding activities (suspended sediment, algae, and bacteria; Rotramel, 1975; Rice et al., 1990); and 3) reproduction along with maternal care (Thiel, 1999). It is common to find inquilines (i.e., cohabiting amphipods, annelids, isopods) utilizing both occu-

Bulletin of Marine Science 27 © 2005 Rosenstiel School of Marine and Atmospheric Science of the University of Miami 28 BULLETIN OF MARINE SCIENCE, VOL. 76, NO. 1, 2005 pied and unoccupied burrows of S. terebrans (Estevez, 1978). The distribution of S. terebrans within a mangrove stand is limited to intertidal regions that are flooded on a regular tidal cycle (Estevez, 1978) and abundance cycles of S. terebrans have been linked with seasonal fluctuations in salinity, temperature, water cover, and food levels (Estevez, 1978). An understanding of the factors that impact mangrove root occupation by S. terebrans is important as the activity of this woodborer can have community-wide impacts. Isopod attack impacts the mangrove tree directly through root architectural changes (Simberloff et al., 1978; Ribbi, 1981), reduced root production, and increased root atrophy (Perry, 1988; Perry and Brusca, 1989; Ellison and Farnsworth, 1990). These changes to the root system not only alter support and nutrient provisioning for the tree but also may indirectly affect organisms that utilize the mangrove roots as either substratum (Sutherland, 1980; Rodriguez and Stoner, 1990; Bingham, 1992; Ellison and Farnsworth, 1992) or protective habitat (Primavera, 1997). Additionally, S. terebrans may have important economic impacts when in high abundance due to considerable damage to maritime structures (Rice et al., 1990; Cragg et al., 1999). This study expands upon the work of Estevez (1978) and addresses two main ques- tions regarding S. terebrans inhabiting prop roots of R. mangle within Tampa Bay: 1) Is the current distribution of S. terebrans continuous within the mangrove habitat of the Tampa Bay region, and if not, then what factors might explain the disjunct distribution?; and 2) Do abundances of S. terebrans differ among the mangrove stands in which they are found in Tampa Bay and, if so, can the differences be accounted for by the demographic features of fecundity, juvenile recruitment, or sex ratios?

MATERIALS AND METHODS

SITE SELECTION.—Eight sites around Tampa Bay (Fig. 1) were selected for study based upon their geographic range from the northern to southernmost part of the bay. All of the sites contained areas of continuous mangrove coverage dominated by red mangroves. Based upon abiotic information obtained from the Hillsborough County Ecological Protection Commission monitoring stations, northern sites on average experience a lower turbidity and salinity level but similar pH, dissolved oxygen, and water temperature compared to the more southern sites within the bay. Within each of the eight locations ten sampling points were haphazardly established along the seaward edge in the intertidal region. Each sampling point consisted of a single R. mangle tree that was tagged with forestry tape. PRESENCE/ABSENCE CENSUS.—Transect samples were utilized to determine the frequency of root attack by S. terebrans at all eight ﬁeld sites using a method similar to Ellison and Farn- sworth (1990). Roots were sampled to determine isopod density in October 1999, February 2000, and July 2000 at all sites. These speciﬁc months were selected as they encompassed times of both high and low isopod abundance (Estevez, 1978). All sites were sampled within 2 wks of each other. Eight transects, 25 m in length, were haphazardly placed parallel to the seaward edge of the mangrove habitat in each study site. Along each transect, 30 random points were selected for tallying of isopod presence/absence. At each random point along the transect the closest unattached aerial roots with one tip was selected for evaluation. An unattached root is a prop root originating from the bole, trunk, and other aboveground roots, which grows down through the water column and eventually attaches to the substratum (Gill and Tomlinson, 1977). Selected roots were located within 1 m of the seaward edge and sub- merged regularly at high tide. Isopod presence was noted if there was visible sign of burrowing activity along the root (≥ 1 burrow). BROOKS AND BELL: DISTRIBUTION AND ABUNDANCE OF SPHAEROMA TEREBRANS 29

Figure 1. The eight study sites around Tampa Bay. Abbreviations are as follows: UTB = Upper Tampa Bay, 4th = Fourth Street, WI = Weedon Island, CRB = Cockroach Bay, PP = Pinellas Point, SKY = Skyway, FD = Fort Desoto, and AM = Anna Maria Island. The distance between sites UTB and AM is 51 km. Map of Tampa Bay courtesy of the Florida Marine Research Insti- tute, Florida Fish and Wildlife Conservation Commission.

ROOT SAMPLING PROCEDURE.—Root sampling was conducted on the same schedule as the transect surveys. Roots were not sampled from Pinellas Point and Skyway because of extremely low isopod abundance within those sites. Similarly, roots were only sampled from Fort Desoto in February and July. Unattached aerial roots located within 1 m of the seaward root edge were destructively sampled for isopod density estimation. Additionally, only roots which displayed signs of burrowing by S. terebrans (≥ 1 burrow) were sampled. Chosen roots contained only one root tip as previous studies suggest that isopods prefer root tips and therefore the presence of multiple root tips might bias density estimates studies (e.g., Perry and Brusca, 1989; Brooks and Bell, 2001a). The five closest attacked roots (which met the above stated criteria) to each sampling point were taken. In the laboratory, all burrows were noted as to their spatial location along the root. Bur- rows were then excavated to determine the presence, size, sex, and reproductive status of S. terebrans colonizers. Individuals were pressed flat under a dissecting scope and the length from the tip of the head to the tip of the pleotelson was recorded (Thiel, 1999). Juveniles were defined as individuals < 5.6 mm and possessed no sign of sexually dimorphic features, in ac- cordance with Estevez (1978) and Venkatakrishnana and Nair (1973). Males were identified by the presence of penes (Venkatakrishnana and Nair, 1973). Adult females were classified as brooding if there were either eggs or embryos present within the brood chamber. Maternal care in which juveniles are clustered at the terminal end of a family burrow (sensu Thiel, 1999) 30 BULLETIN OF MARINE SCIENCE, VOL. 76, NO. 1, 2005 was recorded separately. Additionally, any root that contained an unoccupied burrow inhab- ited by an inquiline isopod was recorded. HABITAT AVAILABILITY.—The density of unattached aerial roots at each study site was de- termined using a 1 m2 collapsible quadrat placed within the prop roots adjacent to each sampling point. The front edge of the quadrat was aligned parallel to the forest edge, which was defined in this study as the furthest extending prop root at the land/water ecotone. The root density measurements were conducted between November 1999 and February 2000. TRANSPLANTATION EXPERIMENT.—A manipulation experiment was conducted in which S. terebrans individuals were transplanted from a donor area of the bay into an area where they were currently absent. A general survey indicated no evidence of burrowing at Bunces Pass (BP; 27°38′N, 82°45′W) prior to the experiment, thus this area was selected as the transplantation site. Weedon Island (WI; 27°56′N, 82°36′W) was chosen as the donor site because it was the closest known site of high levels of S. terebrans along the western shoreline of the bay (Brooks, 2001). The transplant experiment consisted of four different treatments utilizing two different root substrates, root substrate from the donor area and root substrate from the transplant area. All transplanting was performed using cages into which two adult isopods were placed onto severed root substrate. All of the isopods used in the experiment were originally from WI. Cages consisted of fiberglass window screen (2 × 2 mm mesh) and were 20 cm in length and 12 cm in circumference. The window screen was sewn together using monofila- ment line and the cage was then secured 15 cm from the root tip (i.e., enclosing the root tip) using a cable tie. The root tip was selected as the caging site as previous data suggested pref- erential colonization of this root area (Perry and Brusca, 1989; Ellison and Farnsworth, 1990; Brooks and Bell, 2001a). The four treatments were as follows: 1) Sphaeroma terebrans back- transplanted into the donor area (WI) on root substrate from WI; 2) Sphaeroma terebrans back-transplanted into WI on root substrate from the transplant site (BP); 3) Sphaeroma terebrans transplanted to BP on root substrate from WI; 4) Sphaeroma terebrans transplanted to BP on root substrate from BP. All transplantations were done using severed root tips approximately 50 cm in length. The roots chosen for the experiment were unattached aerials, displayed no sign of burrowing, contained only one root tip, and were of a representative diameter of other aerial roots at the site. Several predictions were made a priori as to the survival results: If isopods survived at WI but not at BP, regardless of root substrate, then some abiotic factor at BP was most likely preventing isopod presence. If isopods survived at both locations but only in root substrate originally from WI then some “tree effect” is preventing isopod presence at BP. If isopods survived at both sites regardless of root source then exclusion from BP must be due to either dispersal limitation or some other biotic influence. Thirty-two roots were collected for the experiment from BP and WI on June 1 and 4, 2000, respectively. Twelve hours prior to being deployed in the field isopods were placed within the cages and the cages attached to the experimental roots. Sphaeroma terebrans used in the experiment were collected from attacked roots in WI on May 30, 2000. Isopods were main- tained in the laboratory in an aquarium containing seawater from WI until their deployment in the field. The experiment was started at BP and WI on June 6 and 7, 2000, respectively. All experimental roots were attached to natural prop roots in the site using a cable tie. Roots were placed along the outer root edge of each site and within the intertidal zone. Roots were deployed in a paired fashion (n=16 pairs at each site) such that roots from each site were paired within 1 m of each other and treatment pairs were separated by at least 10 m. All roots and cages were collected 14 d after deployment. The 14-d experiment was based upon both the expected time of isopod mortality due to any inability to feed (Estevez, 1978; Roshaven, 2000) and the decay rate of severed roots (Brooks and Bell, 2001a). Experimental roots and cages were then returned to the laboratory and presence/absence of burrowing and survival of caged isopods recorded. STATISTICAL ANALYSIS.—Frequency of Attack and Density.—Non-parametric analyses were used to examine the data for the frequency of isopod attack along the sample transects BROOKS AND BELL: DISTRIBUTION AND ABUNDANCE OF SPHAEROMA TEREBRANS 31 among the different sites because they could not be transformed to meet the assumptions of normality and homogeneity of variances for parametric analyses. Therefore, two different Kruskal-Wallis One-Way ANOVA on Ranks tests were performed with date and site as the main factors. If Kruskal-Wallis results indicated a significant treatment effect, Dunn’s Method multiple comparison tests were subsequently performed to determine significant differences (Glantz, 1997). The density of burrows and isopods in an attacked root (i.e., average values from the five roots sampled at each point) combined with information on both the frequency of aerial roots which were attacked and the number of aerial roots per square meter were multiplied to esti- mate the number of attacked roots, burrows, and individuals of S. terebrans per square meter. Root, burrow, and isopod densities were all analyzed using a Two-Way ANOVA with date and site as factors. If necessary, transformations were performed to satisfy the ANOVA assumptions of normality and homogeneity of variances. If ANOVA results indicated significant treatment effects, a Student-Newman-Keuls multiple comparison test was subsequently performed to determine differences among individual treatments. Ontogenetic Stage and Sex.—The proportion of juveniles, adults, females, and males were analyzed for differences among dates and sites. Because the density of isopods was highly variable depending upon date and site, proportions were used for all analyses. Transforma- tion did not satisfy the assumptions of normality and heterogeneity of variances for Two- Way ANOVA. Therefore, separate Kruskal-Wallis ANOVA on ranks tests were conducted to identify significant differences by date or site, and the data were visually inspected for any interactions between the two factors. Isopod size distributions were examined for any site-specific differences. Tests of Indepen- dence (Chi Square) were used to examine the equality of median size among sites. Sizes were divided into 0.25 mm categories for analysis. If the median size was not found to be equal among sites, then a Simultaneous Test Procedure for multiple comparisons was performed to determine where independence did not occur (Sokal and Rohlf, 1995). Reproductive Status.—Analyses were used to examine differences between dates and sites in the proportion of brooders or proportion of roots occupied by an inquiline. The data could not be transformed to meet the assumptions of normality and homogeneity of variances for parametric analyses. Therefore, two different non-parametric, Kruskal-Wallis One-Way ANOVA on Ranks tests were performed with date and site as the main factors. A correlation test was performed between the percent of females brooding in a site and the density of isopods found on that sampling date. Transplantation Experiment.—Differences in either the presence of burrowing or isopod survival among experimental treatments were analyzed using RXC tests of independence with Williams’ Correction for small sample size (Sokal and Rohlf, 1995). The categories for the analysis were either the proportion of roots with isopod burrows or the proportion of live isopods recovered from each cage for the donor (WI) and transplant sites (BP).

RESULTS

FREQUENCY OF ATTACK.—Significant differences in the frequency of attacked roots occurred among the study sites in Tampa Bay (P = 0.001, Kruskal-Wallis ANO- VA on ranks; Fig. 2; Table 1). No significant difference was found in the frequency of attacked roots among sampling dates (P = 0.07, Kruskal-Wallis ANOVA on ranks). Cockroach Bay (CB), Fourth Street (4th), Upper Tampa Bay (UTB), WI, and Anna Maria Island (AM) all had root attack frequencies > 50%. In Upper Tampa Bay up to 90% of aerial roots were attacked in October and July. Pinellas Point (PP) and Skyway (SKY) had either no signs of attack (e.g., July) or a low frequency of attack (2%–4%) over all dates. Similarly, Fort Desoto (FD) demonstrated a relatively low frequency of attack compared to the other sites, especially in July. 32 BULLETIN OF MARINE SCIENCE, VOL. 76, NO. 1, 2005

Figure 2. Mean frequency (± S.E.) of Sphaeroma terebrans attack on free hanging aerial roots. Site abbreviations are the same as in Figure 1.

Two-Way ANOVA tests conducted on the density of attacked roots (for all sites except FD, PP, or SKY given their low frequency of attack) indicate that site was a significant factor in the level of isopod attack (Fig. 3; Table 1). The density of attacked roots was significantly higher at UTB and CB than either WI or 4th (Table 1). AM had a significantly lower density of attacked roots compared to the other four sites included in the analysis. BURROW DENSITY.—Examination of the level of isopod attack across Tampa Bay showed that burrow density per attacked root was significantly different among all

Figure 3. Mean frequency (± S.E.) of Sphaeroma terebrans attack based upon aerial root density. Site abbreviations are in Figure 1. BROOKS AND BELL: DISTRIBUTION AND ABUNDANCE OF SPHAEROMA TEREBRANS 33 AM AM th th WI AM WI AM WI th th Oct. Feb. July Oct. Feb. July Oct. Feb. July Oct. Feb. Oct. July Feb. July Oct. Feb. July Oct. Feb. CRB WI AM FD PP SKY WI CRB th UTB CRB 4 UTB CRB 4 CRB UTB WI 4 CRB UTB WI 4 UTB CRB UTB 4th CRB WI AM WI UTB 4th CRB Multiple comparison results UTB 4 = Fourth Street, WI Island,= Weedon CRB PP = = CockroachPinellas Bay, Point, SKY th Treatment effects Treatment Date: P = 0.07 Site: P = 0.001 Date: P = 0.68 Site: P = 0.001 Date × Site: 0.93 Date: P = 0.001 Site: P = 0.001 Date: P = 0.001 Site: P = 0.001 Date × Site: P = 0.99 Date: P = 0.001 Site: P = 0.001 Date: P = 0.001 Site: P = 0.001 Date × Site: P = 0.28 ) 2 (m ) 2 ) 2 Abbreviations are 4 UTB as follows: = Bay, Upper Tampa = Skyway, FD = Fort Desoto,= Skyway, and AM = Anna Maria Island. Frequency of attacked roots of attacked Frequency Density of attacked roots (m Density of attacked Table 1. Multiple comparisons on isopod attack from all sites except FD, PP, and SKY. The sites, forest types, and months sharing an underline are not signiﬁcantly not are underline an sharing months and types, forest sites, The SKY. and PP, FD, except sites all from attack isopod on comparisons Multiple 1. Table different. Metric root per attacked Number of S. terebrans terebrans Density of Sphaeroma Number of burrows per attacked root per attacked Number of burrows (m Density of burrows 34 BULLETIN OF MARINE SCIENCE, VOL. 76, NO. 1, 2005

Figure 4. Mean burrow density (± S.E.) of Sphaeroma terebrans in a root. Site abbreviations are in Figure 1.

sampling dates (Table 1). Values were highest in October and lowest in July. The burrow density per attacked root was surprisingly similar at all sites (Fig. 4). Most attacked roots had between three and five burrows. Consistently, the highest burrow density per root was at UTB (mean = 5.4 burrows), significantly different (P = 0.001) from the other sites (Table 1). Based on attacked root density and burrow density per attacked root, the overall burrow density per square meter of intertidal habitat was calculated (Fig. 5). Burrow

Figure 5. Mean density (± S.E.) of Sphaeroma terebrans’ burrows at all sites. Site abbreviations are in Figure 1. BROOKS AND BELL: DISTRIBUTION AND ABUNDANCE OF SPHAEROMA TEREBRANS 35

Figure 6. Mean density (± S.E.) of Sphaeroma terebrans per sampled root. Site abbreviations are in Figure 1.

density per square meter was significantly higher in October than the other two dates. Lowest densities (burrows m−2) were recorded in July (Table 1). The density of burrows per unit area was also significantly higher in UTB and CB than the other sites. ISOPOD DENSITY.—Individuals of S. terebrans can make more than one burrow, or co-habitat burrows (Estevez, 1978; Thiel, 1999). Therefore analysis was also conducted on the density of individuals present within a root at the time of sampling. Isopod densities per root were significantly different depending upon both date and site (P = 0.001; Fig. 6; Table 1). Densities in October were roughly twice those found in the other months. UTB had the highest isopod density per root in October and July while density was highest at the 4th Street site in February. Interestingly, FD, which had a low frequency of attacked roots, had a similar burrow and isopod density per root as the other sites. Average isopod densities at each site ranged from 2–4 isopods per attacked root. The densities ofS. terebrans per square meter (Fig. 7) differed significantly by date and site (P = 0.001; Table 1: densities in July and February were each significantly lower than in October. UTB and CB had significantly higher isopod densities per square meter than either WI or 4th Street, which both had significantly higher densities than AM). Overall, UTB had the highest isopod density per square meter in October and July while density was highest at CB in February. FD and AM both had a low density of isopods per square meter. ONTOGENETIC STAGE.—The proportion of adults and juveniles differed significantly among the three sampling dates (One-Way ANOVA on ranks, P = 0.001; Fig. 8). Almost no juveniles were found in the February samples, while the proportion of juveniles was highest in July (20%–80% of the population), although this was not significantly different from October. Due to the scarcity of juveniles in the February, analysis of site differences was based only on data from July and October. There was 36 BULLETIN OF MARINE SCIENCE, VOL. 76, NO. 1, 2005

Figure 7. Mean density (± S.E.) of Sphaeroma terebrans at all sites. Site abbreviations are in Figure 1.

also a significant difference among sites in the proportion of juveniles (One-Way ANOVA, P = 0.003). The highest proportion of juveniles was found at AM (39.0%), which was significantly different from all other sites except for UTB (28.8%; Fig. 8). AM also had a significantly lower proportion of adults compared to all other sites except UTB. SIZE DISTRIBUTION.—All sites had approximately the same size distribution with a very broad peak frequency of individuals from 4–10 mm and a median size range of 6.4–7.8 mm (Fig. 9). One exception was FD, where the size distribution was shifted to larger individuals with a narrower peak frequency of 6.5–10 mm and a median size of

9 mm was found. Overall, the median size was not equal among sites (G = 179, Gcrit0.5 = 11.07). Results of the Simultaneous Testing Procedure indicated that the median sizes found at FD (8.7 mm) and CB (7.6 mm) were both significantly different from the median size (7.1 mm) found at the other sites (i.e., UTB, WI, 4th Street, and AM) and each other (G = 53.2). This appears to be due to the adults being slightly larger at CB compared to the other sites. However, the size distribution of isopods collected from FD indicated a paucity of smaller individuals and was significantly different compared to a combined distribution of the other five sites (Kolmogorov-Smirnov:

D=0.48; D.01=0.12). SEX RATIOS.—Overall, females consistently dominated the isopod populations, representing > 60% of the total number of adults. The proportion of females did not differ among sampling dates (One-Way ANOVA on ranks, P = 0.254; Fig. 10) but did differ among sites (One-Way ANOVA on Ranks, P = 0.020). A significantly higher proportion of females was found at UTB (81.1%) compared to AM (61.3%) but this was not significantly different from the other locations. The proportion of males did not differ among sites (Fig. 10) but was significantly higher in February (34.5%) than in July (26.5%) or October (28.1%) (One-Way ANOVA on ranks, P = 0.035). BROODING.—The overall proportion of brooding females was not significantly different among dates (One-Way ANOVA on ranks, P = 0.92) or sites (One-Way ANO- BROOKS AND BELL: DISTRIBUTION AND ABUNDANCE OF SPHAEROMA TEREBRANS 37

Figure 8. Proportion of adult and juvenile Sphaeroma terebrans on all three dates at the different sites. Adults are all individuals ≥5.6mm in length. Site abbreviations are in Figure 1.

VA on ranks, P = 0.14; Fig. 11). The percentage of brooding females generally varied considerably within sites across dates. The highest percentage of brooding females was found at CB in October (29.5%) and July (42.1%), which were almost 2–3× that found in February. In contrast, in February the highest percentage of brooding females across all sites was at FD (23.4%), which was almost 3× that found in October or July. Similar trends were found when the presence of females with small juveniles clustered at the end of their burrow was included in the “brooding” category (Fig. 11B; Brooks, 2001). When maternal care was included, the proportion of brooding females was still not significantly different among dates (One-Way ANOVA on ranks, P = 0.76) or sites (One-Way ANOVA on ranks, P=0.12). Finally, no significant correlation was found between the percent of brooders in a site and the average isopod density (Pearson Product Moment Correlation: P = 0.08). INQUILINES.—The presence of inquiline isopod occupied roots was significantly different among sites (One-Way ANOVA on ranks, P=0.001; Fig. 12). The highest frequency of inquiline occurrence was at AM (range: 6%–60%), which was significantly different from all other sites except FD (6–22%). Root occupancy by inquilines at FD was also significantly greater than UTB as no roots were occupied by inquilines at UTB on any date. The frequency of inquiline occupied roots was significantly different among dates (One-Way ANOVA on ranks, P = 0.005): A significantly higher occupancy rate was found in February compared to July. TRANSPLANTATION EXPERIMENT.—The presence of burrows and isopod survival on transplanted roots were both independent of treatment (RXC Test of Indepen- dence, Williams’ Correction, P > 0.05; Fig. 13). Therefore, neither the site to which 38 BULLETIN OF MARINE SCIENCE, VOL. 76, NO. 1, 2005

Figure 9. Size distribution of Sphaeroma terebrans collected at the study sites over three dates. Site abbreviations are in Figure 1. the isopods were transplanted nor the origin of the roots onto which they were caged impacted their ability to burrow or survive. Interestingly, a higher percentage of roots (regardless of origin) were burrowed into when placed at BP compared to WI. Additionally, isopod survival was higher in roots from BP regardless of experimental location.

DISCUSSION

The distribution ofS. terebrans was not continuous within the mangrove habitat of Tampa Bay, Florida nor was isopod abundance similar at all sites. The northern part of Tampa Bay had a substantially higher occurrence and density of S. terebrans com- BROOKS AND BELL: DISTRIBUTION AND ABUNDANCE OF SPHAEROMA TEREBRANS 39

Figure 10. Proportion of females and males on all three dates at the different sites. Site abbreviations are in Figure 1.

pared to the more southern parts of the bay. Some southern regions of the bay were actually devoid of isopod attack and a distinct boundary was found between Weedon Island and Pinellas Point, where isopod abundance decreased sharply. However, this boundary only appeared on the west side of the bay as there was no similar division on the eastern side. Sharp boundaries in the distribution of S. terebrans with seemingly suitable areas unoccupied have been noted previously (Van Name, 1920: from Estevez, 1978). Previous studies have shown that S. terebrans is distributed from just north of Tampa Bay to the tip of the Florida peninsula, but is absent in the Florida Keys (Ribbi, 1981; Rice et al., 1990). Differences in tree quality such as root architecture (e.g., root diameter, order), root penetrability, water content, burrow integrity, or chemistry may exist that make some mangrove stands unsuitable. However, our transplantation experiments were not able to detect any difference in the ability of S. terebrans to burrow and survive equally well in roots from BP, a site at which isopods were not found, compared to those at WI. This suggests that roots from BP may represent a suitable substrate and that “tree effects” are not limiting S. terebrans from persisting there. It is possible that roots may differ chemically among sites and that the experimental procedure of severing the root may have masked this. However, burrowing began within 24 hrs of initiation of the experiment and it is unlikely that chemical differences would have large effects, as S. terebrans does not actually consume the wood it excavates (Rotramel, 1975). Additionally, there is little evidence that chemical treatments and preservatives impact isopod colonization (Kuhne, 1972; Rice et al., 1990; Cragg et al., 1999). 40 BULLETIN OF MARINE SCIENCE, VOL. 76, NO. 1, 2005

Figure 11. Mean percent of brooding females (± S.E.) at each site for the three different dates. A) Brooding deﬁned as the number of females with eggs or embryos in their brood pouch. B) Brood- ing deﬁned as females with juveniles clustered at the end of their burrow in addition to those with eggs or embryos in their brood chamber. Site abbreviations are in Figure 1.

Regional distribution of S. terebrans may be influenced by several abiotic factors including salinity, water temperature, suspended solids, and tidal influences (Conover and Reid, 1975; Estevez, 1978; Barkati and Tirmizi, 1990). However, the results of the transplantation experiment in this study suggest that abiotic factors within Tampa Bay do not appear to limit the burrowing capabilities or survival of adult S. terebrans. Similarly, in a controlled laboratory study, Roshaven (2000) found that neither the extreme high temperature nor salinity at BP, either independently or combined, limited adult survivorship. Radhakrishnan et al. (1987) also found no correlation with S. terebrans density and salinity or temperature. What remains unknown, however, is whether abiotic factors limit isopod recruitment into these areas, as all previous studies were conducted on adult isopods. Although sites differed in the frequency with which roots were attacked, the density of burrows and isopods in an occupied root was similar. Most attacked roots had BROOKS AND BELL: DISTRIBUTION AND ABUNDANCE OF SPHAEROMA TEREBRANS 41

Figure 12. Mean percent of roots (± S.E.) at a site, which were occupied by an inquiline species. Site abbreviations are in Figure 1. between three and five burrows. Sphaeroma terebrans represents a major component of the wood boring guild utilizing Rhizophora mangrove roots and occupied on average just over 60% (range: 25%–86%) of the intertidal aerial roots surveyed (at six of the eight study sites). This level of attack is within the range found forS. terebrans in Key Biscayne, Florida (36%–81%: Ribbi, 1981), and the Ten Thousand Island region of Florida (55%–61%: Ribbi, 1981). UTB, the northern most site, had the highest occurrence of attacked roots with 86% of the aerial roots surveyed containing burrows. Thus, infestation by S. terebrans in Tampa Bay, which is at the mangrove/salt marsh ecotone, is similar to that of more tropical regions. These results suggest that a strict latitudinal gradient in attack levels may not exist and therefore temperature is prob- ably not controlling the prevalence of S. terebrans attack. The population density ofS. terebrans differs seasonally within Tampa Bay. Isopod abundance was highest in the fall but densities were similar in winter and summer. These temporal fluctuations inS. terebrans density were synchronous around Tampa Bay and similar to the pattern documented for S. terebrans in the Indian River La- goon on the east coast (Thiel, 1999). Similarly, juvenile recruitment periods were consistent across both broad geographic scales (i.e., west versus east coast of Florida) and temporally from year to year (i.e., 1978 versus 1999/2000 in Tampa Bay). The population density pattern of S. terebrans, however, does not appear to be consistent across years as Estevez (1978) found higher isopod abundances in the summer (up to 6×) or fall compared to the winter in Tampa Bay. Howey (1976) also found higher abundances in the spring (4–12×) compared to the winter for a S. terebrans population in the Indian River Lagoon. Variation in density patterns among studies from different years raises the question of whether predictable abiotic factors such as temperature or day length function as cues as opposed to more potentially stochastic parameters (e.g., food levels). The distribution and abundance pattern ofS. terebrans in Tampa Bay does not appear to be limited by habitat (i.e., aerial root density) or abiotic factors (Brooks, 2001). 42 BULLETIN OF MARINE SCIENCE, VOL. 76, NO. 1, 2005

Figure 13. Results of the transplantation experiment presented as frequency of burrowing and frequency of isopod survival.

Moreover, the sex ratio, reproductive status, and ontogenetic stage distribution of S. terebrans were fairly consistent around the bay with the exception of FD. The geo- metric mean size of individuals at FD was 8.4 mm compared to 5.9–6.7 mm at the other sites indicating a lack of juvenile presence within the FD population. Similarly, no juveniles were found at either SKY or PP over the study period (Brooks, 2001). The disjunct distribution of S. terebrans may be due to dispersal limitation. It is likely that rafting in roots that break oﬀ naturally due to atrophy or storm events is a main mode of dispersal for the isopod. Rafting is a common dispersal mechanism for brooding marine invertebrates (e.g., Highsmith, 1985; Helmuth et al., 1994; Hol- mquist, 1994; Worcester, 1994; Ingolfsson, 2000; Brooks and Bell, 2001b) and specifically for mangrove-dwelling invertebrates (Wehrtmann and Dittel, 1990) including S. terebrans (Si et al., 2000). If S. terebrans could survive transport from the Indo- Paciﬁc to the North American tropics and establish (Carlton, 1994) it is surprising that they could not disperse after several decades of occupation (Estevez, 1978) to all mangrove stands within Tampa Bay. Additionally, anthropogenically derived mari- BROOKS AND BELL: DISTRIBUTION AND ABUNDANCE OF SPHAEROMA TEREBRANS 43

time structures (e.g., docks: Rice et al., 1990) should provide steppingstones between mangrove stands for colonization, effectively minimizing inter-stand distances (Virnstein and Curran, 1986; Kurdziel and Bell, 1992). More likely, the occurrence of dispersal may be sufficiently infrequent that the population cannot successfully establish or reproductive activities might be hindered upon establishment. Successful establishment within an area would require reproductive activity or juvenile recruitment. During the course of this study one brooding female was found at the SKY site (Brooks, 2001) and brooding was prevalent at FD. It is unknown whether these individuals were recent colonizers, but these findings suggest that reproduction can occur within these sites and that resources are not so potentially limiting as to prevent egg production. Although brooding occurred, juvenile recruitment was not detected at either PP or SKY. Likewise the size distribution of individuals found at FD was significantly skewed towards adults compared to the other study sites within Tampa Bay. It is possible that site-specific conditions, which allowed survival of adult individuals in the transplantation experiment, may not be conducive to juvenile survival. Sphaeromid isopods have specialized brood pouches that contain organic concentrations that differ from the external environment thus acting as osmotic shelters for the young (Charmantier and Charmantier-Daures, 1994). Additionally, while juveniles are under maternal care, the abiotic conditions of the burrow may be regulated by the parent (Thiel, 1999). However, once outside of the maternal burrow juveniles are exposed to the same abiotic conditions as adults. A lack of juvenile presence may result in these areas existing as “sink” populations (Pulliam, 1988). A source-sink scenario has been suggested for adults of both Ter- ebellides parva Solis-Weiss, Fauchald and Blankensteyn, 1990, a polychaete, and Gol- finigia cylindrata Keferstein, 1865, a sipunculid, living within mangrove habitat in Belize (Ferraris et al., 1994). In Tampa Bay, S. quadrentatum and S. walkeri are commonly found in both occupied and unoccupied burrows (Estevez, 1978; Brooks, pers. obs.). In a detailed study, Thiel (2000) found that only juvenile S. quadrentatum were occupants of burrows when the resident S. terebrans was either reproductively active or exhibiting maternal care. Thiel hypothesized that inquiline juveniles were sufficiently small that they remain undetected by the S. terebrans female but would benefit from the maternal care (i.e., regulated abiotic conditions and generated food/respiration current) much the same as the juvenile S. terebrans present within the burrow (Thiel, 1999). This inquiline relationship however is potentially detrimental to the S. terebrans juveniles as their residence time within the maternal burrow is reduced when inquilines are present (Thiel, 2000). Interestingly, inquiline presence appears to follow a salinity gradient such that no inquilines were present at Upper Tampa Bay but high levels occurred within the lower bay. Inquiline presence may be related to the population density gradient of S. terebrans from upper to lower parts of the bay due to their impacts upon juvenile survivorship. Predation (Perry and Brusca, 1989) and competition (Estevez, 1978; Ellison and Farnsworth 1990; Ellison et al., 1996) have also been suggested to reduce isopod boring and may be yet another reason responsible for the discontinuous spatial pattern of S. terebrans within Tampa Bay. Specifically, fouling by sponges (Ellison and Farnsworth, 1990) and molluscan shipworms (John, 1971) has been found to limit isopod burrowing. However, fouling by sponges was not noted at BP (Brooks, pers. obs.) and ship borers tend to only affect subtidal dead wood roots not the live wood 44 BULLETIN OF MARINE SCIENCE, VOL. 76, NO. 1, 2005 examined in this study (Si et al., 2000). Heavy fouling by oysters and barnacles has been suggested to prevent colonization (Conover and Reid, 1975; Estevez, 1978), although no major differences in the prop root fouling community were noted among sites with varying attack levels, and colonization of new roots by Sphaeroma can be rapid, preceding fouling by other organisms (Brooks and Bell, 2001a). Predation can influence species distributions, but unlike other fouling organisms found on mangrove roots (e.g., barnacles and gastropods) S. terebrans excavates and resides in a burrow. Within its burrow, S. terebrans should have reduced exposure to predation. Risky excursions outside of the burrow to collect food are not likely for the filter feeder. With no vulnerable planktonic stage, only during times of burrow construction would S. terebrans be susceptible to predation. Burrowing is rapid, however, and after only one tidal cycle a burrow can be sufficiently deep that only the dorsal surface of the organism is exposed (Brooks and Bell, 2001a). To date no literature exists to suggest that S. terebrans represents a consistent diet for any mangrove-dwelling organism and the importance of predation pressure is questionable (Brooks and Bell, 2001a).

ACKNOWLEDGMENTS

E. Estevez made many helpful comments on earlier drafts of the manuscript. This work was supported in part by an Aylesworth Fellowship, Tharpe Fellowship, and Old Salt Fishing Or- ganization Fellowship to R.A. Brooks. We would also like to thank two anonymous reviewers for their helpful comments.

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DATE SUBMITTED: 18 April, 2002. DATE ACCEPTED: 4 May, 2004.

ADDRESSES: Department of Biology, SCA 110, University of South Florida, 4202 East Fowler Avenue, Tampa, Florida 33620. Telephone: (813) 974-5420. PRESENT ADDRESS: Coastal Ecol- ogy Conservation Research Group, Florida Integrated Science Center, U.S. Geological Survey, Gainesville, Florida 32653. Telephone: (352) 378-8181. E-mail: .

&lt;I&gt;Sphaeroma Terebrans&lt;/I&gt;

<I>Sphaeroma Terebrans</I>