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Notice: ©1991 Elsevier B.V. The final published version of this manuscript is available at http://www.sciencedirect.com/science/journal/00220981 and may be cited as: Bingham, B. L., & Young, C. M. (1991). Larval behavior of the ascidian turbinata Herdman; an in situ experimental study of the effects of swimming on dispersal. Journal of Experimental Marine Biology and Ecology, 145(2), 189-204. doi:10.1016/0022-0981(91)90175-V J. Exp. Mar. Bioi. Ecol., 1991, Vol. 145, pp. 189-204 189 Elsevier

JEMBE 01533

Larval behavior of the ascidian Ecteinascidia turbinata Herdman; an in situ experimental study of the effects of swimming on dispersal

Brian L. Bingham I and Craig M. Young? 'Department ofBiological Science. State University. Tallahassee. Florida. USA; 2Harbor Branch Oceanographic Institution. Ft Pierce. Florida. USA

(Received II June 1990; revision received 17 September 1990; accepted 10 October 1990)

Abstract: Swimming and non swimming tadpole larvae of the ascidian Ecteinascidia turbinata Herdman were followed in situ by divers to determine whether swimming affects larval dispersal. Swimming affected neither dispersal direction nor time spent in the water column. However, the dispersal rates and distances of swimming larvae were significantly lower than those of nonswimming larvae. Potential paths oflarval dispersal were modeled with subsurface drogues. Movements of both swimming and non swimming larvae differed consistently from surface flow direction in these shallow (1.0-1.5 m) waters, indicating that caution should be used in modeling larval dispersal with drogues, particularly when larvae do not consistently remain in surface waters. In our south Florida study site, E. turbinata colonies were present only on unanchored mangrove prop roots and survival of colonies transplanted into surrounding habitats was very low. Drogue paths demon­ strated that currents could potentially carry E. turbinata between mangrove islands, but behavior of the larvae suggests that dispersal is generally very localized with larvae settling near colonies from which they were released. This behavior differs dramatically from that reported for E. turbinata larvae in a more homogeneous habitat in the northern . The short-distance dispersal of swimming tadpole larvae observed in this study may represent a local adaptation to favor recruitment near parental habitats and to prevent advection to inappropriate sites. Long-distance exchange between isolated islands probably occurs through rafting of adult colonies on fragmented mangrove roots rather than through larval dispersal.

Key words: Ascidian; Dispersal; Ecteinascidia turbinata; Larva; Swimming

INTRODUCTION

Larvae of marine invertebrates are diverse in form, size, and behavior, but one feature common to all but a few crawling benthic forms (Mileikovsky, 1971; Gerrodette, 1981; Fadlallah & Pearse, 1982) is the ability to swim. Given that most larvae expend energy for swimming and that many different kinds oflocomotory structures (uniform ciliation, ciliary bands, ciliated lobes, muscular appendages, etc.) have evolved, swimming must have one or more important functions. A number of possibilities have been suggested,

Correspondence address: B. L. Bingham, Shannon Point Marine Center, Western Washington University, 1900 Shannon Point Road, Anacortes, WA 98221, USA. Contribution 789 of Harbor Branch Oceanographic Institution.

0022-0981/91/$03.50

MATERIALS AND METHODS

STUDY SITE AND HABITAT SURVEY Experiments were done in Pine Channel between Big Pine Key and Big Torch Key in the lower Florida Keys, Florida, USA (22 0 44' N, 81026' W). Pine Channel experiences bidirectional flow due to tidal exchange between the Gulf of Mexico and the Straits of Florida and maximum water depth is :::::; 3 m. Several small keys, composed entirely of red mangroves Linnaeus, are present in the channel. To map potential E. turbinata source populations, we surveyed 17 transects (from 25 to 1000 m in length) between Big Torch Key and the mangrove keys (labelled Keys 1-4) in the center of Pine Channel (Fig. 1). For short transects near keys, divers swam along a 25-m line examining a 0.5 m on each side. For longer transects between keys, a diver was pulled slowly behind a boat. The transects covered large portions of the channel

Florida Peninsula

()' Key 1

50 km I

~ 3

Key 4

1 km

Fig. 1. Study site in the lower Florida Keys, Florida. Arrows indicate the movements of three drogues during a 4.5 h observation period. Points along the drogue tracks show their locations at I-h intervals. Circles represent results of surveys for E. turbinata on mangrove roots.•, abundant; (), rare; 0, absent. 192 B. L. BINGHAM AND C. M. YOUNG and crossed a variety of habitat types. Divers also swam around the edges of the keys examining submerged mangrove prop roots for E. turbinata colonies.

ADULT TRANSPLANTS

Although E. turbinata colonies were present on mangrove roots, they were absent from surrounding substratum. This implied that appropriate habitats were patchily distributed and that larval behavior could be critical if it determined whether or not other mangrove roots were encountered during the dispersal period. However, because it was unknown whether survival was possible in the habitats surrounding the scattered mangrove islands, we transplanted adult colonies on the west side of Key 2 to a scoured limestone bed 2 m directly beneath the roots (seven replicates) and to a seagrass bed 6 m away (nine replicates). Transplants were attached with cable ties to stakes which were driven into the substratum. To control for transplant artifacts, colonies were also removed and reattached directly to the mangrove roots (nine replicates). Survival of the colonies was assessed 36 days after transplant. Remaining colonies were collected and colony wet weights and numbers of zooids were determined. In addition, 10 randomly chosen zooids from each colony were measured (maximum length) and examined for brooded larvae. Measurements were compared with Kruskal-Wallis tests (Zar, 1984). Due to unequal sample sizes, a posteriori pairwise comparisons were made with Spjotvoll & Stoline's test (Kirk, 1982). It appeared that mortality of some transplanted colonies was due to fouling by filamentous algae. To determine if mortality was correlated with the degree of algal overgrowth, we scraped clean a l-cm? area near the tops of five randomly chosen transplant stakes recovered from the seagrass and the limestone beds. Material present in the scrapings was extracted in acetone and Chi a absorbance was read with a fluorometer. Readings were compared with one-way AN OVA.

DISPERSAL OF TADPOLE LARVAE

To measure the effects of swimming on E. turbinata dispersal, we followed individual larvae (swimming and nonswimming) as they moved away from a release point. Swimming larvae (bright orange and ~ 5 mm long) were obtained by placing ripe E. turbinata colonies in a I-gal glass jar and exposing them to direct sunlight. Brooded larvae of the same size and shape were collected from dissected adults and served as nonswimming controls. All larvae were used within 1 h of collection. Dispersal experiments were performed in a shallow (1.0-1.5 m) seagrass bed (com­ posed predominately of Thalassia testudinum Koenig & Sims) ~ 50 m from the west side of Key 2 (the site where adult colonies had been collected). The experiment was done in the seagrass bed because it was impractical to follow dispersing tadpoles among mangrove roots which were heavily encrusted with massive sponges. Furthermore, we were primarily interested in examining the potential influence of swimming behavior on dispersal between islands rather than among the mangrove roots. DISPERSAL OF ECTEINASCIDIA TURBINATA 193

A PVC pole driven into the substratum was used as a starting point for all observa­ tions. A diver released a single larva (swimming or non swimming) from a pipette at a depth of ::::; 20 em (80 em from the bottom); this approximated the height in the water column at which a larva might naturally be released from a parental colony on an unanchored mangrove root. A diver floated at least 0.5 m downstream from the larva and watched it until it was lost from view, generally in the seagrass on the bottom. At that point, a second pole was driven into the bottom. Dispersal directions (8) were measured by determining the bearing from the first to the second pole with a compass. The distance that each larva traveled was measured and an observer recorded the time that the larva was observed, thus enabling us to calculate a dispersal rate. Swimming and nonswimming larvae were alternated to permit pairing for statistical analysis. Measurements were made on two dates, 28 November 1988 and 5 December 1988. No attempt was made to measure water movement on 28 November. On 5 December, however, a wooden drogue (constructed of two 30 x 10-cm boards attached together in a cross and weighted to float horizontally just below the surface) was used to determine current speed and direction. The drogue was attached to a 5-m tether (1.58 mm diameter nylon line) which fed out freely as the drogue moved away from a release point. Current measurements were taken repeatedly during the period that larvae were being followed. In this way, we were able to match a current speed and direction with each of our dispersal measurements. We examined potential larval dispersal distance and direction by following similar drogues (without tethers) which were released 25, 150, and 300 m from the west side of Key 2. We monitored their locations for 4.5 h by taking compass bearings from the drogues to fixed landmarks at 30-min intervals. The drogues were released in the mid-morning near the beginning of an outgoing tide. This approximated conditions ... under which E. turhinata larvae might naturally be released. Swimming speeds of E. turbinata larvae were determined in the laboratory by placing newly released larvae in a large Plexiglas column (1.5 m tall, 25 em diameter) filled with seawater. Larvae swimming directly towards the surface were timed as they passed marks placed at 5-cm intervals on the column.

STATISTICAL ANALYSIS OF LARVAL DISPERSAL

Because environmental features were similar on both days (e.g., strong sunlight, little cloud cover, little wind, smooth water) and because variability in dispersal vectors within dates exceeded that between dates, we pooled data from both sampling dates for all analyses. Comparisons of time spent in the water column, distance traveled and rate of dispersal for swimming and non swimming larvae were made by paired t tests. Only pairs in which both larvae were finally lost in the seagrass on the bottom were used (n = 27). The accuracy of the drogue measurements in predicting larval dispersal was determined by comparing the rates of drogue movement to the dispersal rates of swimming and non swimming larvae with paired t tests. 194 B.L. BINGHAM AND CM. YOUNG

The possibility that swimming does not cause a consistent directional response but simply increases the variation in dispersal parameter was investigated by comparing coefficients of variation (sample x/sample SD) of distance, time, and rate of dispersal for swimming and non swimming larvae. We tested for differences between the coefficients by comparing the ratio of the variances of the log-transformed data to an F distribution as suggested by Lewontin (1966). In addition to the scalar quantities of dispersal, we wished to analyse directional vectors. We did this with a parametric paired sample test for directional data (Zar, 1984). This allowed us to test for differences in the dispersal directions of swimming and nonswimming larvae (esand eN' respec­ tively). We hypothesized that the influence of swimming on dispersal would depend on current speed. We used regression analysis to examine differences in the dispersal vectors of pairs of swimming and nonswimming larvae as a function of current speed. The same method was used to compare dispersal vectors of each treatment (i.e., swimming and nonswimming) to the current vectors as measured with the drogue. To improve the linearity of the data for the regressions, y values (differences in directional vectors) were natural-log-transformed prior to analysis (Chatterjee & Price, 1977).

RESULTS

E. TURBINATA POPULATIONS

Transect surveys covered a variety ofbenthic habitats including beds of T. testudinum, Syringodium filiforme Ascherson, and Halodule wrightii Ascherson, limestone covered with sponges and gorgonians, sand plains, and areas of silt and detritus. However, in > 6000 rrr' of survey area, we did not observe a single E. turbinata colony except as epifauna on unanchored Rhizophora mangle prop roots on several small mangrove keys (Fig. 1).

TRANSPLANTS

Ofthe nine E. turbinata colonies transplanted into the seagrass bed, six (66.7%) died in the 36-day period of the experiment. This was much higher mortality than that experienced by colonies placed on the limestone bed or directly back on the mangrove roots (28.6 and 22.2 %, respectively). Colonies in the three locations differed in numbers

of zooids . colony - I, wet weight, zooid length, and reproductive activity (Table I). Pairwise comparisons revealed that colonies transplanted to the bare limestone were significantly heavier, had larger zooids, and showed much greater reproductive activity than colonies in the other habitats. Colonies recovered from the seagrass bed had

significantly fewer zooids . colony - 1 than those on mangrove roots or on the limestone bed. ChI a measurements showed significantly greater algal overgrowth on the seagrass DISPERSAL OF ECTEINASCIDIA TURBINATA 19S

TABU 1 Measurements of transplanted E. turhinata colonies. Data are presented as means with standard deviations in parentheses. H': Kruskal-Wallis statistic adjusted for tied ranks. *p < O.OS, **P < 0.01.

Measurement Transplant location

Grassbed Root Limestone

------~~------~ Number of zooids . colony I 27.0 74.4 120.0 8.7* (8.7) (S1.9) (93.6) Colony wet weight (g) 2.1 S.4 22.0 IO.S** (2.7) (4.8) (18.4) Zoid length (mm) 7.4 7.8 18.0 10.6** (S.4) (4.S) (3.3) Zooids brooding (~~,) O.O~

bed stakes (2.7 ± 0.5 pg) than on those from the limestone substratum (0.4 ± 0.7 pg; F = 25.99, p < 0.01).

TADPOLE DISPERSAL The large bright-orange E. turbinata tadpoles were easy to follow under the experi­ mental conditions and did not appear to be influenced by the presence of the diver (see

N 1

"'*' ~-_.----:::..::..- "

5 em/sec Fig. 2. Dispersal of swimming and nonswimming E. turbinata larvae measured on 28 November 1988. Observations are drawn as paired samples. Lengths of vectors represent dispersal rate (em' s - I). ---, swimming larvae; ----, nonswimming larvae. 196 B. L. BINGHAM AND C. M. YOUNG ~~ -, " ~ .'l ".. \ \\ " ~, -, ~,, :r -, " ,, "~,\ . , ~"- "- ~ <, \ ".'':

~\~ ~

r ~. " '. \ ~ . '.\~

~ <, ....

. \ \ '>''-'\.:--

' .: ~---- , ' .... \ \ Swimming ~ Non-swimming 5 em/sec , Current

Fig. 3. Dispersal of swimming and nonswimming E. turbinata larvae measured on 5 December 1988. Clusters of vectors represent paired samples and current direction as measured with a drogue weighted to float just below the surface. Lengths of vectors represent dispersal rate (em' s - I). DISPERSAL OF ECTEINASCIDIA TURBINATA 197

TABLE II Paired I tests for dispersal parameters of swimming and nonswimming E. turbinata tadpole larvae. *p = 0.05, ** p = 0.01.

Dispersal Treatment n x SD ------_.. _.- --_.._- I Rate(cm's- ) Swimming 27 9.1 5.3 2.51** Nonswimming 27 10.5 4.5 Time (5) Swimming 27 81.5 53.4 1.21 Nonswimming 27 95.2 55.0 Distance (cm) Swimming 27 687.6 507.4 2.04* Nonswimming 27 908.0 515.3

6 Swimming larvae

y = 3.52 - 0.192x P 0.001 " V} 4 r 2 0.33

Fig. 4. Differences in dispersal vectors ofswimming (es ) and nonswimming (eN)' E. turbinata larvae from current vectors (ee)' as a function of flow rate. Data were transformed to improve the linearity of the relationship. The p values indicate the significance of the regressions. 198 B. L. BINGHAM AND C. M. YOUNG also Young, 1986). On the first sampling day, we followed nine pairs of larvae (Fig. 2). On the second day, we followed an additional 29 pairs (Fig. 3). On both dates, small fishes attacked some of the larvae but immediately released them unharmed (see Young & Bingham, 1987). Statistical analysis of paired data showed no significant difference in the dispersal time of swimming and nonswimming tadpole larvae (Table II). Larvae did, however, differ in dispersal rate and distance with non swimming larvae moving slightly faster and traveling nearly 25%further, on average, than swimming larvae. The rate of movement of the drogue (7.4 ± 3.4 em s - I) was significantly lower than that of both the swimming (t = 3.04, p < 0.01) and the non swimming (t = 4.43, p < 0.01) larvae. Swimming did not increase variation in the rate, time, or distance of larval dispersal (Table 1II), indicating that swimming does not increase the spread of sibling larvae. Neither was there a consistent deviation in dispersal direction of swimming and non­ swimming larvae (F = 1.27, p > 0.25).

TABL!' 111 Comparisons of the coefficients of variation (ev) for swimming and nonswimming E. turbinata larvae. SD~,g = variance of the logarithms of the data. All of the F values are nonsignificant ip > 0.05).

_ .. _------...-.._------. Dispersal Treatment ev SD~)g F

---_... _------Rate Swimming 0.5465 0.1062 1.25 Nonswimming 0.4882 0.0847 Time Swimming 0.6502 0.0851 1.36 Nonswimming 0.5478 0.0625 Distance Swimming 0.7850 0.1909 1.73 Nonswimming 0.5389 0.1101

Regression analysis confirmed our hypothesis that divergence in dispersal directions of swimming larvae from the flow direction depends on flow rate (Fig. 4). However, Fig. 4 shows that a similar relationship held for non swimming larvae; as flow slowed, there were greater deviations in the trajectories of larvae from the flow direction. When the dispersal vectors of swimming and non swimming larvae were compared directly, there was no significant relationship to flow rate (Fig. 5). The drogues we released near Key 2 traveled over 3 km in the 4.5 h that they were followed (Fig. 1). The track of the drogues followed the channel direction until near the end of the outgoing tide. As the current speed fell, the influence of a west wind pushed the drogues toward Key 4. The mean swimming speed of H. turbinata larvae, as measured in laboratory experi­ ments, was 0.78 ± 0.46 cm : s - 1 (n = 10). The maximum observed swimming speed was 1.67 em . s - I. DISPERSAL OF ECTEINASCIDIA TURBINATA 199

6

y = 2.95 - 0.118x P = 0.078 r--. 2 CJ:)Z 4 r = 0.11

Vl CJ:) '--J .. c 2 ---.J .. .. • . • •

0 0 2 4 6 8 10 12 14 16 Flow Rate (em/sec)

Fig. 5. Differences in dispersal vectors of swimming (08 ) and nonswimming (0N ) E. turbinata larvae as a function of flow rate. Data were transformed to improve the linearity of the relationship. The p value indicates the significance of the regression.

DISCUSSION

It is generalIy agreed that swimming speeds of invertebrate larvae are too low relative to ambient currents to have a significant influence on large-scale horizontal movements except as influenced by vertical migrations (reviewed by Chia et aI., 1984). In this study of E. turbinata larval dispersal, swimming did not significantly influence the length of time that larvae were in the water column. Nor did it change the coefficient of variation, and hence the spread oflarvae relative to passive particles. Furthermore, there were no consistent differences in the direction of dispersal of swimming and non swimming larvae. The regression analyses presented in Fig. 4 demonstrate that the deviation in dispersal direction of swimming larvae from flow direction significantly increased as flow rate fell. However, because the same relationship held for non swimming larvae, swimming cannot be invoked to explain this result. The greater divergence seen at low flow may be the result of smalI-scale turbulence which strongly influenced the dispersal direction of larvae that traveled very short distances. This conclusion is substantiated by the analysis of dispersal direction of swimming vs. nonswimming larvae shown in Fig. 5. Although there appeared to be a trend toward greater differences in low flow, variability was high and the regression was nonsignificant, indicating that the magnitude of the divergence was independent of flow rate. This is not surprising since the lowest measured flow (i.e., 1.5 em' s - I) was nearly twice the average swimming speed of E. turbinata larvae as observed in laboratory trials. In this habitat, flow rates lower than larval 200 B. L. BINGHAM AND C. M. YOUNG swimming speeds are probably rare and of short duration. Larvae, therefore, should generally be able to exert little control over their direction of dispersal. Examination of individual dispersal measurements shows that vectors for swimming and non swimming larvae rarely fell exactly on the line of the surface currents (Fig. 3). The discrepancies were probably the result of differences in flow rate and direction with depth; measurements at the surface did not give a complete view of the flow regime to which the larvae were subjected. Contrary to our expectations, the drogue traveled more slowly than either swimming or non swimming larvae despite the fact that the latter were in deeper water which would be expected to flow more slowly. The reasons for this are unclear but may indicate that the drogue was affected by winds. Obviously this is weakness that should be considered in drift-tube and drogue modeling, especially for larvae that do not consistently remain in surface waters. Adult E. turbinata colonies in this study were found only on Rhizophora prop roots on several small isolated keys; mangrove roots on many of the other keys in this area were too shallow to permit survival of E. turbinata colonies at low tide. Moreover, all keys were separated by distances> 1 km in the direction of the prevailing tidal currents. No colonies were present in the extensive Thalassia or Syringodium beds near our study sites, nor were they found growing on the surfaces ofgorgonians as is occasionally seen in some areas. Appropriate habitats, therefore, were very patchy (Fig. I). Transplant experiments indicated that the seagrass beds between mangrove islands were unsuitable for E. turbinata; mortality was high, growth was low, and all reproduc­ tive activity ceased. Chi a measurements suggested that algal overgrowth may have been responsible for these effects. On the other hand, adult colonies attached to stakes in a bare limestone area did extremely well. Mortality was not much greater than that seen in the control treatment and colonies showed sudden increases in size and weight. Significantly, there was a 10-fold increase in the number of zooids brooding embryos, indicating an increased allocation of energy for reproduction. The cause of this dramatic change may have been the sudden increase in food availability as the colonies were removed from competition with the numerous massive sponges present on the mangrove roots. The absence of naturally occurring E. turbinata in the open sand and limestone areas is probably due to a lack of suitable hard substrata for attachment and growth. It has often been stated that morphological elaborations of an organism's propagules may be adaptations for increasing dispersal. This has been especially well documented for terrestrial plants in which seeds possess a variety of features (e.g., small size, buoyancy, wings, tufts, spines, hooks, sticky secretions, succulent fruits) which act to increase the distances that propagules travel and the spread among siblings (Tortora et al., 1970; Harper, 1977). Similarly, larval invertebrates are often equipped with anatomical features such as lipid droplets, gas bubbles, setae, spines or arms which are thought to keep larvae in upper water masses where dispersal is favored (reviewed by Chia et al., 1984). In some cases, larval swimming, as influenced by behavioral adap­ tations (e.g., phototaxis, geotaxis), enable larvae to move away from parental popu­ lations by exploiting water currents (Thorson, 1950; Wood & Hargis, 1971; Mileikovsky, 1972; Sulkin et al., 1980). DISPERSAL OF ECTEINASCIDIA TURBINATA 201 It might be predicted that E. turbinata tadpole larvae seeking to maximize dispersal during their short planktonic period would use their relatively strong swimming ability to reach surface waters where currents are generally strongest. However, our results show that the larvae moved quickly to the bottom thereby decreasing dispersal distances relative to their non swimming counterparts. This behavior may indicate that dispersal in this area is maladaptive and supports the hypothesis of Berrill (1975) that ascidian species in patchy habitats should restrict dispersal in order to maintain a local popula­ tion in a suitable area. The advantages and disadvantages of dispersal, although much discussed, have remained elusive. Strathmann (1980) has argued that many larvae swim much longer than they should in order to obtain maximal advantage from dispersal, and several workers (Shields, 1982; Grosberg & Quinn, 1986; Jackson, 1986) have pointed out that philopatry (the tendency to remain close to one's parent) has few negative consequences and may actually be advantageous under some conditions. In a model that incorporated habitat variability, Palmer & Strathmann (1981) showed that increases in fitness conferred by dispersal reached an asymptote at relatively small scales and determined mathematically that the greatest benefit of dispersal accrues between no dispersal and short-distance dispersal. Olson (1985) presented a model of dispersal based on his in situ observations of larvae of the ascidian Didemnum molle, on a series of patch reefs. This model predicted that at periods of low current, larvae would settle close to the parental population but at high currents would be washed to the next patch. This model may also describe the dispersal of E. turbinata in the Florida Keys study site. If provided with appropriate substratum (i.e., mangrove roots) newly released larvae may settle in 2-5 min (unpubl. data). The majority of larvae probably settle very near to the colonies from which they were released particularly if flow is slowed by the complex epifaunal communities on the mangrove roots. Our drogue study revealed that larvae advected from one island may potentially cross the areas between mangrove keys and settle in another patch. However, given the fact that drogues model only surface water flow and newly released larvae tended to swim rapidly to the bottom, it is difficult to imagine regular dispersal of larvae between keys. The probability that a larva washed away from one mangrove island will reach another suitable mangrove site during its short planktonic period is probably quite low. This could be an important source of larval wastage. A more likely method of transport over long distances is rafting of adults. Strong water flow and heavy epifaunal cover commonly combine to cause Rhizophora roots to break off (Bingham, 1990) and roots, with their associated epifauna, are sometimes found drifting with the currents. In this situation, one could envision locally sustained populations with rare exchange between neighboring keys through rafting of adult colonies. Results of this study suggest that there may not be a stereotypical behavior for E. turbinata larvae. In work done near Turkey Point, Florida in the northern Gulf of 202 B. L. BINGHAM AND C. M. YOUNG

Mexico, Young (1986) followed dispersing E. turbinata larvae and found behavior that differed markedly with that seen in the Florida Keys population (Table IV). Newly released tadpoles did not immediately swim toward the bottom, but spent nearly 90% of their time passively drifting or swimming upwards; both activities which tended to increase dispersal distance.

TABl.E IV Comparisons of the habitats and larval dispersal parameters for E. turbinata populations near Turkey Point, Florida (northern Gulf of Mexico) and ncar Big Pine Key, Florida (Florida Keys). ?, measurement not made.

Turkey Point I Big Pine Key?

------_._--_.'------Habitat Substratum Seagrass, sand Seagrass, sand, mangrove Water depth (m) \.5-2.5 \.0-\.5 Current (em' s I) < 5\.5 (I kn) \.5-14.3 Larval dispersal Age at testing (h)

I Young (1986) and Young (unpubl. data). 2 Present study and Bingham (unpubl. data).

These dichotomous behavioral patterns may reflect adaptations to local habitat conditions. Adult colonies in the Turkey Point population are generally found attached to blades of T. testudinum in extensive seagrass beds; no mangroves are present in that region. Settlement experiments have demonstrated that larvae readily settle on Thalassia blades (Table IV). Appropriate sites are, therefore, numerous and homogeneously dis­ tributed. As a result, selective pressures should not favor reduced dispersal and retention near parental colonies. In contrast, the Florida Keys E. turbinata population was unable to survive in the Thalassia beds; mortality is high and all reproductive activity ceases. In laboratory experiments, larvae settled very quickly when presented with mangrove roots, but would not settle on seagrass blades (Table IV). Larval swimming behavior also differed as newly released tadpoles minimized dispersal by moving directly to the bottom. The DISPERSAL OF ECTEINASCIDIA TURBINATA 203 cause of this behavior is unknown, but may have resulted from a negative phototaxis. In the mangrove root habitats where larvae are naturally released, this behavior might cause them to remain in the darkened area among the roots rather than swimming out into faster flowing water where the probability of advection, and mortality, is high. Further study is needed to test this hypothesis. An important function of E. turbinata larvae is to locate a suitable settlement site where the probability of growth and survival is high. In the patchy mangrove habitat studied, local adaptation appears to have selected for unique swimming and settlement behaviors which minimize dispersal and enable larvae to settle in close proximity to parental colonies. Swimming, in this case, is not a method to enhance dispersal as is the case for some invertebrates, but rather a mechanism to resist advection to unsuitable sites.

ACKNOWLEDGMENTS

We thank L. Cameron, A. Davis, and I. Bosch for valuable field assistance. I. Bosch, L. Cameron, W. Herrnkind, R. Mariscal, D. Simberloff, D. Thistle, R. B. Forward, A. Shanks, and an anonymous reviewer commented on earlier versions of the manu­ script. W. Herrnkind assisted with data analysis.

REFERENCES

Bainbridge, R., 1953. Studies on the interrelationships of zooplankton and phytoplankton. Mar. Bioi. Assoc. U.K., Vol. 32, pp. 385-347. Berrill, N.J., 1975. Chordata: Tunieata. In, Reproduction of marine invertebrates II. Entoprocts and lesser coelomates, edited by A.C. Giese & J. S. Pearse, Academic Press, New York, pp. 241-282. Bingham, B. L., 1990. The ecology of epifaunal communities on prop roots of the red mangrove, Rhizophora mangle. Dissertation, Florida State University, 219 pp. Bousfield, E. L., 1955. Ecological control of the occurrence ofbarnaeles in the Miramichi Estuary. Natl. Mus. Can. Bull. Bioi. Ser., Vol. 137, pp. 1-65. Butman, C. A.; 1987. Larval settlement of soft-sediment invertebrates: the spatial scales of pattern explained by active habitat selection and the emerging role of hydrodynamic processes. Oceanogr. Mar. Bioi. Annu. Rev., Vol. 25, pp. 113-165. Butman, C. A., J. P. Grassle & E.J. Buskey, 1988. Horizontal swimming and gravitational sinking of Capitella sp. I (Annelida: Polychaeta) larvae; implications for settlement. Ophelia, Vol. 29, pp.43-57. Carriker. M. R.. 1961. Interrelation of functional morphology, behavior, and autecology in early stages of the bivalve Mercenaria mercenaria, J. Elisha Mitchell Sci. Soc., Vo!. 77, pp. 168-241. Chatterjee, S. & B. Price, 1977. Regression analysis by example. John Wiley & Sons, New York, 228 pp. Chia, F. S., J. Buckland-Nicks & C. M. Young, 1984. Locomotion of marine invertebrate larvae: a review. Can. 1. Zool., Vol. 62, pp. 1205-1222. Cronin, T. W., 1982. Estuarine retention oflarvae ofthe crab Rhithropanopeus harrisii. Estuarine Coastal Shell" Sci., Vol. 15, pp. 207-220. Davis, A. R., 1987. Variation in recruitment of the subtidal colonial ascidian Podoclavella cylindrica Quoy & Gaimard: the role of substratum choice and early survival. J. Exp. Mar. Bioi. Ecol., Vol. 106, pp. 57-7 I. Fadlallah. Y.II. & J. S. Pearse, 1982. Sexual reproduction in solitary corals: overlapping oogenie and brooding cycles, and benthic planulas in Balanophy//ia elegans. Mar. Biol., Vol. 71, pp. 223-231. Gerrodcttc, T., 1981. Dispersal of the solitary coral Balanophvllia elegans by demersal planular larvae, Ecology, Vo!. 62, pp, 611-6 I9, 204 B. L. BINGHAM AND C. M. YOUNG

Grosberg, R. K. & J. F. Quinn, 1986. The genetic control and consequences of kin recognition by the larvae of a colonial marine invertebrate. Nature (London), Vol. 322, pp. 456-459. Harper, J. L., 1977. Population biology ofplants. Academic Press, London, 892 pp. Herrnkind, W.F., M.J. Butler, IV & R.A. Tankersley, 1988. The effects of siltation on recruitment of spiny lobsters, Panulirus argus. Fish. Bull. NOAA, Vol. 86, pp. 331-338. Jackson, J.B.C., 1986. Modes of dispersal of clonal benthic invertebrates: consequences for species' distributions and genetic structure of local populations. Bull. Mar. Sci., Vol. 39, pp. 588-606. Kirk, R. E., 1982. Experimental design: procedures for the behavioral sciences. Brooks/Cole Publishing, Monterey, California, 911 pp. Lee, H., 1984. Fast swimming speeds of ciliated marine invertebrate larvae: potential importance at the time of settlement. Am. Zool., Vol. 24, p. 131A. Lewontin, R.C., 1966. On the measurement of relative variability. Syst. Zool., Vol. 15, pp. 141-142. Mileikovsky, S.A., 1966. The range of dispersal of the pelagic larvae of bottom invertebrates by ocean currents and its distributional role on the example of gastropoda and lamellibranchia. Oceanology, Vol. 6, pp. 396-404. Mileikovsky, S. A., 1971. Types of larval development in marine bottom invertebrates, their distribution and ecological significance: a re-evaluation. Mar. Biol., Vol. 10, pp. 193-213. Mileikovsky, S. A., 1972. The "pelagic larvaton" and its role in the biology of the World Ocean, with special reference to pelagic larvae of marine bottom invertebrates. Mar. Biol., Vol. 16, pp. 13-21. Mileikovsky, S. A, 1973. Speed of active movement of pelagic larvae of marine bottom invertebrates and their ability to regulate their vertical position. Mar. Biol., Vol. 23, pp. 11-17. Olson, R. R., 1985. The consequences of short-distance larval dispersal in a sessile marine invertebrate. Ecology, Vol. 66, pp. 30-39. Olson, R. R. & R. McPherson, 1987. Potential vs. realized larval dispersal: fish on larvae of the ascidian Lissoclinum patella Gottschaldt. J. Exp. Mar. Bioi. Ecol., Vol. 110, pp. 245-256. Palmer, A. R. & R. R. Strathmann, 1981. Scale of dispersal in varying environments and its implications for life histories of marine invertebrates. Oecologia (Berlin), Vol. 48, pp. 308-318. Rimmer, D. W. & B.F. Phillips, 1979. Diurnal migration and vertical distribution of phyllosoma larvae of the western rock lobster Panulirus cygnus. Mar. Biol., Vol. 54, pp. 109-124. Robertson, A. E. & R. K. Howard, 1978. Dicl trophic interactions between vertically-migrating zooplankton and their fish predators in an eelgrass community. Mar. Biol., Vol. 48, pp. 207-213. Shields, W.M., 1982. Philopatry. inbreeding, and the evolution of sex. State University New York Press, Albany, 245 pp. Singarajah, K. V., 1969. Escape reactions of zooplankton: the avoidance of a pursuing siphon tube. 1. Exp. Mar. Bioi. Ecol., Vol. 3, pp. 171-178. Strathmann, R. R., 1980. Why docs a larva swim so long? Paleohiology, Vol. 6, pp. 373-376. Sulkin, S. D., W. Van Hcukclcm, P. Kelly & L. Van Heukelern, 1980. The behavioral basis of larval recruitment in the crab Callinectes sapidus Rathbun: a laboratory investigation of ontogenetic changes in geotaxis and barokincsis. Bioi. Bull. (Woods Hole. Mass.), Vol. 159, pp. 402-417. Thorson, G., 1950. Reproductive and larval ecology of marine bottom invertebrates. Bioi. Rev. Camb. Philos. s«: Vol. 25, pp. 1-45. Thorson, G., 1964. Light as an ecological factor in the dispersal and settlement of larvae of marine bottom invertebrates. Ophelia, Vol. I, pp. 167-208. Tortora, G.J., D.R. Cicero & H.1. Parish, 1970. Plant form and function: an introduction to plant science. Macmillan, New York, 563 pp. Wood, L. & W. J. Hargis, Jr., 1971. Transport of bivalve larvae in a tidal estuary. In, Fourth Eur. Mar. Bioi. Svmp., edited by D.J. Crisp, Cambridge University Press, Cambridge, pp. 29-43. Young, C.M., 1986. Direct observations of field swimming behavior in larvae of the colonial ascidian Ecteinascidia turbinata. Bull. Mar. su.. Vol. 39, pp. 279-289. Young, C. M. & B.L. Bingham, 1987. Chemical defense and aposematic coloration in larvae of the ascidian Ecteinascidia turbinata. Mar. Bioi., Vol. 96, pp. 539-544. Zar, J. H., 1984. Biostatistical analysis. Prentice-Hall, New Jersey, 718 pp.