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FAU Institutional Repository FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. 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 Ecteinascidia 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. Florida 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 Gulf of Mexico. 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 <iJ 1991 Elsevier Science Publishers B.V. (Biomedical Division) 190 B. L. BINGHAM AND eM. YOUNG including: (1) increased dispersal by movement oflarvae into surface currents (Thorson, 1964), (2) avoidance of predators, either by escape responses (Singarajah, 1969) or by vertical migrations (Robertson & Howard, 1978), (3) habitat selection at the time of settlement (Lee, 1984; Butman, 1987), (4) transport among food patches (Bainbridge, 1953), and (5) control of speed and direction of horizontal advection by vertical move­ ments among water masses (Bousfield, 1955; Carriker, 1961; Wood & Hargis, 1971; Cronin, 1982). Larval swimming speeds tend to be much lower than the speeds of ambient currents (Mileikovsky, 1973; Chia et al., 1984; Butman, 1987). Consequently, most workers have concluded that larvae (with the exception oflarge, active swimmers such as pueruli of lobsters; Rimmer & Phillips, 1979; Herrnkind et al., 1988) should be incapable of significantly altering their horizontal position without using currents (Mileikovsky, 1966; Butman et al., 1988). This prediction, however, is based only on comparisons of laboratory swimming speeds with large-scale flow parameters; little experimental evi­ dence, particularly in the field, is available to support it. Many animals, including colonial ascidians, bryozoans, and some cnidarians, brood embryos to hatching and release short-lived lecithotrophic larvae. Because such larvae spend little time in the water, even minor differences in swimming speed or behavior could have important consequences for the direction of dispersal and the spread of siblings. Although dispersing larvae of several ascidian species have been followed in the field (Olson, 1985; Young, 1986; Olson & McPherson, 1987; Davis, 1987; Stoner, pers. comm.), the relationship between swimming and dispersal has not been investi­ gated experimentally for any invertebrate species. In this paper, we describe experiments that were done to determine whether swimming affects larval dispersal of the ascidian Ecteinascidia turbinata Herdman (Phlebobranchia, Perophoridae). In particular, we wished to test the hypothesis that larvae of this species disperse as passive particles against the alternative that swimming behavior influences the direction, speed, or distance that larvae travel. We also examined adult distributions and did transplant experiments to determine how settlement site, as influenced by dispersal behavior, might contribute to adult survival. We chose E. turbinata as the test species for three reasons: (1) The large bright-orange tadpole larvae are easy to see under field conditions (Young, 1986). (2) Compared to most invertebrate larvae, colonial ascidian tadpoles are very strong swimmers (Mileikovsky, 1973; Chia et al., 1984) and might be capable of influencing their dispersal. (3) In the Florida Keys where this work was done, E. turbinata occurs in a patchy habitat where larval dispersal may be risky and where selective pressures should favor larval behavior which enhances the probability of encountering widely separated patches. DISPERSAL OF ECTEINASCIDIA TURBINATA 191 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 Rhizophora mangle 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
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