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Ascidian Cannibalism Correlates with Larval Behavior and Adult Distribution

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Ascidian Cannibalism Correlates with Larval Behavior and Adult Distribution FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1988 Elsevier Ltd. The final published version of this manuscript is available at http://www.sciencedirect.com/science/journal/00220981 and may be cited as: Young, C. M. (1988). Ascidian cannibalism correlates with larval behavior and adult distribution. Journal of Experimental Marine Biology and Ecology, 117(1), 9-26. doi:10.1016/0022-0981(88)90068-8 J. Exp. Mar. Bioi. £Col., 1988, Vol. 117, pp. 9-26 9 Elsevier JEM 01042 Ascidian cannibalism correlates with larval behavior and adult distribution Craig M. Young Department ofLarval Ecology. Harbor Branch Oceanographic Institution, Fort Pierce, Florida. U.S.A. (Received 24 March 1987; revision received 9 December 1987; accepted 22 December 1987) Abstract: In the San Juan Islands, Washington, solitary ascidians .that occur in dense monospecific aggregations demonstrate gregarious settlement as larvae, whereas species that occur as isolated individuals do not. All gregarious species reject their own eggs and larvae as food, but nongregarious species consume conspecific eggs and larvae. Moreover, the rejection mechanism is species-specific in some cases. Correla­ tion analysis suggests that species specificity of the rejection response has a basis in siphon diameter, egg density, and larval size, but not in number of oral tentacles, or tentacle branching. One strongly cannibalistic species, Corella inflata Huntsman, avoids consuming its own eggs and newly released tadpoles by a unique brooding mechanism that involves floating eggs, negative geotaxis after hatching, and adult orientation. Key words: Ascidian; Cannibalism; Distribution; Larva; Settlement behavior INTRODUCTION Many sessile marine invertebrates, including filter-feeders such as mussels, oysters, barnacles and ascidians, occur in discrete, dense aggregations. Gregarious larval settle­ ment (defined here as preferential attachment on or near established conspecifics) probably explains aggregation in many species (reviewed by Meadows & Campbell, 1972; Scheltema, 1974; Crisp, 1976) but gregarious settlement is only one of many processes that result in small-scale aggregations among sessile invertebrates. Others include spatial variability in mortality of juveniles or adults (Keough, 1986; Young & Chia, 1984), orientation responses that result in nonrandom distribution oflarvae in the plankton (Grosberg, 1982), larval responses to habitat cues not associated directly with adult con specifics (Scheltema, 1974), and hydrographic processes controlling the supply of larvae (Gaines & Roughgarden, 1985; Butman, 1987). Although postsettle­ ment processes can change the grain size or intensity (sensu Pielou, 1977) of an aggregation by eliminating individuals, small-scale clumps cannot be formed by any mechanism unless recruitment initially occurs (either preferentially or otherwise) near con specifics. Moreover, long-term maintenance of a clump implies recruitment to offset adult mortality. Contribution 614 of Harbor Branch Oceanographic Institution. Correspondence address: C. M. Young, Department of Larval Ecology, Harbor Branch Oceanographic Institution, 5600 Old Dixie Highway, Fort Pierce, FL 34946, U.S.A. 0022-0981/88/$03.50 © 1988 Elsevier Science Publishers B.Y. (Biomedical Division) 10 C.M. YOUNG Paradoxically, some of the most formidable predators on planktonic invertebrate larvae are the same benthic filter-feeders that form dense, long-lived aggregations (reviewed by Thorson, 1950; 1966; Young & Chia, 1987). Predation by such filter­ feeders may amount to cannibalism, since conspecific larvae (including kin) are often not distinguished from other food (Cerruti, 1941; Thorson, 1950; Barnes, 1959; Timko, 1979; Young & Gotelli, 1988). In this respect, larval cannibalism can be viewed as a process that counteracts the mechanisms by which aggregations are established and maintained. Intuition dictates that larvae should not recruit into dense aggregations of adult filter-feeders (Thorson, 1950; Woodin, 1976; Cowden etal., 1984; Young & Gotelli, 1988), but such aggregations often include young individuals. Mechanisms by which larvae escape consumption by adults are generally unknown. Have specific mechanisms evolved for minimizing the impact of intraspecific predation on larvae? If so, are the mechanisms present in the adult stage or the larval stage? Larvae of intertidal mussels often settle on filamentous substrata outside adult clumps (Block & Geelen, 1958; Bayne, 1965); juveniles then migrate passively into the clump after they have grown too large to be eaten (Bayne, 1964; Seed, 1969). Eggs of the sand dollar Dendraster excentricus may be protected from adults by their gelatinous coats (Timko, 1979), but this observation begs the question of how larvae (without jelly coats) settle into dense beds of adults (Highsmith, 1982) without being consumed. Although a number of presumed larval defense mechanisms have been documented (reviewed by Young & Chia, 1987), none functions solely in the prevention of cannibalism and very few are thought to be effective against large filter-feeders (Cowden et al., 1984). Larval cannibalism has not previously been documented in the Ascidiacea, a diverse group of benthic filter-feeders. In the present paper, I show that cannibalism occurs in several of the 13 species of solitary ascidians living in subtidal habitats in the San Juan Islands of Washington State and demonstrate that the incidence oflarval cannibalism correlates with small-scale distributional patterns and larval behaviors of the various species. I also discuss the morphological basis of larval rejection, show how brooding reduces cannibalism in one species, and argue that mechanisms preventing cannibalism are appropriate preadaptations for the evolution of gregarious settlement behavior. MATERIALS AND METHODS SOURCES OF ADULT AND LARVAL ASCIDIANS Ascidians were collected by dredging or diving in waters surrounding the San Juan Islands, Washington (map in Young, 1985). One species that occurred rarely in the San Juans, Styela montereyensis (Dall), was collected from intertidal pilings in Neah Bay, Washington. Throughout the study, adults of most species were maintained in large running seawater aquaria at Friday Harbor Laboratories, where they filtered actively and survived for long periods of time (over a year in some cases), feeding on plankton ASCIDIAN CANNIBALISM AND LARVAE 11 that entered through the seawater system. These adults were used as predators in experiments, generally without removing them from their tanks or otherwise disturbing them. Larvae were reared in vitro from gametes spawned in the laboratory or dissected from adults (Young, 1982). Following fertilization, cultures were washed repeatedly to remove excess sperm, then maintained in fingerbowls of filtered seawater resting in shallow, running seawater aquaria to control temperature. The water in each culture was changed several times per day until the tadpoles hatched. Larvae were always used within 24 h after hatching. PREDAnON ON GAMETES AND LARVAE To assay larval predation in the laboratory, I gently pipetted larvae or eggs, one at a time, into the incurrent flows of filtering adult ascidians. Reactions of the adults were observed. Expulsion of larvae or eggs was easily noted, as it was accompanied by a major contraction of the body wall muscles of the adult. In transparent species (Corella injlata Huntsman, C. willmeriana Herdman), it was possible to observe the fates of larvae through the tunic, using a dissecting microscope. If eggs and larvae of all 12 species were offered to adults of all species, 288 different combinations would have to be attempted with sufficient replication for analysis. Because of time constraints and the unavailability of embryos from all species during appropriate work periods, only a few of the potential heterospecific trials were attempted. Spermatozoa removed by dissection from four ascidian species were diluted in seawater, filtered through 100-.um Nitex to remove large particles, then introduced by pipette into the siphons of adult ascidians. Rejection responses were noted, as explained above. LARVAL BEHAVIOR As part of a larger study of comparative larval behavior (Young & Braithwaite, 1980; Young, 1982; Young & Chia, 1985), I investigated substratum preferences of larvae by offering multiple substrata (including adult tunic, rocks, shell fragments, etc.) to groups oflarvae in Petri dishes. Forthis paper, I willpresent only the data comparing settlement on adult tunic and rock, as this comparison gives a simple estimate of gregariousness. Nevertheless, in each experiment, either three or four substratum types were replicated within dishes, arrayed in a Latin square and held in place by agar. During the study, it became apparent that the consistent adult field orientation of Corella injlata (Child, 1927)could reduce the likelihood of cannibalism on an individual's own progeny. I investigated whether the adult orientation originated at settlement or later by allowing tadpoles to settle on a vertical glass plate in a large culture. After settlement, juveniles were cultured vertically on the same plate until their siphons opened. Orientations of the mid-sagittal plane (line between siphons) were then recorded using a dissecting microscope. 12 C.M. YOUNG DISTRIBUTION, POPULATION STRUCTURE, AND ORIENTATION OF ADULTS Small-scale spatial patterns of adult ascidians were
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