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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: ©1988 Marine Biological Laboratory. The final published version of this manuscript is available at http://www.biolbull.org/. This article may be cited as: Young, C. M., Gowan, R. F., Dalby, J., Jr., Pennachetti, C. A., & Gagliardi, D. (1988). Distributional Consequences of Adhesive Eggs and Anural Development in the Ascidian Molgula pacifica (Huntsman, 1912). The Biological Bulletin, 174(1), 39‐46. Reference: Biol. Bull. 174: 39—46.(February, 1988) Distributional Consequences of Adhesive Eggs and Anural Development in the Ascidian Molgula pacifica (Huntsman, 1912) CRAIG M. YOUNG', RICHARD F. GOWAN2, JAMES DALBY JR.3, CATHERINE A. PENNACHETTI2, AND DAVID GAGLIARDI2 Bamfield Marine Station, Bamfield, British Columbia, Canada VOR JBO Abstract. Molgula pacifica (Huntsman) is a recently Molgulidae (Lacaze-Duthiers, 1874; Damas, 1902; Ber rediscovered ascidian that occupies shallow subtidal rill, 193 1) and Styelidae (Millar, 1954, 1962), though rocks on wave-swept coasts ofBritish Columbia. Individ within the Subphylum Urochordata, tailed larvae are uals occur most abundantly at sites with intermediate ex also lacking in the development ofmost thaliaceans (Ber posure at or near 4 m depth. On a scale of centimeters, rill, 1950). Anural development has been previously ob they are highly aggregated. Molgula pacifica is hermaph served in 10 molgulid species (Berrill, 1931), eight of roditic, self-fertile, and oviparous. Embryos develop on which live on sandy or muddy bottoms. Only two uro the bottom without passing through a typical tadpole dele species, Molgula oculata and M. occidentalis, in stage. Each ofthe egg follicle cells contains a single large habit soft bottoms. Conversely, on hard substratum, 13 adhesive vacuole that occupies most ofthe cell volume. of the 15 molgulid species with known developmental Shortly after spawning these vacuoles rupture, causing modes demonstrate normal urodele development (Ber the follicle cells to secrete a sticky mucus coat that ad sill, 1931; Whittaker, 1979; Torrence and Cloney, 1981). heres the egg to the substratum. Juveniles hatch and Both known anural styelids, Pelenaia corrugata (Millar, move away from the chorion using epidermal ampullae, 1954) and Polycarpa tinctor(Millar, 1962), live on sandy as reported for other anural molgulids. Adhesive eggs substrata. Berrill (193 1) reasoned that urodele develop may be an adaptation that permits anural development ment is an ancestral condition that gave rise to anural in high-energy hard-bottom habitats. Egg adhesion may development among sand-dwelling species because lar also explain the small-scale distribution ofthe species. val swimming and habitat selection have little value where the substratum is flat and homogeneous. By exten Introduction sion ofthis argument, he suggested that the few attached “¿.. it is very probable that(anural development) is to be anural species represent reinvasions by sand-dwelling correlated with the outstanding peculiarity ofthe family, forms of the ancestral hard-bottom habitat (Berrill, namely, its unattached sand-flat habitat and its adapta 1931). Whittaker's (1979) discovery ofvestigial tail mus tion to such an existence.―(Berrill,1931) cle acetylcholinesterase in anural species provides mdi Most ascidians pass through a “¿urodele―or tadpole rect support for these ideas. Although we might expect larval stage. Suppression of the tailed tadpole (termed that anural species colonizing rocky substrata would “¿anuraldevelopment―) is known only in the families somehow compensate for their inability to swim, no compensatory features have been described. Received23July 1986;accepted28October 1987. Huntsman (1912) described Molgula pacifica from a 1 Division ofMarine Science, Harbor Branch Oceanographic Institu single specimen collected at Ucluelet, British Columbia. ton, 5600 Old Dixie Hwy., Ft. Pierce, FL 34946 (author to whom cor Besides a redescription by Van Name (1945) based on respondenceshouldbe addressed). this same specimen, nothing more is known about the 2 Department of Biology, University of Victoria, Victoria, British Columbia, Canada V8W 2Y2. biology of this species. We recently discovered a large 3 Department ofBiological Science, Florida State University, Talla subtidal population of Molgula pacijica in Barkley hassee, FL 32306. Sound, British Columbia, approximately 35 km from the 39 40 C. M. YOUNG ET AL. Figure 1. Map ofthe study region on the southeastern edge ofBarkley Sound, British Columbia, Can ada. Arrows indicate subtidal sites that were systematically surveyed for Molgula pacifica populations. Circles attached to the tails ofthe arrows give qualitative density values as follows: closed circle: abundant; open circle:absent;half-shadedcircle:presentin lownumbers. type locality. In this paper, we describe the general char At an intermediate scale, quantitative data were taken acteristics of this species' habitat, give a quantitative at the Blowhole site on the southern shore of Barkley analysis ofdistributional patterns on several scales, pres Sound, where Molgula pacj/ica occurred abundantly. ent a general description of its anural development, and Within each oftwo long surge channels (called Blowhole report an unusual developmental adaptation that may sites 1and 2 hereafter), we counted all individuals in five permit exploitation of high-energy subtidal habitats. A randomly positioned 50 X 50 cm quadrats at each of redescription of the species will be presented elsewhere three depths (6 m, 4 m, 2 m). Within each depth, three (Pennechetti et al., in prep.). habitat types were surveyed: (1) gentle slopes or horizon tal surfaces in channel bottoms, (2) vertical surfaces on Materials and Methods the sides ofchannels, and (3) horizontal or sloping ridges or plateaus between surge channels. The data for each Distributionalsurveys site were analyzed by 2-way ANOVA in which both fac We studied the distribution of Molgula pacifica at tors (depth and habitat) were fixed. three scales. Large-scale qualitative surveys were made at Small-scale (within-habitat) distribution was quanti 16 sites along a 10 km exposure gradient in Barkley fled from underwater photographs taken ofthe rock sur Sound, British Columbia. At each site, at least 4 divers face. At each of 4 sites (3 at Blowhole, 1 at Execution began at 10 m depth and worked up the slope, stopping Rock), we photographed a 6 X 6 grid of contiguous rec to search more carefully at 6 m, 4 m, and 2 m depths. No tangular quadrats on rock walls or steep slopes. Each quantitative data were taken on these survey dives. Field quadrat encompassed an area 15 X 22 cm. Transparen notes consisted of observations on sizes of individuals, cies were projected and counted by at least three individ animal and plant associates, depth ofoccurrence, surface uals before the data were compared with expected ran angles ofoccupied rocks, and wave surge. dom (poisson) distributions using goodness of fit tests. DISTRIBUTION AND ANURAL DEVELOPMENT IN MOLGULA 41 80 dissection, then macerated through 253 @smnitex mono Site 1 Ridge filament mesh. Other individuals released gametes spon Wall taneously in seawater tables. Following fertilization, ex Bottom cess sperm were removed by repeated rinsing with fresh 60 seawater. Cultures were maintained at lO°—12°Cin a shallow, flow-through seawater table. We attempted to induce spawning by light shock by incubating eight mdi viduals in darkness for 12.0 h, then exposing them to the 40@ subdued light ofthe laboratory. Follicle cells ofdissected eggs did not secrete adhesive C,. spontaneously. We induced holocrine secretion for his tological study by placing the eggs in hypotonic seawater E 20 (1 part seawater, 2 parts distilled water). Eggs treated in Ct) this way appeared identical to eggs spawned naturally in the laboratory. Embryos were fixed in Torrence's fixative for 2.5 h, > followed by three 20-minute rinses in Torrence's buffer 2m 4m 6m (Torrence and Cloney, 1981). Embryos were fixed, C rinsed, and dehydrated on ice, then brought to room 80 temperature during the first change ofabso!ute isopropa >@ Site 2 no!. They were embedded in Luft's Epon 812 (Luft, 1961) and sectioned on a Reichert OMU2 ultramicro U) C tome using glass knives. Thin sections were stained with a) 60 uranyl acetate, post-stained with lead citrate, and exam 0 med at 60 kV using a Phillips EM 300 electron micro scope. To aid in the recognition ofmucus, l-@imsections were stained with an aqueous solution of0.25% toluidine 40 blue in 0.5% sodium borate (Humason, 1967; R. Burke, pers. comm.). Living embryos and juveniles were observed and pho tographed on Leitz or Zeiss photomicroscopes using 20 phase contrast, bright field, or Nomarski optics. Results Distribution 2m 4m 6m The distribution ofMolgula pacifica showedclearpat terns at three scales. Figure 1shows the large-scale distri Depth bution, as determined by qualitative surveys, within the southern portion of Barkley Sound and the Deer Island Figure 2. Densities ofMolgulapacifica at three depth/habitat com group. The mouth of the sound experiences the rough binations in two surge channel systems at the Blowhole site. Error bars represent one standard deviation on each side ofthe mean. Data analy surfand surge conditions ofthe open Pacific coast. Wave sis is presented in Table!. action decreases regularly along the southern shore of
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