BULLETIN OF MARINE SCIENCE, 45(2): 253-276, 1989 FORM AND FUNCTION IN THE ASCIDIACEA Patricia Kott ABSTRACT Adult ascidians compensate for their inability to move by the shape of the body, orientation of the siphons, structure of the pharyngeal wall, and consistency of the test. Many of these features appear to enhance the organism's capacity to use mechanical energy available in the environment to maximize its interactions with it. Many are convergent features occurring irrespective of phylogeny while others are major determinants of phylogenetic diversity in the Ascidiacea apparently effected by one or the other pressure for protection from predation or mechanical damage, and for feeding. Species of the Class Ascidiacea (subphylum Tunicata) are solitary or colonial filter feeding organisms surrounded by, or embedded in, an external test secreted by the ectoderm (Goodbody, 1974). They have an atrial (peribranchial) cavity which envelops the dorsum and sides of the large perforated pharynx (branchial sac). This cavity has a dorsal aperture to the exterior either directly or (in many colonial taxa) through cavities (cloacal chambers) in the test (Fig. 1). Gametes and faecal pellets are discharged into the atrial cavity and, with the water filtered through the walls of the pharynx, they are ejected from the body through the atrial aperture (Fig. 1). The flow of water through the body (ciliary current) is generated by cilia lining the pharyngeal perforations (stigmata). Colonies form by replication of individual zooids, the replicates remaining in the one more or less integrated colony, although colonies of many species can be divided, and in some cases are known to clone spontaneously (Ryland et aI., 1984). All species are fixed to the substrate. Throughout the Ascidiacea, the needs to draw in food-laden and oxygenated water, to expel the spent water, to be firmly fixed to a substrate and to be protected from predators, are universal. Morphological responses to the environment must compensate for an inability to move, and for the lack of appendages, mouth parts and many of the sense organs that are available to many other animal groups. The ascidian's advantages are that the test is, with certain limits, flexible-the whole body and the apertures can be contracted by muscular action; and responses to the environment can be effected by growth. Nevertheless, the most conspicuous features (such as general body shape, size, texture of the test and colonial organization) that have allowed the radiation of this group of organisms into almost every marine habitat that exists are characteristics at higher taxon levels-ordinal and familial-rather than at generic and species level. They are accordingly characters imposed by selective pressures and genetically controlled. Within this framework the morphological structures that maximize an ascidian's interactions with particular sets of environmental conditions demonstrate a high degree of convergence. This results in a degree of uniformity in the external appearance of ascidian species, and leads to difficulties in distinguishing taxa. Accounts of morphological adaptations and growth responses to the environ- ment are scattered through the taxonomic literature, often either overlooked or their significance not recognized. In this paper, in memory of Donald Abbott, much of this material is drawn together to document the structures, the novel 253 254 BULLETIN OF MARINE SCIENCE, VOL. 45, NO.2, 1989 b ap me ml -;;: Ul '"o '0 r r 'i' det ;:- <! dct oes int st posterior ventral cap C . baP. } . .". .,.' :,,,,;, ..,'"'' ""'~. ---'.,'": r-:" ....~~~.~.•..~~~";~,'). ccc I',:' ' th sC"~ pb { bs :~;;, t r ab st int :}~: ::~ "'~ pab .~ ~" :.:; \ ;:;i ~I if: h "ii .. ;,:- ~\~Iii, !Ji:,.. ~!<& .~1rL:;,;,~---_~.: Figure I. a, A solitary ascidian (phlebobranch) from the left side (diagrammatic). b, oblique section of a solitary ascidian (diagrammatic). c, aplousobranch zooids opening into a cloacal cavity (diagram- matic). Symbols: ab, abdomen; ap, atrial aperture; bap, branchial aperture; bs, branchial sac; bt, branchial tentacles; cap, cloacal aperture; ccc, common cloacal cavity; dim, dorsal lamina; e, endocarp; end, endostyle; h, heart; int, intestine; me, circular muscles; ml, longitudinal muscles; oes, oesophagus; pab, posterior abdomen; pb, peri branchial (atrial) cavity; r, rectum; st, stomach; stig, stigmata; t, test; th, thorax; vs, ventral vessel. KOTf: ASClDIAN FORM AND FUNCTION 255 and innovative solutions to living that ascidians display, that complement the natural flexibility and plasticity of the test. Accounts ofthe taxonomy and phylogeny of the Ascidiacea are given in Berrill (1950), Van Name (1945), Goodbody (1982), and Kott (1969, 1985). Millar (197 I) and Goodbody (1974), respectively, have discussed the biology and physiology of the class. Generally, unless otherwise indicated, phlebobranch and stolido- branch species referred to in this work are from Kott (1985); and aplousobranch species are from Kott (1972a; 1973; 1980; 1981a, and in preparation I). FEEDING Ascidians are very efficient filter feeders, filtering between 24 and 540 ml per hour per gm wet weight of animal (Goodbody, 1974). Under natural conditions ascidians can be observed with both siphons wide open, while the cilia lining the branchial stigmata pump a stream of water through the branchial wall. Fiala-Medioni (1978a, 1978b) found, in five solitary species (Ciona intestinalis, Phallusia mammillata, Ascidia mentula, Styela plicata and Microcosmus sabatieri), that the feeding rythum was maintained without major changes in the velocity of the feeding current. Spontaneous, rhythmic closure of the siphons accompanied by "squirting" of up to a third of the capacity of the pharynx and the atrial cavity, followed by relaxation and the intake of fresh water (Hoyle, 1953), occurred only at higher temperatures or in connection with the release of gametes (Fiala-Medioni, 1978b, 1978c). Although ciliary activity stops during "squirting," prolonged closure of the apertures and ciliary arrest occurs only very infrequently (Pennachetti, 1984). The filtration membrane is the mucous sheet, secreted by the endostyle and moved dorsally over the inner walls of the pharynx to the dorsal mid-line. It has been shown to be a very fine filter, capable of retaining particles as small as 0.0005 mm (Flood and Fiala-Medioni, 1979; 1981). The amount offood obtained by a filter feeding animal is related to the amount of food the water contains, the time spent filtering and the filtering capacity of the individual (the filtering area, and the effectiveness of the pump-the cilia). There is evidence that all three have been enhanced by selection. As in sponges and other organisms (Vogel, 1978; 1983) various applications of the Bernoulli principle can be seen in the body shape, and in the arrangement, size and ori- entation of the apertures that will ensure not only that the energy expended by the organisms is most effectively used, but also that the energy available in the environment is harnessed to enhance interactions with it. THEAMOUNTOFFOODIN SUSPENSION.The amount of food in suspension in the water taken in by the ascidian is related to the amount in the water current. Shortage of food probably increases the stringency of selection for an increase in filtering capacity. However, in every known ascidian, the amount of food taken in by the organism is maximized by devices that ensure that the incurrent stream of water is separated from and not diluted or polluted by the filtered water con- taining wastes and gametes that is ejected through the excurrent siphon: Relative Velocity of the Incurrent and Excurrent Water. In all solitary ascidians and in separately opening colonial zooids (Clavelinidae, Sigillina spp., Polyci- toridae, Euherdmaniinae, Perophoridae, Polyzoinae) the excurrent aperture is smaller than the incurrent one, and the excurrent stream of water is ejected at I Kott, P., The Australian Ascidiacea Part 2, Aplousobranchia (I). 256 BULLETIN OF MARINE SCIENCE, VOL. 45, NO.2, 1989 greater velocity than that with which the water enters the branchial sac (Hecht, 1916; Figs. 1a, 2e). By adjusting the diameter of one or the other aperture, the zooid can exercise a degree of control over the relative velocity of incurrent and excurrent streams. Fiala-Medioni (l978a, 1978b) observed such velocity changes in the excurrent stream associated with a decrease in the diameter of the excurrent aperture and not associated with any change in ciliary activity. It is possible that the muscular vela that partially occlude the apertures in some species, especially in the Molgulidae, contribute to this control (Fig. 2a, b). Some colonial species have zooids with sphincters controlling their atrial open- ings into internal cloacal spaces rather than directly to the exterior (e.g., Atriolurn Kott, 1983, Leptoclinides, and certain Sigillina spp.; Fig. 2c, d). However, the general trend in colonies with cloacal systems is for the control of the excurrent water to be increasingly exercised by the colony rather than by individual zooids. Polyclinum and Aplidiopsis spp. show an intermediate condition-viz. atrial ap- ertures of individual zooids surrounded by circular muscles can occlude their openings into the cloacal chamber, and, as well, a muscular lip from the body wall above each opening is inserted into the rim of the colonial cloacal apertures so that groups of zooids can control the intra-cloacal pressure of the colony (Fig. 2f). In the highly integrated