The Biology of Ascidians

Adv. mar. Biol., Vol. 9, 1971, pp. 1-100

THE BIOLOGY OF ASClDlANS R. H. MILLAR Dunstaffnuge Marine Research Laboratory, Oban, Argyll, Scotland.

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I. Introduction . .. 11. Feeding .. .. .. A. " h e Feeding Mechanism .. . . . . B. Food . . . . .. .. .. .. .. 111. Breeding .. A. Breedingseason . . . . . . . . . . B. Spawning C. TheLenre IV. Life Cycle: Growth, Succession of Generations and Mortality . . . . . . . . . . . . V. Ecology . . . . A. The Numbers and Biomass of Ascidians . B. Changes in Populations .. .. .. C. Factors Affecting Distribution and Abundance VI. Predators, Parasites. Commensals and Symbionts . A. Predators . . . . . .. .. .. B. Commensals, Parasites and Symbionts . . . . .. . . . . VII. Geographical Distribution A. Shallow-water Ascidians .. .. B. Deep-water Ascidians . . . . .. .. Economic importance . . . . . . .. .. VIII. A. Fouling . . . . .. . . . . B. Food of Man, and of Commercial Fish .. C. Uptake of Harmful Substances .. . . . . . . Ix. References

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I. INTRODUCTION Ascidians have been studied from many viewpoints, and a simple analysis of the entries in the Zoological Record indicates the main interests of recent investigators. Amongst publications appearing, for instance, between 1963 and 1967 and dealing in part or whole with the group, the number of papers having at least some mention of the various subjects used in classifying the entries is as follows : general literature, 70 ; structure, 117 ; physiology, 151 ; reproduction, 34 ; development, 168; evolution and genetics, 31 ; ecology and habits, 90; distribution, 77. Since structure is taken to include histochemistry and cytochemistry, and development to include chemical embryology, it is 1

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evident that physiological, chemical and biochemical studies accoiint for a large proportion of the recent research on ascidians. These aspects are not treated in the present review, which aims rather to survey advances in our knowledge ofthe animal as a whole living organism. Much of the work on structure, evolution and genetics, and most physiological studies are therefore also excluded. No way of selecting topics is entirely satisfactory and the inclusion of some papers and the omission of others may seem arbitrary. Another difficulty in preparing a review of this nature is to decide how old a publication may be and yet be regarded as an advance. I have not chosen a date, but have been guided by whether the matter in a paper has already been dealt with in a review or major contribution devoted to ascidians.

11. FEEDING

A. The feeding mechanism It has long been known that ascidians feed by filtering organisms

and particles from water drawn into the branchial sac through the oral siphon and expelled through the atrial siphon, and that the process involves mucus secreted by the endostyle. Early accounts differ somewhat in detail; thus Roule (1884) described the mucus as passing out from the endostyle and across the inner faces of the branchial walls, where food particles are trapped, but Herdman (1899) thought that food was retained by mucus a t the entrance to the branchial sac. Orton (1913) and Hecht (1918) confirmed Roule’s account of the process. In some particulars, however, Hecht’s description has been modified by subsequent work. He believed that food particles are retained by the stigmata (the openings in the branchial wall) and are trapped in mucus only after being passed by cilia t o the tips of the branchial papillae. But MacGinitie (1939) found that continuous mucous sheets on the branchial walls trap particles from the water before it passes out through the stigmata. This was confirmed by Jmgensen (1949), Jmgensen and Goldberg (1953), Millar (1953a), and Werner and Werner (1954). Although most observers seem to have assumed that ciliary action alone is responsible for moving the mucous sheet towards the roof of the branchial sac, it is possible that muscles play some part, and Hecht (1918) described waves of contraction which bring adjacent rows of papillae together so that the sheet is pushed or pulled across the branchial wall. It is, however, by no means certain that such a process is part of the normal pattern of feeding, neither Werner and Werner (1954) nor Millar (1953a) having observed it in Ciona intestinalis (L.). When it reaches the roof of the sac, the endless filter of mucus is

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gathered by the dorsal lamina or languets and rolled into the form of a cord, which is then pulled into the oesophagus (Millar, 1953a). Jergensen (1949) investigated the efficiency of particle retention in Molgula sp. and Ciona intestinalis, and found that particles of colloidal graphite of 2-46 p were retained by the mucous sheet. In later experiments J~rgensenand Goldberg (1953) showed that Ciona can completely remove graphite particles of 1-2 p, but that protein molecules (haemocyanin and haemoglobin) mainly escape. The fact that some protein molecules are captured, however, suggests that processes other than purely mechanical ones may be involved. Korringa (1952) believed that the electrical charges on the mucus and the food particles of filter-feeding animals may determine whether or not small particles, and molecules, are trapped. I n this connection it is worth noting that vanadium, which is present in high concentrations in certain ascidians, appears to be taken up from the sea water initially by adsorption on the mucus of the branchial sac (Goldberg et al., 1951 ; Bielig et al., 1961). Stephens and Schinske (1961) found that the three species of ascidians which they investigated all removed considerable quantities of amino acids from solution, but there was no direct evidence that mucus was responsible. Not all organisms in the feeding current reach the mucous sheets, since the oral tentacles retain many of the larger particles (Werner and Werner, 1954) and those which reach the branchial sac may fail, in some unknown way, to be incorporated in the mucous sheets, and ase subsequently expelled through the oral siphon (MacGinitie, 1939). Moreover, MacGinitie briefly mentioned the rejection of some particles already caught by mucus and suggested that " cilia bordering the dorsal groove " may be responsible. This interesting possibility deserves further study, since rejection mechanisms play an important part in filter-feedingmolluscs, and might be expected to occur also in ascidians. Although we have little indication of how rejection might take place, there is some indirect evidence that it does, for in Dislaplia cylindricu (Lesson) and Eugyra aernbaeckae Millar the branchial sac was found to contain a mixture of sand and cells of ph-ytoplankton, but in the stomach only the cells were present (Millar, 1960). The basis of selection is apparently not merely the size of particle, since the stomach contained cells as large as the sand grains which had been rejected. Ascidians can also control their feeding by cutting off the secretion of mucus from the endostyle, with or without maintenance of the water current (MacGinitie, 1939 ; Werner and Werner, 1954). The efficiency of feeding depends not only on the ability to filter a wide range of particles but also on the rate of water transport. This has

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been measured using various experimental methods, by Hecht (1916), Jrargensen (1949, 1952), Goldberg et al. (1951), Hoyle (1953) and Cnrlisle (1966). The results vary considerably. Thus Hecht estimated 80 ml/h per g wet weight of animal in the case of Ascidia atra Lesueur, and Jrargensen’s value for Molgula was 540ml/h per g wet weight. It is probable that performance under favourable natural conditions will be higher than in experiments, particularly in those involving considerable interference with the animal, such as Hecht’s method using a tube inserted into the siphon. Hoyle’s (1953) criticism of Hecht’s work is partly invalid, since he failed t o realize that Hecht measured particle velocity in the inhalent, not the exhalent, current. Hoyle believed that ciliary currents would provide insufficient food and oxygen. He measured the water exchange resulting from spontaneous rhythmic contractions in Phallusia mammillata (Cuvier)and concluded that these introduced much more water than the ciliary current. The process he visualized consists of water being drawn into the branchial sac during relaxation of the body, and the water being filtered on the branchial walls with the aid of ciliary currents. However, Jnrrgensen (1955) did not accept this idea and calculated that in Ciona at least 30 times as much water is transported by ciliary action as by rhythmic contractions. One advantage claimed for feeding by body contractions is the ability to regulate the rate of feeding by varying the frequency of contraction, and Hoyle found the frequency to increase at lower food concentrations. It is evident that the role of spontaneous contraction needs further investigation, especially in relation to feeding. Indirect evidence for the adequacy of ciliary currents is based on the available particulate organic matter in the sea, and Jnrrgensen (1955) concluded that ascidians can meet their needs from this source.

3. Food Despite our knowledge of the mechanism of feeding, little is known of the food itself. Phytoplankton and organic particles in suspension apparently constitute the bulk of the food of many species. For instance, in Paramolgula gregaria (Lesson),a mainly Subantarctic species which attains a length of over 20cm, the gut was found to contain principally unicellular planktonic algae and diatoms, and only a little sand and animal remains (Millar, 1960). The waters of the Patagonian Shelf, where the specimens were collected, are rich in phytoplankton which, not surprisingly, constitutes the food of even such a large-bodied species. And in Microcosmus sulcatus (Coquebert) the branchial sac has been found to contain organisms (bacteria, diatoms and radiolarians) characteristic of the water immediahly above the substratum (Costa,

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1960). In other species the gut contents vary, perhaps according to the local water conditions. Kott (1952, 1964) and Millar (1955a, 1963, 1966a) noted large quantities of mud in the gut of Ascidia sydneiensis Stimpson, but the same species may contain algal cells, diatoms and peridineans, with little inorganic matter (Millar, 1960). Subtle differences appear to exist in the food of related species living in the same area, as with Ascidia nigra (Savigny) and A . interrupta Heller (Goodbddy, 1966). In this case, differences in the arrangement of the oral tentacles may be responsible, although there might be some variation in the food content of the water since the species occupy somewhat different ecological niches. Little experimental work has been done on the nature and quantity of food required by ascidians, but Milkman (1967) maintained cultures of Botryllus schlosseri (Pallas) in sea water containing the centric diatom Cyclotellanana Hustedt at a concentration of 1-2 x 106 cells/ml. Apart from filter-feeders which accept a wide range of material suspended in the surrounding water, there is an ecological group of ascidians which appear habitually to take in bottom deposits. Amongst shallow-water species Styela coriacea Alder and Hancock is apparently a deposit-feeder (Diehl, 1957), but it is the small-bodied deep water species living on a soft muddy substratum which have most commonly developed this habit. The gut contents of these animals are similar to the surrounding sediment, and the small size of the body allows the oral siphon to draw in sediment from the loose interface of the substratum and water (Millar, 1970). I n these animals the gut was found to contain, in addition to inorganic material, small brown “cells ” and many bacteria. Those abyssal ascidians with a long stalk, such as Culeolus spp. may, however, live with the oral siphon some distance above the sediment, and their gut contents have been found to lack the bottom deposits common in sessile forms (Millar, 1959a). Although ascidians probably originated in shallow seas with a rich plankton and in consequence evolved the filter-feeding mechanism which most of them still possess, a number of species penetrated into deep water. Of these, a very few have abandoned the original feeding mechanism in favour of a quite different kind, adapted to taking larger organisms and bottom material. In Octacnemus Moseley, Hexacrobylus Sluiter and Gasterascidia Monniot and Monniot the perforated branchial aac is replaced by an unperforated tube or sac which is obviously incapable of filtering particles from a current of water. Instead, relatively large animals such as ostracods, nematodes, copepods and other crustaceans are taken (Ritter, 1906; Madsen, 1947; Millar, 1959a, 1970; Monniot and Monniot, 1968). These occur in the gut together with

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quantities of sediment, but whether the animals are captured alive and selectively, or merely engulfed along with the sediment is not known. The modifications to the oral siphon, which include enlargement and great muscular development, suggest active capture, but alternatively they could be adaptations for scooping up large quantities of bottom deposit (Millar, 1970). Nevertheless, Monniot and Monniot (1968) regard the structure of Gasterascidia sandersi Monniot and Monniot as adapted, not only to a predatory habit, but to movement over the substratum, an ability which may enable this ascidian to capture prey. One further problem which awaits investigation concerns the feeding habits of the curious interstitial ascidians described in a series of papers by C. and F. Monniot (see Monniot, 1966). Some of these species, which rarely exceed 3 mm in length, move amongst the sand grains of the substratum, and presumably feed on organic particles or organisms in the interstitial water. The branchial structure, although modified, is essentially similar t o that of filter-feeding ascidians.

111. BREEDING Reproduction in ascidians takes three forms : asexual reproduction by budding, which occurs only in some families ; fission of colonies, a process recorded in few species ; and sexual reproduction or breeding, which occurs universally throughout the group.

A. Breeding season

A number of methods can be used t o investigate the timing and duration of the breeding season. (i) Macroscopic or microscopic examination of specimens collected at intervals throughout the year shows the cyclic activity of ripening, filling and emptying of the gonads, and in certain species or populations only the presence of spent gonads in the samples indicates the onset of spawning (Millar, 1964a, 1960; Diehl, 1957) ; in other cases information of this kind complements studies by more direct methods. Establishing the period when animals have full gonads with ripe gametes does not, however, do more than define the period within which breeding may occur, given the appropriate stimulus, and species are known which have full gonads throughout the year, but which only breed successfully (judged by the settlement of larvae) in a more restricted period (Raja, 1963). Some workers have used artificial fertilization or spontaneous spawning of animals brought into the laboratory at intervals, t o provide a criterion of ripeness (Hirai and Tsubata, 1956; McDougall, 1943; Levine, 1962).

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(ii) Plankton samples give direct evidence of breeding, but in practice the method seldom has been used, owing to the difficulty of identifying ascidian larvae and to their brief appearance in the plankton, Brewin (1946), Lutzen (1960) and Dybern (1965) are amongst the few who have used plankton samples in this way, and the value of this approach is illustrated in Fig. 1which clearly shows the breeding season of a population of Ciona intestinalis in the Gullmar Fjord, Sweden (Dybern, 1965).

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FIG. 1. Seasonal occurrence of larvae of Ciona inhfinali.9 a t Stromnara, Sweden, as shown by the number of larvae per plankton scrmple (redrawn after Dybern, 1965).

(iii) The commonest approach has been that used in fouling studies ; test panels are placed in the sea at intervals and examined periodically for the presence of attached animals. Owing to the difficulty of identifying very young specimens, however, species are often recorded only some time after settlement, and in areas where growth is slow the breeding season may be considerably longer than that recorded. Another source of error arises from the requirement of certain species for a clean surface and others for an already fouled surface, before larval attachment will take place (Scheer, 1945; Goodbody, 1962), and the consequent doubt whether the absence of a species from test panels may have resulted from the unsuitable condition of the surface rather than from the absence of breeding. Any heavy mortality amongst the very young settled ascidians may also conceal the occurrence of breeding. (iv) Studies of size-distributions in natural populations may indicate the breeding period, by showing the appearance of new generations through the identification of peaks in the histograms (Allen, 1953;

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Diehl, 1957; Dybern, 1965,1969b ;Millar, 1952, 1954b, 1960 ;Sabbadin, 1955, 1957). Statistical analysis of size distribution in the adult populations, using the probability paper method (Harding, 1949 ; Cassie, 1950), should further refine estimates of the dates of larval settlement, but the method has not yet been used in ascidian studies. Temperature is generally recognized as a major factor controlling the sexual reproduction of marine invertebrates. Hutchins (1947), in discussing the bases for temperature zonation in geographical distribution in the sea, noted two situations in which temperature requirements will limit breeding : at the summer poleward boundary, beyond which the sea is too cold to permit breeding ; and at the winter equatorial boundary, beyond which it is too warm. Towards these geographical boundaries the timing and duration of the breeding season can be expected to show variations from the pattern prevailing over the main part of the range of a species. In only a few ascidian species is sufficient information available to test these ideas. The influence of temperature on the breeding season may be seen in Ciona intestinalis, a particularly favourable species since it occupies such a wide latitudinal range, and Dybern (1965) has summarized the observations of other workers (Berrill, 1935a; Orton, 1914, 1920; Millar, 1952; Sabbadin, 1957 ; Komarovsky and Schwartz, 1957 ; Millard, 1952 ; Runnstrclm, 1929, 1936) and added fresh evidence from Swedish populations. He showed that f. typica breeds during all or most of the year in the Mediterranean, and that the season is progressively restricted to the summer months towards the northern parts of its range. Runnstrclm (1927, 1929, 1936)had concluded that f. typicu is divided into a number of races each with its own breeding temperature characteristics, but Dybern doubts whether Runnstrclm’s experiments and hypothesis were sound. This, however, is a disagreement about genetic differentiation ; the controlling influence of temperature on the breeding season is not in dispute. Botryllw schlosseri is another species of wide distribution whose breeding season in a number of localities is known (Lo Bianco, 1909; Millar,1952 ;Sabbadin, 1955;L’Hardy, 1962 ; Polk, 1962). It is evident from Fig. 2 that the duration of breeding is progressively restricted, presumably by temperature, towards the cooler more northerly parts of the geographical range. An instance of the very restricted breeding season at the distributional limit of a species was investigated in Pelonuia corrwata Goodsir and Forbes (Millar, 1954a). At its southern boundary this boreo-arctic species breeds over a period of only 2-4 weeks in January and February, when the sea temperature is near its yearly minimum.

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F I ~2.. Geographical variation in the breeding season of Bolryllua echlosaeri (from data in L’Hardy, 1962 ; Lo Bianco, 1909 ; Miller, 1952 ; Polk, 1962 ; Sabbadin, 1955). Sea temperatures at a, Naples, b, Millport (Scotland) and c, Venice.

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SimilarlyStyela rustica (L.), a north polar species, breeds in January and February in the southern part of its range (Lutzen, 1960). Unfortunately in neither case is the breeding season known in more northerly areas.

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FIG.3. Breeding of Dendrodoa groaaularia. Percentage of semplos with incubating embryos or larvae, in different size groups of adrdts. Essex (England), o----o,Millport (Scotland).Sea temperaturesat Essex, full line; and at Millport. broken linc.

Even over a comparatively short distance variations in the temperature regimes are reflected in the breeding cycle. Thus Dendrodoa grossularia (Van Beneden) in the Firth of Clyde breeds continuously from early summer until autumn with only a slight reduction in August, but in Esscx reproduction stops altogether for a short period in the summer (Fig. 3) (Millar, 1954b).

TEE BIOLOGY OF ASCIDIANS

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Fro. 4. Breeding of ascidiana on Scottish west coast, as shown by percentage of samples with incubating embryos (0-0) or larvae (.----a) (C-H, J, B). In A the condition of gonads indicated breeding. In B, I and L embryos and larvae are not represented separately. A, Pelonaiu corrugata; B, Dendrodoa groaaularia; C , Aplidium pailidurn; D, Sidnyum turbinatum; E, Aplidium nordmanni; F, A . punetum ; 0,Polydinum aurantium ; H, Didemnum candidum ; I Diploaoma lkkrianum ; J, Liaaodinum argylleme ; K, Clavelina lepadiformia ; L, Botryllua achloaaeri. Sea temperature in 1952, and in 1953. 0-0 (after Millar, 1958e).

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In addition to examining the behaviour of one species in different places we may look for evidence of temperature effects by comparing the breeding seasons of several species in the same area, bearing in mind the position which each occupies within its total geographical range. Thus a group of species on the Scottish west coast shows a north boreoarctic species at the southern limit of its range breeding briefly in the winter, south boreo-arctic species breeding over a long period, and south boreal species with a short summer period (Fig. 4) (Millar, 1958a).

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Amongst the ascidians of Asamushi, Japan, Hirai (1963) recorded some species as breeding in summer, and others only in autumn or winter and these restricted seasons may also relate to the position occupied by the species within their total distribution. In tropical waters a much longer reproductive season is possible. Goodbody (19 6 1 4 found that Ascidia nigra, Diplosoma macdonaldi Herdman and Symplegmu viride Herdman settled throughout the year in Kingston Harbour, Jamaica, although not at a uniform rate. Two of the species showed marked peaks, which did not, however, correlate obviously with variations in any environmental factor. As Goodbody noted, the peaks were of settlement and could have indicated greater larval survival rather than greater spawning activity. Prolonged breeding with an interruption in winter was found in a species-probably a Pyura-at Madras, India (Raja, 1963). Since the sea temperature in Madras harbour varies only between about 26°C and 29°C (Sebastian, 1953) other environmental factors may have imposed the seasonal cycle on reproduction, Elsewhere in warm waters Weiss (1948) observed a similar pattern of long but interrupted breeding in Botryllus planus (Van Name) and Botry1loh-h nigmm Herdman at Florida, U.S.A., and Didemnum candidum lutarium Van Name settled continuously but not uniformly. In warm seas with a marked seasonal temperature cycle ascidians may also breed throughout the year, with periods of greater and lesser intensity. Skerman (1959), in a study of fouling at Auckland, New Zealand, found at least four species which probably settle in every month. Here the mean annual range of sea temperature is about 11*7OC,but the temperature rarely falls below 11°C. It appears that in regions with a relatively high winter temperature, breeding is possible throughout the year, even when there is a large seasonal fluctuation in temperatures. Relatively little is known of the reproductive patterns of ascidians in polar seas, because of the difficulty of collecting in these regions throughout the year. Millar (1960) produced some evidence that subantarctic and antarctic species do not breed during the southern winter, and although larvae were present in specimens of Sycozoa sigillinoides Lesson collected in eight months of the year, it is not known how long they had been retained in the colonies or when they were released. Other compound species were found to have larvae during three or four summer months. In solitary species the evidence from the state of gonad development suggests a breeding period confined to the least cold months. Brewin (1946) studied ascidians from Portobello, New Zealand, and

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concluded that species of the primitive families had a longer breeding season than those of more highly evolved families, but to generalize from these observations would require a closer examination, bearing in mind also the variation in season due to the location of species within their total ranges. Although water temperature largely controls breeding, the termination of the season does not appear to be closely related to a particular critical temperature. Several species in the Plymouth area cease breeding while the water is still warm and food supply ample for adult needs (Berrill, 1935b), and Dybern (1965) concluded that Ciona intestinalis stops spawning in autumn because of changes in the gonads brought about by falling temperature rather than by a critical temperature. There is some evidence, however, that gametes are not released until a certain temperature is reached (Huus, 1941) and that this is the temperature below which larval development is abnormal or impossible (Knaben, 1952). B. Spawning Spawning in oviparous forms appears generally to take place at a particular time of day and the resulting synchronization throughout a population will increase the chances of fertilization. Ciona intestinalis and Molgula manhattensis (De Kay) release eggs and sperm one to one and a half hours before sunrise (Castle, 1896; Conklin, 1905; Berrill, 1947a) and Corella parallelogramma (Miiller) (Huus, 1939), and Styela partita (Stimpson) do so in the late afternoon (Castle, 1896; Conklin, 1905; Rose, 1939). Hirai and Tsubata (1956) found that Halocynthia roretzi (Drasche) kept in the laboratory for a few days repeatedly spawned in the late morning. The mechanism controlling synchronous release of gametes in Corella parallelogramma depends on illumination following a period of darkness (Huus, 1939). Huus (1941) later suggested that a hormone may be involved. In Ciona intestinalis and Molgula manhattensis the gametes are shed approximately 4 and 24 minutes respectively after the animals are exposed to light, and the most effective light is of a wave-length 500-700 mp (Whittingham, 1967). Lambert and Brandt (1967) also studied the effect of light on the spawning of Ciona intestinalis, and after comparing the action spectrum for light-induced spawning with the absorption spectrum of cytochrome c, concluded that this or some other haemoprotein may be the receptor material. Although somewhat beyond the scope of the present review it is worth noting that many attempts have been made to discover whether

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a functional relationship exists between the neural complex (ganglion and neural gland) and sexual activity and this work has been summarized by Dodd (1955) and by Hisaw et al. (1966). Despite conflicting experimental results and the discovery of neurosecretory cells in the ganglion (Dawson and Hisaw, 1964), it is at least doubtful if the neural complex is essential to the act of spawning, for Hisaw et al. noted normal gonad development and discharge of gametes in animals deprived of the complex for periods of up to a year. Nevertheless, the experiments of Sengel and Kieny (1962)) Sengel and Georges (1966) and Bouchard-Madrelle (1967) all strongly suggest that the neural complex has some influence on the development of the gonads and on spawning. 1. Development and release

C. The larva

Most solitary forms release their gametes into the sea, where fertilization and development take place, but almost all compound ascidians retain their eggs until the larva is complete and able to swim. A number of ways have been adopted of protecting the embryos during development, by retaining them within the oviduct, the atrial cavity or a brood pouch of the zooid, or in the test matrix of the colony. The most elaborate method yet discovered is in the New Zealand species Hypsist o mfasmerianu (Michaelsen)(Brewin, 1956a). In this species the ovary produces a single egg, only 25 p in diameter, which develops into a large larva in an oviducal brood pouch, there receiving nourishment through a pair of larval endodermal tubes. During the whole developmental period of 5& months, attachment to the parental zooid is maintained, and the resulting larva is very complex, with numerous buds. The advanced stage of development attained by the larva before release must be of considerable advantage in founding the new generation. A similar objective is achieved, in quite a different way, by the solitary Polycurpa tinctor (Quoy and Gaimard). Here the egg is very large (730 p in diameter) and rich in yolk, and develops within the atrial chamber directly into a miniature ascidian, without the intervention of a larval stage (Millar, 19628,). Larvae escape from the parent colony in various ways, according t o the site of incubation. I n most species the developing embryos are retained in the thorax and the larvae pass out directly through the atrial siphon where this opens on the surface of the colony, or via the common cloaca1 cavities. I n Euherdrnania claviformis Trason (1957) observed the passage of mature embryos from the oviduct to the atrium of the zooid, a process taking about 10 minutes, while the passage through the atrium lasted 3 4 5 0 minutes. Apparently the immature

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larva was retained in the oviduct until in the final stages of development it had become narrow enough to pass the oviducal sphincter. Thoracic contractions, initiated by the presence of the tadpole in the base of the atrial cavity, then moved it forward and out through the siphon. A similar process may take place in Pycnoclavella stanleyi (Berrill and Abbott) (Trason, 1963). Levine (1962) observed some larvae of Eudistoma ritteri Van Name to leave the parent by active swimming and others to be carried out passively by the exhalent current, and in Metandrocarpa taylori the larvae may be expelled by vigorous contraction of the zooid (Abbott, 1955). In some genera, notably Distaplia and Sycozoa, the embryos and larvae are accommodated in an outgrowth of the thorax containing the terminal part of the oviduct. In Distaplia the brood pouch with its larvae becomes separated from the zooid which eventually dies and the colony then contains numerous isolated pouches. These are exposed and release their larvae when the common test of the colony disintegrates, following the disappearance of the zooids (Berrill, 1948a). The same process apparently occurs in Sywzoa (Millar, 1960), and in Synoicum adureanum (Herdman) (Kott, 1060) which is one of the few species of the family Polyclinidae in which larvae are not released through the atrial cavity. A somewhat different mechanism exists in those ascidians with a small zooid and a large egg which is unable to pass forward through the thorax. Here a single embryo generally develops at a time and as it grows, bulges from the zooid perhaps to be released by rupture of the body wall. Examples in the family Clavelinidae are Eudistoma digitatum Millar, E . vastum (Millar), and Distaplia durbanensis Millar (Millar, 1963, 1964a). In Botrylloides the tadpole breaks through the body wall to reach the common cloaca1 space (Berrill, 1947b). The family Didemnidae shows the greatest specialization in this direction, for the eggs pass downwards from the abdomen directly into the test of the colony, there to be fertilized and undergo their dcvelopment. An exception in the Didemnidae is Diplosomu cupuliferum (Kott), in which fertilization and development take place in the abdomen of the zooid (Lafargue, 1968). Release of didemnid larvae must involve partial or complete dissolution of the test matrix, and it is perhaps not surprising that they sometimes metamorphose while still within the colony (Millar, 1952). Kott (1969) has suggested that zooids are also produced from larvae retained in the colonies of the unrelated Synoicum adareanum and Distaplia cylindricu. There is some evidence that larvae, like gametes, may be released principally at certain times of day, since Grave and McCosh (1924)

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It. H.BlILLAR

observed the larvae of Peropbra viridis (Verrill) being shed from colonies in the early morning, and there may be periodicity also in Botryllus schlosseri (Grave and Woodbridge, 1924). In Molgula citrina (Alder and Hancock), however, no definite period of release has been observed, under laboratory conditions (Grave, 1926),nor in Metandrocarpa taylori (Abbott, 1955). 2. Structure

Throughout the group many structural variations have appeared in the larva, as illustrated in Fig. 5 which shows the principal forms now known. We still have little idea, however, of the functional significance of the different kinds of adhesive papillae, anterior ampullae and epidermal vesicles which vary widely and have been used in interpreting the phylogeny of ascidians (Kott, 1969). The simplest type of larva, which probably represents the ancestral form, has an ovoid trunk with three conical adhesive papillae in a triangular arrangement, and no ampullae or epidermal vesicles. This form occurs in the Cionidae, Diazonidae, Ascidiidae, Corellidae, Pyuridae, Molgulidae and most of the solitary members of the Styelidae, and the larva is generally small, with a trunk from 0-15-0-30 mm in length. It is amongst the compound ascidians (families Clavelinidae, Polyclinidae, Didemnidae and subfamily Botryllinae) that the greatest modifications in larval structure have appeared. Here the papillae are usually borne on stalks, and often have a terminal cup with a central cone of secretory cells, but notable exceptions are the invaginated tubular papillae of Euherdmania (Trason, 1957; Millar, 1961a) (Fig. 5, no. 10) and Pycnoclavelh (Berrill, 1950; Trason, 1963) (Fig. 5 , no. 2) and the narrow elongated structures of Eudistoma fantasianum (Kott, 1957a) and E. digitatum (Millar, 1964a) (Fig. 5 , no. 8). The dual nature of the ascidian tadpole (Grave, 1935;Berrill, 1955; Millar, I966b), which serves the larval purposes of distribution and site selection and also carries the rudiments of the adult, has profoundly affected larval structure. Thus, amongst the compound forms, the rudimentary adult may already show small buds, or differentiated blastozooids as in Diplosoma (Fig. 5 , no. 17) and Polysyncraton magnilarvum (Millar, 196213) (Fig. 5, no. 16), or a sufficient set of blastozooids to constitute a small colony shortly after larval attachment, as in Hypsistozoa fasmerianu (Brewin, 1956a, 1959) (Fig. 5, no. 4). Larval size, too, is greatest amongst the compound forms. In many of these the larval trunk is 0.5-1.0 mm in length-considerably greater than the average size amongst the simple forms-and in a few it is much larger. Amongst the giants are the larvae of Polysyncraton magnilarvum at

FIQ.5. Types of ascidian larvae. Tho tail is not shown. The scale lines under the larvae show their relative sizes. 1, Clavelinu lepadiformia ; 2, Pycmclavdla atanleyi ; 3. Diatnpliu roaea ; 4, Hypaialoroafaamerkzna ; 5, s y w w a sigdlinoidea ; 6, Cyatodyles dellechinjei ; 7, Ewliatoma illolum ; 8 , Eudiatoma fanlasianum ; 9, Polycilor crystallinwr ; 10, Euherdmania claviformia ; 11, Peeudodiatoma arboreacena; 12, Aplidium nordmaiini; 13, Polyclinum auraniium ; 14, Symicum georgianum ; 15. Didemnum helgolandicum; 16, Polyayncrafan magnilanrum : 17, Diploaoma Iiaterknum ; 18. Diazona vwlacea ; 19, Tylobranehion apecioeum : 20, Cwna inteatinalia; 21, Aacidia rnentula; 22, Perophora lialeri; 23, Styela parlila; 24, Dendrodoa groasularia; 25, Dextrocarpa aolitaria; 26. Botrylloidea leachi ; 27, Pyura microcornus ; 28, Molgulo citrina (redrawn from authors mentioned in the text).

18

R. H. MILLAR

1.3 mm (Millar, 1962b), Eudistom fantasianum a t 1.5 mm (Kott, 1957a))Polyeitor circes a t 2.5 mm (Millar, 1963))Hypsistozoa fmmeriana at 2.5 mm (Brewin, 1956a, 1950)and Eudistomdigitatum a t 4 4 - 4 6 inm (Millar, 1964s). The functional significance of larval structure has been interpreted by Berrill (1955) in relation to the choice of a suitable site for adult life. Within the order Enterogona the large solitary forms live in places whcrc their small simple larva is adequate for site choice, but the compound forms have a more specialized habitat requiring a larger more efficient larva. Berrill traces a similar correspondence betwcen larval type and adult habitat through the families of the order Pleurogona. In particular the family Molgulidae shows an adaptive loss of the larval ocellus, for many molgulids live on sublittoral sand and mud, where larval reactions to changes in light intensity (shadow reflex) are unimportant or definitely disadvantageous. A further step has been taken by a number of the sand-dwelling molgulid species, by elimination of the larval stage, and the same adaptation has arisen independently in response to similar habitat requirements in the styelids Pelonaia corrugata Forbes and Goodsir (Millar, 1954a) and Polycarpa tinetor (Quoy and Gaimard) (Millar, 1962a). 2.0

3

1.6-

0)

14-

0

a*

1.2-

W W

,a

1.0-

m

:.

-B

fl

c

0.8-

0.8-

rA

0.4-

0.2-

1

0!2

0!4

0!6

0!8

l!O

112

114

l!6

I

1.8

I

2.0

I

2.2

1

Tail length, m m FIG.6. Swimming s p e d in relation to size of larva (from data in Berrill, 1931).

19

THE BIOLOGY OF ASCIDIANS

3. Behaviour The ascidian larva has a characteristic pattern of behaviour, consisting of an initial period when it swims upwards (positive phototropism and negative geotropism) followed by a period when it swims or sinks downwards (Grave, 1920, 1926; Mast, 1921; Grave and Woodbridge, 1924 ; Sebastian, 1953). The initial phase serves to distribute larvae, and it is in the second phase that the critical reaction is elicited in response to a decrease in light. The larva then swims towards dark areas, which in nature tend to be the vertical or lower surfaces of rocks etc. At this time a large tailed larva is advantageous since it is able to turn, swim quickly and attach to the substratum (Berrill, 1955), and Berrill (1931) has shown that the larger the larva, the faster it swims

.-

30-

Q. CI

CI

I

0

0

1 I. .

0.1

0.2

0.3

0 I

04

. I

0.5

1

0.6

Diameter of egg. mm

Pra. 7. Relationship bctwecn longth of lerval life and size of egg, in various species. The vcrtical lincs indicate the range of larval life within a spocios, whom this is known (from data of authors mcntioncd in text).

The duration of free swimming life under laboratory conditions varies from a few minutes to several days, according to species. With the exception of a few in which the embryo is nourished from the parental zooid, large larvae develop only from large yolky eggs, and might be expected to have correspondingly long swimming periods. However, Fig. 7, based on information from several sources (Grave, 1921, 1935; Berrill, 1931, 1935a, 1947b, 1948a, b, c, 1950; Millar, 1951, 1954b; Brewin, 1959; Sebastian, 1953, 1954) shows no strict relationship between larval duration and egg size (taken as a measure of larval A.X.B.--8

2

20

R. H. MLLdR

size). But since the larval yolk remains largely unused, to be carried over into the adult stage (Berrill, 1950), the energy available to the larva to maintain its swimming bears little relation to the amount of visible yolk. There is also considerable variation in the larval period within species (Fig. 8) (Grave, 1920, 1822, 102G; Gravc and McCosh, 1924; Grave and Nicoll, 1940; Grave and Woodbridgc, 1024; Cloney, 1961; Levine, 1962). Grave and Woodbridge (1024) considered whether the wide differences in Botrgllus might have a gcnctic basis, but found no morphological evidence of this in thc resulting colonies. If the phenomenon also occurs in nature i t may ensure that some larvae settle near the parents whereas others, more widely dispersed, eiiablc the spccics to explore more distant habitats. Lambert ( 1968) recorded considerable a

.a

9

10

Hours Fro. 8. Range of larval life within species. a, Molgula cifrina (redrawn from Grave, 1926); b, Eolryllus achloaaeri (redrawn from Grave and Wooclbritlgc, 1924); c, Perop h o m viridia (rodrawn from Grave and McCosh, 1924).

local settlement of Corella willmeriana Herdman when the population was large, and the inference is that many larvae settled quite soon after hatching. Polk (1962) made a similar observation on Botryllus schlosseri in a dock at Ostend, where larval settlement was dense near the parent stocks but sparse only 1 km away. These events could also result from gregarious settling behaviour (see p. 48). 4. Settlement

At the end of its free swimming phase the larva becomes attached to the substratum and metamorphoses, but in spite of many studies (see Berrill, 1950 ; Lynch, 1961), the controlling factors are not understood. Various substances which have been found to induce fixation include tissue extracts (Grave, 1935) and copper (Glaser and Anslow, 1949), but the experiments of Whittaker (1964) cast doubt on the role of copper. Experimental results in any case must be applied with caution to

TEE BIOLOGY OF ASCIDIAXS

21

natural conditions and do little more than suggest some possibilities. Grave (1935) believed, however, that a metabolic product of swimming activity is essential for metamorphosis. Nevertheless, larvae irnmobilized by narcotization will metamorphose at about the same time as free swimming controls (Bell, 1955), and although metabolic products may be concerned, their effect does not appear to be related in a simple way to the muscular activity of the larva. Fixation to the substratum is not always essential for metamorphosis; Cloney (1961) for instance found that, although most larvae of Boltenia villosa (Stimpson) in a culture attach before metamorphosing, others do not. The larvae of Eudistomu ritteri Van Name also vary in this respect (Lcvine, 1962), and Carlisle (1961) reported postmetamorphic stages of Diplosomu listerianum (Milne Edwards) and Cionu intestinalis in the plankton of the Plymouth aquarium. It may be usual for a proportion of the larvae, failing to contact a solid object, to metamorphose while still planktonic and subsequently to become attached. Ciona retains the ability to fix itself even as an adult (Berrill, 1929; Millar, 1953a). Before fixation takes place the larval papillae become sticky and in some species this precedes contact with the substratum. Thus in Perophora viridis a drop of viscid material is secreted by each papilla towards the end of the free-swimmingperiod and attachment follows contact with a solid surface (Grave and McCosh, 1924). In Eudistomu ritteri the papillae are already in an everted condition while the larva is swimming (Levine, 1962). Rapid eversion of the papillae, with exposure of the adhesive surface, precedes attachment in Euherdmunia claviformis (Ritter) (Trason, 1957) and in Pycnoclavella stanleyi (Berrill and Abbott) (Trason, 1963). Trason (1963) believed that a band of circular muscles in the larval trunk of E . claviformis may cause eversion of the papillae. Although the family Polyclinidae have a different kind of papilla, consisting of a goblet containing central secretory cells, extrusion is also effected by deformation of the papilla, which forces out the secretory cells and the secretion (Grave, 1920; Sebastian, 1954). In this case the mechanism is unknown, for there do not appear to be muscles in the papillae. Very little is known regarding the choice of substratum by the larva, or indeed if much choice is exercised. The presence of nerve fibres in the adhesive papillae of botryllid larvae (Grave, 1934) suggests that some response is made, presumably on contact with solid surfaces, but there is nothing to indicate whether surfaces are tested until a suitable one is found for attachment. Goodbody (1963a) believed that larvae of Ascidia nigra may be attracted to iron, since unpainted iron develops a dense growth of the species. It is possible, however, that observed

22

R. H. MlLLAR

differences in population densities may have resulted from variations in

thc surface texture rather than from differential settlement, since

texture may affect the security of attached larvae and young stages. Nevertheless, he also observed that, while larvae of A . nigra will settle on almost any clean surface, those of A. interrupta Heller apparently require a degree of fouling on the substratum before they will settle. There is scope for experiment and observation in this field to show whether the physical and chemical nature of the surface is important or whether, as Dybern (1963)found in Cionu,the requirement is simply for a site with generally adequate conditions for adult life. 5. Evolution

Many authors have discussed the origin of the tadpole larva in relation to the ancestry of the vertebrates, but little fresh evidence has appeared recently. Both Berrill(l955) and Millar (1966b)take the view that this particular larval form arose within the tunicates. An elongated muscular body may have been a consequence of the loss of external ciliation due to the development of test. Jefferies (1968), however, believes that the tadpole may indicate the line of descent from Cambrian members of the subphylum Calcichordata (Jefferies, 1967), a view implying that the ancestral tunicates were free-swimming animal8 which later adopted a sessile habit for the adult while retaining a pelagic larva. Whatever may be the significance of the ascidian tadpole in this context, the striking similarity in the fine structure of the larval ocellus and the vertebrate eye (Dilly, 1961)can scarcely be a coincidence or the result of convergent evolution.

IV. LIFE CYCLE:GROWTH,SUCCESSION OF GENERATIONSAND MORTALITY The life cycle of solitary ascidians is relatively simple, and can be analysed as the establishment of the new individual, its growth, breeding and death; and appropriate measurements can be made at each stage. In compound forms asexual reproduction introduces a complication, and the resulting colony is to be regarded as the biological unit. It undergoes a complex series of changes involving various degrees of decay, renewal and, occasionally, division. Increase in body length has been used almost universally as a measure of growth in simple ascidians, and although filr from ideal, since the rclationship between length and weight is rarely known, it does givc a useful index. Practical difficulties arise because the body in most species is attached to a solid object which may interfere with easy and accurate measurement, and the habit of contracting when disturbed

23

THE BIOLOGY OF ASCIDIANS

further reduces accuracy. Most growth studies have been made by measurements in successive samples of a population, and in only a few cmes have individuals been followed. That the two methods give sufficiently similar results is indicated by population studies on Ciona intestinalis in a Scottish harbour (Millar, 1952) and growth rates obtained by measurements of marked individuals in an aquarium on the same coast (Millar, 1953a) (Fig. 9). The pattern is a simple one. Animals settle in the summer, make only limited growth in that year, stop growing in winter, and quickly grow to full size in the following spring and summer. But in other areas the timing of events is different, 121

I

.I

I

I " M ' A

' M ' J

' J

'

A

'

H

'

o

'

N

'

~

'

Fro. 9. Growth of Cionn intestinalis. Each line represents the body length ofan individual in a population in aquarium tanks at Millport. The black circles are the mean body lengths in samples of a population in a nearby dock (redrawn from Miller, 1953a and from data in Miller, 1952).

and, fortunately, this widespread species has been studied in a number of places where the prevailing conditions, and in particular the temperature regime, vary considerably. Dybern (1965) has reviewed the results and concludes that there is " a clear relation between age, growth, spawning and embryonic development, on the one hand, and the environmental temperature conditions, on the other ". Since sexual maturity is at least partly related to body size (Millar, 1952),the growth rate affects the timing of spawnings in the season a d . consequently the succession of generations. Table I, taken from Dybern (1965), summarizes the results of numerous workers (RunnstrBm, 1927, 1936; Berrill, 1935a; Orton, 1914, 1920; Millar, 1952; Sabbadin, 1957; Komarovsky and Schwartz, 1957; Millard, 1952; Pbrhs, 1952;Lo Bianco, 1909 ;Scheer, 1945). The population structure vanes markedly through-

TABLEI. SUMMARYOF

Temperature

hTo.of generations per year

Main spawning periods

0 to 500 m

<6OC

(1

Notknown

(6°C

of Norway of Norway

ca. 100 m 0 to 5 m

- 1to 20°C

6 to 9°C

<1 2

6 to 18°C 8 to 23°C

of Sweden of Sweden

15 to 30 m 0 to 10 m

- 1 to 18°C

5 t o 15°C

1 2

Not known May-June Aug.-Sept June(-July) MayJune (July-)Aug.Sept. Autumn Spring (Summer) Greater part of the year

Sub-Arctic

KJ

RELATIONSHIP TO TEMPERATURE OF Ciona inteatinalia f. typica

Depth

Region

West coast West coast in poller West coast West coast

THE

South coast of England (Plymouth)

Surface water

6 to 16°C

2(to 3)

French Mediterranean coast

Surface water

10 to 26°C

At least 3

Gulf of Naples

Surface water

13 to 27°C

At least 3

Sub-tropical and tropical

Surface water

20 to 32°C

3 to 4 or

more

I+

Temperature tolerance range Larvae Adults

Zygote4

8 to 22OC 8 to 22OC

8 to 23°C (at any rate in winter) The whole 14 to 27°C year (in winter upper limit is possibly at 23 to 24°C) Not known Upper limit is probably sometimes above 30°C (e.g. at Suez)

0 to 21°C (on Murmansk coast)

- 1 to 30°C 6 to 24°C-1 to ca. 30°C 6 to 24°C - 1to 08.30"C

8 t o 40°C

'

THE BIOLOGY OF ASCIDIAN’S

26

out the geographical range of the species, but as a rule two generations live side by side for much of the time. Comparisons drawn from populations living in widely separated regions are suspect because of the possible existence of physiological races (Runnstram, 1927, 1929, 1936), although Dybern doubts the evidence for these. The effect of temperature is clearly shown, however, by a comparison of the growth and annual cycle of C. intestinalis in two British docks, one of which was subject to heating by a power station (Millar, 1952; Naylor, 1965a, 1965b) (Fig. 10). In a single population, too, the growth rate rises with the temperature, and Sentz-Braconnot (1966)found that Ciona settling in the early part of the summer reached Jan

Feb Mar *Pr

May

1 I

0

90

Jun

@

0 V

Ju 1

d

Aue

SeP

-

Oct

Nov

40 20

Dec

0

2

4

6

E

l

0

Body length, cm

FIQ.10. Effect of temperature on growth and annual cycle in Ciona inleatidia ; A, in a dock at Ardrossen, Scotland, and B, in a heated dock at Swansee, Wales (redrawn from Neylor, 1966b).

26

R. H. MlLLAR

only 1-3 cm in 45 days, but later in the summer grew to 4-5 cm in the same time. Similarly, Corella willmerianu in coastal waters of Washington, U.S.A., completes its life in 5 months if it settles in time to grow rapidly during summer but takes 7-8 months if growing more slowly in winter (Lambert, 1968).Under favourable conditions, growth to sexual maturity is rapid, and specimens of Molgula manhattensis only three weeks old can release eggs (Grave, 1933). Faster growth, earlier death, and a quicker succession of generations appear to be characteristic of life in warm water and, in the almost total absence of information on available food, temperature is justifiably regarded as of priinc importance. In British waters Cionu lives for 12-18 months (Orton, 1914, 1920; Millar, 1952),but in the tropics for only a few months and in sub-Arctic waters probably for a few years (Dybern, 1965). Curiously enough it is known to survive for two or more years at Marseilles (PkrAs, 1946) and at Millport, Scotland, young specimens brought in from the sea lived in the aquarium t o an age of about 38 years (personal unpublished record). Other solitary ascidians have been less studied but appear t o have similar life cycles. Ascidiella aspersa (Miiller)lives for 12-18 months in British waters (Millar, 1952; Gage, 1966), but on the Norwegian coast its life varies from one to three years, according t o water temperature (Dybern, 1969a). Corella parallelogramma is also essentially an annual, but Ascidia mentula Muller may live for at least three years (Dybern, 1969a). Millar (1954b) found that Dendrodoa grossuluria has a life span of 18-24 months on British coasts, and that three generations arc simultaneously present in the population. The maximum age of Styela coriacea is about 20 months, and three or four generations are produced annually (Diehl, 1957). In only a few species does the animal bear any clear evidence of its age, but in the genus Chelyosoma the test is divided into a number of hard plates with concentric lines (Fig. 11). These apparently represent

Fro. 11. Cklyosorno rnacleayanvrn ; dorsal view of e specimen in its fourth year, showing plates with growth lines (redrawn from Huntsman, 1921).

THE BIOLOGY OF ASCIDIANS

27

winter growth checks, and Huntsman (1921) found that C . macleayanum Broderip and Sowerby continues t o grow for more than four years in Alaskan waters, C . productum Stimpson for more than three years and G. columbianum Huntsman for only one year. Although species with a wide latitudinal range show great variation in tho life cyclc, which can be compressed into a few months in the warni part of tlic range, warm-water species of restricted distribution tnny not havc such a rapid tuni-over of generations or such a short life. Thus Ascidia nigra in Jamaica attains an age of 18-22 months (Goodbody, 1962). Styela plicata (Lesueur), a warni-water species of rather wide distribution, appears t o live for 5-6 months in warm years and 7-8 months in cold years (Kanatani et al., 1964). Est,imates of the life span of a species do not, of course, imply that t he whole population dies more or less simultaneously, although catmast,ropliicniortalitics have been recorded, as in three species in ,Jamaica which were decimated by a sudden influx of fresh water following heavy rain (Goodbody, 196lc). Sudden high mortalities are soinctimcs due to the death of the organisms on which the ascidians liavc scttlcd, McDougall (1943) having noted cases of the rapid disappearance of Styela plicata and Atlolgula manhuttensis when their supporting Bugula and Tubularia died. Amongst other causes of mass niortality is low winter temperature, and the fate of Ciona intestinalis, Jlolgula inanhattensis and Styela plicata, in the lagoon of Venice is incntionccl clscwhere (Sabbadin, 1957). In the absence of such dramatic events, much of the mortality can be ascribed to the activity of predators and competitors, and ultimately to t'lic onset-of senescence (Goodbody, 1962). Goodbody (1961a, 1963a) was able to follow the course of events in populations of Ascidia nigra. During the six wccks after settlement 97-08% of the young ascidians usiiiilly died, with ext.rcmes of lOOyoand 82.5%. The different survival rii.t,cs iirc related t.0 differences in the associated plant and animal c~otnriiuiiit,ics,sonic members of which may have competed with the young :iscidi;ins or physically displaced them. After this critical cwly period the prcssurcs appear to be much less, and the individuals which survive it have a good chance of completing their potential lifespan. Kot undil 18-22 months after settlemcnt is there another sharp tlrcliiie in nuinbers, and a t this t>imethe animals probably die of old age (Fig. 12). In cornpound forins, as already noted, thc existence of a colony with it,s niiiny zooitls undergoing t'hcir own cycles of growth, budding and ninkes the assessment of growth more difficult than in the rcgenen~t~ion, solitary f o r m . The simplest approach relies on successive measure-

28

R. H. MILLAR

50

De ys FIG. 12. Aacidia nigra. Survival curve for three groups, appearing on test panels in August (.--.), September (-------)and October (..........) (redrawnfrom Goodbody 1962).

ments of the areas of colonies in a population (Millar, 1952). Although this method may be satisfactory in the botryllids, in which colonies in nature generally remain intact and discrete, the work of Oka (1942) and

10

20

30

Days

FIQ.13. Polycilor mufabilis. Growth of a group of colonies derived by division of one parent colony. The total area of the daughter colonies is plotted on a logarithmic scale, against time (redrawn from Oka and Usui, 1944).

THE BIOLOGY OF ASOIDIANS

29

Oka and Usui (1944) showed that colonies of Polycitor mutabilis Oka divide repeatedly. Division takes place both by simple fission, and by colonial budding in which zooids extruded from the parent colony give rise to new colonies. Moreover, colonies of this species undergo cyclical expansion and contraction. By considering all the daughter colonies derived from one original colony as a composite unit Oka and Usui were able to show that the area plotted on a logarithmic scale bears a linear relationship to time (Fig. 13). Division of the colony also occurs in Didemnum candidum Savigny (Carlisle, 1961) and Archidistoma aggregatum Garstang (Nakauchi, 1966a), and here, too, the area of all the daughter colonies would have to be used in growth studies. Sabbadin (1960) measured the growth of Botryllus schlosseri, not by the area of colonies, but by the number of zooids, and found this to vary so widely that in the fifteenth generation of blastozooids different colonies contained between 1 and 97 zooids. Growth is further complicated by periodic rejuvenescence, with parts of the colony proliferating while other parts degenerate. Earlier, it had been shown for the same species that the zooids may double in number every two or three days and that a fast-growing colony attains 1 000-2 000 zooids within a month of its establishment (Grave, 1933). Growth may be interrupted and later resumed, and Nakauchi ( 1966b) observed that colonies of Aplidium multiplicatum (Sluiter) increased in size until, at a temperature of about 3OoC, breeding took place. At this time growth of the colony ceased, and the zooids regressed and divided ; only later, when the sea temperature had fallen to 25OC did the buds develop into new zooids. Then active life and growth of the colonies were resumed, followed by further breeding. It is not clear whether interruption of growth was associated primarily with breeding or with the high temperature. The involved questions of the physiological control and mechanics of budding are beyond the scope of this review and have been discussed by Berrill (1951), but it may be stated that in general " the phases of maximum sexual and asexual reproduction alternate " (Berrill, 1935b), with the sexual process confined to summer. After the breeding season the zooids usually undergo a process of budding and the colonies may pass the winter in a relatively inactive condition, in some cases being reduced to masses of dormant buds. Temperature affects the balance between regression of zooids and subsequent differentiation into new zooids, as Barth and Barth (1966) showed in Perophora viridis Verrill. It appears, however, that in some species low temperature merely retards recovery of the colony, and Vernay (1955) found that the buds of Synoicum argue slowly develop into functional zooids throughout the

30

It. H. ItULLAR

winter. Similarly Archidistoma aggregatum and Diazona violaeea Savigny develop during the winter (Berrill, 1948b, 1948~).In functional colonies of Metandrocarpa taylori Huntsman asexual reproduction takes place throughout the year (Abbott, 1953), but is least intensive when breeding is in progress, in the summer (Haven, 1967). Sabbadin (1955) recorded budding in Botryllus schlosseri at all seasons, although the process was slower in winter. Naukauchi (1966a) considered that budding is of two functional types. One of these involves resorption of the zooid, is an adaptation to adverse conditions, and may take the form of hibernation (Clavelina, Diazona, Syndiazona, Perophora) or aestivation (Aplidium multiplicatum) ; the other, which is not accompanied by resorption of the zooid, occurs in favourable conditions and results in growth of the colony (Perophora, botryllids, polycitorines and some polyclinids). The alternation of the sexual and asexual process in compound ascidians is therefore a complex pattern of events, further complicated by the fact that in some genera all buds can reproduce both sexually and asexually whilst in others different sets of buds are restricted to one method (Ivanova-Kazas, 1967). A few compound ascidians, in which the colony is very distinctly divided into stalk and head, show particularly clearly a cyclic degeneration and regeneration. Sycozoa sigillinoides Lesson has a long, narrow, sometimes branched stalk surmounted by heads containing the functional zooids. Following breeding, the heads disintegrate or break off, leaving headless stalks containing buds derived from the vascular processes of zooids (Caullery, 1909; Salfi, 1925) (Fig. 14). In this reduced state the stalks recall the overwintering condition of certain species of Polyclinidae. The stalks of Sywzoa subsequently grow new heads, when the buds develop into zooids which secrete fresh test material (Millar, 1960). It would be interesting to know whether the whole process is repeated year after year. In the related genus Hgpsistozoa, one of the most highly evolved of all compound ascidians, having a very complex embryonic and larval development (Brewin, 1956a),the colony is also divided into a stalk and head, and, as in Sycozoa, breeding is followed by dissolution of the head which is later replaced through the activity of zooids at the top of the stalk. Hypsistozoa illustrates the alternation of sexual and asexual processes (Fig. 15), and it is interesting to note that budding and growth of the colony occur in summer and autumn whereas sexual reproduction is confined to the winter and spring, thus reversing the more usual seasonal sequence. A plentiful supply of plankton is available during gonad maturation and embryological development (Brewin, 1956a), and may be particularly im-

THE BIOLOGY OF ASCIDIANS

31

a

1 FIO.14. Sycozon aigillinoidee. Colonies. a, with stalk and fully developed heads; b, with hoadlcss stalks; c, with new heads developing from an old stalk.

portant since the parent zooids nourish the embryos for several months . Colonies not only may divide, but in some species may fuse. Bancroft (1903) found in Botryllus sp. and Botrylloides sp. that unrelated colonies would not fuse, but that closely related colonies might do so. Further investigations by Oka and Watanabe (1957, 1960) and by Mukai (1967) revealed something of the genetic basis of the phenomenon but the extent t o which fusion occurs in nature remains uncertain. The life-span, like the growth-rate, is more difficult t o determine in compound than in simple ascidians, because of their periodic reduction and regeneration. There may even be grounds for regarding the colony of some species as potentially immortal (Sabbadin, 1960). I n the field it is difficult t o identify and follow the fate of individual colonies, and

32

R . H. ‘MTT.T.bR

FIQ.16. HypGtozoa jaameriana. Annual cycle of sexual and asexual reproduction (redrawn from Brewin, 1966af.

laboratory studies raise doubts about how far the observed events correspond to those taking place in nature. A few observations indicate the longevity of certain species (Table 11). The causes of death in compound forms, other than by the activity of predators (see p. 48) are little known, but presumably are similar to those applying to simple ascidians. Intraspecific competition may sometimes eliminate the less vigorous specimens, according to Bancroft (1903), who also noted that colonies of Botryllus lost vigour and shrank before dying, apparently from old age. A further cause of death, which affects compound and solitary forms dike, is detachment from the substratum, when the animals may drift away to unsuitable conditions or be cast ashore. Schwartz et al. (1960) studied Aplidium cowtellatum (Verrill)in Sinepuxent and Chincoteague Bays, which are shallow landlocked areas on the east coast of the U.S.A. Specimens were common but unevenly distributed, and in the more

33

THE BIOLOGY OF ASCIDIANS

TABLE11. LIFE-SPAN OF SOME COMPOUNDASCIDIANS Clavelinu picta C . oblonga Hyp8iatozoa faameriuna Perophota bermdensis D i p l o e m lblerianum Diazona violacea Bott$h sch~oeseri

Botrylloidea leachi

at least 3 years 13 years at least 24 years 1-2 years 1-1+ years 4-5 years under 1 year 1- 1 years 12-20 months at least 2 years

+

Berrill, 1932 Berrill, 1932 Brewin, 1959 Berrill, 1935b Millar, 1952 Berrill, 194% Bancroft, 1903 Millar, 1952 Sabbadin, 1955 Dybern, 1969s

sandy parts many were moved by wave action, resulting in heavy mortalities amongst populations established on unstable bottoms.

V. ECOLOGY A. The numbers and biomass of mcidians The part played by ascidians in the economy of the sea is poorly understood, and only recently has quantitative information started to accumulate. Certainly in some kinds of habitat they are of little importance (Picard, 1965), but elsewhere are sufficiently numerous to merit attention. Their place in fouling communities-often a dominant one-has been mentioned, and the instance noted by Elroi and Komarovsky (1961) of a wet weight of Ciona intestinulis amounting to many kg/m2 illustrates the importance of the group in certain circumstances. In natural communities, too, ascidians are sometimes amongst the dominant groups, as Abbott (1966) found in an area surveyed near Cape Thompson, Alaska. The most striking examples of dominant ascidian species are to be found amongst the family Pyuridaa. On parts of the coast of New Zealand, rocks may be covered by a single species (Oliver, 1923), and the Pyura-zone is also one of the most characteristic features of the intertidal rocks of the coast of New South Wales, Australia, where Pyura praeputialis (Heller), a species occurring along 1 000 miles of coast, covers a band 2 f t in width (Dakin et al., 1948). The related Pyura stolonifera (Heller) occupies the same ecological niche on South African shores, sometimes over a vertical zone of 34 f t (Morgans, 1959), and Pyura chilensis Molina, a species of similar habit, forms a dense cover on rocky shores in Chile (Gutihez and Lay, 1965). Sheltered shores, too, may provide very favourable conditions, and Lewis and Powell (1960) found Ascidiella aspersa and C i o m intestidis to be dominant over all other animal species on parts of the Scottish coast.

34

R. H. MILLAIt

In sublittoral arcas species of the family Molgulidae are sometimes strikingly prolific, and Dragovich and Kelly (1964) found molgulids to be the most numerous organisms in trawlcd samples in Tampa Bay, Florida. Abbott (1951) recorded a mass of Bostrichobranchus digonas Abbott cast up on a Florida beach and forming a belt 4-6 in wide and about 100yd long, indicating the abundance of the species in an adjacent sublittoral arca. And at Point Barrow, Alaska one short haul brought up a dredge one third filled with thc molgulid Rhizomolgula globularis (Pallas), and containing little else (MacGinitie, 1955). Large areas of the bottom in the shallow inshore parts of the Gulf of Naples are " literally covered " with Ascidiella aspersa, which is there the dominant animal (Parenzan, 1959), and in the harbour of Genoa ascidians are abundant with C i o m intestinulis a very important species in the quantitative composition of the sessile benthos (Relini, 1962). The frequent descriptions of escidians as " abundant " or " in great numbers " testify to the significant role which they must play in many parts of the sea. Nevertheless, rather few measurements have been madc of their abundance. Quantitative studies of the sublittoral fauna are more easily made on soft than on hard substrata, and most of the data have resulted from the use of grabs applied to sandy and muddy areas. A benthic survey of Scottish and adjacent waters indicated maximum ascidian densities in some places of about 100 per m2for Eugyra arenosa (Alder and Hancock) and Polycarpa Jibrosa (Stimpson) and of nearly 200 per m2for Pelonaia corrugata Forbes and Goodsir (Thompson, 1930 ; 1931 ; 1932 ; 1934). During an investigation of the fauna of brackish ponds in Japan, Kikuchi (1964) estimated the biomass of different animal groups and the figures show that ascidians could constitute about an eighth of the total benthic crop. Somewhat similar figures were obtained by Pdrhs (1967) for a typical coastal detritus fauna in the Mediterranean, where ascidians accounted for 11.5y0, 10.Syo and 0% of the total dry weight of the bottom fauna a t three stations, although in numbers of specimens they represented only 0.7%) 2.6% and 0% respectively. At two stations on a muddy detritus bottom 60.3% and 19.3% of the total fauna by dry weight were ascidians and 5.3% and 2.2% of the total number of specimens. The discrepancy between estimates of importance using dry weight and numbers is, of course, explained by the relatively large size of the ascidians compared t o that of other animals. Sanders (1960) listed 76 species in a soft-bottom community in Buzzards Bay, U.S.A., and the only ascidian, Bostrichobranchus pilularis (Verrill), ranked sixteenth in order of numerical abundance but second in order of dry weight. This species accounted

THE BIOLOGY OF ASCIDIANS

35

for 0.26% of the fauna by number of individuals and 2349% of the total dry weight. One of the few estimates of the standing crop of ascidians on natural hard substrata was made by Gutikrrez and Lay (1965) who recorded Pyura chilensis at a density of 320 per m2with a mean individual weight of 350 g. Under favourable natural conditions Ciona intestinalis may attain population densities of 1 500-5 000 per m2 (Dybern, 1963), and Ascidiella scabra (Miiller) at Bohuslan, Sweden, 1 000 per m2 (Dybern, 1969b). C. Monniot (19654 records Microcosmus vulgaris at a density of several hundred per m2 on stones dredged from 120 m in the Gulf of Lions. It is evident that the group may form an important component in the fauna of some loose and solid substrates, and may sometimes play a significant or even dominant part in the economy of coastal waters.

B. Changes in populations Estimations of population density and biomass should take account of seasonal and year-to-year variations. Seasonal changes in the structure of the population depend on reproduction, growth and mortality, and have been referred to in sections 111 and IV, but little is known regarding the way in which ascidian populations vary over a period of years. Fouque and Franc (1953) noted that Ascidia mentula, Ascidiella aspersa and Ciona intestinalis decreased markedly on the shore near Dinard, France, within the space of one year, whereas Polysyncraton lacuzei Giard did not. In another part of the same region Molgula manhattensis declined from a very abundant species to a rare one. No explanation was found for these events but it is sornetimcs possible to relate faunistic changes with environmental changes, as for example when several species of ascidian penetrated to parts of the Rance estuary in France following dry summers (Fischer-Piette and Gaillard, 1950). And the appearance of Molgula manhattensis in the Caen canal was obviously made possible only by the increased salinity following the influx of sea water (Durchon, 1948). Some instances of this kind probably represent short-term fluctuations and species are generally in a state of dynamic equilibrium ;in other cases there may be a more lasting change. Carlisle (1954a)recorded a continued rise in the numbers of Trididemnum niveum (Giard) at Plymouth between 1951 and 1954 until in some places it had become the most abundant ascidian. He suggested that the species may have arrived from the French coast with the large brown alga Laminuria ochroleuca De La Pylaie and be increasing along with it. Certainly a few species, having found their way to new areas either by natural means or through human

36

R. H. MlLLAR

agency, rapidly become established. Styela clava Herdman was accidentally introduced to the south coast of England from far eastern waters, and multiplied until it became the dominant ascidian in some localities (Carlisle, 1954b ; Houghton and Millar, 1960 ; Stubbings and Houghton, 1964). Small numbers have been found recently on the French side of the English Channel and the species is expected to spread further along European coasts (C. Monniot, 1970). An instance ofemore local introduction is Botryllus schlosseri, first seen within the sluice-dock at Ostend, Belgium in 1960, having apparently been introduced on oysters imported from Holland; in the space of a few months it had reproduced and spread extensively (Polk, 1962). Even without human intervention the constitution of an ascidian population is not static and there is obviously e great need for longterm quantitative studies.

C . Factors affecting distribution and abundance The local distribution of species presents many ecological problems, and the striking differences in ascidian faunas of apparently similar habitats (Prenant, 1928) for the most part still await explanation. 1. Substratum The nature of the substratum is one of the factors determining the presence or absence of ascidian species, most of which either live attached to solid objects or are adapted to life on loose deposits. A few, however, have taken advantage of the fact that the test is a living and plastic tissue able to respond to differences in the substratum. Thus some specimens of Nicrocosmus sulcatus are attached by the base of the body to a solid object, but others develop rhizoids which form a network penetrating the soft deposit and securely anchoring the animal (Costa, 1960). An almost identical case was recorded by Savilov (1958) in the unrelated Chelyosoma mucleayanum Broderip and Sowerby. Responses to differences in the substratum and to other environmental factors may account for much of the variability so often noted in ascidians. For example P6rQs (1946) was able to relate the type of colony in Polyclinum aurantium to the sand-content of the water and to the space available. The remarkable plasticity of the body, and especially the test, enables the adult not only to modify its shape and mode of attachment but also confers a limited freedom of movement. Carlisle (1961) observed movement over the substratum in several species, in one case amounting to 8 cm in three months, and according to Lafargue (1968) Monniot found that colonies of Diplosoma would move away when

THE BIOLOQY OF ASCIDIANY

37

pricked by a needle. Behaviour of this kind may allow the animal to make adjustments of its position in response t o local changes such as the encroachment of other sessile organisms or displacement of the substratum. Most ascidians are fixed to a solid object, and although some seem to have little preference for organic or inorganic surfaces, others appear to be selective. Perhaps the success of Ciona intestinalis is partly due to a catholic taste in Substrata, for it lives on rock, shells and other inorganic things and also on Zostera and algae (Dybern, 1963). Several species of the family Pyuridae live on rocks and in addition on the hard cuticle-like surfaces of large brown algae, on dead calcareous algae, and on other ascidians with a hard superficial layer of test, but are not found on living calcareous algae or on soft brown algae (C. Monniot, 1965a). It is not clear whether this preference is determined solely by the hardness of the surface or by its chemical nature. In the Baltic Sea Styela eorincea uses the shells of living Astarte borealis in preference to stones (Dybern, 1969~). Many species of Ascidiidae, Botryllinae and Didemnidae frequently occur on living algae, and some like Aplidium pallidurn (Verrill) apparently prefer the surface of living plants. (One of the synonyms of that species-Aplidium zostericola Giard-refers to this fact). Of the species of the family Didemnidae occurring in a small area, Lafargue (1968) noted that two (Trididemnum delesseriae Lafargue and Diplosoma singulare Lafargue) required a flexible substratum, another (Diplosomalisterianum (Milne Edwards) ) occurred more frequently on flexible than on rigid supports, and the remaining eleven species lived on a rigid substratum or on both types. Amongst species attached to either algae or inorganic surfaces, there may be preferences for certain kinds of alga, and Dybern (1969b) found Ascidiella scubra (Miiller) t o be common on laminarians, fucaceans, Halydris siliquosa and Delesseria sanguinea, but not on polysiphonians and furcellarians. The abundance of some species is limited by local shortage of suitable hard substrata, as on parts of the Scottish coast where Ascidiella aspersa is moderately common but becomes very numerous when additional surfaces are placed in the water (Millar, 1961b). But even in the presence of suitable objects, it has been observed that the numbers of certain pyurids may be limited if the objects are far apart (C. Monniot, 1965a). Soft loose substrata present particular problems t o sessile animals, but numerous ascidians, of several families, have adopted this habitat, and three kinds of adaptation have evolved. The commonest is the production of test filaments, which penetrate the deposit and become coated with particles, thus effectively fixing the body in position

38

R. I€. Nm.T.AR

(Fig. lGa and b). Numerous examples are to be found amongst the Molgulidae, some in the Styelidae, and in the Pyuridae there are species in which this adaptation occurs only in individuals which happen to be on loose sediment (C. Monniot, 1965a). The second type of adaptation is the possession of a stalk with a a

C

mm

f Flo. 16. Adaptations to loose substrata. a, Bathyatyeloiclea enderbyanua ; b, Dicatpa pacibra; c , Polycatpa delta; d, Eugyra wrnbaeekae; e, Heteroatigma fagei; f, move-

mont of Heterostignra fagei amongst sand grains (c, redrawn from Monniot and Monniot, 1968; e, f, redrawn from Monniot and Monniot, 1981).

TEE BIOLOGY OF IWCIDIANS

39

tuft of basal filaments which anchor the animal (Fig. 16c and d). It

may be more accurate to say that species with a stalk are able to take advantage of soft deposits, and that stalked rock-dwelling forms were pre-adapted for this habitat. Amongst the Pyuridae the short-stalked Pyura legumen Lesson living on hard inshore substrata may indicate the ancestral form from which P . bouvetemis (Michaelsen) evolved. In P . bouvetemis the development of filaments appears to be a response to the kind of substratum, for some specimens instead have a small basal plate (Millar, 1960), more suitable for attachment to solid objects. It haa been suggested that the stalk of P . bouvetemis may be too thin and flexible to support the body off the substratum (Millar, 1960),but Kott (1969) contests this view, and cites underwater photographs taken by the USNS " Eltanin " showing some specimens of the related P . georgianu (Michaelsen)with the body well above the sea-bed. Further striking examples of stalked species are the molgulid Eugyra aernbaeckae Millar, 1960, an Antarctic ascidian living in depths of 55-400 m, and the abyssal genus Culeolw. The third way in which ascidians have become adapted to life on soft bottoms is the more radical one of becoming interstitial animals. The discovery of interstitial ascidians was made by Weinstein (1961), who described Psammostyela delamurei, a small sand-dwelling styelid from shallow water in the Mediterranean. Since then a number of other species have been found in European waters (see F. Monniot, 1965,1966 for references) and one known species (Heterostigma separ drnbackChristie-Linde, 1924) has also been added to this ecological group (F. Monniot, 1966). Despite the systematic diversity-interstitial species are now known from the families Ascidiidae, Corellidae, Styelidae, Pyuridae and Molgulidae-certain features are held in common. F. Monniot (1966) has listed these as : small body size ; shape of body (flattened or, more usually, spindle-shaped), lack of pigmentation, mobility, incubation of embryos and a kind of neoteny. Mobility is perhaps the most noteworthy character. It results from a modification of the muscular activity which in attached ascidians merely achieves contraction of the body, but enables these specialized forms to creep amongst sand grains (Fig. 16e and f). Many species living on a loose substratum are neither interstitial nor stalked, but nevertheless are intimately affected by the nature of the sediment. Glkmarec and Monniot (1966) found a close relationship between the distribution of ascidian species and the granulometric composition of the soft sea-bed off Brittany, France, and concluded that ascidians are good ecological indicators of the nature of the sediment. The ascidian fauna of the Patagonian Shelf affords further evidence of

40

R. H. MlLLAR

the way in which the coarseness of the deposit affects the occurrence of species (Millar, 1960). Substrata which are classed as loose sediments may nonetheless have sufficient hard surfaces to support a population of species not adapted for living directly on sand or mud, as in the case of Ascidiella scubra (Muller) (Dybern, 1969b). Often such species make use of the shells of living molluscs, or the surface of benthic animals including other ascidians. In this way, for instance, Styela coriacea maintains a population in deep muddy areas of the Firth of Clyde, by growing on the upper valves of the mollusc Chlamys septemradiata (Miiller), 42% of which may carry the ascidian, to the number of 2-5 on each Chlamys (Allen, 1953). In the Baltic Sea the same species occurs on the shells of Astarte borealis, some 20% of which have at least one specimen (Dybern, 1969~). And Molgula manhattensis has been found attached to the siphons or shell of 23.5% of specimens of the bivalve Mya arenaria L. cast up on a beach in New Jersey, U.S.A. (Aldrich, 1955). The mesogastropod Trichotropis cancellata Hinds lives on unstable shelly substrata and its hairy surface provides attachment for at least three species of simple ascidian (Yonge, 1962). Appearances can sometimes be deceptive, when species normally confined to solid substrat.es are present on mud. Bouchet (1962) found Ciona and Ascidia mentula living on a soft muddy bottom and only on close examination realized that the animals were in fact attached to the roots of Zostera embedded in the bottom. Ascidians with a hard test themselves serve for the attachment of other ascidians, and 21 species have been found as epibionts on the test of Microcosmus sabatieri Roule on fishing grounds off Banyuls-sur-Mer, France (C. Monniot, 1965b). This large ascidian plays an important part in the ecology of the area, since together with its attached organisms numbering some 200 species it builds up large living complexes known as " blocs B Microcosmus ", which greatly influence the local productivity of the sea-bcd Thus

Fro. 17. Various methotls of attachment on looso substrata. a, Halocynthia papillosa; b, Polycarpa pornaria; c , d, MicrocoemuR ~ u l (redrawn ~ t ~from Costa, 1960).

THE BIOLOGY OF ASCIDIANS

41

Microcosmus effectively constitutes an extension of the rocky shore habitat on to the area of loose sediments and supports a rocky shore fauna. In contrast Halocynthiapapillosa L., another large free-standing ascidian, is devoid of epibiotic forms, possibly owing to its densely papillated test (Costa, 1960). Loose deposits may be sufficiently varied to provide a number of distinct micro-habitats within a single area and accommodate species of diverse requirements, as in the Bay of Marseilles, where the three large ascidians Halocynthia papillosa, Microc o s m ~sulcutus and Polycarpa pomaria (Savigny) have different relationships with the substratum, as indicated in Fig. 17 (Costa, 1960). In a detailed study of the fauna of coralline substrata off Banyuls Laubier (1966) listed the microhabitats of 21 species of ascidian. Only three were photophilic and ten preferred shade ; four lived as epibionts on other organisms-chiefly Bryozoa, hydroids and gorgonianswhereas eleven were attached directly to the hard substratum ; and a variety of preferences was shown for the upper, lateral or lower surfaces of objects. It is evident that, even with the small number of environmental factors considered, most species had a definable microhabitat.

FIQ.18. Distribution of Microcoanzw, aabatieri and M . v d g a r k near Banyuls. Vertical lines, 11.1. sabatieri very abundant ; light dots, M . eabatieri dominant ; horizontal lines, M . eabatieri and M . vulgarie; heavy dots, M . vulgarie abundant (redrawn from Monniot. 1965b).

42

R. € MILIAR I.

Local differences in the distribution of related species, but on a somewhat larger scale, were shown by a survey of the sea bed off Banyuls (C. Monniot, 1965b), where Microcosmus sabatieri and 111.vulgaris were dominant in adjacent areas defined more or less closely by contours of depth (Fig. 18). Numerous faunistic studies of sublittoral areas have given rise to the concept of biocoenoses, communities or associations, but whether or not such assemblages are held together by biological as well as physical factors (see Jones, 1950),it is generally agreed that they exist, and that they can usually be characterized by a set of species. P6rBs and Picard (1958) noted that certain kinds of sea-bed are rich in ascidians, and P&Bs (1967) included ascidian species amongst the animals characteristic of a number of biocoenoses in the Mediterranean. Of four biocoenoses recognized by Bellan et al. (1961) in an area off Corsica one was marked by the abundance of a species of Diazonu, and another was divisible into two facies typified respectively by Polyclinum aurantium Milne Edwards and by various compound ascidians together with Microcosmus sulcatw. Parenzan ( 1959) included eight ascidian species amongst the 47 animals characterizing one facies in the Gulf of Naples, and a Dendrodoa grossularia community has been recognized at Roscoff (Cabioch, 1961). 2. Salinity Ascidians in general are animals of rather high salinity water, although a number of species can withstand varying degrecs of dilution. Osmotic regulation takes place, but difficulties imposed by the large body surfaces, and by the absence of excretory tubules (Barrington, 1965)may restrict penetration into very diluted water. Ciona intestinalis is amongst the species with a wide salinity tolerance, and Dybern (1967) noted that it occurs in areas of the Black Sea having a salinity of under 20%, and also at Suez where the salinity reaches 40-41%,. The lower limit appears to be about 1I%,, both for the adult and the developmental stages, and Dybern's experimental results help to explain the distribution which he recorded around southern Scandinavia. In a similar way the local distribution of Ascidiella scabra (Muller) in the Skagerak and Kattegat is determined by a requirement for average salinities above 24%,, although the adult can withstand occasional reductions to 15%, (Dybern, 1969b). The prevailing salinity was also found to be the most important physical factor determining the presence or absence of a number of ascidian species in different parts of two marine ponds in Norway (Dybern, 1969a) (Table 111). Of these species Molgula munhttensis

43

THE BIOLOGY OF ASCIDIANS

certainly withstands salinities lower than the 23%, recorded since it has been taken from parts of the St. Lucie estuary, Florida, with values as low as lo%,,and even lower at certain tidal states (Gunter and Hall, 1963). Other species known to survive diluted sea water are Ecteinascidia turbinuta Herdman, found by Calder et al. (1966) at 22-47%, and Styeb coriacea which withstands 15%, (Diehl, 1957). S. coriacea and Dendroha grossularia live and breed in the Baltic Sea at a salinity of about 12%, (Dybern, 1969~). According to C. Monniot (1965s) pyurid species are excluded from areas with salinities below about TABLE111. LOWERLIMITSOF SALINITY TOLERANCE OF AVCIDIANS I N NORWEQIAN MARINEPOOLS ~~

Salinity

specie.¶ Clavelina lepadijormia Cwna inteatinalie Corella parallelogramma Ascidia callosa A . conchilega A . mentula A . virginea Ascidiella aapersa A . scubra * Dendrodoa grossularia *Styela ruatica Botrylloides leachi * Botryllua schlosseri * Boltenia echinata Molgula citrina M . manhatten& ~

~~

~~~

x0

14 12 18 30 30 20 20 18 18 20 20 16 23 26 17 23

~

Too few specimens to show clearly the salinity limits.

20%,. In certain places low salinity may preclude breeding owing to the sensitivity of the zygotes, embryos or larvae, while permitting the maintenance of the more tolerant adults. Such populations depend on recruitment by immigrant larvae during periods of higher salinity (Dybern, 1967, 196913). This may apply also to Ascidiella mpersa in the Norwegian ponds, for Knaben (1952) found that salinities below 28%, prevented the development of eggs. But even within a single species different populations show different ranges of tolerance, according to the prevailing salinity in which the adults have been living and this represents a phenotypic rather than a genotypic adaptation (Dybern, 1967, 1969b).

44

R. R. MILLAR

3. Temperature Water temperature is a major factor controlling the occurrence of ascidians but has been considered more often in relation to geographical than to ecological distribution ; in pwticular the ways in which it sets thc limits of distribution by influencing reproduction, have been examined (see Section 111, p. I)). Indeed, temperature is less likely to be a critical factor affecting local distribution than is either salinity or the nature of the substratum, but a few cases of local effects have been recorded. Low winter temperature killed Ciona intestinalis, Styela plicata and Molgula manhattensis but not Botryllus schlosseri in the lagoon of Venice, which has a great annual temperature range but is free from the complicating factor of fluctuating salinity (Sabbadin, 1958). In sheltered semi-enclosed areas and in docks, where great numbers of a few species may be present, it is often difficult to separate the effects of high temperature from those of other factors. But Naylor (1965s) observed marked changes in the numbers and the relative abundance of Ciona iatestinalis and AscidieEla aspersa in the docks at Swansea, Wales, following changes in the water temperature produced by the discharge of heated eMuent from a power station, over a period when other factors were comparatively steady. The response of the two species was complex and resulted in A. aspersa being dominant in winter and spring and Ciona intestinalis in summer and autumn. Effects of this kind depend less on lethal temperatures than on alterations in growth rates and the period and success of breeding (see Sections I11 and IV), although temperature limits for normal embryonic development (Runnstrom, 1929; Knaben, 1952) may determine whether a species succeeds locally. When temperature and salinity both vary, each may modify the effect of the other, but often the extremes do not coincide, and in that situation temperature may be less important than salinity (Dybern, 1969a). 4. Turbidity

Ascidians, being filter-feeding animals, are affected by the amount and nature of suspended matter in the surrounding water, but there are few observations to indicate the importance of this factor in nature. C. Monniot (1965a) discovered that at a depth of 90 m near Banyulssur-Mer a current of 0.5-1 knot raised clouds of sediment from the seabed on which pyurid ascidians were living. A moderate amount of suspended matter appeared to be beneficial, but too much led to clogging of the branchial feeding mechanism and subsequent death. In species bearing a rich epifauna, the death of attached organisms can damage the ascidians by encouraging pollution. Monniot also records

T H E BIOLOGY OF ASCIDIANS

45

the destruction of an abundant population of Ascidia sp. following disturbance of the sea-bed and increased turbidity. The importance of the silt-content is indicated by the presence of fewer ascidians in silty than clear water, on Scottish shores (Lewis and Powell, 1960). Moreover, the effect was more marked in the small compound forms, than in the large Ascidia mentula which withstood turbid conditions. Sediments rich in organic matter may favour certain species by ensuring adequate food in the overlying water, and the presence of Microcosmus sulcatus is said t o indicate such conditions (Carpine, 1964). 5. Light

The influence of light on ascidian larvae-r rather the spacial variation in light intensity-is well known (see Section III), and is one of the principal factors controlling micro-distribution. C. Monniot (1965a) reports that the distribution of Microcosmus sabatieri in the Gulf of Lions is strictly related t o the amount of illumination received, so that on the open sea-bed the upper limit is 15 m, on vertical surfaces facing south 7-8 m, and facing north 3-4 m, and on under surfaces 50cm. A survey of the Gullmar Fjord, Sweden, showed that C i o m intestimlis occurs sparingly on shallow horizontal surfaces, and about 75% of all specimens live on steeply sloping rock walls and overhanging ledges and in caves (Dybern, 1963). It is the larval choice of shaded places for settlement which determines this pattern of distribution, but although little is known of the effect of light on the adults, the development of strong pigmentation in individuals living in shallow unshaded areas (Dybern, 1963) suggests a need for protection from strong light. This is likely t o be more important in species with a thin transparent test than in those having a thick opaque test, and could have been one of the factors favouring the evolution of the ocellus and the associated shadow reflex of the larva which facilitates the choice of shaded areas. The direction of illumination may affect the orientation of the adult body. Ciona intestinalis has been observed t o grow in aquaria so that the long axis of the body and more especially the siphons, are aligned with the direction of the prevailing lighting (Millar, 1953a). I n nature the resulting posture will generally present the oral siphon to falling food particles and may also be useful in ensuring that the body grows up from the substratum. 6.

Biotic factors

The gregarious settlement of marine invertebrate larvae has recently received some attention (see Thorson, 1964 for references), and a few

46

R. H. B f I I L A B

ascidians have been cited as possible examples (Grave, 1935 ;Glaser and Anslow, 1949). Littoral species may be gregarious, but live in such a complex environment that it would be difficult for an observer to separate the results of gregarious behaviour from those of other phenomena. In the sublittoral region, however, a much simpler situation exists, and C. Monniot (19654 believes that the micro-distribution of a number of species points to gregarious settlement of their larvae. Thus Bolteniopsis prenenti Harant was found in isolated groups of 30-40 individuals. Microcosmus vulgaris Heller showed similar aggregations separated by apparently suitable areas which were unoccupied, and Molgula manhattensis, M . occulta Kupffer and Dendrodoa grossularia (Van Beneden) provided further examples. C. Monniot (1965b) further states that in the formation of the characteristic “ blocs Microcosmus” on the sea bed off Banyuls-sur-Mer, the first species to become attached attracts larvae of its own species and only later those of others. Lambert ( 1968) observed that larvae of Corella willmeriana Herdman tended to settle near adults, but the settlement of larvae close to adults is not in itself conclusive evidence of gregarious behaviour, because the adults may influence larval behaviour in the same way as inanimate objects projecting from the substratum, by altering the pattern of light and shade or the flow of water ;gregarious settlement concerns a response of the larvae to the presence of living adults of the same species. There is scope in this field for experiments, particularly as the larvae of some simple ascidims are readily obtained by artificial fertilization. Another biotic factor is suggested by an observation of Goodbody ( 196 1 b) that panels uscd in experiments on settlement failed to develop a normal community-of which ascidians formed a prominent partwhen placed close to mature sponge-anemone-ophiuran communities. Sponges were thought to be responsible, but the way in which they suppressed other communities is not known. We have seen that the nature of the sea-bed influences ascidians, but they themselves presumably have a significant effect on the surface which they populate if they are sufficiently numerous. Diehl (1957) noted the deposit of faeces on the surface of the sediment surrounding Styela coriacea ; and the clarification of turbid water by Ciona (Berner, 1944) involves the removal of suspended organic and inorganic particles from the water and their deposition on the bottom. A dense population of Ciona,such as that recorded by Elroi and Komarovsky (1961) may filter as much as 11 000 l/h over every m2 of substratum occupied, assuming the filtration rate determined in experiments by Goldberg et al. (1951). Even in the less dense populations more commonly occurring in this and other species, these animals must remove much

THE BIOLOGY OF ASUIDIANS

47

plankton from the sea and also contribute significant amounts of metabolites. A further influence which ascidians may have on their environment is in stabilizing a loose substratum, and many sand and mud-dwelling species have abundant test fibrils which bind particles of the surrounding deposit. The molgulid Bostrichobranchus pilularis is an example, in which the body is coated with mud. Moreover, specimens are loosely attached to one another (Van Name, 1945), and evidently constitute 8 living mat on the surface of the sea-bed. The abundance of this species in some areas (Abbott, 1951) suggests the important r d e which such ascidians may play in fixing soft deposits. It is more surprising to find ascidians playing a part in the formation of reefs, but Renouf (1937) has described how, together with sponges, they assist in cementing slabs and boulders on steep rocky banks of the shore. New techniques may assist advances in unexpected directions, and the increasing use of free diving methods has not only clarified the relationships of ascidians to their substratum but also helped in taxonomic studies. For example, Lafargue (1968) examined the didemnids of a limited area off the coast of Brittany, France, and her separation of a number of closely related species, using anatomical characters, is supported by differences of microhabitat in respect to depth, illumination, rigidity of the substratum, and proximity to sediment. Another aspect of local distribution which until recently has received little attention is the extent to which a single species may be divided into sub-populations. It is now known, however (Sabbadin and Graziani, 1967), that Botryllus schlosseri in the Lagoon of Venice has genetically controlled sub-populations existing under the same ecological conditions but a few miles apart. Similarly, sub-populations exist under different ecological conditions at the same location. It is possible that variations in the colonies of species of Didemnidae presbnt a parallel case, for the different forms tend to live in different microhabitats (Lafargue, 196 8). VI. PREDATORS, PARASITES,COMMENSALS AND SYMBIONTS c Organisms are associated in various ways, which have been discussed and defined by Cheng (1967). Predation, parasitism and commensalism are important aspects of ascidian biology and I have used these terms in accordance with Cheng’s definitions, but symbiosis, implying mutual metabolic benefit by associated organisms (which Cheng recognizes as mutualism) is apparently of little significance within the group.

48

R. H. MILLAR

A. Predators Predators are often recognized as such by the remains of their prey found during the examination of stomach contents. Only a few ascidians, however, have parts-the calcareous spicules and in some the test-which sufficiently withstand digestion to be identified. It is not surprising, then, that there are few records of ascidians forming part of the diet of commercial fish, and it may be largely for this reason that they are commonly regarded as distasteful. Thompson (1930, 1931) stated that ascidians are not of much general importance in the diet of fish, although Ascidiella scabra (Muller) sometimes is the chief item of food of the haddock in areas where both species are common. Rae (1956, 1967) also records the occasional presence of ascidians in the stomach of cod and lemon sole, the latter taking both solitary and colonial forms. Some West Indian fish frequenting coral reefs eat " tunicates '' (presumably ascidinns), which constitute 10-28% of the stomach contents according to the species of fish (Randall and Hartman, 1968).

Amongst animals with a very varied diet, crabs are known to take ascidians. Bancroft (1903) found that colonies of Botryllus schlosseri in aquarium tanks at Naples were eagerly attacked by crabs, but Botrylloides leachi was soon rejected and the crabs quickly recognized it as distasteful. The relatively constant appearance of Botrylloides leachi may help would-be predators in learning t o avoid the species ;the colour pattern of Botryllus schlosseri by comparison is very variable. Beaven (1956) described how a single Blue Crab (Callinectessapidus) accidentally confined in a cage along with young oysters and Molgula mnhattensis apparently ate all the ascidians in preference to the oysters. The conditions were, admittedly, unnatural as they are in most feeding experiments, but the observation at least indicates that ascidians may be taken in nature on quite a large scale. According to Goodbody (1963a), polychaetes probably fed on young specimens of Ascidia nigra which he had under observation. Starfish have rarely been recorded as predators of ascidians, but are known to be the chief enemies of Pyura chilensis Molina (Gutihez and Lay, 1965). It is amongst the molluscs that some of the main enemies are to be found, or at least they are more frequently recorded, but in part this results from their being less active, spending more time in attacking their prey, and being therefore more readily observed. Of the prosobranch gastropods Erato voluta (Montagu) feeds on Botryllus schlosseri and Botrylloides leachi, inserting its proboscis through the oral siphon of the zooid (Fig. 19) (Fretter, 1951), and several other species of the

THE BIOLOGY OF ASCIDIANS

49

molluscan super families Lamellariacea and Cypraeacea appear t o prefer ascidians to other prey (Fretter and Graham, 1962). Lamellaria perspicua (L.) possibly lives entirely on colonial ascidians. Velutina velutina (Miiller) attacks Ascidia a n d a pyurid species (Ankel, 1936) and Diehl (1956) has described how it bores through the test of Styela wriacea remaining with its prey for about 2 days until nothing remains but an empty test. This gastropod also lays its eggs on the ascidian and appcers to spend much of its time in association with it. Fusilriton oregonensis feeds on Halocynthia aurantium (Pallas), both in the field and laboratory (Smith, 1070), although this ascidian is believed t o be relatively free of prcdators. Milkman (1967) found that the snail Mitrella lunata attacked Botryllus schlosseri grown in laboratory

FIG.19. Ercrto volutu feeding on BotryZlua schloeaeri (redrawn from Frettor, 1951).

culture vessels, and it probably also does so in nature. The opisthobranch gastropod Pleurobranchus membranaceus (Montagu) preys on both compound and solitary ascidians. Yonge (1949) has described how it waits until the ascidian opens its siphons, then quickly thrusts the proboscis in and feeds on the soft tissues, but it also has other methods of attack and may bore through any part, of the test of large ascidians (Thompson and Slinn, 1959). A number of nudibranch molluscs (Goniodoris nodosus (Montagu), G. castanea Alder and Hancock and Ancula cristata (Alder))feed on the colonial Diplosomu listerianum, Botryllus schlosseri and Botrylloides leachi, and on the solitary Dendrodoa grossularia. Idulia elegans also attacks the solitary Polymrpa pomuria (Savigny) (Hoffmann, 1926). An interesting parallel t o the feeding habits of these gastropods is to be found amongst the turbellarian flatworms, some of which habitually feed on ascidians. Cycloporus papillosus Lang attaches itself t o colonies of Botryllus and Botrylloides, by its ventral sucker, and, in-

60

R. € MrLLAR I.

serting its pharynx within the colony, extracts whole zooids which pass intact into the gut (Jennings, 1957). Where the prey is larger, as in the solitary species Corella willmeriana Herdman, the flatworm Eurylepta leoparda Frceman enters the branchial sac before attacking the tissues, rolling itself into a tubular shape to pass through the oral siphon (Lanibert, 1968) ; after 3-7 days only the test remains. Experiments made by Lambert suggest that this flatworm feeds only on Corellu willmeriana and refuses other solitary and colonial species. This recalls earlier work by Crozier ( 19 17), who found that specimens of Pseudoceros crozieri would feed only on the species of ascidian with which they had previously been associated. Finally, amongst the mammals, the Grey Seal has been noted t o take ascidians (Rae, 1968), although these probably form a very small part of a varied diet. Man can also be included amongst the predators since some of the larger ascidians are collected for food in the Mediterranean and Chile (Harant, 1951) and in Japan (Tokioka, 1953). If an ascidian is common and large it is sometimes used for bait, as in the case of Pyura praeputialis (Heller) in Australia (Hedley, 1915)) where local populations may be depleted by fishermen (Pope and McDonald, 1968). In South Africa a few species also serve as bait (Harant, 1951). Apart from such deliberate gathering, large quantities of ascidians must be destroyed accidentally in the course of commercial fishing, and where they are regarded as pests, as on oyster beds, they may be systematically dredged and destroyed (Cole, 1956).

3. Commensals, parasites and symbionts It is generally a fairly simple matter to decide if one animal preys upon another, but other kinds of association between species-phoresis, commensalism, mutualism and parasitism-are often difficult to distinguish in practice. No doubt most cases of such association could be classified if the physiology of the partners had been studied, but such studies involving ascidians are rare. Many instances of commensalism are known in which ascidians act as the hosts, and their suitability is doubtless due to the large branchial and atrial cavities, the filter-feeding habit which brings continuous supplies of food and water, the relative ease of entry to the cavities, and the absence of effective defensive mechanisms. The Crustacea contain some of the best known commensals, of which the notodelphyid copepods are particularly widespread. Species of this family are almost exclusively associated with ascidians. Schellenberg (1922) listed 89 species, and others have since been added (Illg, 1958 ;Illg and Dudley, 1961, 1965). Little is known of the effect of these

51

THE BIOLOOY OF ASCIDLANS

copepods on their host, but the presence of large numbers can scarcely be without some effect ; Illg (1958) took about 300 specimens of a species of Doropygus from the branchial sacs of 20 specimens of an ascidian in addition to 28 amphipods, five polychaetes and two pinnothcrid crabs from the branchial or atrial cavities. And, according to Gotto (1067), several individuals of Notodelphys allmuni often inhabit even small specimens of Ascidiella aspersa. Moreover some of the copepods are quite large in relation to the cavity they inhabit, and a single specimen may occupy fully half of the branchial sac (Gotto, 1961). Nevertheless, the host generally shows no sign of ill effects, and Corella parallelogramma infected with Ascidicola rosea Thorell appeared to survive, feed and spawn as well aa uninfected specimens (Gotto, 1957). This suggests B long-established evolution of the commensal species in association with the host species. Adaptation is evident in the life cycle of this copepod, for the female bearing fertilized eggs movcs from the ascidian’s oesophagus to the stomach, where the eggs are deposited and hatch, but the nauplii retain the inner egg membranes while passing through the ascidian’s intestine and rectum, being freed from the membranes only after leaving the anus (Gotto, 1957). An opposite migration by the ripe females, from the stomach to the branchial sac, occurs in another ascidicolous copepod, Enteropsis sphinx (Aurivillius), whose nauplii are presumably released through the oral siphon (Gotto, 1961). Another adaptation by a commensal is the timing of breeding in Ascidicola rosea Thorell, which produces its larvae when a newly settled generation of the host Ascidiella aspersa is established and can be infected at an early stage (Gage, 1966). Although many copepods live as commensals in ascidians, others have adopted a more or less parasitic existence, some in cysts within the tissues or blood vessels, but the life histories are almost entirely unknown (Illg, 1958). One of the most remarkable is Gonophysema gullmarensis Bresciani and Lutzen (Fig. 20), a species living in the body wall of Ascidiella aspersa, surrounded by a blood space from which the parasite, lacking both mouth and gut, presumably obtains its nourishment (Bresciani and Lutzen, 1960). Since the average number of parasites in a host appears to be about three, however, and the size only from 1-8 mm, little damage may result. The parasite is surrounded by a thin membrane of host tissue, indicating some reaction on the part of the ascidian. But the colonial Distaplia unigerrnis Ivanova-Kazas has no detectable reaction to the presence of parasitic copepods (Ivanova-Kazas, 1966). In addition to the Notodelphyidae, the copepod families specially associated with ascidians either as commensals or parasites are the A.M.B.--B

3

52

R. H. MILLAR

Lichomolgidae, Archinotodelphyidae, Ascidicolidae and Enterocolidae. In these, certain specics occur in several ascidians, but others appear to be much more host-specific (C. Monniot, 1961, 19658). C. Monniot (1961) has also found that some of the copepod species characteristically occupy particular parts of the branchid sac and that there appears to be no antagonism between species occupying the same host. What factors determine the incidence of commensalism or parasitism, and whether there is any chemical attraction leading to infection are unanswered questions. At.

‘Pb .

.

FIQ.20. Gonophyaema gullmarensia in the body wall of Aacidielln nsperaa. 8. with egg

sacs protruding int.o tho atrial cavity ; b, soen in a transverse section of the branchid region of tho ascitlian (redrawn from Bresciani and Liitzen, 1960). At., atrium; G., gonad of parsuite; Ph., pharynx.

A few amphipods are commensal in solitary or colonial ascidians (Harant, 1931) and infection may amount to almost 100% of the host species (C. Monniot, 1965a). Amongst the decapods also there are instances of commensalism. Several species of Pontonia are reported from solitary ascidians (Oka, 1915; Kemp, 1922; Sluiter, 1927). In view of the large size of the crustaceans these authors considered that the host was entered only by the larval Pontonia, but Harant (1931) found that adult P . $avomaculata Heller taken experimentally from Ascidia mentula and Phallusia mammillata repeatedly made their way back into the branchial sac. This ability, together with the apparently unsuitable food which the crustacean would find in the branchid sac (Sluiter, 1927) suggests that Pontonia may shelter within the ascidian and leave it at intervals to make feeding excursions. It would be interesting to investigate how

THE BIOLOGY OF ASCIDIANS

53

the ascidian reacts when the Pontonia enters its siphon, which would normally close on being stimulated. But if the ascidian accepts its guest, what is the advantage to the host? It is striking to see, as I have, specimens resembling a Pontonia, of length 2-7 cm, in the branchial sac of Ascidia interrupta itself only 7.3 cm long (Fig. 21). Also amongst the decapod Crustacea a few species of the pea-crabs Pinnotheres have adopted the branchial sac of simple ascidians as their residence (Harant, 1931 ; Salfi, 1939 ; MacGinitie and MacGinitie, 1949).

Fia. 21. Aaridin interrupfrc with a large commonsel. possibly a species of Z'onfonin, in tho branchial sac.

Although nothing is known of the host's reaction, there is some evidence that the pea-crabs and the amphipod Leucothoe spinicarpa will tolerate each other, but will not accept the alpheid Pontonia flavomaculata (Harant, 1931), and i t would be surprising if some sort of exclusion did not take place in the restricted micro-habitat offered by an ascidian branchial sac. Few molluscs live as commensals with ascidians, the best known being the bivalve Musculus marmoratus (Forbes) found in the test of Ascidia mentula and less commonly Ascidiella aspersa and other European species. Brewin (1946, 1948) records the presence of mussels from several species of ascidians in New Zealand. Another was found in the test of Herdmania momus (Savigny) (Das, 1938), over 40 individuals sometimes inhabiting a single specimen.

54

R. H.MILLAR

Bourdillon (1950) found that the mussel does not penetrate the test of its host, but merely makes a depression by pulling the shells down after attaching byssus threads. The mussel is apparently not attracted by the ascidian, but preferentially settles down on the test following an accidental encounter. The bedding reaction, however, is probably a response to a chemical factor of the test, since it occurs even when an eviscerated test is offered. There can be little question of mutual benefit from the association, and the ascidian tolerates the mussel without suffering by its presence. A few gastropod molluscs have adopted a similar home in the ascidian test (Harant, 1931). C. Monniot (1965a) found polychaetes in the cloacal cavity of Microcosmus multitentaculatus Tokioka and the nemertine Tetrastemma vittatrtm in 90% of Microcosmus sabatieri Roule collected at Banyulssur-Mer. As already mentioned in relation to copepods, the distinction between commensalism and parasitism is difficult to establish, but undoubted parasites of ascidians are numerous amongst other systematic groups (Harant, 1931 ; F. Monniot, 1965) although we still know little of the effect on the host or of its response. One hydroid species, Endocrypta huntsmani (Fraser) has been reported from the branchial wall of ascidians (Fraser, 1937). What is often termed symbiosis, and more strictly mutualism, implies some degree of metabolic dependence between the partners. Droop (1963) has reviewed the significance of relationships between certain animals and symbiotic algae, and both he and Yonge (1937) pointed out that these animals usually have intracellular digestion. The fact that in ascidians digestion is extracellular may explain why they so seldom have symbiotic algae. Smith (1935) found that a number of tropical species of Didemnidae have algae in the cloacal cavities or the test, but doubted whether the ascidians could benefit from the association. PBrits (1960) also described algal cells in a species of Trididemnum from the Red Sea and Tokioka (1967) found zoochlorellae in lacunae of the common test of Trididemnum cyclops Michaelsen from the Gilbert Islands, and embedded in the test substance of T . v i d e (Herdman) from the Philippine Islands. In the last named species the zoochlorellae are apparently surrounded by the densely packed calcareous spicules of the test and it is uncertain if efficient photosynthesis would take place in such a situation. The following Indonesian didemnid species are also reported to have zoochlorellae in spaces of the test (Tokioka, 1967): Lissoclinum patella (Gottschaldt), Lissoclinum pulvinum (Tokioka), Diplosoma virens (Hartmeyer). A remarkable case was found by

THE BIOLOQY OF ASCIDIANS

55

Eldredge (1967), in which the larva of Diplosoma virens (Hartmeyer) was seen to have special pouches filled with conspicuous green algae ; the anatomical modification of the larva suggests that the relationship here is regular and possibly of mutual benefit.

VII. GEOGRAPHICAL DISTRIBUTION Many factors must have played a part in determining the present pattern of geographical distribution of species. Changes in the positions of land and sea masses during geological times were undoubtedly important, and have been used for instance to explain the widespread occurrence of certain species in the West Indies, Mediterranean and Indo-Pacific (Huus, 1927). Hydrographic conditions, too, have varied and may have influenced speciation and the isolation of species (Knox, 1963). The biological characteristics of the group have also to be taken into account. Amongst these is the short pelagic life of the larva which restricts dispersal, and Huus (1927) has shown that few ascidian larvae could be expected to survive oceanic transport over distances greater than 500 km. Transport on driftwood and algae, and in recent times on ships, is a more likely means of dispersal across wide and deep seas. The spread of species along coastlines, however, is less subject to restrictions imposed by larval biology and will be limited chiefly by the occurrence of unfavourable features in the environment, such as unsuitable substrata, temperatures which do not permit breeding, and other factors discussed elsewhere in this review. Studies of the zoogeography of ascidians are rather few. One of the most detailed was made by Hartmeyer (1923, 1924) who analysed the ascidian faunas of the Arctic and Boreal and interpreted them in relation to hydrographic conditions. The papers by Thompson (1930,1931,1933, 1934) were in part a translation of Hartmeyer’s work to which were added records from Scottish and adjacent waters. Huus (1937) included a review of world distribution in his major work on ascidians, PQrks (1958) has dealt with Mediterranean species, Oka (1935) and Tokioka (1963) with those of the Japanese seas and Kott (1969) with the Antarctic species. I n addition, many taxonomic papers describing collections from diverse areas give some consideration to questions of distribution and faunistic affinities. One of the principal obstacles to resolving questions of geographical distribution, faunistic relationship, and the origin of faunas is the unequal effort which has been made in different regions. The ascidians of several areas are now quite well known, but for certain large and important regions information is scanty. This is particularly SO in the waters of the Indian peninsula, and much of the Pacific and Atlantic

56

R. 11. MILLAR

coasts of South America. Moreover, the accounts of these faunas which have been extensively studied reflect the varying viewpoints of different systematists, some of whom have been more ready than others to create new species. A. Shallow-water ascidians Assuming that most of the species are now known in the areas which have been reasonably well studied, it is of interest to look at the relative richness of the faunas. In doing so it is necessary to compare like with like, by taking areas defined by the homogeneity of their faunas and having regard to the hydrographic conditions, sudden changes in which, over a short distance, often determine faunistic boundaries. Figure 22 shows the approximate number of ascidian species believed to occur in the main shallow-water zoogeographical regions. The regions are broadly those defined by Ekman (1953), but with some local modifications adopted by students of particular areas. It is evident that certain faunas are much more diverse than others, the Mediterranean, Indo-Malayan, southern Japanese and northwestern Pacific faunas being notably rich in species, the polar seas, subantarctic and temperate North American Atlantic less so, and in general the warm-water faunas have most species, although not necessarily most individuals. It should be noted, incidentally, that the total number of species throughout the world is not the sum of the numbers of all the regions, because by no means all species are confined to one faunistic area, many being shared by adjacent or even by several more distant areas. The warm-water regions, which will be considered first, are remarkable both for their richness and for the number of species of wide distribution. And some genera, such as Eudistomu, although not confined to warm regions, find by far their greatest development there.

Indo- West-Pacijc This is a very large region comprising the coasts of the Indian Ocean, the Indonesian archipelago, the western Pacific north to about Tokyo, and the northern, as well as much of the western and eastern coasts of Australia. Although relatively homogeneous, the region can be divided into a number of faunistic areas. Southern Japan The ascidian fauna of Japanese and immediately adjacent waters is very diverse, Tokioka (1963) having listed 277 species. These are divisible into four faunistic groups :

I

Scale: no. of species

I50 I

Fro. 22 Estimated number of species of ascidians in the main zoogeographical areas, but escluding abyssal species. A, Southern Japan; B, Indo-Malaya ; C, Western Indian Ocean ; D, Red Sea ; E, Northern Australia (Damperian); F, Northern .Australia (Solanderian) ; G, Eastern Australia ; H, South-eastern Australia (Maugean); I, Southern Australia (Flindersian) ; J, South-

western Australia (Baudinian); K,tropical West Africa ; L, tropical and subtropical American Atlantic ; 31, Mediterranean ; N, tropical and subtropical American Pacific ; 0, boreal European Atlantic ; P. boreal American Atlantic ; Q, temperate north-eastern Pacific ; R, tempcrate north-western Pacific ; S, Arctic ; T,Antarctic ; U, Antiboreal South American ; V, Kew Zealand (Aupourian) ; W,New Zealand (Cookian) ; X,New Zeeland (Forsterian); Y, South Africa (south coast); Z, South Africa (Namaqua).

cn

4

68

R. H. 1. 2. 3. 4.

MILLAR

northern cold water species (north of Hokkaido and Korea); cosmopolitan species ; north-temperate species (all four main islands) ; warm-water species (southern part of Honsyu Island).

Some 74% of the total occur in southern Japanese waters, although only about 18% are strictly warm-water species belonging to the warm Indo-West-Pacific faunistic region and not extending north of the middle of Honsyu Island. These results confirm and amplify the earlier work of Oka (1935), who distinguished between the northern and southern elements in the endemic ascidians of Japan. The faunistic boundary passing through Honsyu Island corresponds closely to an abrupt change in the temperature regime brought about by the opposition of cold south-flowing and warm north-flowing currents, and emphasises the importance of temperature in determining distribution. The occurrence of 16 species in both southern Japanese and West Indian waters (Tokioka, 1963) is a remarkable example of the wide distribution of tropical ascidians.

Indo-Malaya The sub-region extending from the Indian sub-continent to the southern coasts of China, and including the Malay archipelago, is known to be one of the richest in species of any part of the seas. Unfortunately the collecting effort has been very uneven, relatively little being known of the ascidians of Indian waters, whereas those of the Malay archipelago and neighbouring waters have been well studied, principally by Herdman (1881, 1882, 1886), Sluiter (1885, 1904, 1905, 1909), Van Name (1918) and Tokioka (1950, 1955, 1967). As always, it is difficult to arrive at the total of good species in the area, but I estimate that there are about 178 already described. Allowing that less intensive collecting has been done there than in southern Japanese waters, the islands of Indonesia must be regarded as comparable in richness. Nevertheless there may be marked local differences in numbers of species and individuals as Van Name (1918) found in the Philippine Islands. Only statistical analysis of the results of planned collecting would show whether such differences result from inadequate sampling or are real and relate to local variations in habitat. Western Indian Ocean Many fewer species are recorded for the western part of the IndoWest-Pacific, which includes the eastern African coast and the islands of the western Indian Ocean. The area has been but poorly investigated,

THE BIOLOQY OF ASCIDIANS

59

and the papers by Michaelsen (1918, 1919a, 1920a) remain the chief source of information, but it may well be true of ascidians, as of other groups, that the western part of the Indo-West-Pacific region is significantly poorer in species than Indo-Malaya.

Red Sea About 53 species of ascidian are known from the Red Sea and the results of Michaelsen (1919b, 1920b) and Kott (1957b) demonstrate only a small endemic element. The occurrence of the majority of species also in other parts of the Indo-West-Pacific, as far eastwards as Indonesia and northern Australia, emphasizes the essential unity of the ascidian fauna of this large region. The modest number of species in the Red Sea may be partly a result of rather uniform and extreme environmental conditions. North-west, north and north-east Australia The northern coastal waters of Australia, from about 29'5 in the west to about 33"s in the east, support a warm-water and tropical fauna. The Torres Strait divides this coast into an eastern (Solanderian) and a western (Dampierian) province, each with perhaps about 50 species. Despite the evidence from echinoderms that these provinces have distinct faun= (Clark, 1946), there is some doubt whether ascidian distribution supports the clear separation. Analysis of Kott's (1957a, 1962, 1963) results shows that 20% of the species examined occur in both provinces, but this low figure may be due to the scarcity of records, since more complete collections from the northern coast (Kott, 1966) indicate that 76% of the species occur in both provinces. Kott (1966) found a strong relationship between the ascidian faunas of northern Australia and those of Indonesia, the Philippines and Japan. Only the Didemnidae provided species with a range extending across the Indian Ocean to the east African coast ; it may be significant that this is, systematically, the most difficult of all ascidian families and therefore the one in which there may be the greatest temptation to place specimens in species known to occur in other parts of the region. The fauna of the southern coasts from about Perth to Sydney is distinct and shows some a0inity with that of New Zealand and even with cooler more southerly areas according to Kott (1963), who also found evidence of subdivision of the south coast ascidian fauna. Tropical and subtropical West Africa The strictly tropical fauna of West Africa appears to extend from about 15"N to 15'5, and a related subtropical Mauretanean fauna from

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R. H. MILLAR

15”N to the Straits of Gibraltar (Ekman, 1953). Over 70 species are known from the tropical part (Michaelsen, 1915; Millar, 19538, 1965), and although this relatively small number may be to some extent the result of incomplete knowledge it nevertheless indicates less favourable conditions than those of tropical areas of the Indo-West-Pacific region. Michaelsen (1915) did not stress a faunistic connection between the Guinea fauna and that of the West Indies, but Millar (1953b) found a collection of ascidians from Ghana to consist of a large endemic element, a small pan-tropical element and a small but interesting element comprising species also recorded from the West Indies. A similar result was shown by material from the “Atlantide ” Expedition (Millar, 1965),and PQrAs(1949) noted that 25% of the ascidians which he examined from Senegal were also known from the West Indian area.

Tropical and subtropical American Atlantic Hydrographic conditions indicate Cape Hatteras (35ON) as the northern limit of the eastern American warm-water region and a point south of Rio de Janeiro as the southern limit. Over much of the southern part of this area, however, the fauna is poorly known and it is difficult to determine how closely the faunistic boundaries correspond to the hydrographic ones. My estimate of about 83 species is based on the accounts of Van Name (1945), Rodrigues (1962, 1966) and Millar (1958b, 1961a, 1962~). This is only a modest fauna for a warm-water region, being scarcely greater than the relatively poor ascidian fauna of West Africa, and contrasts with the richness of other systematic groups. It has already been noted above that several species are common to the warm-water faunas of the western and eastern Atlantic. The Mediterranean Although geographically the Mediterranean looks like an entity, hydrographically and faunistically it is not sharply separated from the eastern Atlantic. This has long been recognized in other animal groups, and was confirmed by PQrAs(1958,1967)for the ascidians. He listed 130 Mediterranean species, of which 32% occur also in the temperate part of the Atlantic. More than half of these Atlanto-Mediterranean species do not extend into the eastern basin of the Mediterranean and are presumably Atlantic in origin. Within the Mediterranean there is a marked faunal division between the western and eastern basins, confirmed by the low percentage of ascidian species known from both basins. But half of all the species are endemic, and the fact that this proportion is much higher than amongst hydroids is explained by P&As

THE BIOLOGY OF ASCIDIAXS

61

as a result of the shorter pelagic life of ascidians. The remainder comprises mainly small numbers of widespread species, and species occurring throughout warm waters. Only one species is common to thc Mediterranean and thc Rcd Sea.

Tropical and subtropical American Pacijic From the Gulf of California in the north to about 4"S,on the coast of Peru, a warm-water fauna exists, part of which is tropical. The difficulty of fixing the northern limit of the region, for ascidians as for other groups, has been noted by Van Name (1945),and is due to the presence of cool water quite close to the coast far south on the Pacific side of the United States. However, it is established that the Gulf of California has a tropical ascidian fauna (Ricketts and Calvin, 1939). The southern limit of the region is not precisely known because the fauna is insufficiently described. The total of about 45 species indicates a poor fauna. Few of them other than circumtropical species occur also in the Atlantic American area. In other animal groups, including crabs and echinoderms, although the percentage of species common to the Atlantic and Pacific sides of Central America is also small, there is a substantial number of shared genera. Such comparisons of genera have little significance in ascidians, since most genera are of very wide occurrence. Boreal European Atlantic The whole temperate North Atlantic could be taken as a faunistic unit, but the eastern and western sides are sufficiently distinct to be considered separately. On the European coast the northern and southern limits are approximately the North Cape in Norway and the western end of the English Channel. The papers of Hartmeyer (1923,1924) and hback-Christie-Linde (1922,1923, 1928, 1934)remain the major zoogeographical accounts of the European boreal ascidians, and subsequent work (Thompson, 1930, 1931, 1932, 1934;Millar, 1966c) has done little more than fill in certain details. The total now stands at about 74 species, and although new species will doubtless be found, particularly from specialized habitats not hitherto examined in detail, it is not to be expected that the list will be greatly lengthened. The ascidian fauna is considerably poorer than that of the Mediterranean with its 130 species, although as we have seen the Mediterranean is not faunistically sharply cut off from the Atlantic. Few ascidians are strictly endemic to the European boreal region, and most of those which are centred there extend either northwards some way into the Arctic or southwards as far as the western basin of

62

R. H. MILLAR

the Mediterranean. Polyclinum aurantium, Aplidium nordmanni, Corella parallelogramma, Pyura tesselata and Microcosmus claudicuns are perhaps the species most nearly endemic, since none extends into the Arctic and, although all occur in the Mediterranean, P6rBs (1958) notes them as rare. Boreal species living on the continental slope may penetrate southwards beyond the latitudinal limit applying in littoral and inshore areas. Thus at depths of a few hundred metres in the Bay of Biscay an ascidian fauna exists which has more affinity with that of Scandinavia than with the fauna of the adjacent French coast (C. Monniot, 1969). Amongst the large Boreal-Mediterranean and Arctic-Boreal elements the limits for individual species in some cases at least appear to depend on temperatures which limit breeding (Millar, 1954a, 195413). A number of European ascidians are known also from the western Atlantic. Many of these are northern species with a more or less continuous distribution including Iceland and southern Greenland. The bridge formed by these islands together with the Wyville-Thompson Ridge accounts for the presence of species on each side of the otherwise impassable barrier of the deep Atlantic Ocean (Huus, 1927, 1936). Huus and Knudsen (1950) remarked that all of the 33 species known from Iceland, with a single exception, occur also on both the western and eastern sides of the Atlantic. Similarly, Lutzen (1959) showed that a high proportion of ascidians from Greenland are also known from both European and American coasts, although only some penetrate southwards into European boreal waters. Within the region the Baltic Sea constitutes an area of highly specialized conditions, characterized by the low and variable salinity. As noted elsewhere (p. 42) few ascidians can withstand very reduced salinities, and their limited powers of osmotic and ionic regulation (Barrington, 1965) account for a failure of the group as a whole to penetrate much beyond the transitional zone of the Belt-sea. Thus only three out of ten species collected from the Oresund and Kattegatt extended to areas of markedly reduced salinity (Millar, 1959b), and Dybern (1967)states that of about 30 species in the more saline approaches to the Baltic only three can be found in the southern Baltic proper. The distributional maps of Hartmeyer (1923, 1924) confirm the poverty of the Baltic ascidian fauna.

Boreal American Atlantic Ekman (1953) accepts Cape Hatteras as approximately the southern limit of the temperate fauna of the Atlantic coast of North America. The northern limit, although more difficult to establish, is taken to be

THE BIOLOGY OF ASCIDIANS

63

somewhere near Cape Cod. The ascidian fauna of the region is an impoverished one and includes only about 46 species. A number of these are common to both sides of the Atlantic, and Huus (1927) noted that 24 of the 28 European boreo-arctic species but only 4 out of 46 European boreal and south boreal species occur also on the American coast.

Temperate north-euatern Pacijic The Pacific coast of North America, from lower California to the Alaskan peninsula, forms one faunistic unit, with more or less distinct subdivisions, and Van Name (1945) distinguishes an element centred on the coast of northern California and another on the coast of British Columbia. Water along most of the coast is rather uniform in temperature. The ascidian fauna is not rich, with only about 43 species (Tokioka, 1963), several of which occur over a large north-to-south range. Tokioka contrasts this with the richer fauna of the north temperate waters of the western Pacific, and notes in particular the scarcity of species of Pyura and the absence of Polymrpa, Microcosmus and the subfamily Diazoninae on the American side. Temperate north-western Pacijic The coastal area from about the middle of Honsyu Island, Japan northwards to the eastern coast of the Kamchatka Peninsula constitutes one faunistic region, occupied by temperate and cool-water species. Within this area some 73 cool-water species, and 152 north temperate-water species of ascidian are recorded (Tokioka, 1963), representing a very rich fauna. A number of these occur also on the Pacific coast of North America. Arctic The whole of the Arctic is a fairly homogeneous zoogeographical unit, with only partial longitudinal division into areas having distinct faunas. Hartmeyer (1904) noted this with regard to ascidians, and confirmation is found in subsequent work by Hartmeyer (1923, 1924), h b a c k (1922, 1923, 1928, 1934) and Van Name (1945). The distributional maps in Hartmeyer’s account of the Ingolf Expedition show how commonly Arctic species, especially those of the high Arctic, have a circumpolar distribution. There appear to be about 80 species of Arctic ascidians, and the fauna is not only quite rich in species but locally very rich in individuals. MacGinitie (1955) and Abbott (1966) found them to be one of the dominant groups of marine invertebrates at Cape Thompson, Alaska. In any given area the ascidian fauna itself

64

R. 11. MILLAR

is oftcii dominated by a few species, as in the Canadian Arctic, whcrc of 27 ascidian species identified, thrcc (Boltenia ovifera, Boltenia echinnla and Ascidia callosa) accounted for about half of all specimcns collccted (Trason, 1964). The Arctic ascidian fauna is, naturally enough, most closely allied to that of the colder parts of the boreal regions of the Atlantic and Pacific Oceans; and the eastern Pacific shows more afinity to the Arctic than does the western Pacific (Tokioka, 1963). The land mass encircling much of the Arctic Ocean can account for the relatively uniform nature of the fauna, but for the gap made by the North Atlantic and the Greenland Sea. The submarine ridges linking northern Europe, the Faeroes, Iceland and Greenland may have formed a bridge across which species could pass (Huus, 1927, 1936), but Liitzen (1959) suggests an alternative or additional route of ascidian migration, by way of the unbroken shelf bordering the north polar sea, possibly during periods when the Arctic was less cold than now.

Antarctic The Antarctic region is one of the most clearly defined of the worlds zoogeographic divisions, and its northern limit coincides rather closely with the abrupt change in water temperature indicated by the Antarctic Convergence. It is distinguished, too, by the sudden increase in depth at the edge of the shelf, and the Antarctic shelf fauna is in consequence somewhat isolated from neighbouring shelf faunas. Two divisions have been recognized : the high-Antarctic sub-region consisting of the continental coastal area and the low Antarctic sub-region including South Georgia and Shag Rock Bank (Ekman, 1953). Knox (1960) accepts these provinces, but Kott (1969) in dealing with Antarctic ascidians takes the South Georgian province to include the Bellingshausen Sea, the Antarctic Peninsula, and the South Shetland, South Orkney and South Sandwich Islands. The shelf fauna of the region contains about 73 ascidian species, this total being based on the most recent accounts by Vinogradova (1962a) and Kott (1969), but excluding some doubtful species. In other invertebrate groups most species seem to occur fairly generally in suitable habitats around the continent (Mackintosh, 1960) and Kott (1969) mentions five ascidians as circumpolar, although others appear to be more localized. The South Georgian province, as defined by Kott, contains a mixed fauna, and she named six ascidian species which extend southwards into it from the Subantarctic. Material collected by the " Discovery " from South Georgia proper contained 15 species also known Zrom adjacent Subantarctic areas, out of a total of 32 species

THE BIOLOGY OF ASCIDIANS

66

(Millar, 1960). The faunistic relationship between South Georgia and the Magellanic and Falklaiid Islands area of the Subantarctic is also confirmed by the results of the Norwegian Antarctic Expeditions of 1928-30 (Millar, 1968). The mixed nature of the South Georgian fauna corresponds to a temperature regime intermediate between the Antarctic and cold temperate (Knox, 1960). As a whole the Antarctic has a large endemic element (Kott, 1969). A comparison has sometimes been drawn between the richness in species of the Antarctic and the relative poverty of the Arctic (Ekman, 1953). This contrast is not borne out by the ascidians, which havc about as many known species in the north as in the south polar areas ;it is not likely that a very unequal collecting effort is responsible for this result, because the ascidians of both regions have been described from most of the major expeditions. Kott (1969) speculated on the characteristics of the ascidian fauna of the Antarctic and Subantarctic. She concluded that viviparity is especially common, as shown by the prevalence of the Molgulidae, Agnesiidae and Polyzoinae. The evidence is rather slight since for instance only a few of the southern molgulids have been proved to be viviparous, although the disposition of the oviducts sometimes suggests that the eggs may be retained. Moreover the Polyzoinae are widely distributed in temperate and warm waters and their viviparous habit seems to be unrelated to polar conditions. Longevity and the large size of individuals or coIonies are frequent characters (Millar, 1960 ; Kott, 1969) and may be related to the richness of phytoplankton as well as to low temperature. Protective siphonal closing mechanisms are also mentioned by Kott, but it is doubtful whether they are particularly frequent in Antarctic ascidians, and indeed their relevance to Antarctic conditions is not clear. Kott also considered tho fauna to have many primitive elements, the families Agnesiidae and Corellidae being cited. The former has few species and is certainly well represented in south polar seas, but the Corellidae, with the possible exception of abyssal species, are as well represented in other areas. There is, too, little reason to regard the Corellidae or Agnesiidae as more primitive than the Ascidiidae, which has few Antarctic species.

Antiboreal Between the Antarctic Convergence and the Anti-boreal Convergence (or Subtropical Convergence) is an extensive area, containing a number of small isolated islands. I n addition, the south-eastern and south-western coasts of South America and thc South Island of New

66

R. H . MILLAR

Zealand lie within the same region, although the tempcrature regimes are not identical.

Antiboreal South America The ascidian fauna of the Patagonian Shelf, Magellan area and Falkland Islands is by now fairly well known mainly as the result of work by Herdman (1882, 1886), Michaelsen (1900, 1007), h n b a c k (1938, I050), Van Name (1945), Millar (1960) and Kott (1969). I

1 1 -4 I

I

I

I

,

I

I

I

I

I

Fic. 23. Distribution of A, Aplidium fuegiense ; B,StyeZa pnesderi; C, Polyoa opuntia; D, Alloeocnrpa iricruaiana ; E, Pyura legumen ; F, Paramolgula gregaria.

estimate that there are about 37 ascidian species in this fauna. The strongest affinity is with the fauna of South Georgia, as demonstrated by the ‘‘ Discovery ” collections in which 15 out of 24 species are also known from that island (Miller, 1960). The following species are either exclusively or mainly found in the area and may be taken as characteristic of its ascidian fauna : Aplidium fuegiense Cunningham, Styela paessleri Michaelsen, Polyzoa opuntia Lesson, Alloeocarpa incrustam (Herdman), Pyura legumen (Lesson) and Paramolgula pegaria (Lesson) (Fig. 23).

THE BIOLOGY OE ASCIDIANS

67

Antiboreal (Subanlarctic)islands

A number of islands in the Southern Ocean are of particular interest since they are subject to approximately the same water temperatures but are separated by great distances and sometimes by very deep water. Kott ( 1969) recognizes a Kerguelen province encompassing Kerguelen, Heard and Macquarie Islands. Although a number of species are apparently endemic to Kerguelen Island, others occur also at Macquarie Island some 90' of longitude to the east. She concludes that, despite its relative nearness to Campbell and Auckland Islands, Macquarie has more affinity to Kerguelen than to these islands, and only one ascidian species, Molgula sluiteri (Michaelsen), extends from the South Island of New Zealand and Chatham Island to Macquarie Island. The ascidians of Campbell and Auckland Islands are known mainly from the studies of Bovien (1921)) Michaelsen (1922, 1924) and Brewin (1950~~).Of the few species recorded, Didemnum studeri Hartmcyer, Corella eumyota Traustedt and Polyzoa reticulata (Herdman) are characteristically Subantarctic, and the islands appear to have been populated from that region rather than from nearby New Zealand, despite the contrary conclusion by Kott (1969). If this is true, the ascidians conform to the faunistic pattern of the molluscs (Hedley, 1916) rather than of the sponges and echinoderms (Ekman, 1953). The Chatham Islands and the relatively shallow Chatham Rise connecting them to the South Island of New Zealand have an ascidian fauna described by Sluiter (1900), Michaelsen (1922, 1924) and Brewin (1956b). Brewin showed it to have a close alliance with the ascidian fauna of New Zealand, 21 of the 33 Chatham species being known from there. No distinctly southern element is present, in contrast to the situation in the Campbell and Auckland Islands. The Chatham Islands lie farther north and, unlike the Campbell and Auckland Islands are subject to warm northern water in addition to cool southern water. The Tristan da Cunha group, like the Chatham Islands, lies near thc Antiboreal Convergence. Occupying a very isolated position between South Africa and South America, these islands appear to have an ascidian fauna, so far as can be judged from the very scanty records, which has some affinity with that of southern South America but none with the South African fauna (Millar, 1967). N e w Zealand Knox (19GO) recognized the Aupourian, Cookian and Forsterian provinces, and my estimates of respectively about 81, 35 and 58 ascidian species are based for the most part on a series of papers by

68

R. H. MILLAR

Brewin (1946, 1948, l950b, 105Oc, 1950d, 1051, 1952a, 1952b, 1954, 1957, 1958a, 1958b, 1960). In some cases it is possible to recognize closely related species with allopatric distribution, as Pyura pachydermatina (Herdman) from the South Island, P . spinosissima Michaelsen from the North Island, and P . chathamensis Brewin from the Chatham Islands (Brewin, 1952b ; Knox, 1063). Distributions of this kind may have resulted from past fluctuations in the position of the boundary between the warm and cold watcr masscs, for which geological evidence exists (Knox, 1963). Other regions of the sea rich in species may also have been subject to such changcs in hydrographic boundaries which promotc speciation.

South Africa The coastal and off-shore waters of South Africa, like those of New Zealand, are influenced by the proximity of warm and cool currents. On the east coast the fauna is tropical at least as far south as Durban, but the south coast from about Algoa Bay to Cape Point supports a distinct fauna. The third faunistic division is the Namaqua fauna, occupying the coast from Cape Point to 18"s and is subject to the cool Benguela Current and to the upwelling of cold deep water. South African ascidians have been extensively studied, by Hartmeyer (1911, 1912, 1913), Michaelsen (1904, 1915, 1923, 1934) and Millar (1955a, 1962b, 1964a), and some 84 species may be recognized, according t o my estimate. A large and representative collection amounting to 69 species taken from coastal waters between Morrumbene on the tropical east coast and Saldanha Bay in the southern part of the Namaqua area showed 39% warm-water, 22% cold-watcr, 4% ubiquitous and 35% south-coast components (Milhr, 1062b). These figures are in quite good agreement with those of Stephenson (1944) for littoral animals as a whole. About half of the South African ascidians are endemic, and the general affinities of this fauna are with the adjacent areas of the warmer Indian Ocean. There is, however, evidence of some relationship with the Antiboreal fauna, in the presence of Aplidium retiforme (Herdman) which also occurs at Kerguelen, Corella eumyota Traustedt, which is widely distributed in southern waters, and Agnesia glaciata Michaelsen (Millar, 1962b). The endemic Sycozoa arborescem Hartmeyer marks the occurrence of a genus characteristic of the Antarctic, Subantarctic and western Pacific. One may conclude that, in the main, the South African ascidian fauna has bcen derived from the Indo-west-Pacific but that a small element originated from the Antiboreal, possibly in a geological period when the Antiboreal Convergence lay farther north than at present.

THE BIOLOGY O F ASCIDJANS

69

Tho ascidians of othcr parts of the world havc been so little investigated or the studies havc bccii so spccializcd-as tho taxonomic rcview of tho Dideninidan: of tlic lndo-Pncific (Eldredgc, 1967)-that general spcculation 011 their faunistic relationships is unprofitable. B. Deepwater aseidium

A number of vertical zones have been recognized in the deep water beyond the shelf, but the terminology and limits applied to them have varied considerably (Hedgpeth, 1957 ; Vinogradova, 1962b). Vinogradova (1969a)recognized a bathyal zone from 500-3 000 m mainly on the slope, an abyssal zone from 3 000-6 000 m constituting most of the sea-floor, and an ultra-abyssal zone in depths greater than 6 000 m and corresponding t o the hadal zone of Bruun (1956). The upper limit of the abyssal zone is somewhat arbitrary, and Ekman (1953) has emphasized that it is not the same in all parts of the oceans. Many abyssal species certainly extend up to 2 000 m and this is the depth which I am taking as the upper boundary. Whether the floor below 6 000 m supports a distinctive fauna is not certain. According to Wolff (1960) it does, but Menzies and George (1967) believe that there is little evidence supporting the view. Very few ascidians have been found at such depths, although they do occur down to 8 430 m in the Kuril-Kamchatka Trench (Vinogradova, 1969a, b, 1970). In less extreme depths there exists a moderately rich ascidian fauna representing several families (Table IV, below). This fauna is known mainly from the accounts of Herdman (1882, 1886, 1888), Verrill (1885), Ritter (1907), Sluiter (1904),Hartmeyer (1911,1912),Michaelsen (1904),Millar (1955b, 1959a, 1964b), Monniot and Monniot (1968) and Kott (1969), whose records are incorporated in Fig. 24. In addition to the bathymetric divisions, geographical divisions are also to be recognized in the abyssal parts of the sea. Ekman (1953) broadly divided the deep seas into the Atlantic, Indo-Pan-Pacific, Antarctic, Arctic, Mediterranean, Red Sea and Sea of Japan. Following a review of subsequent faunistic studies, Vinogradova (1956, 1962b) proposed thc scheme used in Fig. 24, which recognizes more subdivisions. The validity of the geographical areas depends on the distinctness of their faunas, and there is some evidence that the abyssal faunas of the oceans show a measure of independence from one another. Vinogradova (1962b) concluded that, for a number of invertebrate groups taken as a whole, the proportion of endemic species in the Atlantic Ocean is 76%, in the Pacific Ocean 73.2% and in the Indian Ocean slightly over 50%.

60

40 20

0 20

40

60

90

60

30W.

0

30.5.

60

90

I20

150

180

150

120

90

FIG.24. Records of ascidians from water deeper 'than 2 000 m. Zoogeographical divisions : A, Pacific-North-Indian area ; A( 1)Pacific sub-area ; A( la) North Pacific Province ; A( Ib) West Pacific Province ;A( Ic) East Pacific Province ;A(2), North-Indian sub-area ; B, Atlantic area ;B(1) Arctic sub-area ;B(2) Atlantic sub-area; B(2a) North Atlantic Province ;B(2b) West Atlantic Province ; B(2c) East Atlentic Province ; C, Antarctic area; C(1) Antarctic-Atlantic sub-area; C(2) Antarctic-Indian-PacSc sub-area; C(2a) Indian Province; C(2b) Pacific Province.

TABLE IV ASCIDIANS FROM DEPTHS GREATERTHAN 2 000 M Speciea Family Clavelinidac ? Podoclavella sp. Distaplia galathem Millar Hypsistozoa obscura Kott Protoholoroa pedunculata Kott Polycitor fungiforinis Millnr ? Eudhtorna vitreum (Sars) Family Polyclinidae Aplidiuna abyssuna Kott Synoicurn tentaculaluna Kott Pharyngodictyon inirabile Herdman Family Didemnidae Leptoclinulea faeroensis Bj erkan Family Corellidae ? Chelyoeoma inaequale Redl korzev Abyssascidia rcycillii Herdman Corynaeculia su hmi Herdman Corellopsis tranalucula Xllar Benthaecidia michaelseni Ritter

Localitiea

Depth (m)

Reference8

2800 4410 6006 2818-5000

Kott, 1969 Millar, 1959 Kott, 1969 Kott, 1969

5187-5251 2078

Millar, 1970 Millar, 1970

58"OG'S 44"55'\1:

46" 16's 48'27'E

6006 2800 2928

Kott, 1969 Iiott, 1969 Herdniaii, 18SG

37'25'N 73@06'\V

2895

Van Kame. 1916

07'21"

3638

Van Xamc, 1945

4680-5900

Herdman. 1882 ; Millar, 1959 Hartmeycr, 1911 ; 1912 ; 1923-24; Herdman. 1582 Millar. 1970 Rittcr, 1907

58'06's 44"55'\V 3G031'S 178'38'W 08"lO'S 81'08'W 55'54's 58"59'\\' ; 56'18's 37"04'\\' ; 57"04'S 70'59'W ; 64"Ol'S 67"44'W ; 65'37's 123"55'\V 48'34'5 36'04'W 55'37'X 56"08'\V

08"lO'S 8l008'\V

79"02'W

32'10's 175'54'W; 42'42's 131'10'E

58'01's 44"45'\\' ; 61'50'5 56@27'\\'; 33'31's 74'43'1V ; 433-5858 46'66's 45@31'E; 54"17'S 27"25'\\' ; 63"lG'S 57'5l'E 07"30'S 81"25'\\' 33"03'N 120"42'\\;

5857-5858 3927

TABLEIV-wntd ~

Species Family Hypobythiidae Hypobythiw calycodes Moseley ? Megalodicopia hkna Oka Family Agnesiidae Agnesia depessa Millar

A d a g e bi;jida Millar Family Ascidiidaa Bathyascidia VaBCuloaa (Herdman) Family Octacnemidae 0ota;cnernw bythiw Moseley Octacnemw, herdrnani Ritter Family Styelidae Styela sericata Herdman

Styela rnilleri Ritter Styela p d l a Herdman Styela sqmrnosa Herdman Styela bathybia (Bonnevie) Styela loculosa Monniot and Monniot

Lomlities

37'41"

177'4W

~~

Depth (m)

~

References

5220

Moseley, 1876

13'15'5 78'06W

5234-5314

Kott, 1969

24'12" 63'23W-24'28'N 63'18W; ?5'25'S 47'09%; ? 36'34'5 14'08'E 09'22" 89'33W; 07'35'5 81'24W

4820-5860

Millar, 1955; 1959

3517-5841

Millar, 1970

53'55's 108'35%

3510

Herdman, 1888

2'33% 144'04'E ; 36'23% 177'41%

1957-2640

5'17's 85'19W; 6'54'5 83'34W

40634087

Moseley, 1876; Millar, 1959 Ritter, 1906

24'12" 63'23W-24'28'N 63'18W; 5'32% 78'41'E ; 3510-5860 1'56" 77'05'E ; 3'23% 44'04'E ;5'25'5 47'09% ; 7'24'5 48'24% ; 25'11's 59'59% ; 36'31's 178'38W; 36'34'5 178'57W ; 39'45's 159'39% ;43'58'5 165'24% ; 45"51'S 164'32% ; 53'55's 108'35%; 68"03'S 130'46W 33'01" 121'32W; 9'23" 89'32W; 1'42" 7'51%; 3281-4077 06'21T 80'41W; 10'15's 95'41W 36'10'N 42'42'5 75'12" 57'50'N

178"O'E 134'10'E 3'20% 54'06W; 38'16"

71'47W

3751 4758 2195 2864-3369

Herdman, 1888 ; Kott, 1969 ; Millar, 1955; 1959; 1970

Millar, 1959; 1969; Ritter, 1906; Van Name, 1945 Herdman, 1886 Herdman, 1882 Bonnevie, 1896 Monniot and Monniot, 1968; Millar, 1970

Family Styelidae

Minostyela clavata K o t t ? Styela nordenakjoldi Michaelsen Styela sp.? Cnemidocarpa bythia (Herdman) Cnemidocarpa bathyphila Millar Cnemidocarpa bifurcata Millar Cnemidocarpa peruviana Millar Cnemidocarpa digonaa Monniot a n d Monniot ? Cnernidocarpa drygalskii (Hartmeyer) Cnemidocarpa sp. Polycarpa albatrossi (Van Name) Polycarpa pseudoalbatrossi Monniot and Monniot Dicarpa simplex Millar Dicarpa paci$ca Millar

Bathyoncuo diacoideua Herdman Bathyoncuo herdmani Michaelsen Bathyoncuo minutus Herdman Bathyoncua mirabilia Herdman

58"18'S 16Oo03'W 13'15'5 78'06'W

3587-3817 5234-5314

Kott, 1969 Kott, 1969

59'57'5 32'09'5 42'42'5 01'03'N

136'37'W 3386-3477 176'35'W; 32'10'5 177'14'W; 32'10'5 175'54'W; 4400-7000 134'10'E ; 43'58'5 165'24'E ;45'51'5 164'32'E 18"40'W-00"58'N 18'37'W 5250-5300

Kott, 1969 Herdman, 1882 ; Millar, 1959 Millar, 1955

9'23"

89"32'W

3570

Millar, 1964

3369-5760

Millar, 1970 Monniot and Monniot, 1968 Van Name, 1945

07'32'5 81'26'W; ? 57'50"

54'06'W

38'46"

70'06'W

2886

06'21"

SO"41'W

3281

9'23" 89'32'W 39'26" 70'33'W 38'30" 69'08'W 37'38" 73'16'W 9'49'5 114'13'E 39'26" 70'33'W 40'33" 9'23" 9'25" 9'15" 35'41"

; 39'05" ; 38'24" ; 5'32" ; 38'46"

3570 70'44'W ; 38'46" 7O"OG'W ; 2598-4350 71'52'W; 38'22" 70'17'W; 78'41'E ; 1'56" 77'05'E ; 70'06'W

2496-2886

35"24'W-40°34'N 35'52'W ; 36'38'5 178'21'W ; 2470-4600 89'32'W 3514-4050 89'22'W ; 9'24" 89"27'W; ? 9'22" 89'33'W; 89'29'W; 9'23" 89'32'W ; 6'08's 82'41'W 157'42'E 4209

Millar, 1959 Millar, 1969 ; Monniot and Monniot, 1968; Van Name, 1945 Monniot and Monniot, 1968 Millar, 1955; 1959 Millar, 1964; 1969; 1970 Herdman, 1886

63'16's 57'51'E

4636

Michaelsen, 1904

38'09"

5718

Herdman, 1886

2928

Herdman, 1882

156'25'W

46'16'5 48'27'E

TABLEI V - e o n t d Depth (m)

References

3'54" 8'22'W; 1'42" 7"51'E ; 1'03" 18"40'W0'58" 18'37'W; O"42'N 5"59'W ; 3'23's 44'04'E ; 4"OO'S 8"25'E ; 4"47'S 46'19'E ; 5'25% 47'09'E ; 29'42's 33'19'E ; 40"lO'S 6"05W; 45'47% 164'39'E ; 45"51'S 164'32'E ; 63'16's 57"51'E l"03" 18"40'W-0°58'N 18"37'W 55"37'N 56'08'W

2550-5300

Michaelsen, 1904 ; Millar, 1955; 1959

5250-5300 2078

Millar, 1955 Millar, 1970

63'16% 57'51'E

350-4636

Michaelsen, 1904

46'46's 45'31'E ; 64'48's 44'26'W

2928-4548

Herdman. 1912

Localities

Species Family Styelidae Bathyst yeloides enderbyanus (Michaelsen)

Hemistyela pilosa Millar Kuekenthalia borealis (Gottschaldt) Family Pyuridae Bathypera splendens Michaelsen Pungulus antarcticus Herdman Pungulus cinerew Herdman Culeolua murrayi Herdman

46"16'S 58'06's 35'41" 62'03's 65'37'5

48'27'E; 55"52'S 24'49'W; 55"54'S 58"59W; 2818-5918 59'27'W; 64'01's 67"44'W 157'42'E ; 55'01's 44'20'W; 55'54's 58'59'W; 2818-6207 129"38'W; 62'39'5 64"02'W; 64'01's 67'44'W; 121"06'W; 65'37'5 123"55'W; 66"ll'S 102"28'W

Culeolus moseleyi Herdman Culeolus pyramidalis Ritter

O"33'S 151"34'W 33'01" 121"32'W ; 32'54"

121°15'W; 9'23"

89'32'W

Culeolus recumbens Herdman 46'46'5 45"31% 13'26" 145"40'E Culeolua inversus Oka 47'26" 07'53'W ; 40'33" 35'24'W-4Oo34'N 35"52'W ; Culeolus suhmi Herdman 39'22" 68'25W; 37'25% 71'40'W; 5'32" 78"41'E ; 3'38" 78'15'E 3"23'S 44'04'E ; 5'25% 47'09'E ; 14'20's 45"09'E ; 44'18's 166"46'E ; 44"33'S 49'19'W 62"54'S 118'52'E 4e016'S d S D 2 7 ' E

3800

Herdman, 1882 ; Kott, 1969 Hartmeyer, 1911 ; 1912; Herdman, 1882 ; Michaelsen, 1904; Kott, 1969; Vinogradova, 1970 Herdman, 1882 Ritter, 1907 ; Van Name, 1945 Herdman, 1882 Oka, 1928 Herdman, 1882 ; Kott, 1969 ; Millar. 1955; 1959; 1969; Van Name, 1945 Vinogradova. 1962

2986

Hnrdrnnn

4438 3570-4066 2475-3594 3500 2894-5329

. 1852

Family Pyuridae Culeolua uachakovi Redi korzev Culeolics willemoesi Herdman Culeolus parvus Millar Eupera chuni Michaelsen ? Heteroetigma singulare (Van Name) Family Molgiilidae Molgula bathybia (Hart meyer) Afolgula verrilli (Van Name) illolgulu galatheae Millar ilfolgula sp. dfolgula (.Volguloides) imtnziizda (Hartmeyer)

3lolgctla (.llolgtcZoules) sphaeroidea Millar Family Hesacrobylidac Hexucrobylus indicus Oka

46'41.5"

3500

Redikorzev, 1941

4209 3500-4893 4990 5005

Herdman, 1886 Millar, 1969 ; 1970 Michaelsen, 1904 H a r a n t , 1929

63'16's 57"Bl'E

4636

H a r t meyer, 1912

40'29" 66"04'\\' 1 ' 4 2 3 7'5l'E ; 0'42" 5'59'\V 36'34's 14'08'E: 3"56'S 118"26'E ; 20'29's 103"26'JV ; 32'03's 72"40'\V GO"57'S 5G052'\V

3237 2550-5160 4893 1788-5929

7'35'8 8i024'\V; 10'13's 80"05'L\..

5825-6328

Van S a m e , 1912 Millar, 1959 JIillar, 1970 K o t t , 1969 ; 3Iilltir, 1959; 19G9; Van S a m e , 1945 Millar, 1970

39"26'S 70"33'\\' ; lO"07'S 89'50'\V ; 5'325 58"41'E ; l"j(j'N 77'05'E ; 8"52'5 49'25'3

891-5020

3.5'41" 36'34's 2"56'N 38'54"

147O28'E 157'42'E 14'08'E ; ? 56'37's 34'48'W 1l"4O'W 21'06'W; 36'54's 2OC46'\V

Hexacrobylics paanantatodes 45'5 1'S 164"32'E Sluiter Oligotrema psatnmites Bourne 60'57% 56"51'\V Oligotrema sp. 8"lO'S 81"08'\V Gmterascuiia sandersi 36'23" 67"58'\V ; ? 45~~34'3 Gc02'E Monniot antl Monniot

4400 2672-3020 6006 4618-4680

K o t t , 1969 ; llillar, 1959; 1969; 1970; O h , 1913 Jlillar, 1969 Boiirnr. 1903 Kott. 1969 3Ionniot a n d Jlonniot , 1968

Vinogradora (1969b, 1970) has recorded the following species from the Kuril-Kamchatka Trench: Sif ttlrr pellirrtloarc Vinogratlova, c. robusfus \'ino&radova, C'. murrnyi Herdman, C . longipeduculolua Vinogratlova antl Ponreztleolcta bicristntus Vinogratlova. Citleolua Icnuia Wnogradova,

8

s s 8

s E 0

m

0 ul

m

0

0

4 0 ul

8 0 ul

*

o

N

o

o

g

o 0

0 ul

THE BIOLOGY OF ASCLDIANS

77

My own estimates for the ascidian species, based on the published records, are: Atlantic Ocean 72%, Pacific Ocean 68% and Indian Ocean 43% (Millar, 1970), and the group appears to support the view that abyssal faunas show zoogeographical divisions. Certain features of the ascidians, however, such as the plasticity of body form, seasonal changes in structure, and a high degree of variability, have led to uncertainty in the recognition of species, well illustrated by the synonymy proposed by Kott (1969) for Cnemidocarpa nordenskjoldi and for Culeolusmurrayi Herdman. I n the presence of such uncertainties, which are common in abyssal species where identification often rests on few specimens, reliable conclusions on specific endemism are difficult to reach, and it may be useful to consider small distinctive genera, and pairs or groups of similar species whether or not these ultimately prove to represent a single species. By choosing taxa with highly unusual characters-and these are frequent in abyssal forms-we may be confident that we are not dealing with species merely having a similar appearance through adaptive convergence. Styela loculosa Monniot and Monniot and Minostyela clavata Kott, which are characterized by a peculiar form of gonad quite unlike that of any other known ascidian, show a kind of bipolar distribution (Fig. 25). Another group of highly aberrant abyssal ascidians comprises Hexacrobylus indicus Oka (synonym H . arcticus Hartmeyer) and H . psammutodes Sluiter (Fig. 26). Oligotremapsammites Bourne is evidently of the same group of species, but is known only from a depth of 92 m. Kott (1969) believed that all of these represent one species, and although I do not accept this opinion in view of the structural differences in the pharynx, oral tentacles and gut, there is no doubt that the species form a closely related group with a marked systematic separation from other ascidians. The distribution is wide (Fig. 26) and cuts across the boundaries of several regions. The genus Culeolus presents another interesting case, and whether or not Kott (1969) is right in taking 11 of the described species as synonyms of C. murrayi Herdman the great difficulty in separating species underlines the advantage of grouping all together for the present purpose. The wide distribution (Fig. 26) lacks records principally in the Indian Ocean and north polar seas. The last example is the genus Corynascidia (Fig. 25). C . suhmi Herdman is known from widely separated areas and although not recorded from low northern or southern latitudes, it may be expected to occur in most of the deep oceans (Kott, 1969). As known at present its distribution suggests some degree of bipolarity. C. sedem Sluiter and C . herdmuni Ritter have been taken in depths less than 2 000 m from Indonesia and the North Pacific respectively.

FIQ.26. Known distribution ofHezacrobylua indicua ( 0 ) Hexacrobylua . indicuo < 2OOOrn (a), Hexacrobylua paammalodee ( 0 ) .culwlua spp. (a), Bothyetyeloides enderbyanuo (*).

THE BIOLOQY OF ASCIDIANS

79

If we can rely on these few cases where it is reasonably sure that we are dealing with one species or at most a few closely related species, there is less evidence t o support the view that abyssal ascidians conform to the zoogeographic divisions proposed by Ekman and by Vinogradova. Rather they appear t o be widely distributed in the abyssal regions and a t most tend t o have either an equatorial distribution or t o occur in higher latitudes of both the northern and southern hemispheres. There is therefore conflict between these conclusions based on the one hand on all recorded species and on the other on aberrant or very distinctive species. Only if these groups of distinctive ascidians proved t o consist of separate, although similar, species, would the contradiction be removed, with the conclusion that a considerable degree of specific endemism exists. The distribution of abyssal ascidians as a whole is by no mcanR uniform, even within a single region, as Sokolska (1969) shows for the Pacific Ocean. An analysis of all occurrences in the abyssal Pacific recorded by the main deep-sea expeditions shows the ascidians t o be much more restricted than, for example sponges, which might be expected t o have rather similar requirements. IMPORTANCE VIII. ECONOMIC A. Fouling In comparison with some other groups of marine animals thc ascidians cannot be said to have great economic importance. As fouling organisms, however, they are significant and contribute largely t o the problem of growth on the hulls of ships, on buoys and floating structures and on fixed harbour installations. The list of over 100 ascidian species in “ Marine Fouling and its Prevention ” (Woods Hole Oceanographic Institute, 1952) indicates their potential importance, although many of the species recorded are not sufficiently abundant t o be harmful. Almost any shallow-water species in which the adult is normally attached to a firm substratum may appear in a fouling community. Ascidians have been studied as they occur on ships’ hulls (Berner, 1944 ; Skerman, 1960), but more often workers have used test panels or blocks which are examined periodically t o follow the course of fouling (Weiss, 1948 ; Sentz-Braconnot, 1966 ; Relini, 1964 ; Stubbings and Houghton, 1964 ;Allen and Wood, 195.0 ; Elroi and Komarovsky, 1961 ; Kawahara, 1962; Nair, 1962 ; Raja, 1963 ; Skernian, 1959). Whatever methods of asscssment are used, it is evident that ascidians form a major part of the fouling community in many regions of the world. Of

80

R. 11. MILLAR

about 22 ascidian species listed in a report on marine fouling (Organization for Economic Co-operation and Development, 1966), four were classed as principal fouling species, and a number of workers have noted the group as contributing the dominant fouling organisms (Relini, 1964; Stubbings and Houghton, 1964 ; Berner, 1944; Scheer, 1945; Weiss, 1948; Skerman, 1959; Kawahara, 1962). Often they are not prominent in the early stages of the development of a sessile community, but become the principal organisms in later stages. Thus Berner (1944) found that on ships’ hulls at Marseilles there was a regular succession, from Enteromorpha, through Bryozoa and sessile annelids to barnacles and Ciona intestinulis. In Kingston Harbour, Jamaica the primary colonizers were algae and barnacles, but the ascidians Didemnum conchyliatum (Sluiter) and Ascidia nigra became and remained dominant for many months (Goodbody, 1963b). The sequence, and the species involved, naturally vary with the location, and in California, U.S.A., six stages in fouling were recognized, one of which was dominated by an almost pure growth of Cionu, which was subsequently replaced by mussels and barnacles (Scheer, 1945). At Auckland, New Zealand, the initial settlers were barnacles and hydroids but these subsequently gave way to oysters and the ascidian Microcosmus kura Brewin (Skerman, 1959). Similarly in Japanese waters, Styelaplicata became one of the two dominant species in the later stages of fouling (Kawahara, 1962). The relative importance of ascidians depends on the season at which surfaces are exposed to fouling, and ReIini (1964) found that at Genoa, Italy, they were most abundant on test panels in winter, but varied considerably in abundance from year to year. This was also the experience of Elroi and Komarovsky (1961) with Ciona at Haifa, Israel, and of Stubbings and Houghton (1964) during their study of Chichester Harbour, England, where Diplosoma Zisterianum gradually declined in numbers over a period of several years. Some idea of the importance which ascidians may have in the fouling of vessels is given by the numbers recorded by Elroi and Komarovsky (1961), who estimated 2 500-10 000 specimens of Cionu per m2 of exposed plate ; the individuals reach a length of 25 cm, and the total wet weight on 1 m2 was 140 kg. Under favourable conditions Ascidiella aspersa may settle a t the rate of 1 800/m2 per day (Millar, 1961b). It is not so much the weight of the animals which creates a problem, for their under-water weight is not great, but the additional friction which they cause to a moving ship. This must vary in a complex way with the size, shape and roughness of the body, but has not been studied. On floats and other stationary objects ascidians are

THE BIOLOGY OF ASCTDTANS

81

troublesome mainly because they have to be removed when the structures are painted. The settlement and growth of ascidians m;iy also bc a problcin in fisheries. In oyster culture, for example, they often smother surfaces intended for the settlement of the molluscan larvae, impede dredging, or contribute to the silting of oyster beds (Cole, 195G; Waugh, 1957; Millar, 1961b ; Hancock, 1969). Some degree of control can be achieved by treating the settlement surfaces with chemicals (Loosanoff, 1960; Waugh, 1957). Accidental transport is a conscquence of fouling, and has accounted for the introduction of Styela clava to the south coast of England, probably from Korean waters (Carlisle, 1954b ; Houghton and Millar, 1960). The species has subsequently multiplied and spread t o the extent that it is now the dominant large ascidian in certain sheltered coastal waters. It is probable that the widespread occurrence of Ciona intestinulis and Diplosomu listerianum in the harbours of many countries is likewisc the result of introductions on ships’ hulls. Certain structural and biological characters help to cxplain why ascidians are important as fouling organisms. Firstly, because the branchial cavity is large, the total volume and surface area of an individual are high in relation to the tissue weight, and an ascidian therefore occupies a large space or covers a large area. Secondly, being efficient filter-feeders, they grow fast and can outpace many of their competitors. Larval behaviour, too, pre-adapts them as fouling animals, since the larvae initially swim upwards, reaching the surface layers of water where they encounter floats and ships’ hulls, to which they attach themselves. Moreover, the short pelagic life of the larva favours heavy settlenient near the parents, and in harbours there is generally a stock of adults. Some species, in addition, are resistant to reduced salinity or to pollution (Huus, 1933; Berner, 1944; SentzBraconnot, 19GG; Dybern, 1967, 196%; Diehl, 1957; Van Name, 1945; Gunter and Hall, 1963; Dragovich and Kelly, 1964), and these are conditions met in harbours, where fouling on ships is a problem.

B. Food of man, and of commercial fish In some countries, mainly those of the far East and certain parts of the Mediterranean, ascidians are eaten by man and are sufficiently important to merit an entry in the F.A.O. Yearbook of Fishery Statistics (Food and Agriculture Organization, 1964). Microcosmus sulcatus, and occasionally Styela plicata and Polycarpa pomuria are taken in the Mediterranean (Harant, 1951),Halocynthia roretzi in Japan, where it is cultured in the north of Honsyu (Tokioka, 1953), and Pyura chilensis

82

R.

11. MILLAR

in South America (Van Name, 1945). Margalino and de Stefan0 (1960) found that the flesh of Microcosmus sulcutus is almost as digestible as whole egg, and the protein content higher. Such is their abundance in some localities that ascidinns have been considered as a possible source of cellulose, vanadium, protein and other chemicals (Elroi and Komarovsky, 1961 ; Hebant-Joder, 1965), and although the investigations have been confined to warm waters they might encourage a similar approach applied to some of the dense and fast-growing populations encountered in certain temperate areas. The part played by ascidians in the diet of commercial fish, and their occasional use as bait, have been mentioned elsewhere (p. 48).

C . Uptake of harntful substances Since the advent of nuclear weapons and nuclear power stations the presence of radionuclides in the sea and their uptake by marine organisms have received considerable attention. So far as ascidians are concerned the practical importance of the uptake of radioactive materials is the possibility that they will be concentrated in the tissues and passed on to man, either when ascidians are eaten or indirectly through the consumption of commercial fish which themselves feed on the ascidians. According to Bryan (1963) Ciona intestinalis shows a low concentration factor for 13'Cs in all tissues, and Strohal et al. (1969) found factors of 70 and 90 for Phallusia mammillata and Microcosmus sulcatus. go,, is of particular importance as an artificial radionuclide, but factors of only 1 and 4 were obtained by Strohal et al. for P . mammillata and M . sulcatus. These workers found Zn t o be eoncentrated by a factor of 940 in both species, although Ciona intestinalis has a factor of 6 600 (Vinogradov, 1953). Co and Fe are also of interest as pollutants, and 1Microcosmus sulcutus has factors of 1 350 and 40 000 respectively, the corresponding factors for Phallusia mammillata being 400 and 18 000 (Strohal et al., 1969), and for Ciona intestinalis, 400 and 200 respectively. It is evident that there may be some danger, in certain areas of the sea subject to radioactive pollution, of radionuclides passing up the food chain to man. IX. REFERENCES Abbott, D. P. (1951). Boatricliobranchue digonaa, a new molgulid ascidian from Florida. J . Waah. A d . Sci. 41 (9), 302-307. Abbott, D. P. (1953). Asexual rcproduction in the colonial mcidian M e t u ? m carpa taylori Huntsman. Univ. Calif. Piibb 2001.61 ( l ) , 1-47. Abbott, D. P. (1955). Larval structuro and activity in tho aacidinn Melandrocurpa taylori. J . Morph. 97,569-594.

THE BIOLOGY OF

83

ASCIDTANS

Abbdt, D. 1’. (1966). Tlio Asciclicuis. I n “Etivironnicwt of tlio (hiin Tlioinpson region, Ala~ka”. Chapter 30, pp. 839-841. Utiitcd States Atomic Energy Commission. Aldrich, F. A. (1955). A tiow symbiotic reletiorixhip involving hfolgula mutihulleneie (De Kay) etid M y a arenaria L. Notul. Nat. No. 274, 1-3. Allen, F. E. and Wood, E. J. F. (1950). Invcstigations on undcrwator fouling. 11.The biology of fouling in Australia : rcsults of a year’s research. Awl. J . vnar.freahwat. Rea. 1, 92-105. Allen, J. A. (1953). Observations on tho epifauna of tho deep-water muds of the Clyde Sea Aroa, with special reference t o Chlamys aeptemradiata (Miiller). J . Anim. Ecol. 22, 240-260. Ankel, W. E. (1936). Prosobranchia. Tierwelt N. -u. Oslsee 9b. 1-240. Lnbiick-Christie-Lindc, A. (1922). Northern and Arctic Invertebrates in tho collection of tho Swedish Stato Museum (Riksmuseum). VIII. Tunicata. 1. Styelidae end Polyzoidae. K. menaka VetenakAkarE. Handl. 63 (2), 1-62. ~nback-Christic-Litido,A. (1923). Northorn and Arctic Invertebrates in thocollection of tho Swodish State Musoum (Riksmuscum). IX. Tunicata. 2. BotrylM a e : reproductivo organs of Metrocarpa (n. gcn). leachi Savigny and Botryllua schlosaeri Pallas. 63 (9), 1-25. Ilrnbiick-Christie-Linde,A. (1924). A remarkable Pyurid tunicato from Novaya Zemlya. Ark. 2001.16, 1-7. Amback-Christie-Linde, A. (1928). Northern and Arctic Invertcbratcs in the collection of the Swedish State Muscum (Riksmuscum). IX. Tunicata. 3. Molgulidae and Pyuridae 4 (9), 1-101. hbiick-Christie-Linde, A. (1934). Northern and Arctic Invertebratrs in tho collection of tho Swedish State Museum (Riksmuseum). XII. Tunicata. 4. Cionidae, Ascidiidae, Agneaiidae, Rhodoaomatdae 13 (3), 1-91. Kmbiick-Christie-Lindo, A. (1938). Ascidiacea. Further 2001. Reaults Suied. Antarc.!. Exped. 3 (4), 1-54. ~.mbiick-Christic-Linde, A. (1950). Ascidiacea. Further 2001. Result8 Swed. Anturct. Exped. 4 (4), 1-41. Bancroft, P.W. (1903). Variation and fusion of colonies in compound ascidians. Proc. Calif. A d . Sci. Third series, 3 ( 5 ) , 137-186. Barrington, E. J. W. (1965). “ The biology of Hemichordata and Protochordata.” Oliver and Boyd, Edinburgh and London. Barth, L. G. and Barth, L. J. (1966). A study of rogrcssion and budding in Perophora v i d k . J. Morph. 118, 451-459. Beaven, G. F. (1956). Crabs eat sea squirts or Molgula. M d Tidewat. News, 13 (11, 3.

Bell, L. G.E. (1955). Effect of chlorctone on tunicatc cmbryos. Nature, Lond. 175, 1048.

Bellan, G., Molinicr, R. and Picard, J. (1961). Distribution et particularit& des pcuplements benthiques de 1’6tage circalittoral des paragcs do Bonifacio (Corm). Rapp. P . -v. Rdun. Commn int. Explor. scient. Mer MMilerr. 16 (2). 523-527.

Berner, L. (1944). Lo peuplement des coquos do bateaux B Marseillc. Bull. Inst. ochnogr. Monaco. No. 858, 1-44. Berrill, N. J. (1929). Studies in tunicato devclopment. Part I. Gcncral physiology of dovelopment of simple ascidians. Phil. Trans. R . SOC.Ser. B, 218, 37-38.

A.Y .B ,-0

4

84

R. H. MILLAR

Berrill, N. J. (1931). Studies in tunicate development. Part 11. Abbreviation of development in the Molgulidae. Phil. Trans. R. SOC. Ser. B, 219, 281-346. Berrill, N. J. (1932). Ascidians of the Bermudas. Biol. Bull. mar. bid. Lab., Woods Hole 62 (l), 77-88. Berrill, N. J. (193th). Studies in tunicate development. Part 111. Differentid retardation and acceleration. Phil. Trans. R. SOC.Ser. B, 225, 255-326. Berrill, N. J. (1935b). Studies in tunicate development. Part IV. Asexual reproduction. Phil. Trans. R. SOC.Ser. B, 225, 327-379. Berrill, N. J. (1947a). The development and growth of Ciona intestinalis. J . mar. bid. ASS.U . K . 26, 616-625. Berrill, N. J. (1947b). The developmental cycle of Botrylloides. Q. J1 microsc. Boa’, 88, 393-407. Berrill, N. J. (1948a). Budding and the reproductive cycle of Distaplia. Q. JZ microsc. Sci. 89, 253-289. Berrill, N. J. (1948b). Structure, tadpole and bud formation in the ascidian Archidistoma. J . mar. biol. Ass. U . K . 27, 380-388. Berrill, N. J. (1948~).The development, morphology and budding of the ascidian Diazona. J . mar: biol. ASS.U . K . 27, 389-399. Berrill, N. J. (1950). “ The Tunicata with an account of the British species.” Ray Society, London. Berrill, N. J. (1951). Regeneration and budding in tunicates. Biol. Rev. 26, 456-47 5. Berrill, N. J. (1955). “ The Origin of Vertebrates.” Clarendon Press, Oxford. Bielig, H.-J., Jost, E., Pfleger, K., Rummel, W. and Seifen, E. (1961). A d nahme und Verteilung von Vanadin bei der Tunicate Phallusia mamillata Cuvier. (Untersuchungen iiber Hamovanadin, V). Hoppe-Seyler’s 2.physiol. Chem. 325, 122-131. Bonnevie, K. (1896). Ascidae Simplices and Ascidae Compositae from the NorthAtlantic Expedition. Norw. N.-Atlantic Exped.. 1876-78, Zool. 23, 1-16. Bouchard-Madrelle, C. (1967). Influence de l’ablation d’une partie ou de la totalit6 du complexe neural sur le fonctionnement des gonades de Ciom inte8tinalis (Tunicier, AscidiacB). C . r. hebd. Sdanc. Acad. Sci. Paris, 264D, 2055-2058. Bouchet, J.-M. (1962). Btude bionomique d’une haction de chenal du bassin d’Arcachon (chenal du Courbey). Bull. Inst. ocdanogr. Monaco, No. 1252, 1-16. Bourdillon, A. (1950). Note sur le commensalisme des Modiolaria et des Ascidies. Vie Milieu, 1 198-199. Bourne, G. C. (1903). Oligotrema psammites: a new ascidian belonging to the family Molgalidae. Q. J l . Microsc. Sci. 47, 233-272. Bovien, P.(1921). Ascidiee from the Auckland and Campbell Islands. Vidensk. Meddr dansk naturh. Foren. 73, 33-47. Bresciani, J. and Liitzen, J. (1960). Gonophysema gullmarensis (Copepoda parasitice). An anatomical and biological study of an endoparasite living in the ascidian Ascidiella aspersa. I. Anatomy. Cah. Biol. mar. 1, 157-184. Brewin, B. I. (1946). Ascidians in the vicinity of the Portobello Marine Biological Station, Otago Harbour. T r a m . R. Xoc. N . Z . 76, 87-131. Brewin, B. I. (1948). Ascidians of the Hauraki Gulf. Part I. Trans. R. Boo. N . Z . 77, 115-138. Brewin, B. I. (1950a). The ascidians of the sub-antarctic islands of New Zealand. Cape Exped. Ser. Bull. 11, 1-11.

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