Doliolida
Introduction

This group was mentioned for the first time in 1835, when Quoy and Gaimard referred to the genus Doliolum in their report on the "Astrolabe" expedition to the tropical Pacific. The study of these tunicates intensified by the second half of the last century, when scientists started to comprehend that these animals had extraordinary life cycles (see Neumann, 1906; Garstang, 1933; Braconnot, 1970).

Doliolids are characterized by a typical alternation between asexual (oozooids) and sexual (blastozooids) generations, which is characteristic of the class Thaliacea. However, the blastozooids present several different successive forms that make their life cycle especially complex (e.g. Brien, 1948; Braconnot, 1970, 1971a; Godeaux, 1957, 1990).

life cycle Doliolida

All the known life cycles have been observed in species of the family Doliolidae, in which fertilized eggs develop free in the pelagic habitat into larvae that are usually tailed and swimming (except in Dolioletta gegenbauri, dol-larva, where larvae lack a tail and are non-swimming, Braconnot, 1968, 1970). Larvae undergo metamorphosis, producing barrel-shaped oozooids with branchial and atrial apertures in a terminal position (dol-young oozooid). The oozooid has a ventral stolon which generates buds. These primary buds migrate over the side of the body of the oozooid to attach on a postero-dorsal appendix. Gradually, by losing most of its viscera (viz. the branchial wall, endostyle, and gut degenerate), each oozooid transforms into another stage, called nurse (dol-nurse). The muscular bands remain narrow (Doliolina intermedia) or become wide but separate from one another (Dolioletta gegenbauri -dol-nurse and Doliolina muelleri -Doliolina muelleri 2), or fused into a continuous sheath (Doliolum denticulatum -Doliolum denticulatum 3 and D. nationalis).

In Dolioletta gegenbauri, the buds attach to the dorsal appendix, arranged into three rows (dol-nurse, dol-gastrozooids). The buds of the external rows produce a first generation of blastozooids, called gastrozooids, which remain attached to the appendix and are in charge of collecting food for the colony by means of filter feeding. The buds of the central row, on the other hand, develop into another type of barrel-shaped zooids, called phorozooids (dol-phorozooid), which serve as dispersal vehicles for the sexually reproducing gonozooids (dol-gonozooid). These latter types of zooids develop from buds fixed on a ventral process of each phorozooid, where they remain attached when the phorozooids detach from the colony.

Doliolina muelleri does not seem to form long-lasting colonies on the dorsal appendix of the nurse. Instead, each phorozooid detaches very soon, leaving its place to the next one (Braconnot, 1970).

In all cases, mature gonozooids detach from the phorozooids to feed and swim independently. Sexually mature gonozooids are protogynous hermaphrodites. In some species, such as Doliolum denticulatum and D. nationalis, fertilization seems to take place in the ovary itself; whereas in other species, such as Dolioletta gegenbauri (e.g. Braconnot, 1974; Godeaux, 1990), it occurs after shedding. Self fertilization is possible in Doliolum (Braconnot, 1974).

A different life cycle, with phorozooids forming other phorozooids in their ventral appendix, has been observed in the species Doliolum nationalis from the Mediterranean Sea. Gonophorozooids, presenting gonads and a ventral peduncle with buds at the same time, have also been found (Braconnot, 1967, 1971a, 1974, 1977; Braconnot and Casanova, 1967). And De Decker (1973) reported an absence of gonozooids throughout a two-year period of observations off the southwestern coast of Africa. Similar observations have been made by Tavares (1967) off Brazil, and by Godeaux (1973) in the Indian Ocean.

Doliolids can feed on particles of wide-ranging size, from bacteria to flagellates, diatoms, and other phytoplankton species (e.g. Braconnot, 1971b). They collect food particles by means of a fine mucous filter, secreted by the endostyle. This net with entangled particles is ingested. Water is driven through this filter by ciliary action, instead of the muscular peristalsis used by salps (Fedele, 1921). Accordingly, filtering and swimming functions are separate in doliolids, which can remain almost stationary while feeding (Alldredge and Madin, 1982). Little is known about the mesh-size of the pharyngeal filter of the doliolids, and data on minimum particle sizes efficiently retained not only differ but are somewhat contradictory. Deibel (1985a) observed that Dolioletta gegenbauri fed on the <35 µm fraction, but he found no evidence of grazing on large diatoms and dinoflagellates. Deibel and Paffenhöfer (1988) studied the feeding mechanism of Doliolum nationalis by means of high-speed cinematography. Using two phytoplankton species as food (4.5 and 12 µm in diameter), these authors found that the smallest particles were not efficiently retained, but the animals could ingest large Ceratium spp. The motion pictures suggest that this species has unique adaptations for the manipulation of the particles, enabling it to inhabit the particle-rich waters of the continental shelf. Crocker et al. (1991) studied the feeding rates of D. gegenbauri on natural assemblages of diatoms (>100 µm in diameter) and bacteria (0.2-5.0 µm in diameter), concluding that both types of particles were collected with equal efficiency. Bone et al. (1997) re-examined feeding in doliolids, but they failed to estimate mesh dimensions. They observed wide variations in filtration rates.

Swarms of doliolids, covering hundreds of square kilometres, have been recorded frequently (e.g. Berner, 1967; De Decker, 1973; Atkinson et al., 1978; Deibel, 1985a; Paffenhöfer and Lee, 1987). This is a consequence of asexual reproduction that permits rapid multiplication and explosive population increases, probably related to favorable environmental conditions (e.g. Braconnot, 1963; Deibel, 1982a). If we add to this reproductive pattern the high feeding rates of these animals (e.g. Deibel, 1982b; Crocker et al., 1991), the result can be depletion of a wide range of particle sizes from large areas of the sea (e.g. Deibel, 1985a; Deibel and Paffenhöfer, 1988; Paffenhöfer et al., 1995).

Concerning the flows of matter and energy to other trophic levels, little is known about the predators of the doliolids, since they can hardly be recognized in the stomach contents of other animals (Alldredge and Madin, 1982). Studies based on the fecal pellets of Dolioletta gegenbauri, suggest that the contribution of doliolids to the vertical flux apparently depends on their diet. It has been demonstrated that the feces derived from natural food do not sink or sink very slowly, in contrast with the feces produced by animals fed on cultured diatoms or other selected algae representing bloom conditions (e.g. Pomeroy and Deibel, 1980; Bruland and Silver, 1981; Deibel, 1990; Fortier et al., 1994).