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The Velar Ciliature in the Brooded Larva of the Chilean Oyster Ostrea chilensis (Philippi, 1845).

O. R. CHAPARRO [1]

R. J. THOMPSON [2,*]

C. J. EMERSON [3]

Abstract. The Chilean oyster (Ostrea chilensis) broods its offspring almost to the settlement stage (about 8 weeks). Larvae are maintained inside the infrabranchial chamber of the female. Samples from all embryo and larval developmental stages were obtained from mantle cavities of brooding females and analyzed by scanning electron microscopy, with particular attention to the velar structures.

All embryos and the earliest veliger stages of O. chilensis are devoid of cilia. Cilia first appear when shell length reaches 290-300 [micro]m, and the first cilia to grow on the velum form the outer preoral cilia. In larvae 340 [micro]m long, all the ciliary rings on the velum can be distinguished. These are the apical cilia (AC), inner preoral cilia (IPC), outer preoral cilia (OPC), and adoral cilia (AOC). The absence of the apical tuft in both O. chilensis and the closely related species O. edulis represents an adaptation to brooding by the embryos and larvae, but the lack of the postoral cilia (POC) in O. chilensis and the lack of cilia in the embryonic and early veliger stages are associated with an extreme brooding condition in this species.

Introduction

Most bivalve molluscs exhibit external fertilization of the gametes followed by the development of pelagic larvae. In some species, however, there is a totally benthic or brooded larval development, and in other cases a period of brooding is followed by a pelagic phase (Pechenik, 1979, 1986). In brooding species the eggs, embryos, and larvae are retained in the interlamellar spaces of both demibranchs or of the inner or outer demibranchs only; alternatively, they may be confined to brood sacs, marsupia, mucous masses, capsules, or other specialized structures (Ockelmann, 1964; Solis, 1967; Franz, 1973; Mackie et al., 1974; Heard, 1977; Mackie, 1984; Tankersley and Dimock, 1992, 1993; Gallardo, 1993).

Brooding is a characteristic common to all members of the subfamily Ostreinae (Harry, 1985). All species of the genus Ostrea brood their embryos in the infrabranchial chamber (Millar and Hollis, 1963; Galtsoff, 1964; Chanley and Dinamani, 1980; Harry, 1985; Cranfield and Michael, 1989). Brooding in oysters can be very short, as in O. puelchana (3 days, Morriconi and Calvo, 1980; 3 to 9 days, Fernandez Castro and Le Pennec, 1988), or very long, as in O. chilensis (6 to 12 weeks; Toro and Chaparro, 1990). In addition to having the longest period of brooding, the Chilean oyster produces the fewest eggs (3500 to 152,000) of any Ostrea species, with the largest egg diameter (approximately 250 [micro]m), the largest pediveliger at the time of release (approximately 450 [micro]m), and the shortest pelagic phase (minutes to 24 hours) (review by Toro and Chaparro, 1990).

Pelagic larvae possess structures specialized for swimming and feeding, but it is unlikely that brooded larvae have the same requirements, especially if the brooding period is long, as in the Chilean oyster (8 weeks). In many species, brooded larvae do not ingest particles, often because the brooding female provides nutrition through the biochemical reserves in large eggs, as in O. chilensis, or through body fluids or nurse eggs. Strathmann (1978) has described the adaptations of some nonfeeding brooded larvae. In other cases, the female concentrates phytoplankton and other suspended material from the external environment for the use of the larvae, as suggested by Buroker (1985) for Ostrea spp. and by Mackie (1979) for freshwater bivalves (Pisidiidae), and as demonstrated in O. chilensis by Chaparro et al. (1993). The present paper examines the velar ciliature of the larva of O. chilensis, an extreme case in which the larva is brooded for almost the entire developmental period, and compares the ciliature mor phologically with that of the planktotrophic larvae of related species, particularly other ostreids.

Materials and Methods

Samples of oysters (Ostrea chilensis) were obtained at intervals throughout the brooding period (October to January) during 1992, 1993, and 1994 from a natural bank in the Quempillen estuary in the northern part of Chiloe Island (41[degrees]52'S; 73[degrees]46'W), in the south of Chile. On each sampling date, several female oysters were opened and their embryos or larvae removed. In this way, all larval development stages were sampled. Larvae were prepared for scanning electron microscopy (SEM) following Hadfield and Iaea (1989).

Larvae were anesthetized for about 10 min in a [MgCl.sub.2] solution isotonic with seawater, then fixed for 1 h in ice-cold 3% glutaraldehyde in 0.2 M sodium cacodylate buffer, pH 7.4. Fixed samples were rinsed in the buffer solution twice and post-fixed for 1 h in ice-cold 1% [OsO.sub.4] in 0.2 M sodium cacodylate, pH 7.4. The specimens were then rinsed two or three times with buffer solution and then once with distilled water before being dehydrated in a graded series of ethanol (Cragg, 1985).

For SEM, dehydrated specimens were critical-point dried from liquid carbon dioxide in a Polaron E3000 drying apparatus. Dried larvae were attached to aluminum viewing stubs with double-sided tape and then coated with gold in an Edwards S150A sputter-coater. When necessary, larval shells were broken with a fine needle to expose the internal structures (Cragg, 1985, 1989). Coated samples were viewed in a Hitachi S570 scanning electron microscope operated at an accelerating voltage of 20 kV. Micrographs were recorded on Polaroid Type 665 positive/negative film, and stereopairs taken with a 10[degrees] tilt angle difference.

Each brood of larvae was processed separately. Although all larvae from a given brood were at the same developmental stage, as an additional precaution at least 30-50 larvae from each brood were observed by SEM before micrographs were taken, to ensure that the structures observed were common to all of them. Measurements based on SEM are approximate, owing to foreshortening effects related to the depth of field, the tilt angle, and the curvature of the sample.

Early development stages

The earliest development stages are naked, with no cilia (Fig. 1). Only when the embryo reaches the earliest veliger stage, with a shell length of about 290 [micro]m, is the first ciliary growth observed. Cilia appear on the upper part of the velum, and owing to their location and arrangement on the velum, they are presumed to form the future ring of outer preoral cilia (OPC) (Fig. 2a, b). These cilia are about 11-14 [micro]m long. At this stage they are separate, with a tendency to join each other in the middle basal part of the cilia. At the same time, a group of short cilia develops in the mouth region and begins to cover the food groove. These cilia are shorter than those in the putative OPC ring, and are randomly distributed (Fig. 2c).

After 25-30 days of brooding (shell length 315-320 [micro]m), a clear pattern of single or compound cilia has emerged which persists for the remainder of the larval phase. The ciliary belts composing the velum are shown schematically in Figure 3. Larvae exhibit a very well synchronized ciliary growth pattern, with all larvae from the same brood being at the same developmental stage.

Distribution of cilia on the velum

The ciliature of a larva of shell length 400 [micro]m is shown in Figure 4A. A concavity about 70--80 [micro]m in diameter is visible in the most central and apical sector of the velum (Fig. 4B). Located in its base is a group of small cilia, the apical cilia (AC), which are randomly distributed and are not organized into the apical tuft characteristic of planktonic veligers, but lie in the same position. Surrounding this depression is a bare region about 60 [micro]m wide, delimited by a single belt of cilia constituting the inner preoral ciliary (IPC) ring.

Inner preoral cilia

The IPC form a ring of single cilia (Fig. 4C), each one about 15--20 [micro]m long. Outside the PC ring is a naked area, 9--10 [micro]m wide, which is surrounded by a large ring of OPC.

Outer preoral cilia

The OPC form a band, about 10--15 [micro]m wide, of two rows of cirri, or composite cilia (Waller, 1981), which are oriented radially from the center of the velum (Fig. 4D, E). This is the dominant ring in the velum because of its width and the size and complexity of its cirri. Each cirrus is roughly 80 [micro]m long and is composed of 50--100 cilia, which are in contact with each other for almost all their length. The width of the cirrus is about 1 [micro]m, and each one is separated from its neighbor by a nonciliated space of about 1.5-2 [micro]m.

Adoral cilia

The remainder of the velum (adoral area), from the OPC to the dorsal margin of the shell, is covered by a carpet of individual, short cilia (8-12 [micro]m) known as the adoral cilia (AOC), which also cover the crest and floor of the food groove (the sides are not visible) and the external part of the mouth. No differentiation in the form of the AOC is apparent, although in some areas there are a few cilia of different length, and in the floor of the food groove the cilia are shorter than the rest of the AOC (Fig. 4F, G). Short cilia can also be seen on the base of the external part of the mouth (Fig. 4H). There is no clearly identifiable postoral ciliary band of the type identified in larvae of Ostrea edulis by Waller (1981). Below the food groove and close to the mouth lie several lobes, which resemble the tumescent cells identified by Waller (1981) in O. edulis.

Discussion

The inclusion of a pelagic larva in the life cycle of most marine bivalve molluscs is accompanied by anatomical adaptations, especially those associated with the velum, and is characterized by rapid development to the prodissoconch stage. These features allow the larva to survive for long periods in the water column, and the velum is an adaptation for planktonic life (Cragg, 1989). Many papers on the early development of bivalves have shown the presence of cilia on some parts of the embryo or larva, or covering the entire surface (Allen, 1961; Carriker, 1961; Bayne, 1976; Amor, 1981; Fitt et al., 1984; Gustafson and Lutz, 1991). In most cases the cilia appear at the earliest stages of embryonic development (Gallardo, 1989). The few studies that have been undertaken on brooded embryos or larvae have shown that cilia first appear at later stages of development: Ostrea lurida, trochophore stage (Hopkins, 1936); O. edulis, trochophore stage (Horst 1883--1884, in Waller, 1981). However, the present study shows th at in the Chilean oyster all embryonic stages, together with the trochophore and early veliger, are totally devoid of cilia. This is one of the few cases known in which cilia are totally absent at such a late stage of development in a bivalve. From the illustrations in Beauchamp (1986), it can be inferred that advanced, shelled veligers of the brooding clam Lasaea subviridis are also naked. This species exhibits direct development, and no pelagic phase has been detected (Beauchamp, 1986), an observation that would explain the absence of cilia during the larval stages. Oldfield (1964) demonstrated that the area normally occupied by the ciliated velum is replaced in L. rubra by an unciliated structure she termed the "cephalic mass," implying a specialization for brooding more extreme than is seen in the Chilean oyster. Thus loss or modification of the velar ciliature represents one of the most important and visible adaptations for brooding in a bivalve mollusc.

Cilia begin to develop when the shell length of the Chilean oyster larva is about 290 [micro]m. By the time the larva reaches about 300 [mirco]m, the cilia have developed completely and remain throughout the rest of the larval phase. The present study supports the contention of Winter et al. (1984) and Toro and Chaparro (1990) that the brooding period in O. chilensis is the longest of any Ostrea species for which information is available. There is little necessity for swimming because the larva spends only a few hours in the water column and is competent to settle immediately after being released (Solis, 1973; Cranfield, 1979). According to Millar and Hollis (1963), the shortened pelagic phase in the larva of O. chilensis is an adaptation for survival in a habitat characterized by strong currents.

The absence of cilia during much of larval life may be considered an adaptation to brooding. The encapsulated embryos of many marine invertebrate species lacking pelagic larvae bear structures that appear to be functionally significant only in free-swimming larval stages. In some encapsulated embryos, those cilia normally associated with swimming in pelagic larvae serve to rotate the embryo within its capsule, presumably aiding the larva in the ingestion of fluid albumen and in gas exchange (Fretter and Graham, 1962). Hadfield and Iaea (1989) reported an extreme case in which encapsulated larvae of the gastropod Petaloconchus montereyensis showed an absence or reduction of some velar structures that are very important in closely related species with a pelagic larva. On the other hand, in another encapsulated gastropod (Turritella communis), cilia develop in the very earliest embryonic stages, even though these cilia are not required for swimming (Kennedy and Keegan, 1992). The velar lobes of many encapsulate d gastropod veligers are known to participate in the breakdown and ingestion of nurse eggs (Fioroni, 1966), and in others the velum is greatly modified for aiding in the ingestion and perhaps in the breakdown of external nurse yolk (Hadfield and Iaea, 1989).

In Chilean oyster veligers, ciliary development is well-synchronized within a brood. Immediately after the cilia have completely developed, the larvae start to ingest particles. Thus the cilia are required for feeding more than for swimming, although data from endoscopy show that the larvae are not completely immobile, but exhibit a specific circulation pattern inside the mantle cavity of the female (Chaparro et al., 1993). The larval circulation is driven by water currents produced by the female rather than by the larval velum. Furthermore, although the velar cilia are very active when the female has stopped pumping, the larvae move very little, and it is not clear whether they are capable of swimming at this stage.

The composition of the ciliary bands on the velum is similar, but not identical, to that of the closely related species Ostrea edulis, described by Waller (1981). Both these species have a short apical ciliary (AC) ring and no apical tuft, unlike the pelagic larvae of many other bivalves (Allen, 1961; Carriker, 1961; Ansell, 1962; Gruffydd and Beaumont, 1972; Bayne, 1976; Boyle and Turner, 1976; Chanley and Chanley, 1980; Amor, 1981). The reduced development of the AC ring in the Chilean oyster larva may be explained by a reduced sensory function during the brooding phase, and also by the short larval pelagic phase. A sensory function has been proposed for the AC because they are very short, appear to be unsuitable for locomotion and food-gathering, and are underlain by the cerebral ganglion (Hickman and Gruffydd, 1971). According to Hodgson and Burke (1988), the apical tuft remains in the larva of Chlamys hastata until the earliest veliger stage, but in the Chilean oyster larva the AC never develop into a t uft.

A ring composed of single cilia (inner preoral cilia, IPC) has been identified between the AC and the OPC in the Chilean oyster veliger. A similar structure has also been described by Waller (1981) for O. edulis, by Hodgson and Burke (1988) for Chlamys hastata, and by Elston (1980) for Crassostrea virginica. No clear function has been identified for this band (Waller, 1981). Although the IPC ring is situated in such a position that it could entrain food particles, it lies far from the mouth and the AOC and is separated from the nearest ciliated pathway to the mouth by a nonciliated zone. Waller (1981) therefore concluded that the IPC probably do not play a role in food capture and are more likely to function as an upcurrent tactile receptor.

The outer preoral cilia (OPC) form the most prominent ciliated ring in the velum of O. chilensis, as they do in several other bivalve larvae including O. edulis (Waller, 1981), Chlamys hastata (Hodgson and Burke, 1988), and Crassostrea virginica (Elston, 1980). In some species the ring is composed of a single row of cilia in the early larval stages (e.g., the D-stage veliger of C. hastata), but more developed larvae of C. hastata have two rows (Hodgson and Burke, 1988), as do all stages of the veliger in O. edulis (Waller, 1981). The OPC ring is believed to function in locomotion and feeding (Strathmann et al., 1972; Strathmann and Leise, 1979; Wailer, 1981), and it is normally the most prominent ciliated structure on the velum (Waller, 1981). Furthermore, Bayne (1971) showed that long cilia, presumably the OPC, on the velum of the pediveliger of the mussel Mytilus edulis provide the main force for swimming and also create the feeding currents.

In O. chilensis, a wide band of short adoral cilia (AOC) covers an area of the velum limited in the uppermost part by the OPC ring and in the lowest part by the shell. In the middle of this band lies the food groove. The ciliature is uniform throughout the band, although the cilia in the floor of the food groove are a little shorter. The cilia of the upper and lower regions of the AOC band are in close contact with the groove. These cilia are probably responsible for transferring particles caught by the other ciliary bands to the food groove. In many specimens of O. chilensis veligers, pieces of mucous strings or globules could be distinguished in the food groove, presumably moving towards the mouth. It may be significant that some descriptions of feeding in lamelli-branch veligers (e.g., Yonge, 1926) refer to a mucous string carrying food particles to the mouth, since the efficiency of a system that lacks postoral cilia may be improved by the presence of mucus (Bayne, 1976). Waller (1981) indicated that the AOC are in close contact with the compound cilia of the OPC when the latter are at the bottom of their effective beat; this is probably the mechanism by which the OPC transfer the entrained particles to the AOC band to be moved to the mouth.

The velar bands are almost identical in O. chilensis and O. edulis, the principal difference being that in the latter the postoral cilia (POC) represent a single cirral ring located at the base of the velum, in contact with the shell edge (Erdmann, 1935; Waller, 1981), whereas the POC were not visible in this study on the Chilean oyster and are probably not present. On a cautionary note, however, Strathmann et al. (1972) pointed out that some authors have not mentioned the POC when describing mollusc larvae that feed and have a well-developed preoral band. These authors suggested that in many cases this may have been an oversight, or a result of confusing the shorter cilia of the postoral band with the cilia of the food groove. However, owing to the central position of the food groove on the velum of the Chilean oyster larva, it would be easy to distinguish between food groove cilia and POC, were the latter present.

Waller (1981) associated the POC band in O. edulis with both swimming and particle capture. The latter has been described by Strathmann et al. (1972), who showed that many marine invertebrate larvae can continue swimming without feeding, presumably by stopping the beat of the POC. This band appears to be very important in filter-feeding, especially in the larvae of taxa which employ the opposing band mechanism proposed by Strathmann et al. (1972) and Strathmann (1978)--bivalves, annelids, echiurids, sipunculids, and entoprocts. In this system both preoral and postoral rings are essential for filter-feeding by the larva (Strathmann et al., 1972), and provide an efficient mechanism to capture particles. In this context, the POC ring identified by Waller (1981) in O. edulis may serve to catch particles passing the tips of the cirri of the preoral band, and may also play a more direct role in particle retention and rejection (Strathmann et al., 1972).

The food collected by the cirri is moved to the adoral ring and then to the mouth, where oral compound cilia are present. These may function in selecting or rejecting food particles before they enter the mouth (Hodgson and Burke, 1988).

Whatever the characteristics of the POC band, Hodgson and Burke (1988) have suggested that it may play a role in particle capture, although Strathmann (1987) has shown that the larvae of other invertebrate taxa catch particles by using only one cirral ring. In the Chilean oyster, the particle-catching mechanism was not identified in the present study, but the apparent absence of the second (POC) ring may imply that only one ciliary band is involved, probably because the brooded larva does not need to concentrate particles since the brooding female is performing this function. Furthermore, endoscopic observations have shown the larval velum to be in close contact with mucous strings from the food grooves on the gills of the female (Chaparro et al., 1993). The resolution of the endoscope was insufficient to determine whether larvae were ingesting the mucous string, but the presence of larvae in the food groove, their orientation, and their behavior suggested that this was probable; furthermore, marker particle s introduced into the ambient seawater were later observed in the gut of the larva. Thus the absence of the POC may represent another adaptation of the Chilean oyster larva for brooding. Hodgson and Burke (1988) identified secretory cells among the velar cilia of the pectinid Chlamys hastata, but such cells have not been described in other bivalve larvae, although several authors have suggested or assumed that mucus is involved in the collection of particles (Yonge, 1926; Erdmann, 1935; Strathmann et al., 1972; Waller, 1981). Hodgson and Burke (1988) suggested that mucus produced by the velum serves principally to bind entrained particles into a string, which travels along the food groove, thereby ensuring the retention of the particles. Pieces of mucus were detected in the food groove of the larva of the Chilean oyster during the present study. The origin of this material could not be clearly ascertained, but two possibilities may be suggested: first, that pieces of the mucous string are taken from the food grooves of the female's gill; and second, that mucus is produced by the larva, as described by Hodgson and Burke (1988) in C. hastata.

The absence of the POC band is consistent with the short pelagic phase of the pediveliger in O. chilensis because there is no requirement to filter food particles from the water column and no necessity to swim for a long time as a dispersive strategy, since the population is confined to its own estuary. The pediveliger is competent to settle on the first hard substrate that it encounters after release. Typical settlement distances are variously given as 10 cm (Padilla et al., 1969) and 40 cm (Solis, 1973) from the female parent.

Morphological adaptations of marine invertebrate larvae have been described by Strathmann (1978). The larvae of some oligomeric taxa (e.g., Bryozoa, Phoronida, Brachiopoda, Hemichordata) have a single band system and have eliminated the planktotrophic stage. These taxa have lost or modified some larval structures, such as the band of cilia that captures particles. The gut is often incomplete, and the mouth, anus, or both may be absent. In some mollusc species with nonfeeding larvae, the metatroch and food groove have been lost; in contrast, other gastropod larvae, which are also not filter-feeders, retain the opposing band system, even when the larvae are not planktotrophic (Strath-mann, 1978). It is clear that many species have modified some larval structures, allowing the larva to adapt more completely to the environment in which it is developing. The Chilean oyster is one such example: the morphological modifications of the velum are essential for the adaptation by the species to brooding the larva inside the mantle cavity of the female--a very different environment from that experienced by a planktonic larva. Furthermore, in O. chilensis and O. lutaria, which have the longest incubation periods of all the ostreids, the larval shells differ structurally from those of other oysters (Chanley and Dinamani, 1980). In particular, the shells of the two larvae are equivalve and edentulous, but it is not clear whether these features represent the ancestral condition or are adaptations to brooding (Chanley and Dinamani, 1980).

Acknowledgments

A large part of the field research was carried out in the Estacion Experimental de Quempillen, Ancud, Chile, and in the Instituto de Biologia Marina de la Universidad Austral de Chile, to whose staff we extend our appreciation. Financial help came from operating grants to ORC by the Fondo Nacional de Investigacion Cientifica y Tecnologica-Chile (Fondecyt 1930364 and 1980984), by the International Foundation for Sciences-Sweden (IFS A/0846), and by the Direccion de Investigacion of the Universidad Austral de Chile, and from a research grant to RJT from the Natural Sciences and Engineering Research Council-Canada (NSERC). ORC's stay in Canada was made possible by fellowships from the International Development Research Centre-Canada (IDRC) and NSERC (through a Networks of Centres of Excellence programme, the Ocean Production Enhancement Network). We also thank the Canadian International Development Agency (CIDA) for support during the preparation of the manuscript.

(1.) Instituto de Biologia Marina, Universidad Austral de Chile, Casilla 567, Valdivia, Chile

(2.) Ocean Sciences Centre, Memorial University of Newfoundland, St. John's, Newfoundland, Canada A1C 5S7.

(3.) Biology Department, Memorial University of Newfoundland, St. John's, Newfoundland, Canada A1B 3X9

(*.) To whom correspondence should be addressed. E-mail: thompson@ morgan.ucs.mun.ca

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Author:CHAPARRO, O. R.; THOMPSON, R. J.; EMERSON, C. J.
Publication:The Biological Bulletin
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Date:Aug 1, 1999
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