JOURNAL OF MORPHOLOGY 238:93-107 (1998)

Giant Pelagic Larvae of (Polychaeta, Annelida)

ALEXANDER B. TZETLIN* Department of Invertebrate Zoology, Biological Faculty, Moscow State University, Moscow, Russia

ABSTRACT The microscopic anatomy of giant pelagic larvae of Phyllodoci- dae was studied using routine histological, SEM, and TEM techniques. The larvae consist of two distinct regions: a large spherical trochophore measuring up to 2 mm in diameter and a posterior, long (up to 10 mm length), narrow rudiment of the adult body with up to 120 segments. The larvae have an unusual mixture of larval and adult features, including a very complex, well- developed brain and ganglia in the ventral nerve cord, and only a single pair of protonephridia located in the hyposphere of the trochophore. A muscular pharynx is not developed. The intestinal wall, especially in the trochophore region, consists of endodermal cells containing considerable nutritive mate- rial in the form of yolk-like globular inclusions. The digestive tract of all larvae was empty. The position of the frontal sensory organ and the pro- totroch, the structure of the parapodia and setae, and the three pairs of tentacular cirri dictate inclusion of the larvae in the family Phyllodocidae. The relatively enormous size and unusual pattern of development of the adult body may be adaptations for a long pelagic life and rapid settlement of the , which inhabits slopes of islands and underwater mounts located far apart. J. Morphol. 238:93-107, 1998. o 1998 Wiley-Liss, Inc. KEY WORDS: pelagic larvae; Phyllodocidae; Polychaeta, Annelida

The Phyllodocidae is a large family of lin, '86; Bartolomaeus, '87, '89, '94; Smith including both benthic and pe- and Ruppert, '88; Smith, '92), but only a few lagic forms, traditionally considered as a species have been investigated: group that has retained some archaic charac- mucosa, P maculata, P fragilis, viri- ters (Ushakov, '72; Pleijel, '91; Eibye-Jacob- dis, Eteone longa, and finally Lopadorhyn- sen, '93). Since Kleinenberg (1886) first de- chus spp. There are no or only poor, fragmen- scribed metamorphosis of the phyllodocid tary data on the larval morphology and Lopadorhynchus, the development and meta- development of most of the 20 or so genera morphosis of Phyllodocidae have been under and more than 200 species of the family. intensive investigation, and these data have Here, we describe some aberrant giant been discussed in the scope of evolutionary larvae from the plankton samples of the morphology of invertebrates: the origin of Soviet expedition vessels Academic adult nervous system in Trgchozoa (see Petrovsky, Professor Vodyanitsky and Odys- Meyer, 1898;Beklemishev, '64; Akesson, '67), sey, collected during 1983-1985. All of the larval and postlarval metamerism (see Iva- larvae were found in the northwestern part nov, '28; Sveshnikov, '78), evolutionary rela- of the Indian Ocean from the Seychelles to tionships of the pericalimma (endolarva) the Gulf of Aden. The material had been larva and true trochophore (see Minichev and Starobogatov, '72; Salvini-Plawen, '80, '88), and the origin of larval and adult ne- phridia in (Bartolomaeus, '94). A Contract grant sponsor: Russian State Program in Biodiver- sity; Contract grant number: N2-1-93; Contract grant sponsor: number of detailed studies in morphology, Russian Fund for Basic Researches; Contract grant number: N development, and ultrastructure of pbhyllodo- 95-04-12737. cid larvae have been published (e.g., Akesson, *Correspondence to: Alexander B. Tzetlin, Dept. of Inverte- brate Zoology, Biological Faculty, Moscow State University, Mos- '67; Lebsky, '70, '74; Blake, '75; Cazaux, '75, cow 119899, Russia. '85; Ospovat, '78; Lacalli, '81, '86, '88; Usha- E-mail:[email protected] (home) kova and Evdonin, '85; Zavarzina and Tzet- [email protected] (office)

o 1998 WILEY-LISS, INC 94 A.B. 1'ZETLIN kept in a 4% formaldehyde solution since its RESULTS collection more than 10 years ago. Preserva- Although the material was collected at tion of the tissues is thus not perfect but different times and localities, all of the lar- sufficient to provide data on larval struc- vae were similar, allowing a general descrip- tures. tion of their morphology. The numerous studies of phyllodocid mor- phology (cited above) make it possible to External morphology supplement our results with up-to-date infor- In overall appearance the larvae consisted mation on this subject. of a large trochophore body bearing a rudi- ment of adult trunk on its vegetative pole. MATERIALS AND METHODS The trunk rudiment comprised 100 or more About 20 specimens of unidentified aber- setigerous segments and a pygidium (Fig. 1; rant larvae were found in the samples col- see also Fig. 4A). lected by Dgedy net and pleuston trawl dur- Dochophore region. The trochophore re- ing the 1983-1984 voyages of the Russian gion is spherical, ranging in diameter from research vessels Academic Petrovsky, Profes- 1.0 - 1.5 mm. Its episphere bears a ciliated sor Vodyanitsky, and Odyssey. All larvae were sensory organ consisting of a transverse strip collected in the northeast Indian Ocean from of cilia on the frontal surface. Two ocelli the Seychelles to the Gulf of Aden (Table 1). flank it. The highly developed prototroch The material was fixed in total together with consists of densely spased cilia up to 66 pm the whole planctonic sample in a solution of in length. The mouth lies just posterior to 4% formaldehyde in sea water. It remained the prototroch and is surrounded with a in the solution for 10 years. Larval speci- ciliary field (Fig. 1).No neurotroch is seen. mens selected for histological and TEM stud- The lower hyposphere forms a collar that ies were postfixed in 1% osmium tetroxide, covers the first segments of the rudimentary dehydrated in a series of alcohol and acetone adult trunk. dilutions, and embedded in Epon. Semithin Rudiment of adult trunk. The length of sections (two sagittal and two transversal the rudiment is correlated with the number series) were made from larvae N 1- 4, (from of setigerous segments present and, in differ- Seychelles, 04031r18S, 55O13'5 E, depth 0-10 ent specimens, segments ranged from 33- m, 19 Dec., 1983, RN Academic Petrovsky, 120. The maximum length observed in our voyage N 14), with glass knifes on a Dupont specimens was 12 mm. Setigerous segments Ultracut microtome and stained in 1% tolu- each bear uniramous parapodia, each idine blue. Ultrathin sections for TEM obser- equipped with an aciculum and six com- vations were cut on an LKB-3 Ultracut mi- pound heterogomph setae, as well as dorsal crotome with diamond knives, stained in leaf-shaped and ventral parapodla1 cirri (Fig. lead citrate and uranyl acetate, and then 2A,D). The setal shaft exhibits numerous examined with a JEM-100b microscope. long acuminate teeth (see Fig. 5B).

TABLE 1. Material examined Depth Number RN, voyage Data Latitude Longitude Type of net (meter) of spec. Comments Academic Petrousky, vo. N 14 04.11.1983 12"05,5'N 45"401E Pleiston trawl 0 4 Gulf ofAden Academic Petrousky, vo. N 14 23, 11, 1983 11°44,5'N 45"10,5'E Djedi net 10-0 1 Gulf ofAden Academic Petrousky, vo. N 14 23,11, 1983 11°44,5'N 45"10,5'E Djedi net 500-100 4 Gulf ofAden Academic Petrousky, vo. N 14 24, 11, 1983 11°45,7'N 45"55'E Pleiston trawl 0 4 Gulf ofAden Academic Petrousky, Sevchelles (Silhou-

vo. N 14 19,12, 1983 04"31118S 55"13'5E Djedi net. 10-0 5 ette) ' Academic Petrovsky, Seychelles (Silhou- vo. N 14 19,12, 1983 04"31r18S 55"13'5 E Djedi net. 50-25 1 ette) Prof. Vodyanitsky, Underwater moun- vo. N 16 1.05, 1984 0°26,3'N 56"00fE Djedi net. 50 1 tain "Equator" Underwater moun- Odyssey, vo. N 33 30,5, 1984 1Oo12,00'N 56"04'E Djedi net. 100-0 1 tain "Error" GIANT LARVAE OF PHYLLODOCIDAE

fro

Fig. 1. Giant larva of Phyllodocidae g. sp. with 36 setigerous segments. Lateral view. Col, collar; te, tentacular cirri; e, eye; fro, frontal organ, mo, mouth. Scale=500 pm. A.B. TZETLIN

Fig. 2. Giant larva of Phyllodocidae g. sp. Frag- rudiment with rudiments of anal cirri, 90 setigerous ments. A: Middle region of the trunk rudiment, dorsal segments. D: Parapodium of the trunk rudiment. Scales: view. B: Posterior region of the trunk rudiment, 35 A=350 pm, B= 160 pm, C=400 pm. setigerous segments. C: Posterior region of the trunk

Aciculae approach 132 pm in length and by the throchophoral collar, bear four pairs 3.5 pm in thickness. The proximal setal re- of tentacular cirri in a pattern of 1-2-1. gion up to articulation is about 130 pm long. Pygidial structure varies with the number of The first three segments, partially covered setigerous segments. Specimens with 70- GIANT LARVAE OF 100 segments bear two small pygidial cirri, vacuoles are only half the diameter (100 pm whereas those with 35-55 segments have on average) of those present in trochophore- only two small papillae at the pygidial end region intestinal cells. The vacuoles gradu- (Fig. 2B,C). ally decrease in number and size from trocho- phore to pygidium. Internal morphology The intestinal lumen passing through the midpart of the segments narrows to a diam- Epithelium and cuticle. A simple tall eter of 6.6 pm. The rudiment intestinal epi- epithelium delimiting the trochophore re- thelium generally exhibits a few short sur- gion is overlain by a larval cuticle in which face microvilli, although intestinal cells in diffuse collagen fibers make up an amor- posterior segments to the pygidium and the phous matrix penetrated with numerous epi- meristematic zone lack microvilli. Moreover, thelial microvilli. Cuticle thickness in the epithelial cells in this distal region of the trochophore region is -200 nm. The epithe- intestine project freely into the lumen and lium varies in height from 37 urn on the do not contact each other. No specimens frontal side to 43 pm on the side of trocho- examined contained food remains in their phore, opposite the mouth. The epithelium intestinal lumen. of the episphere and posterior hyposphere is rich in glandular cells that contain large Nervous system. The nervous system oblong cisternae filled with secretory prod- consists of a well-developed brain, circum- uct. (Figs. 3,6A, B, D). esophageal connectives, and a ventral nerve cord. The brain, subepithelial in the larval The adult trunk rudiment is covered by a episphere, consists of massive frontal lobes thin epithelium -3 pm in height. The overly- that contain neuropil, distinctly divided into ing cuticle, 0.4 pm thick, is of the "adult" frontal and posterior areas (Figs. 3, 6B). type, exhibiting several mutually orthogo- Optic lobes (optic ganglion), which are poste- nal layers of collagen fibers (Fig. 7). rior to the frontal lobes, contact the eyes Digestive tract. A mouth surrounded by directly. Circumesophageal connectives origi- a ciliated field opens into the larval intestine nate in the brain, extend two roots around . The intestine exhibits a wall consisting of the endodermal mass, and join in the ven- tall, ciliated cells, apparently lacking micro- tral part of the trunk rudiment, in the region villi, and containing yolk-like reserve vacu- covered by the collar. Posteriorly the circum- oles averaging 22 pm in diameter. The intes- esophageal connectives exhibit two pairs of tinal lumen consists of a narrow space segmental trunk ganglia. A third pair, lo- between these cells. A mass of endoderm cated ventrally on the third setigerous seg- almost completely occupies the internal cav- ment, comprises the first ganglionic pair of ity of the trochophore region ( Figs. 3,8). the well-developed, extensively ganglion- A rudiment of muscular axial proboscis ated ventral nerve cord (Fig. 5C). Each gan- lies in the episphere, forming a compact glion of the ventral nerve cord contains - 180- structure dorsal to the endodermal mass 200 neurons, whereas interganglionic (Figs. 3, 6C). Its lumen is covered with the regions of the cord lack neuron cell bodies "larval type" cuticle. Apoorly developed basal (Figs. 3,5C, D). membrane surrounds the rudiment and is lFunk rudiment. The body wall of the partly covered by cytoplasmic extensions of trunk rudiment is composed of epidermis mesodermal cells. and a longitudinal muscle layer consisting of In the hyposphere, the lower part the four bands, ventral and dorso-lateral pairs spherical mass of trochophoral endodermal (Figs.4, 7). Longitudinal myocytes are ar- cells becomes the intestine of the rudimen- ranged into a monolayer with their narrow tary adult trunk. The intestinal lumen is surfaces resting on the basal lamina and quite narrow here (Figs. 3,5B). At the termi- their nuclei located in noncontractile exten- nation of the pygidium the ectodermal anus sions (Fig. 7). establishes a complete intestinal tube (Figs. Additionally, parapodial muscle complexes 2,3,5D, E). and bundles of oblique muscle are present in Intestinal cells of the rudimentary adult each segment of the trunk rudiment. trunk are also filled with vacuoles contain- Larval mesenchyme consists of cells whose ing yolk-like reserve materials, but here, the meandering extensions turn around the in- A.B. TZETLIN

/ i dmsn Y~V lint

Fig. 3. Giant larva of Phyllodocidae g. sp. Sagittal lmc, longitudinal muscle cell; me, mesoderm; mo, mouth; section. Part of the trochophore endodermis is everted ne, neuropil; pnf, protonephridium; pr, prototroch; rpr, from the mouth. Br, brain; col, collar; dmsn, dorsal proboscis rudiment; sgn, segmental ganglia; vnc, ven- mesenterium; dsp, septum; ep, epidermal epithelium; tral nerve cord; ylv, yolk-like vacuole. Scale=700 pm. fro, frontal organ; glc, gland cell; lint, intestinal lumen; GIANT LARVAE OF PHYLLODOCIDAE

Imc lint dbv me

int

vbv

omc

Imc / nu vnc

Fig. 4. Larva of Phyllodocidae g. sp. Transverse sec- tinal lumen; lmc, longitudinal muscle cell; mpc, muscle tion through middle region of the trunk rudiment. of parapodial complex; me, mesoderm; nu, nucleus; omc, Slightly schematic, after TEM reconstruction. Co, body oblique muscle; vbv, ventral blood vessel: vnc , ventral cavity; dbv, dorsal blood vessel; int, intestine; lint, intes- nerve cord; ylv, yolk-like vacuole. Scale = 50 pm. 100 A.B. TZETLIN

Fig. 5. Lama of Phyllodocidae g. sp. A: General view. sagittal section, midregion of the trunk rudiment, semi- Trochophore entodermal intestine is partially everted thin section. E: Detail of the same section, intestine and from the mouth. SEM. B: Compound setae (parapodia of septa. Col, collar; dsp, septum; int, intestine; lint, intes- the midregion of the trunk rudiment). SEM. C: Detail of tinal lumen; sgn, segmental ganglion; ylv, yolk-like vacu- parasagittal section, hyposphere and anterior region of ole. Scales: A = 400pm, B = 8 pm, C,D = 94 pm, E = the trunk rudiment, semithin section. D: Detail of para- 24 pm. GIANT LARVAE OF PHYLLODOCIDAE 101

Fig. 6. Larva of Phyllodocidae g. sp. Details of the ment, D: Gland cells in the epidermis of the trochophore, sagittal section through trochophore region. k. Pro- semithin section. Ep, epidermal epithelium; glc, gland totroch and mouth with entodermal intestine partially cell; me, mesoderm; ne, neuropil; pr, prototroch. everted from the mouth. B: Brain. C: Proboscis rudi- Scale = 50 pm. testine, muscular proboscis rudiment, and formed by myocytes are only developed ven- the brain, passing through the intercellular trally and the coelomic space above the intes- spaces of the larval body (Figs. 8,9 ). Inter- tine remains open over the length of the segmental septa of the trunk rudiment, entire body. A.B. TZETLIN nce

Fig. 7. Lama of Phyllodocidae g. sp. Fragment of the nal muscle cell; nu, nucleus; mf, contractile part of the body wall of the trunk rudiment, transverse section. muscle cell, ce, noncontractile part of the longitudinal Ventro-lateral muscle band (after TEM). Co, body cav- muscle cell. Scale = 1pm. ity; cu, cuticle; ep, epidermal epithelium; lmc, longitudi- GIANT LARVAE OF PHYLLODOCIDAE

int

Fig. 8. Larva ofPhyllodocidae g. sp. Detail of entoder- ittal section. After TEM. B1, basal lamina; co, body ma1 intestine epithelium with yolk-like vacuoles and cavity; int, intestinal cell; me, mesoderm; nu, nucleus; mesoderm in the hyposphere of trochophore region. Sag- ylv, yolk-like vacuole. Scale = 1 pm.

Excretory system. A pair of protone- plasmic cap, formed by a nephridial duct phridia is present in the trochophore region wall cell (Fig. 9). Duct cells are ciliated but of the larva. Each of the 10-15 terminal cells only extend a few scattered microvilli into has a cilium surrounded by a filtration weir the relatively large duct lumen (-4 pm in of 15 microvilli (microvillar rod). Distally, transsection). It was not possible to deter- the microvillar rod is surrounded by a proto- mine the number of cells forming the chan- A.B. TZETLIN

Fig. 9. Larvae of Phyllodocidae g.sp. Details of proto- cap of the channel cell. After TEM. Ctc, cilia of the nephridium. A: Filtration weir and nucleus of terminal terminal cell; ch, channel of the protonephridium; dce, cell. B: Nephridial duct, transversal section with distal duct cell; df, distal part of the filtration weir; me, mesoder- part of the filtration weir surrounded by protoplasmic mal cell; mr, rnicrovillar rod; nu, nucleus. Scale = 1.2 p. nel. An ECM was not observed associated DISCUSSION with the microvillar weir, but this may be Several characters dictate the inclusion of artifact. No excretory organs were found in this distinctive pelagic larva in the family trunk segments. Phyllodocidae. These are the position and GIANT LARVAE OF structure of the frontal sensory organ; ab- that correspond to those of adult bottom- sence of an apical tuft of cilia; a collar, formed dwelling phyllodocids. For example, the by the hyposphere, covering the first setiger- brain is subdivided into anterior and poste- ous segments of the trunk rudiment (Cazaux, rior regions. The posterior division is con- '75 , '85; Sveshnikov, '78; Lacalli, '81; Zavar- nected with eyes and the well-developed neu- zina and Tzetlin, '86); shape and localization ropil runs to the circumesophageal of tentacular cirri on the first three seg- connectives. All these characters are compa- ments (tentacular formula 1-2-1); unira- rable to those seen in adult mous parapodia with foliose prominent dor- (Lebsky, '70) and rather more complicated sal cirri and compound heterogomph setae than the central nervous system usually pre- with setal shaft exhibiting numerous long sent in $rochophore and metatrochophore acuminate teeth (Pleijel, '93); and displace- larvae (Akesson, '67; Ospovat, '78; Lacalli, ment of the first two pairs of segmental '88). Furthermore, the paired segmental gan- ganglia of the ventral nerve cord onto circum- glia are also similar to those of adult Eulalia esophageal connectives (Lebsky, '70; Ospo- viridis (Lebsky, '70; Ushakova and Evdonin, vat, '78; Eibye-Jacobsen, '93). '84). Tentacular cirri, parapodia, muscle cells Furthermore, the distinctive body cavity, of the parapodial complex, and serially ar- lacking a peritoneum, covered by somatic ranged muscular elements correspond to longitudinal muscles, and exhibiting incom- those of phyllodocid adults (Pleijel, '93) while plete septa formed by myocytes, is typical for prostomial appendages are still absent. phyllodocids as is the monolayer of longitudi- One pair of protonephridia, located in the nal myocytes that form the body wall (Zavar- hyposphere, is typical for phyllodocid trocho- zina and Tzetlin, '89; Bartholomaeus, '94; phores. Normally, these protonephridia dis- Ivanov and Tzetlin, in prep.). Protonephridia appear in the two-segment-stage metatro- also resemble those reported from phyllodoc- chophore, along with the appearance of serial ids: the 14-15 regularly spaced microvillar segmental nephridia (Bartolomaeus, '89). rods forming the terminal cell weir are iden- Conversely, larvae examined in this study tical to protonephridia from the phyllodocids have protonephridia in the hypochere at least Eulalia viridis, and Phyllodoce (Anaitides) until the development of 100 or more seg- mucosa and I! fragilis examined by Lebsky ments, which still do not exhibit their own ('74), Smith and Ruppert ( '88), and Bartolo- maeus ('89). However, these larvae from the serial nephridia. The protonephridia in the Indian Ocean show an unusual combination hyposphere more closely resemble adult seg- of larval and adult features. Normally, nedo- mental nephridia of than chaetae of phyllodocids have no more than they do larval protonephridia (Bartolomaeus, 10 segments (Sveshnikov, '78; Cazaux, '85) '89) in terms of the number of terminal cells with rudiments of prostomial appendages and the diameter and construction of the usually appearing on segments 10-12 (Ospo- channel. vat, '78), but two cases of polysegmented Despite well-developed myocytes forming phyllodocid nectochaetae have been reported, the body wall and incomplete septa, mesoder- ~amely,the larvae of Lopadorhynchus (see mal cells that surround the intestine both in Akesson, '67) and pelagic larvae of Phyllo- the trochophore and in the trunk rudiment doce sp. described by Blake ('75). However, are nonspecialized cells bearing numerous the Lopadorhynchus larvae have no more lamina-like flattened cytoplasmic exten- than 15 segments and adults have maxi- sions, typical for larval mesoderm of polych- mally 35. Larvae with 13 segments have the aetes. Basal laminas are weakly developed. full number of episphaerial antennae and a I believe that the planktotrophic larvae well-developed muscular axial proboscis. The undergo two stages of development before pelagic phyllodocid nectochaetae found off settlement occurs: (1)growth of an actively the Northern California coast by Blake ('75) feeding, exceptionally large trochophore and had up to 22 segments. The larvae with (2) development of the trunk rudiment. If 12-22 segments already had four antennae these larvae were lecithotrophic, we would of the adult type on the episphere and a expect the adults to produce large oocytes. well-developed muscular axial proboscis. However, neither oocytes nor mature eggs In contrast, the pelagic larvae described with a diameter >1.0 mm have been de- in this study had over 100 segments. They scribed from phyllodocids or from polych- also exhibited several well-developed organs aetes in general. 106 A.B. 'I'ZETLIN In lecithotrophic larvae, yolk material is Bartolomaeus, T. (1994) On the ultrastructure of the usually located not only in endoderm but coelomic lining in the Annelida, Sipunculida and Echiu- rida. Microfauna Marina 9:171-220. also in tissues of mesodermal origin (Zavar- Beklemishev, K.V. (1964) Principles of Comparative zina and Tzetlin, '91; Tzetlin, in prep.). Yolk- Anatomy of Invertebrates, 3rd ed. Moscow: Publ. House like material was observed in the intestines Nauka (in Russian). of actively feeding pelagic trochophores of Blake, J.A. (1975) The larval development of Polychaeta from the northern California coast. 111. Eighteen spe- Lopadorhynchus (Akesson, '67). In these lar- cies of . Ophelia 14:23-84. vae, we have only found yolk material in the Cazaux, C. (1975) Reproduction et developpement lar- intestine, not in any other tissues. vaire de Phyllodoce laminosa Savigny 1818, Cahiers The presence of larvae in the coastal area de Biologie Marine 16:541-549. Cazaux, C. (1985) Developpement larvaire de l'annelide of the Seychelles Islands and the Gulf of polychete Phyllodocidae Eteonepicta Quatrefages 1865 Aden and as well as in the area of undersea dans le bassin d'Arcachon. J. Exp. Mar. Biol., Ecol. 85: mounts (Error, Equator) leads me to the 191-209. suggestion that the unknown benthic adult Eibye-Jacobsen, D. (1993) On the phylogeny of the Phyl- stage of these phyllodocids inhabits the floor lodocidae (Polychaeta, Annelida): an alternative. Z. Zool. Syst. Evo1.-forsh. 313174-197. of the shelf and slope zone of the Indian Ivanov, P.P. (1928) Die Entwicklung der Larvalsegmente Ocean. bei den Anneliden. Z. Morph. Okol. Tiere 10:62-161. The very large size and unusual pattern of Kleinenberg, N. (1886) Die Entstehung des Annelides development of the adult body may be an aus der Larve von Lopadorhynchus. 2. Wiss. Zool. 44:l-227. adaptation for an extended pelagic life and a Lacalli, T. (1981) Structure and development of the rapid settlement of a species that inhabits apical organ in trochophores of Spirobranchus polyc- the slopes of islands and undersea moun- erus, and Phyllodoce mucosa tains located far from each other. It is also (Polychaeta). Proc. R. Soc. Lond. B 212:381-402. likely that the delayed appearance of prosto- Lacalli, T. (1986) Prototroch structure and innervation in the trochophore larva of Phyllodoce (Polychaeta). mial appendages and the muscular axial Can. J. Zool. 64:17&184. proboscis, both structures needed for ben- Lacalli, T. (1988) The larval reticulum in Phyllodoce thic life or at least for macrophagy, reflect (Polychaeta, Phyllodocidae). Zoomorphology 108:61- the extensive period of active filter feeding 68. Lebsky, V.K. (1970) Construction of the nervous system by the pelagic stage. The very few findings of Eulalia uiridis (L) (Polychaeta, Phyllodocidae). Do- the larvae do not give real matter for com- klady Akademii Nauk USSR 190:1486-1489 (in Rus- parison with geographical distribution of sian). other midoceanic invertebrate larvae Lebsky V.K. (1974) Fine construction of the protonephro- '90; Scheltema, '92). mixia of polychaetes Eulalia viridis. 1. Toward the (Scheltema and Rice, protonephridial function. Tsytologia 16:685-689 (in Russian). ACKNOWLEDGMENTS Meyer, E., 1898. Untersuchungen zur Entwicklungsge- schichte der Anneliden. Trudy Kazan University 31: Thanks to Dr. Riva Margulis (State Uni- 3-356. versity of Moscow) for providing the author Minichev, Y. and Y. Starobogatov (1972) The problem of with material. For valuable and helpful dis- torsion process and promorphological rearrangement in larvae of trochophore . Zoologichesky Zhur- cussions and suggestions, the author is in- nal, 51:1437-1449 (in Russian). debted to Dr. Thomas Bartolomaeus, Dr. Ospovat, M. (1978) Studies on the development of the Fredrik Pleijel, Dr. Mary E. Petersen, and nervous system in Phyllodoce (Polychaeta, Phyllodoci- two anonymous reviewers. Special thanks to dae). Zoologichesky Zhurnal57:987-997 (in Russian). Dr. Frederick Earrison for his care and cor- Pleijel, F.(1991) Phylogeny and classification ofthe Phyl- lodocidae (Polychaeta) Zool. Scripta 20:225-261. rection of the English version of the manu- Salvini-Plawen, L. (1980) Was ist eine Trochophora? script. Eine Analyse der Larventypen mariner Protostomier. Zool. Jb. Anat. 103:389-423. Salvini-Plawen, L. (1988) Annelida and Mollusca - a LITERATURE CITED prospectus. In W. Westheide, C. 0. Hermans (eds.): hesson, B. (1967) On the nervous system of the Lopado- Microfauna Marina. The Ultrastructure of Polych- rhynchus larva (Polychaeta). Arkiv Zool. ser. 2,20:55- aeta. Stuttgart: Gustav Fisher Verlag. 78. Scheltema R. S. (1992) Passive dis~ersalof lankt tonic Bartolomaeus, T. (1987) Ultrastruktur des Photorezep- larvae and the biogeography of siblittoral species. In tors der Trochophora von Anaitides mucosa Oersted Guiscppe Colombo, Irenco Ferrari, Viktor Ugo Ceccher- (Phyllodocidae, Annelida). Microfauna Marina 3:411- elli, ~k;nigioRossi (eds.): Marine ~utro~h~cationand 418. population Dynamics. Fredensberg, Denmark: Olsen Bartolomaeus, T. (1989) Ultrastructure and develop- and Olsen, pp. 195-202. ment of the nephridia in Anaitides mucosa (Annelida, Scheltema R. S. and M. E. Rice (1990) Occurrence of Polychaeta). Zoomorphology 109:15-32. teleplanic pelagosphaera larvae of sipunculans in tropi- GIANT LARVAE OF

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