Polychaetes Rhynchonerella Angelini and Alciopa Reynaudii ( Polychaeta: Alciopidae)

FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1988 Springer. This manuscript is an author version with the final publication available at http://www.springerlink.com and may be cited as: Eckelbarger, K. J., & Rice, S. A. (1988). Ultrastructure of oogenesis in the holopelagic polychaetes Rhynchonerella angelini and Alciopa reynaudii ( Polychaeta: Alciopidae). Marine Biology, 98(3), 427‐439. doi:10.1007/BF00391119 Marine Biology 98,427-439 (1988) Marine ;.~~ BiolOgy © Springer-Verlag 1988 Ultrastructure ofoogenesis in the holopelagic polychaetes Rhynchonerella angelini and Alciopa reynaudii (Polychaeta: Alciopidae) K.J. Eckelbarger 1 and S. A. Rice 2 1 Reproductive Biology Program, Harbor Branch Oceanographic Institution, 5600 Old Dixie Highway, Fort Pierce, Florida 34946, USA 2 Division of Science and Mathematics, University of Tampa, Tampa, Florida 33606, USA Abstract Introduction Ultrastructural features of oogenesis were examined in the The Alciopidae is one of six holopelagic polychaete fami pelagic polychaetes Rhynchonerella angelini and Alciopa lies whose representatives spend their entire life history in reynaudii which were collected from Bahamian waters by a the water column. Alciopids have evolved a number ofspe manned submersible during 1979 and 1980. No definiti ve cialized features for pelagic existence, including two large, ovary was detected in either species. Oogonia are released highly developed eyes whose structure and function have into the coelom as packets of cells, where they undergo mi been described (Hermans and Eakin 1974, Wald and Ray totic division while surrounded by an envelope of sheath port 1977), and long, thin bodies that are transparent or cells. Cytokinesis is incomplete, resulting in intercellular translucent in life. Very little is known about the repro bridges between oogonia. Oocytes undergo early stages of ductive biology of any pelagic polychaete family, and noth meiosis characterized by the presence of synapsed chromo ing regarding oogenesis. Some general observations on the somes, followed by a period of rap id cytoplasmic and nu reproductive biology and evolution of alciopids have been clear growth. Oocytes are released from the packets in made (Rice 1980, 1984), and Rice (1987) published infor ; the early vitellogenic phase into the coelom, where mation on behavior, sperm morphology and sperm storage I they und ergo yolk synth esis as solitary coelomic cells. organs in fourteen alciopid species from the western At l··· Vitellogenesis includes both auto synthetic and hetero lantic Ocean. synthetic processes. Autosynthesis involves the fusion of Alciopid polychaetes are believed to have arisen from secretory vesicles formed by the combined activity of ancestral stock similar to the present-day phyllodocid the rough endoplasmic reticulum and Golgi complex, with Eulalia spp. (Dales 1955, Ushakov 1972). Because phyl convoluted electron-dense tubular bodies of ·unknown lodocids are generally benthic in habit, an investigation of origin. Heterosynthesis involves the intense uptake of the reproductive biology of some alciopid species is of in exogenous precursors through endocytosis and their fusion terest to determine if alciopid gametogenic processes have into nascent yolk bodies which, in turn, are presumed diverged concomitantly with adult morphology. The pres to fuse with autosynthetically-derived yolk bodies. No ent paper describes the ultra structural feature s of oogenesis nutrient stores were detected in somatic tissues. Early and in two widely distributed alciopids, Rhyn chonerella an middle stages of vitellogenic oocytes were absent from the gelini and A lciopa reynaudii. coelom. This absence combined with the high level of en docytotic activity suggests that vitellogenesis occurs rap idly. These features, in combination with the presence of Materials and methods an exceptionally thin body wall and gut, might serve as re lated adaptations for pred ator avoidance by the mainte The specimens of alciopids used in this study were col nance of relatively low tissue-density. Alciopid, phyl lected by one of us (SAR) from the northwest Providence lodocid, and nereid polychaetes share some common re Channel, Bahama Island s, using the "Johnson-Sea-Link" productive features including the presence of "dispersed" . submersible operated by Harbor Branch Oceanographic ovaries, clusters of syncytial germ cells which und ergo Institution. A small number of A lciopa reynaudii Audouin meiosis while enveloped by somatic cells and the release & Milne Edwards, 1833 was collected in September 1979 of oocytes from the clusters prior to vitellogenesis. and April 1980 from a depth range of 60 to 240 m, while a greater numb er of Rhyn chonerella angelin! (Kinberg, 1866) 428 K.J. Eckelbarger and S.A. Rice: Ultrastructure of oogenesis in alciopids was collected in June 1979 and April 1980 at a depth of Gametogonial phase 122 m. Specimens of R. angelini closely fit the taxonom ic descriptions of Stop-Bowitz (1948), Dales (1957) and Dales The smallest germ cells observed are interpreted as and Peter (1972), but those of A. reynaudii showed some oogonia, and measure about l l rzrn in diameter, with differences which will be presented in a separate publi circular or oval nuclei measuring about 8.0 .um (Figs. I and cation . All collections were made at night , because the al 6). The nuclei contain granular, densely-staining chrom a ciopids were attracted to the subm ersible's floodlights. tin, and a single nucleolus consisting of a central pars Live individuals were returned to the surface and fixed amorpha and a surrounding, anastom osing chromatin immed iately for examination by light microscopy and fiber, the nucleolonema (Fig. 7). The cytopl asm is sparse, transmission electron microscopy (TEM). In order to esti and contains large (up to 2.0 .urn in length), spherical mito mate the degree ofsexual maturity in the population, three chondria with tubular cristae (Figs. 8, 9, 14), a single Golgi female Rhyn chonerella angelini were processed for paraffin complex (Fig. 15), free ribosomes, one or two centrioles histology to examine the distribution of oocyte stages. (Fig. 15), and scattered clumps of granular aggregates Specimens were fixed in Hollande's fixative, dehydrated ("nuage") of presumed nuclear origin (Fig. 14). The cells through ascending concentrations ofethanol, exchanged in typically have a smooth outline and the plasmalemma toluene, and embedded in TIssuePrep paraffin. Sections lacks microvilli. However, long, thin extensions of ooplasm were cut at a thickness of 10.urn, and stained in Cason 's from each oocyte that interdigitate with adjacent germ cells modification of Mallory-Heidenhain stain (Cason 1950). were common (Fig. 6: inset). All germ-cell stages from every tenth section ( IOO.um in The cell membranes of adjacent oocytes are attached by tervals) were counted and staged to avoid counting the maculae adhaerentes, and oocytes are connected by inter 90.um mature eggs twice. cellular bridges or fusomes (Figs. 8 and 9). The intercellu For electron microscopy, specimens were fixed for 2 h lar bridges in both species are circular in cross section and at room temperature in 2.5% glutaraldehyde buffered with about 1.0 to l.3.um in diameter (Fig. 10). The outer surface 0.2 M sodium phosphate, and postfixed in I % osmium of the bridge plasmalemma is covered by a dense fuzzy tetroxide buffered with 1.25% sodium bicarbonate. Speci coat, with a thinn er electron dense band just inside the mens were identified following postfixation and then were bridge plasmalemma. In rare sections of oocytes of A lciopa dehydrated in increasing concentrations of ethanol, trans reynaudii, rod-shaped bodies extended from the surface of ferred through two changes of propylene oxide, and the bridge into the intercellular space between the oocytes embedded in Epon. The sections were cut on a Porter (Fig. 8). In both species,(Figs. 8-10, 13), a number of Blum MTI-B ultramicrotome with a diamond knife, rounded or elongate, amorphous bodies is usually present stained with aqueous saturated uranyl acetate and lead within or near the bridge which form a circular pattern citrate, and examined with a Zeiss EM9-S2 transmission when viewed in transverse section (Fig. 10). In fortuitous electron microscope. sections, microtubules were positioned within the bridge in an axial direction. We observed no more than two bridges per germ cell. Each oogonial cluster is enveloped by sheath cells Results (Figs. I, 2, 5, 6, II , 12) that are presumably derived from the peritoneum. Several sheath cells surround each packet No definitive ovary was observed in either Rhynchonerella and interdigitate with each othe r. They are generally flat angelini or A lciopa reynaudii. Both species possess a "dis tened, with bean-shaped nuclei and relatively few or , "; persed ovary" consisting ofcoelomic germ-cell clusters sur ganelles. In Rhyn chonerella angelini, the sheath-cell nuclei rounded by an envelope of somatic cells which we have have patches of condensed chrom atin lining the inner sur termed "sheath cells", after Fischer (1975). In one speci face of the nuclear envelope (Figs. 5 and II ) while in men (A. reynaudiii , a mitotically-dividing oogonium was A lciopa reynaudii, the nuclei contain a uniformly electron observed within an oocyte cluster (Fig. 6). dense chromatin (Figs. 6 and 12).

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