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FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1980 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. (1980). An ultrastructural study of oogenesis in Streblospio benedicti (Spionidae), with remarks on diversity of vitellogenic mechanisms in Polychaeta. Zoomorphologie, 94(3), 241‐263. doi:10.1007/BF00998204 euLO ~ \ Zoomorphologie 94,241 -263 (1980) Zoomorphologie © by Springer-Verlag 1980 An Ultrastructural Study of Oogenesis in Streblospio benedicti (Spionidae) , with Remarks on Diversity of Vitellogenic Mechanisms in Polychaeta Kevin J. Eckelbarger* Harbor Branch Foundation, Inc.,RR I, Boxl96,Fort Pierce, Fla. 33450, USA . Summary. The ultrastructural features of oogenesis were examined in the spionid polychaete Streblospio benedicti. Paired ovaries are attached to the genital blood vessels extending into the coe lomic space from the circumintes tinal sinus. The genital blood vessel wall is composed of flattened, peritoneal cells, large follicle cells and developing oocytes. Vitellogenesis occurs while the oocytes are attached to the blood vessel wall. Two morphologically distinguishable types of yolk are synthesized. Type I is synthesized first by an autosynthetic process apparently involving pinocytosis and the conjoined efforts of the Golgi complex and rough endoplasmic reticulum. Type II yolk appears later through a heterosynthetic process involving the infolding of the oolemma and the sequestering of materials from the blood vessel lumen by endocytosis. During this process, blood pigment molecules appear to be incorporated into endocytotic pits, vesicles and eventually the forming yolk body. The significance of heterosynthetic yolk formation to the general reproductive strategies of polychaetous annelids is discussed. A. Introduction Streblospio benedicti Webster, 1879, is a larviparous, deposit-feeding, estuarine polychaete, widely distributed on the east and west coasts of North America and parts of Europe and South America (Foster, 1971). It has been described as an opportunistic species (Grassle and Grassle, 1974) and an indicator of organic pollution in the marine environment (Felice, 1959; Wass, 1967; Grassle and Grassle, 1974; Young and Young, 1978). Benthic populations of S. benedicti can reach enormous densities particularly in response to a variety of environmen tal perturbations. Experimental field studies have shown that densities exceeding 400,000 per m 2 can be attained within azoic sediment boxes in less than 10 days / (McCall, 1977). • The author is grateful for the very capable technical assistance of Ms. P.A. Linley and the many stimulating discussions with Dr. Stan Rice. Contribution No. 156, Harbor Branch Foun dation, Inc. 0340-6725/80/0094/0241/$04.60 242 KJ. Eckelbarger Streblospio benedicti is a semi-continuous spawner as defined by Olive and Clark (1978). In northern latitudes, S. benedicti reproduces primarily during the summer and fall months (Dean, 1965; Simon and Brander, 1967; Grassle and Grassle, 1974). In southern Florida waters, however, reproductive individ uals are present most of the year. Sexual maturity is reportedly reached in about a month following settlement (Grassle and Grassle, 1974). Developing eggs are incubated in dorsal brood pouches prior to the release of larvae into the plankton (Campbell, 1957; Dean, 1965; Collier and Jones, 1967). Oogenesis occurs rapidly with vitellogenesis taking place entirely within the ovary. Two types of yolk are found within the mature egg, one of which appears to be formed heterosynthetically, a feature recently reported for the first time in another polychaete (Eckel barger, 1979). Although a general description of larval development in Streblospio benedicti is available (Campbell, 1957; Dean, 1965), little is known of its reproductive biology and nothing concerning oogenesis. Due to the unusual mode of yolk synthesis and the scarcity of information regarding gametogenesis in this ecolog ically important polychaete, an ultrastructural investigation of oogenesis was undertaken. B. Materials and Methods Female specimens of Streblospio benedicti in various stages of sexual maturity were collected from the shallow water s of the Indi an River estuary in S1. Lucie County, Florid a. Genital segments were cut into small pieces and prepared for electron microscopy following the procedures outlined in Eckelbarger (1979). Thin sections of embedded tissue were cut on a Porter-Blum MT-2 ultramicro tome with a diamond knife, stained with aqueous, saturated uran yl acetate followed by lead citrate and examined with a Zeiss EM9-S2 electron microscope . C. Observations The ovaries of Streblospio benedicti are paired organs situated on the convoluted genital blood vessels which extend laterally into the coelomic space from the circumintestinal sinus in the middle and posterior body region . Oogenesis is unsynchronized within the ovary and therefore nearly all stages of development can be observed in histological sections. Mitotically-dividing gametogonia were never observed although they are assumed to exist. Spireme oocytes in the zygotene or pachytene phases of meiotic prophase are encountered commonly as are a variety of post-pachytene oocytes in various previtellogenic and vitellogenic stages. J. Follicle Cells The genital blood vessel wall (Figs. 1 and 2) is composed partially of large , interdigitating cuboidal or squamous follicle cells, derived from the peritoneum, which lie on a discontinuous layer of thin, sinuous peritoneal cells. The latter Oogenesis in Str eblospio benedict; 243 1 Fig. 1. Diagrammatic representation of transverse section through genital blood vessel of Streblospio benedicti illustrating morphological relationship between oolemma and perivasal ooplasm and ad jacent peritoneal cells and basal lamina in previtellogenic (I), early vitellogenic (2) and late vitelloge nic (3) oocytes cells contain scattered thick and thin filaments and a few mitochondria. Nuclei or other organelles were never observed. The peritoneal cells rest on a thin basal lamina, as do the follicle cells where the latter come in contact with the vessel lumen. A part of the blood vessel wall is also occupied by developing germ cells that partially rest on the peritoneal cells and the underlying basal lamina but never on the follicle cells (Fig. 3). However, the follicle cells surround 244 K.J. Eckelbarger the majority of oocytes and partially encapsulate the entire ovary. The follicle , cell sheath is incomplete in places, permitting parts of some oocytes to contact each other. The surfaces of a few oocytes, particularly the larger ones, are in direct contact with the coelomic fluid. Within the blood vessel, a red, extracel lular blood pigment is present with a sufficiently high molecular weight to give it a distinctive, particulate appearance in the electron microscope (Figs. 2 and 24). The polymeric molecules measure 22-25 nm in diameter. Follicle cells contain large (4.5-6.0 11m), spherical nuclei with scattered patches ofperipheral, condensed chromatin and a single characteristic, nucleolus about 1.5 11m in diameter. The cytoplasmic surface of the nuclear envelope is covered with ribosomes. The most prominent feature of the cells is the presence of abundant rough endoplasmic reticulum (RER), frequently in the form of large, tightly packed whorls or parallel arrays (Fig. 4). Some free ribosomes are present as well as scattered oblong mitochondria with long, tubular cristae (Fig. 6). The follicle cells are also characterized by the presence of numerous organelles which morphologically resemble Iysosomes . They contain cytomem branes closely resembling mitochondria (Fig. 5). and RER (Fig. 6), enclosed by an isolation membrane. The enclosed mitochondria have a denser matrix than the mitochondria within the cytoplasm. In addition, one also observes heterogeneous, membrane bounded dense bodies containing an amorphous elec tron dense material, granules and a membranous component that frequently appears as a myelin configuration (membrane whorls) (see arrows, Fig. 6). From one to several Goigi complexes are frequently observed in close association with these inclusions (Fig . 7). The Golgi have a small number of saccules and are usually in close association with cisternae of the RER. Two products appear to be released from the mature face of the organelle in the form of numerous, small (50-70 nm), coated vesicles and larger (up to 200 nm) membrane-bounded electron dense droplets. Occasionally, multivesicular bodies are observed. Follicle cells lack cytoplasmic continuity with germ cells or other follicle cells but adjacent fol1icle cells are periodically attached by small desmosomes. Follicle cells remain in intimate association with most developing oocytes throughout oogenesis but never possess microvilli or other specializations of the plasmalemma. Specialized junctional complexes have not been observed between germ cells nor have intercellular bridges been encountered. 2. Previtellogenic Oocytes These oocytes have a germinal vesicle diameter ranging from 9 to 20 11m. The smallest of these have little cytoplasm and a circular nucleus containing very sparse, scattered chromatin and occasionally a small , eccentric nucleolus (Fig. 4). The cytoplasm of large previtellogenic oocytes (Fig. 8) contains free ribosomes, Fig. 2. Transmission electron

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