HUNTER and MACEWICZ: ATRESIA IN NORTHERN ANCHOVY OVARY 



ering to the follicle. The thecal cells do not change 

 until hydration when they become even flatter and 

 have a stringy appearance. 



3) Yolked Oocytes — Oocytes in this class range 

 from 0.45 to 0.80 mm (major axis), and all contain 

 yolk spherules or globules throughout the region 

 between the periphery of the oocyte and the 

 perinuclear zone (Y, Fig. Ic, d). As vitellogenesis 

 continues, the yolk varies from spherules in the 

 smaller oocytes to large globules in the larger 

 ones. Just prior to spawning (<24 h) the globules 

 fuse to form yolk plates (Fig. Ih). Such oocytes are 

 excluded from this oocyte class, this characteristic 

 being diagnostic of the last class (hydrated oo- 

 cytes). The nucleus of oocytes in the yolked oocyte 

 class is oval with numerous nucleoli. The 

 granulosa cells have a wide rectangular shape in 

 cross section and a large oval nucleus; their walls 

 are clearly evident in sagittal section where they 

 form polyhedrons. The zona radiata is a wide, 

 striated, eosinophilic band until hydration when it 

 stretches thin and the striations disappear. 



4) Hydrated Oocytes — These oocytes range in 

 size from 0.75 to 1.2 mm (major axis) (H, Fig. Ig, h). 

 Hydration (rapid uptake of fluid by the follicle, 

 Fulton 1898) begins when the nucleus has mi- 

 grated to the animal pole (M, Fig. le, f) and yolk 

 globules first fuse to form yolk plates, and it ends 

 when the hydrated oocyte is ovulated. The nucleus 

 of hydrated oocytes is not visible except in the 

 earliest phase because after the nucleus migrates, 

 the nuclear membrane disintegrates dispersing 

 its contents into the cytoplasm. During hydration 

 all yolk globules fuse into plates and the oocyte 

 expands greatly, stretching the granulosa and 

 thecal cell layers. At this time, the granulosa cells 

 in cross section appear as long, thin rectangles, the 

 thecal cells are extremely flat and have a 

 stringlike appearance, and the zona radiata is 

 very thin and lacks striations. Hydrated oocytes 

 are the most ephemeral of all oocyte classes since 

 this stage lasts for less than a day, whereas the 

 other stages are always present in reproductively 

 active anchovy ovaries. Migratory nuclei may be 

 seen as early as 24 h before ovulation, but hy- 

 drated oocytes in which all globulues are fused to 

 form yolk plates do not occur earlier than 12 h 

 before spawning. We have never observed atre- 

 sia in hydrated oocytes; apparently, in northern 

 anchovy, nearly all hydrated oocytes are ovu- 

 lated. 



Atretic Stages 



The nomenclature and general characteristics 

 used for the four atretic stages given below follow 

 those of Bretschneider and Duyvene de Wit (1947) 

 and Lambert (1970a). In the initial stage of the 

 atretic process (alpha (a)), the entire oocyte is 

 resorbed including the yolk, if present, by the 

 hypertrophying granulosa cells of the follicle. In 

 the next stage (beta (^)), the major degeneration 

 and resorption of the follicle (granulosa and thecal 

 cells) occurs. In the third (gamma (y) ) and fourth 

 (delta (8)) atretic stages, regression of the theca 

 and granulosa cells continues, greatly reducing 

 the size of the follicle, and a yellow-brown pigment 

 appears. The histological characteristics used to 

 identify these stages are outlined below. 



1) Alpha (a) Stage Atresia — In the alpha stage 

 of atresia the oocyte is resorbing leaving only the 

 follicular layers. The early phase of alpha stage 

 atresia is characterized by the disintegration of 

 the nucleus, evident by an irregular shape, and a 

 granular, dark basophilic staining, and the disin- 

 tegration of some of the yolk globules, indicated by 

 less refractive globules, fused globules, or globules 

 expanded and of less regular shape (Fig. 2a, b, c). 

 The zona radiata slowly dissolves as indicated by 

 the loss of striations and uneven diameter (Fig. 

 2b). In subsequent phases of alpha atresia, 

 granulosa cells enlarge and, upon rupture of the 

 zona radiata, invade the degenerating oocyte (Fig. 

 2d). Yolk adjacent to the invading granulosa cells 

 liquifies (loses all structural integrity and appears 

 as a homogeneous eosinophilic area) and becomes 

 phagocytized by the granulosa cells as indicated 

 by the presence of yolk in the vacuoles of these 

 cells. The basophilic staining cytoplasm is also 

 resorbed by the granulosa cells. In the alpha stage 

 of atresia, blood capillaries and vessels are numer- 

 ous in the thecal connective layer which does not 

 proliferate or invade the oocyte but remains as a 

 thin layer covering the granulosa cells. The alpha 

 stage ends when resorption of the oocyte is com- 

 plete (all cytoplasm and yolk are gone). The result- 

 ing structure (beta stage) is usually much smaller 

 than the original oocyte. The subsequent atretic 

 stages (beta-delta) are steps in the resorption of 

 the remaining follicle and the structure at this 

 point is called an atretic follicle, the term atretic 

 oocyte being reserved for only the alpha stage of 

 atresia. 



In unyolked oocytes the alpha stage process is 

 similar but without yolk (Fig. 2e, f). The nucleus 



123 



