Ovarian balls (Floating ovaries) of Rhadinorhynchus niloticus Mohamadain, 1989 from the Nile perch Lates niloticus Linnaeus, 1758; an electron microscope study
A. M. El-Siefy
Perfil de Orcid, y 
Publicado en línea: 16 jul 2024
Páginas: 194 - 200
Recibido: 07 feb 2024
Aceptado: 25 mar 2024
DOI: https://doi.org/10.2478/helm-2024-0014
Palabras clave
© 2024 A. M. El-Siefy et al., published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Unlike the typical ovaries found in other female helminths, the Acanthocephala possess distinctive structures referred to as the ovarian balls, sometimes called the free ovaries or the floating ovaries. They appear, suspended in the fluid-filled metasoma and are responsible for egg production. In addition, the process of fertilization takes place inside the ovarian balls (Crompton & Nickol, 1985; Herlyn, 2021). The ovarian balls are early initiated from ovarian primordia during larval development (Mehlhorn, 2001).
The reproductive system of a female acanthocephalans consists of one or two ligament sacs, which contain the mature ovarian balls, and a unique efferent duct system. The latter facilitates the entry of the spermatozoa to the female body cavity and the exit of mature eggs from the body cavity to the outside (Asaolu, 1980; Mehlhorn, 2001). In adult worms the ligament sacs rupture (only in Palaeacanthocephala) and the ovarian balls are released and become free floating in the pseudocoel (Crompton & Nickol, 1985).
Describe the ovarian ball of adult female Compare the structure and organization of Study the way of fertilization, as far as possible, in order to give new insights into the reproductive biology of the genus
A total of 30
Adult females of
Specimens for SEM were dried in a critical-point drying machine using liquid carbon dioxide as a transitional medium. The dried female worms were carefully broken on metallic stubs, onto which the ovarian balls might be dropped out of the body cavity. Coating with gold was done under vacuum conditions using a JEOL JFC-1100E ion-sputtering device (Tokyo, Japan). Examination was carried out with a stereoscan JEOL JS M-5400 LV (Tokyo, Japan) operating at 15 kV.
Specimens for TEM were washed in propylene dioxide and embedded in Spurr’s epoxy resin. Semi-thin sections were stained with methylene blue and examined with a light microscope fitted with a digital camera for photomicrography (Conn
Ultrathin sections were mounted on copper grids and double-stained with uranyl acetate and lead citrate. Examination was carried out in a JEOL 1010 (Tokyo, Japan) transmission electron microscope operated at 80 kV. Measurements were done using ImageJ program
All procedures were performed according to the guidelines for the care and use of animals and approved by the animal research ethics committee of Minia University, which was under an approval number: ES40/2020.
Semi-thin cross sections of female
A – Photomicrograph of a semi-thin section of female
The ovarian ball of
Ultra-thin sections of the ovarian balls exhibited three distinct primary areas: a central oogonial syncytium, a peripheral cellular zone and a somatic supporting syncytium surrounding them (Fig. 2A). The outer surface of the ovarian ball revealed numerous microvilli-like outgrowths bordering the superficial supporting syncytium (Figs. 2A – C). The oogonial syncytium is irregular in shape and located in the center of the ovarian ball. It is densely populated with numerous nuclei and functions as the germinative core, in which the oogonia are formed (Figs. 2B, C). The oogonia are formed by the detachment of portions of the cytoplasm, each containing one nucleus, from the oogonial syncytium. The cellular zone represents the peripheral part of the ovarian ball and contains many oocytes in different stages of development (Fig. 2C). The peripheral part is where fertilization takes place. The supporting syncytium is mainly formed of a cytoplasm containing various inclusions such as nuclei, mitochondria, endoplasmic reticulum, (Figs. 2D, 3A, B) golgi bodies, annulate lamellae, and lipid droplets. In case the ovarian ball is inseminated, a spermatozoon can be observed inside, surrounded by a cytoplasmic sheath (Fig. 3A). The cytoplasm supporting the oogonial syncytium is referred to as the “medullary supporting syncytium”, whereas that surrounding the cellular zone is known as the “cortical supporting syncytium (Crompton & Whitfield, 1974 and Crompton & Nickol, 1985). (Figs. 3B).
Transmission electron micrographs (TEM) of the ovarian ball of
TEM of the ovarian ball of
The initial stage in oocyte development is the formation of oogonia, which originate from the oogonial syncytium. The free oogonia forms primary oocysts to secondary oocysts then mature oocysts. But, in our figures the primary oocytes are not clearly differentiated from secondary oocytes. So, we preferred to use the terminology developing oocytes that refer to both primary oocytes and secondary oocysts. In this stage, each nucleus becomes enveloped by a small amount of the cytoplasm and a membrane, transforming into an oogonium. The latter measures 4.7 – 5.4 (5.16) μm in length by 4.0 – 4.4 (4.22) μm in width. Thereafter, the newly formed oogonia increase in size and undergo development to become developing oocytes (Fig. 3C).
The developing oocyte measures 6.0 – 11.9 (8.7) μm in length by 6.7 – 12.2 (8.18) μm in width. It is characterized by a large centric nucleus that measures 3.9 – 5.3 (4.6) μm in length by 3.5 – 5.1 (10.1) μm in width. The nucleus is surrounded by a little cytoplasmic content and inclusions (Fig. 3D). Upon further development, the developing oocyte gives rise to a mature oocyte.
TEM of the ovarian ball of
The mature oocyte measures 12.9 – 19.4 (17.1) μm in length by 12.4 – 19.3 (15.3) μm in width. It exhibits a distinct polarity when the nucleus migrates to one pole of the cell, near the plasma membrane, assuming an eccentric position. The nucleus measure 5.2 – 8.6 (6.9) μm in length by 4.3 – 4.1 (4.2) μm in width. Concurrently, there is an increase in the cytoplasmic volume which is accompanied by the elaboration of a number of inclusions. (Figs. 4A, B). The cytoplasm of the mature oocyte contains numerous mitochondria and two distinct types of other inclusions: large, faint-colored yolk granules and smaller, more electron-dense eggshell granules (explanation: Marchand & Mattei (1980) stated that the protein fraction in the cytoplasmic dense granules is involved in the formation of the egg shell (Fig. 4B).
In case the mature oocyte is not-fertilized, it undergoes atresia, as shown in figure 2C. On the other hand, in case it is fertilized, the process of fertilization takes place in three main steps. The first step is the penetration of the spermatozoon into the ovarian ball. The spermatozoon is longer than the oocyte and as a result it is folded around itself multiple times to move through the ovarian ball. Upon successful penetration, the surrounding supporting syncytium envelops the spermatozoon with a cytoplasmic sheath that facilitates its movement towards the oocyte (Fig. 3A). In the second step the spermatozoon initiates penetration of the oocyte (Figs. 5 A, B). The third step involves the complete penetration of the spermatozoon into the oocyte, thus reaching the nucleus (Figs. 5C, D). In this stage, the cytoplasmic sheath, which surrounds the spermatozoon break and begin to disappear. Many sections of the folded spermatozoon can be seen in the same oocyte.
After penetration, the mature oocyte undergoes immediate modification (Fig. 5C); 1. The surrounding cytoplasmic sheath of the spermatozoon begins to degenerate; 2. The volume of the oocyte is noticeably decreased and, at the same time, a post-fertilization space is formed around it; 3. The shell granules which are scattered in the cytoplasm of the oocyte start to move towards the surface of the oocyte and aggregate to form the fertilization membrane. The latter is the first future shell membrane of the developing acanthor.
The present study is the first, which describes the ultrastructure of the ovarian ball of adult female
Previous studies have described the structure of the ovarian ball in different genera of the Acanthocephala. Tkinson and Byram (1976) stated that the ovarian ball of female
TEM of the mature oocyte of
The present study identified two types of inclusions within the mature oocyte: large, faint-colored yolk granules and smaller, more electron-dense egg-shell granules. Marchand and Mattei (1980) described amorphous electron-opaque protein and a granular polysaccharide. Crompton and Whitfield (1974) and Peura
The steps of fertilization recorded in the present study coincides with the findings of Marchand and Mattei (1980) for the acanthocephalan
Regarding juveniles, Peura