Protandrous Hermaphroditic Reproductive System in the Adult Phases of Mothocya renardi (Bleeker, 1857) (Cymothoidae: Isopoda: Crustacea) -Light and Electron Microscopy Study

Abstract

The reproductive system of Mothocya renardi (Bleeker, 1857), a protandrous hermaphroditic cymothoid that infects the belonid fish Strongylura leiura Bleeker, 1850, is characterized using light and electron microscopy. Three protandrous hermaphroditic adult phases are identified: male, transitional and female. Each phase includes a paired reproductive system, one on either side of the gut. Each consists of three lobed testes, followed by an ovary, then a vas deferens that opens into a penis on the same side. During the male phase, all testis lobes are filled with germ cells at various stages of spermatogenesis and spermeogenesis. Primary and secondary spermatogonial cells are confined to the peripheral side of the testis lobe. The ovary shows peripheral germarium and a large number of yolkless oocytes encircled by follicle cells. The oviduct emerged from the ovary mid laterally and its distal end was found to be sealed. The exceptionally elongated spermatozoon consists of a head and a long filamentous tail. The spermatozoa are found organized into characteristic bundles to form spermatophores, and these are also packed in the vas deferens during the male phase. During the transitional phase, on the other hand, testes appear to be withered, but the vas deferens contains spermatophores. The ovary shows yolky oocytes encircled by follicle cells. During the female phase, the testis lobes appear as thin, empty, and sac like, and the extremity of the vas deferens is closed. Ovaries contain yolky oocytes and more prominent oviducts than male and transitional phases. The present paper also discusses the pattern of correlation between 1) the ovarian and brood cycles and 2) the ovarian and molt cycles.

Keywords: Follicle cells; Oocytes; Ovary cycle; Protandrous hermaphroditism; Spermatophores.

Fig. 1.

Mothocya renardi (Bleeker, 1857): Reproductive system during the male phase. A, Hermaphroditic reproductive system showing testis lobes, ovary, vas deferens, and oviduct (4X); B, spermatophores: unstained (10X); C, spermatozoa: unstained (100X). O: ovary, TL: testis lobe, VE: vas deferens, OD: oviduct, AVD: anterior vas deferens, PVD: posterior vas deferens, S: spermatophore, T: tail, A: acrosome, H: head.

Fig. 2.

Mothocya renardi (Bleeker, 1857): Testis lobe during the male phase. A–D, Semithin sections (CS; 1 μm: toluidine blue stained). A, Acini and androgenic gland (100X); B, wall showing muscle band (100X); C, somatic accessory cells and germ cells during different stages of maturation (40X); D, enlarged view showing somatic accessory cells (100X). E, Histological section (CS; 4 μm: haematoxylin-eosin) showing spermatogonial cells (100X). F, Primary and secondary spermatogonia (100X). Sc: spermatocytes, Sac: somatic accessory cell, W: wall, Ag: androgenic gland, M: muscle layer, SSg: secondary spermatogonia, Sg: spermatogonia, N: nucleus, Psg: primary spermatogonia.

Fig. 3.

Mothocya renardi (Bleeker, 1857): Histology of testis lobes during the male phase. A, Semithin section (LS; 1 μm: toluidine blue) showing spermatocytes during meiotic division. B–E, Cross sections (4 μm: haematoxylin-eosin) showing the spermatids during different maturation stages. Sc: spermatocytes, Sd: spermatid, ImS: immature spermatozoa, T: tail, N: nucleus, H: head, Sac: somatic accessory cell.

Fig. 4.

Mothocya renardi (Bleeker, 1857): Electron micrograph of the testis lobes during the male phase: A1, Spermatocyte (4800X); A2, spermatids (9300X); A3, somatic accessory cells and portion of spermatophore (2900X); B1, cross section through spermatozoan head (4800X); B2, longitudinal section through spermatophore (4800X); B3, cross section through spermatozoan tail (6800X); C1, spermatozoan head region (6800X); C2, spermatozoan tail, acrosome and extracellular tubules (6800X); C3, spermatozoan acrosome and tail (18500X); D1, spermatozoan tail surrounded by extracellular tubules (11000X); D2, spermatozoan tail (30000X) showing transverse striations and central lumen (insight: wall of spermatozoan tail with double membrane); D3, a portion of spermatozoan tail showing central lumen filled with electron-dense granules (68000X). Sc: spermatocyte, N: nucleus, M: mitochondria, Pm: plasma membrane, Sd: spermatid, T: tail, H: head, Sac: somatic accessory cell, A: acrosome, Ect: extracellular tubule, Sz: spermatozoa, S: spermatophore, Edg: electron-dense granules, Ts: transverse striations, Dm: double membrane.

Fig. 5.

Mothocya renardi (Bleeker, 1857): Ovary during the male phase. A, Semi thin section (LS; 1 μm; toluidine blue) showing germarium and previtellogenic oocytes encircled by follicle cells (100 X). B, Electron micrograph of ovary (LS; 0.5 μm) showing previtellogenic oocyte encircled by follicle cells (1400X). N: nucleus, n: nucleolus, Pm: plasma membrane, Oo: oocyte, Gz: germinal zone, Ow: ovarian wall, C: cytoplasm, Fc: Follicle cell, V: vacuole.

Fig. 6.

Mothocya renardi (Bleeker, 1857): Electron micrographs of the cross sections of the vas deferens during the male phase showing spermatophore. A, Head regions (3200X); B, tail regions (6800X); C, tail regions showing central lumen with electron-dense granules (30000X). N: nucleus, T: tail, H: head, Ect: extracellular tubule, S: spermatophore, Edg: electron-dense granules, L: lumen.

Fig. 7.

Mothocya renardi (Bleeker, 1857): Reproductive system during the transitional phase. A, Reproductive system showing oocyte-filled ovary, spermatophore-filled vas deferens, and oviduct (4X); B, histological section (LS; 4 μm; hematoxylin-eosin) through vas deferens showing spermatophores (20X); C, histological section (LS; 4 μm; hematoxylin-eosin) through ovary showing yolky oocytes (20X). O: ovary, TL: testis lobe, OD: oviduct, AVD: anterior vas deferens, PVD: posterior vas deferens, Oo: oocyte, N: nucleus, n: nucleolus, Fc: follicle cell, S: spermatophore.

Fig. 8.

Mothocya renardi (Bleeker, 1857): Reproductive system during the female phase. A, Ovary during the previtellogenic stage (4X); B, ovary during the previtellogenic stage showing oocytes (10X); C, ovary at Vg1 (4X); D, ovary at Vg2 connected with hepatopancreas (4X); E, ovary at Vg4 (4X); F. ovary during the spent stage (4X). O: ovary, TL: testis lobe, OD: oviduct, VD: vas deferens, Oo: oocyte, Gz: germinal zone, Op: ovarian pouch, Hp: hepatopancreas, Re: residual oocytes.

Fig. 9.

Mothocya renardi (Bleeker, 1857): Histological section of the ovary during the female stage. A, previtellogenic stage showing germinal zone and previtellogenic oocytes (20X); B, Vg1 stage (10X); C, Vg1 oocytes showing nucleus and follicle cells (100X); D, Vg3 oocytes (10X); E, Vg5 (4X); F, spent stage (40X). Oo: oocyte, Gz: germinal zone, N: nucleus, n: nucleolus, Fc: follicle cells, Fc1: follicle cell -1, Fc2: follicle cell -2, C: cytoplasm.

Fig. 10.

Mothocya renardi (Bleeker, 1857): Electron micrograph of the ovary during the previtellogenic stage. A, germinal zone (2900X); B, highly convoluted (arrows) ovarian wall (6800X); C, haemocytes in the ovary (4800X). Ow: ovarian wall, Gz: germinal zone, H: haemocytes.

Fig. 11.

Mothocya renardi (Bleeker, 1857): Female stage. Correlation between (A) ovarian cycle and brood development; (B) ovarian cycle and molt cycle.