Differences in Swim Bladder Histology of Anguilla bicolor bicolor at Various Stages of Sexual Maturity

https://doi.org/10.22146/jtbb.74702

Nur Indah Septriani(1*), Muhammad Ardillah Rusydan(2), Gizela Aulia Agustin(3), Nareta Defiani(4), Fajar Sofyantoro(5), Ariel Hananya(6), Dwi Eny Djoko Setyono(7)

(1) Faculty of Biology, Universitas Gadjah Mada, Yogyakarta, Indonesia 55281
(2) Faculty of Biology, Universitas Gadjah Mada, Yogyakarta, Indonesia 55281
(3) Faculty of Biology, Universitas Gadjah Mada, Yogyakarta, Indonesia 55281
(4) Faculty of Biology, Universitas Gadjah Mada, Yogyakarta, Indonesia 55281
(5) Faculty of Biology, Universitas Gadjah Mada
(6) PT. Delos Teknologi Maritim, Jl. Salak No.38, RT.6/RW.2, Guntur, Kecamatan Setiabudi, Kota Jakarta Selatan Daerah Khusus Ibukota Jakarta 12980
(7) National Research and Innovation Agency (BRIN) Gunungkidul, Yogyakarta, Indonesia 55861
(*) Corresponding Author

Abstract


The current study observed the histological differences of the swim bladder of the tropical eel, Anguilla bicolor bicolor, as an adaptation resulting from hydrostatic change. A total of 15 eels were collected from Pasir Puncu, Keburuhan, Purworejo and Segara Anakan, Cilacap, Indonesia in June 2017, September 2020, and April 2021. The eels were grouped into 4 stages based on the silvering stage and sex, namely: yellow undifferentiated, yellow female, silver male, and silver female. The average length and body weight of yellow undifferentiated eels were 255.07 ± 45.91 mm and 13.66 ± 8.5 g, respectively; for yellow female, the values were 374.35 ± 41.51 mm and 56.5 ± 12.02 g; for silver male, the values were 432.43 ± 15.15 mm and 140.29 ± 13.85 g; and for silver female were 702 ± 0.00 mm and 545 ± 11.31 g. The present study successfully recorded the histological structure of the swim bladder of A. bicolor bicolor in silver male and silver female stages. Silver males and females displayed a greater significant development of the swim bladder than yellow stages in the gas gland, mucosa, and submucosa layers. These results suggest that an increase in the gas gland thickness allows a greater contribution from gas to gas secretion, the mucosa exerts a mechanical effect on the newly formed gas bubbles, and the submucosa thickness reduces gas conductivity from the swim bladder wall.

 


Keywords


silver eel; yellow eel; gas gland; mucosa; submucosa

Full Text:

PDF


References

Aoyama et al., 2003. Short-Distance spawning migration of tropical freshwater eels. Biological Bulletin, 204, pp.104 –108. doi: 10.2307/1543500

Arai, T. & Abdul Kadir, S.R., 2017. Opportunistic spawning of tropical anguillid eels Anguilla bicolor bicolor and A. bengalensis bengalensis. Scientific Reports, 7, pp.1-17. doi: 10.1038/srep41649

Bertin, L., 1956. Eels, a biological study, London: Cleaver-Hume Press Ltd.

Beullens, K. et al., 1997. Sex differentiation, changes in length, weight and eye size before and after metamorphosis of European eel (Anguilla anguilla L.) maintained in captivity. Aquaculture, 153(1-2), pp.151–162. doi: 10.1016/S0044-8486(97)00019-7

Bowmaker, J.K. et al., 2008. Eel visual pigments revisited: The fate of retinal cones during metamorphosis. Visual Neuroscience, 25(3), pp.249–255. doi: 10.1017/S0952523808080152.

Cresci, A., 2020. A comprehensive hypothesis on the migration of European glass eels (Anguilla anguilla ). Biological Reviews. 95(5), pp.1273–1286. doi:10.1111/brv.12609.

Drechsel, V. et al., 2022. Aquaporin expression and cholesterol content in eel swim bladder tissue. Journal of Fish Biology, 100, pp.609-618. doi: 10.1111/jfb.14973

Durif, C. et al., 2006. Impact of silvering stage, age, body size and condition on reproductive potential of the European eel. Marine Ecology Progress Series, 327, pp.171–181. doi: 10.3354/meps327171.

Ege, V., 1939. A revision of the genus Anguilla Shaw, a systematic, phylogenetic and geographical study (Dana-Report No. 16)., Carlsberg Foundation; C.A. Reitzels Forlag; Oxford University Press; Bianco Luno.

Fange, R., 1958. Structure and function of the gas bladder in Argentina silus. Quarterly Journal of Microscopical Science, 99(1), pp.95–96. doi: 10.1242/jcs.s3-99.45.95

Geffroy, B. & Bardonnet, A., 2016. Sex differentiation and sex determination in eels: consequences for management. Fish and Fisheries, 17(2), pp.375–398. doi: 10.1111/faf.12113.

Hagihara, S. et al., 2012. Morphological and physiological changes of female tropical eels, Anguilla celebesensis and Anguilla marmorata, in relation to downstream migration. Journal of Fish Biology, 81(2), pp.408–426. doi: 10.1111/j.1095-8649.2012.03332.x.

Hatakeyama, R. et al., 2022. Developmental features of Japanese eels, Anguilla japonica, from the late leptocephalus to the yellow eel stages: an early metamorphosis to the eel‐like form and a prolonged transition to the juvenile. Journal of Fish Biology, 100(2), pp.454–473. doi:10.1111/jfb.14956.

Helfman, G. et al., 1987. Reproductive ecology of the American eel. In Common strategies of anadromous and catadromous fishes. American Fisheries Society, Symposium 1, Bethesda, Maryland, pp.42–56. ISBN 0-913235-42-3

Huyen, K.T. et al. 2022. Morphological characteristics and population structure of Marbled Eel (Anguilla marmorata) in Thua Thien Hue, Vietnam. Journal of Applied Animal Research, 50, pp.54-60. doi: 10.1080/09712119.2021.2018326

Kleckner, R.C., 1980a. Swim bladder volume maintenance related to initial oceanic migratory depth in silver-phase Anguilla rostrata. Science, 208(4451), pp.1481–1482. doi: 10.1126/science.7384792.

Kleckner, R.C., 1980b. Swimbladder wall guanine enhancement related to migratory depth in silver phase Anguilla rostrata. Comparative Biochemistry and Physiology Part A: Physiology, 65(3), pp.351–354. doi: 10.1016/0300-9629(80)90041-9.

Layton, C., Bancroft, J. & Suvarna, S., 2018. Fixation of tissues. In Bancroft’s Theory and Practice of Histological Techniques E-Book. Amsterdam: Elsevier, p. 40.

Marshall, N., 1972. Swim bladder organization and depth ranges of deep-sea teleosts. Symposium of the Society of Experimental Biology, 26, pp.261–272.

Melia, P. et al., 2006. Age and growth of Anguilla anguilla in the Camargue lagoons. Journal of Fish Biology, 68(3), pp.876–890. doi: 10.1111/j.0022-1112.2006.00975.x.

Morris, S.M. & Albright, J.T., 1975. The ultrastructure of the swimbladder of the toadfish, Opsanus tau L. Cell and Tissue Research, 164(1). doi: 10.1007/BF00221697.

Okamura, A. et al., 2007. A silvering index for the Japanese eel Anguilla japonica. Environmental Biology of Fishes, 80(1), pp.77–89. doi: 10.1007/s10641-006-9121-5.

Pankhurst, N.W., 1982. Relation of visual changes to the onset of sexual maturation in the European eel Anguilla anguilla (L.). Journal of Fish Biology, 21(2), pp.127–140. doi: 10.1111/j.1095-8649.1982.tb03994.x.

Pankhurst, N. W., & Lythgoe, J. N. 1982. Structure and colour of the integument of the European eel Anguilla anguilla (L.). Journal of Fish Biology, 21(3), pp. 279–296. doi:10.1111/j.1095-8649.1982.tb02833.x

Pankhurst, N.W. & Lythgoe, J.N., 1983. Changes in vision and olfaction during sexual maturation in the European eel Anguilla anguilla (L.). Journal of Fish Biology, 23(2), pp.229–240. doi: 10.1111/j.1095-8649.1983.tb02898.x.

Pankhurst, N.W. & Sorensen, P. W., 2011. Degeneration of the alimentary tract in sexually maturing European Anguilla anguilla (L.) and American eels Anguilla rostrata (LeSueur). Canadian Journal of Zoology, 62(6), pp.1143-1149. doi: 10.1139/z84-165

Pelster, B., 2013. The swimbladder. In Eel Physiology. Enfield: CRCPress), pp. 44–67.

Pelster, B., 2015. Swimbladder function and the spawning migration of the European eel Anguilla anguilla. Frontiers in Physiology, 5, 486. doi: 10.3389/fphys.2014.00486.

Prem, C. et al., 2000. Swim bladder gas gland cells produce surfactant: in vivo and in culture. American Journal Physiologicy Regulatory Integrative Comparative Physiology, 279(6), R2336–R2343. doi: 10.1152/ajpregu.2000.279.6.R2336

Righton, D.A., Aarestrup, K., & Jellyman, D., 2012. The Anguilla spp. migration problem: 40 million years of evolution and two millennia of speculation. Journal of Fish Biology, 81, pp.365–386

Schneebauer, G. et al. 2021. Expression of transport proteins in the rete mirabile of european silver and yellow eel. BMC Genomic.86 (822): 1-15. doi: 10.1186/s12864-021-08180-2

Schneider, C.A., Rasband, W.S. & Eliceiri, K.W., 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), pp.671–675. doi: 10.1038/nmeth.2089.

Smith, F.M. & Croll, R.P., 2011. Autonomic control of the swimbladder. Autonomic Neuroscience, 165(1), pp.140–148. doi: 10.1016/j.autneu.2010.08.002.

Sugeha, H.Y., Jatmiko, I., & Muhammad, S., 2009. Sexual development of the tropical short-finned eel Anguilla bicolor bicolor of the Segara Anakan Waters, Central Java, Indonesia. Jurnal Perikanan Universitas Gadjah Mada, 11(1), pp.108-123. doi: 10.22146/jfs.2988

Tesch, F.W., 2003. The Eel, 3rd edn. Ed. by J. E. Thorpe, Oxford: Blackwell Science.

Van Wichelen, J. et al., 2022. Glass eel (Anguilla anguilla L. 1758) feeding behaviour during upstream migration in an artificial waterway. Journal of Fish Biology, 101(4), pp.1047-1057. doi: 10.1111/jfb.15171.

Vøllestad, L.A. & Jonsson, B., 1986. Life-history characteristics of the European Eel Anguilla anguilla in the Imsa River, Norway. Transactions of the American Fisheries Society, 115(6), pp.864–871. doi: 10.1577/1548-8659(1986)115<864:LCOTEE>2.0.CO;2.

Wenner, C.A. & Musick, J.A., 1974. Fecundity and gonad observations of the American Eel, Anguilla rostrata , migrating from Chesapeake Bay, Virginia. Journal of the Fisheries Research Board of Canada, 31(8), pp.1387–1391. doi: 10.1139/f74-164.

Wolfe, D., 2019. Tissue processing. In Suvarna SK, Layton C, Bancroft JD (eds) Bancroft’s theory and practice of histological techniques. London: Elsevier, pp. 73–83. doi: 10.1016/B978-0-7020-6864-5.00006-2.

Yamada, Y. et al., 2001. Morphological and histological changes in the swim bladder during maturation of the Japanese eel. Journal of Fish Biology, 58(3), pp.804–814. doi: 10.1111/j.1095-8649.2001.tb00532.x.

Yamada, Y. et al., 2004. Monthly changes in the swim bladder morphology of the female Japanese eel Anguilla japonica in the coastal waters of Mikawa Bay, Japan. Ichthyological Research, 51(1), pp.52–56. doi: 10.1007/s10228-003-0195-1.

Zacchei, A.M. & Tavolaro, P., 1988. Lateral line system during the life cycle of Anguilla anguilla (L.). Bolletino di zoologia, 55(1–4), pp.145–153. doi: 10.1080/11250008809386611.



DOI: https://doi.org/10.22146/jtbb.74702

Article Metrics

Abstract views : 363 | views : 255

Refbacks

  • There are currently no refbacks.


Copyright (c) 2023 Journal of Tropical Biodiversity and Biotechnology

Creative Commons License
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.

Editoral address:

Faculty of Biology, UGM

Jl. Teknika Selatan, Sekip Utara, Yogyakarta, 55281, Indonesia

ISSN: 2540-9581 (online)