Research Article
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Studies on organogenesis of Cyprinus carpio var. koi with reference to histological perspectives

Year 2025, Volume: 8 Issue: 1, 39 - 51

Sivakumar Kandhasamy , Muthupriya Palanichamy , Meenakshi Sivalingam Valliappan , Kareem Altaff

Abstract

The objective of the current study was to investigate the histological characteristics of larval organogenesis in Cyprinus carpio var. koi. The eggs and several developmental stages of C. carpio var. koi larvae were preserved in Bouin's fluid. Histological examinations were conducted daily from the first day after fertilisation (DAF) to the 12th DAF and the 16th, 24th, 32nd, and 40th DAF. Histological examinations of C. carpio var. koi eggs revealed the development of an embryonic disc, followed by the formation of the neural tube and embryonic eyes on the second day after fertilisation (DAF). The just-emerged larvae have distinct eyes and a neural tube that has undergone differentiation into the brain. Following that, an examination was conducted on the development of the digestive system, swim bladder, gills, skin, and fins. The ontogeny developments were categorised into five distinct stages. During larval development, the initial two stages have exhibited variations in their organogenesis. The larvae head was aligned and devoid of the yolk, but their body was connected to the yolk sac and gill arches, which were visible between the 3rd and 5th days after fertilisation (DAF), and their total length range was 4.35-6.83mm. The digestive system had a linear configuration, with an enlargement in both the dorsal and ventral regions of the body on the ninth day after fertilisation (DAF). During the 10th to 17th developmental stages, larvae have a total length range of 11.23-14.35mm. The operculum, gill lamella, and dorsal fin were developed in this stage. Between the 24th and 40th days after fertilisation (DAF), the larvae acquired a fin, a coiled gut, and well-developed accessory glands and their total length was measured between 15.01 and 23.68mm.

Keywords

C. carpio Ontogeny Histology Larval rearing

Ethical Statement

The experiments were conducted in accordance with the guidelines and regulations established by the Committee for Control and Supervision of Experiments on Animals (CCSEA), Department of Animal Husbandry and Dairying, Ministry of Fisheries, Animal Husbandry and Dairying, Government of India and the experimental protocol was approved by Institutional Animal Ethical Committee (Karpaga Vinayaga Institute of Medical Sciences and Research Institute, Tamil Nadu, India) (No: 181GO/ERE/S/15/CPCSEA dated 04.12.2018).

Supporting Institution

Karpaga Vinayaga College of Engineering and Technology & The New College

Thanks

We would like to the Managements, the Principals of Karpaga Vinayaga College of Engineering and Technology, Chengalpattu – 603308 and The New College, Chennai - 600014 for providing laboratory facilities to complete the work.

References

  • Adamek, M., Oschilewski, A., Wohlsein, P., Jung‐Schroers, V., Teitge, F., Dawson, A., Gela, D., Piackova, V., Kocour, M., Adamek, J., Bergmann, S.V., Steinhagen, D. (2017). Experimental infections of different carp strains with the carp edema virus (CEV) give insights into the infection biology of the virus and indicate possible solutions to problems caused by koi sleepy disease (KSD) in carp aquaculture. Veterinary Research, 48(1). https://doi.org/10.1186/s13567-017-0416-7
  • Behrouz, A., Moghadam, M., Rezaei, S., Abbasi, H. (2014). Larval organogenesis of Schizothorax zarudnyi (Nikolskii, 1897) (Cyprinidae): histological aspects. Journal of Fisheriessciences.com. https://doi.org/10.3153/jfscom.201416
  • Boulhic, M. and Gabaudan, J. (1992). Histological study of the organogenesis of the digestive system and swim bladder of the dover sole, Solea solea (Linnaeus 1758). Aquaculture, 102(4), 373-396. https://doi.org/10.1016/0044-8486(92)90190-v
  • Burggren, W. and Pinder, A. (1991). Ontogeny of cardiovascular and respiratory physiology in lower vertebrates. Annual Review of Physiology, 53(1), 107-135. https://doi.org/10.1146/annurev.ph.53.030191.000543
  • Cajado, R., Oliveira, L., Silva, F., Zacardi, D. (2021). Early development of the neotropical fish known as long sardine Triportheus auratus (Valenciennes 1850) (Characiformes, Triportheidae). Journal of Applied Ichthyology, 37(5), 759-769. https://doi.org/10.1111/jai.14228
  • China, V. and Holzman, R. (2014). Hydrodynamic starvation in first-feeding larval fishes. Proceedings of the National Academy of Sciences, 111(22), 8083-8088. https://doi.org/10.1073/pnas.1323205111
  • Du, S., Devoto, S., Westerfield, M., Moon, R. (1997). Positive and negative regulation of muscle cell identity by members of the hedgehog and TGF-β gene families. The Journal of Cell Biology, 139(1), 145-156. https://doi.org/10.1083/jcb.139.1.145
  • Duester, G. (2022). Towards a better vision of retinoic acid signaling during eye development. Cells, 11(3), 322. https://doi.org/10.3390/cells11030322
  • Grimaldi, A., Tettamanti, G., Martin, B., Gaffield, W., Pownall, M., Hughes, S. (2004). Hedgehog regulation of superficial slow muscle fibres inxenopusand the evolution of tetrapod trunk myogenesis. Development, 131(14), 3249-3262. https://doi.org/10.1242/dev.01194
  • Jonz, M. and Nurse, C. (2003). Neuroepithelial cells and associated innervation of the zebrafish gill: a confocal immunofluorescence study. The Journal of Comparative Neurology, 461(1), 1-17. https://doi.org/10.1002/cne.10680
  • Jonz, M. and Nurse, C. (2005). Development of oxygen sensing in the gills of zebrafish. Journal of Experimental Biology, 208(8), 1537-1549. https://doi.org/10.1242/jeb.01564
  • Leis, J. (2007). Behaviour as input for modelling dispersal of fish larvae: behaviour, biogeography, hydrodynamics, ontogeny, physiology and phylogeny meet hydrography. Marine Ecology Progress Series, 347, 185-193. https://doi.org/10.3354/meps06977
  • Liu, W. and Cvekl, A. (2017). Six3 in a small population of progenitors at E8.5 is required for neuroretinal specification via regulating cell signaling and survival in mice. Developmental Biology, 428(1), 164-175. https://doi.org/10.1016/j.ydbio.2017.05.026
  • Ługowska, K. and Kondera, E. (2018). Early development of vimba (Vimba vimba) at different temperatures and temperature-related anomalies. Aquaculture Research, 49(6), 2336-2344. https://doi.org/10.1111/are.13670
  • Luo, G., Hofmann, C., Bronckers, A., Bradley, A., Karsenty, G. (1995). BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Development, 9(22), 2808-2820. https://doi.org/10.1101/gad.9.22.2808
  • Martins, M.L., Cardoso, L., Furtado, W., Tancredo, K.R. (2018) Histopathology guide for freshwater fish. Editora UFSC, Florianopolis
  • Milan, D., Jones, I., Ellinor, P., MacRae, C. (2006). In vivo recording of adult zebrafish electrocardiogram and assessment of drug-induced QT prolongation. American Journal of Physiology Heart and Circulatory Physiology, 291(1), H269-H273. https://doi.org/10.1152/ajpheart.00960.2005
  • Miquerol, L. and Kelly, R. (2012). Organogenesis of the vertebrate heart. Interdisciplinary Reviews Developmental Biology, 2(1), 17-29. https://doi.org/10.1002/wdev.68
  • Mohale. H.P., Sarang, N., Desai, A.Y. (2020) The common carp and its culture systeme management. Academia Publications, Delhi.
  • Morcillo, J., Martı́nez-Morales, J., Trousse, F., Fermin, Y., Sowden, J., Bovolenta, P. (2006). Proper patterning of the optic fissure requires the sequential activity of BMP7 and SHH. Development, 133(16), 3179-3190. https://doi.org/10.1242/dev.02493
  • Muthupriya, P., Sivakumar, K., Altaff, K. (2022). The Early Organogenesis of Carassius auratus (Cyprinidae): A Histological Perspectives. International Journal of Zoological Investigations, 8(1), 219-234. https://doi.org/10.33745/ijzi.2022.v08i01.025
  • Nebeker, A., Savonen, C., Stevens, D. (1985). Sensitivity of rainbow trout early life stages to nickel chloride. Environmental Toxicology and Chemistry, 4(2), 233. https://doi.org/10.1897/1552-8618(1985)4[233:sortel]2.0.co;2
  • Nowlin, W., Drenner, R. (2000). Context-dependent effects of bluegill in experimental mesocosm communities. Oecologia, 122(3), 421-426. https://doi.org/10.1007/s004420050048
  • Qin, J., Fast, A.W. (1997). Food selection and growth of young snakehead Channa striatus. Journal of Applied Ichthyology, 13, 21–25.
  • Ramcharitar, J., Higgs, D., Popper, A. (2006). Audition in sciaenid fishes with different swim bladder-inner ear configurations. The Journal of the Acoustical Society of America, 119(1), 439-443. https://doi.org/10.1121/1.2139068
  • Sakai, N., Insolera, R., Sillitoe, R., Shi, S., Kaprielian, Z. (2012). Axon sorting within the spinal cord marginal zone via robo-mediated inhibition of N-Cadherin controls spinocerebellar tract formation. Journal of Neuroscience, 32(44), 15377-15387. https://doi.org/10.1523/jneurosci.2225-12.2012
  • Saltys, H., Jonz, M., Nurse, C. (2005). Comparative study of gill neuroepithelial cells and their innervation in teleosts and Xenopus tadpoles. Cell and Tissue Research, 323(1), 1-10. https://doi.org/10.1007/s00441-005-0048-5
  • Schulz‐Mirbach, T., Metscher, B., Ladich, F. (2012). Relationship between swim bladder morphology and hearing abilities–a case study on Asian and African cichlids. Plos One, 7(8), e42292. https://doi.org/10.1371/journal.pone.0042292
  • Sivakumar, K. (2005). Freshwater fish and prawn larval rearing using indigenous live-feed. PhD thesis, University of Madras. India, 1-135.
  • Thorsen, D., Hale, M. (2007). Neural development of the zebrafish (Danio rerio) pectoral fin. The Journal of Comparative Neurology, 504(2), 168-184. https://doi.org/10.1002/cne.21425
  • Uemonsa, T., Sakagami, K., Yasuda, K., Araki, M. (2002). Development of dorsal–ventral polarity in the optic vesicle and its presumptive role in eye morphogenesis as shown by embryonic transplantation and in ovo explant culturing. Developmental Biology, 248(2), 319-330. https://doi.org/10.1006/dbio.2002.0737
  • Witeska, M., Sarnowski, P., Ługowska, K., Kowal, E. (2013). The effects of cadmium and copper on embryonic and larval development of ide Leuciscus idus l. Fish Physiology and Biochemistry, 40(1), 151-163. https://doi.org/10.1007/s10695-013-9832-4
  • Wu, G., Yang, Y., Zeng, L. (2007). Kinematics, hydrodynamics and energetic advantages of burst-and-coast swimming of koi carps (Cyprinus carpio koi). Journal of Experimental Biology, 210(12), 2181-2191. https://doi.org/10.1242/jeb.001842
  • Zhou, W., Boucher, R., Bollig, F., Englert, C., Hildebrandt, F. (2010). Characterization of mesonephric development and regeneration using transgenic zebrafish. American Journal Physiology Renal Physiology, 299(5), F1040-F1047. https://doi.org/10.1152/ajprenal.00394.2010
  • Zimmer, A., Wright, P., Wood, C. (2017). Ammonia and urea handling by early life stages of fishes. Journal of Experimental Biology, 220(21), 3843-3855. https://doi.org/10.1242/jeb.140210

Studies on organogenesis of common carp Cyprinus carpio var. koi with reference to histological perspectives

Year 2025, Volume: 8 Issue: 1, 39 - 51

Sivakumar Kandhasamy , Muthupriya Palanichamy , Meenakshi Sivalingam Valliappan , Kareem Altaff

Abstract

The objective of the current study was to investigate the histological characteristics of larval organogenesis in Cyprinus carpio var. koi. The eggs and several developmental stages of C. carpio var. koi larvae were preserved in Bouin's fluid. Histological examinations were conducted daily from the first day after fertilisation (DAF) to the 12th DAF and the 16th, 24th, 32nd, and 40th DAF. Histological examinations of C. carpio var. koi eggs revealed the development of an embryonic disc, followed by the formation of the neural tube and embryonic eyes on the second day after fertilisation (DAF). The just-emerged larvae have distinct eyes and a neural tube that has undergone differentiation into the brain. Following that, an examination was conducted on the development of the digestive system, swim bladder, gills, skin, and fins. The ontogeny developments were categorised into five distinct stages. During larval development, the initial two stages have exhibited variations in their organogenesis. The larvae head was aligned and devoid of the yolk, but their body was connected to the yolk sac and gill arches, which were visible between the 3rd and 5th days after fertilisation (DAF), and their total length range was 4.35-6.83mm. The digestive system had a linear configuration, with an enlargement in both the dorsal and ventral regions of the body on the ninth day after fertilisation (DAF). During the 10th to 17th developmental stages, larvae have a total length range of 11.23-14.35mm. The operculum, gill lamella, and dorsal fin were developed in this stage. Between the 24th and 40th days after fertilisation (DAF), the larvae acquired a fin, a coiled gut, and well-developed accessory glands and their total length was measured between 15.01 and 23.68mm.

Keywords

C. carpio Ontogeny Histology Larval rearing

References

  • Adamek, M., Oschilewski, A., Wohlsein, P., Jung‐Schroers, V., Teitge, F., Dawson, A., Gela, D., Piackova, V., Kocour, M., Adamek, J., Bergmann, S.V., Steinhagen, D. (2017). Experimental infections of different carp strains with the carp edema virus (CEV) give insights into the infection biology of the virus and indicate possible solutions to problems caused by koi sleepy disease (KSD) in carp aquaculture. Veterinary Research, 48(1). https://doi.org/10.1186/s13567-017-0416-7
  • Behrouz, A., Moghadam, M., Rezaei, S., Abbasi, H. (2014). Larval organogenesis of Schizothorax zarudnyi (Nikolskii, 1897) (Cyprinidae): histological aspects. Journal of Fisheriessciences.com. https://doi.org/10.3153/jfscom.201416
  • Boulhic, M. and Gabaudan, J. (1992). Histological study of the organogenesis of the digestive system and swim bladder of the dover sole, Solea solea (Linnaeus 1758). Aquaculture, 102(4), 373-396. https://doi.org/10.1016/0044-8486(92)90190-v
  • Burggren, W. and Pinder, A. (1991). Ontogeny of cardiovascular and respiratory physiology in lower vertebrates. Annual Review of Physiology, 53(1), 107-135. https://doi.org/10.1146/annurev.ph.53.030191.000543
  • Cajado, R., Oliveira, L., Silva, F., Zacardi, D. (2021). Early development of the neotropical fish known as long sardine Triportheus auratus (Valenciennes 1850) (Characiformes, Triportheidae). Journal of Applied Ichthyology, 37(5), 759-769. https://doi.org/10.1111/jai.14228
  • China, V. and Holzman, R. (2014). Hydrodynamic starvation in first-feeding larval fishes. Proceedings of the National Academy of Sciences, 111(22), 8083-8088. https://doi.org/10.1073/pnas.1323205111
  • Du, S., Devoto, S., Westerfield, M., Moon, R. (1997). Positive and negative regulation of muscle cell identity by members of the hedgehog and TGF-β gene families. The Journal of Cell Biology, 139(1), 145-156. https://doi.org/10.1083/jcb.139.1.145
  • Duester, G. (2022). Towards a better vision of retinoic acid signaling during eye development. Cells, 11(3), 322. https://doi.org/10.3390/cells11030322
  • Grimaldi, A., Tettamanti, G., Martin, B., Gaffield, W., Pownall, M., Hughes, S. (2004). Hedgehog regulation of superficial slow muscle fibres inxenopusand the evolution of tetrapod trunk myogenesis. Development, 131(14), 3249-3262. https://doi.org/10.1242/dev.01194
  • Jonz, M. and Nurse, C. (2003). Neuroepithelial cells and associated innervation of the zebrafish gill: a confocal immunofluorescence study. The Journal of Comparative Neurology, 461(1), 1-17. https://doi.org/10.1002/cne.10680
  • Jonz, M. and Nurse, C. (2005). Development of oxygen sensing in the gills of zebrafish. Journal of Experimental Biology, 208(8), 1537-1549. https://doi.org/10.1242/jeb.01564
  • Leis, J. (2007). Behaviour as input for modelling dispersal of fish larvae: behaviour, biogeography, hydrodynamics, ontogeny, physiology and phylogeny meet hydrography. Marine Ecology Progress Series, 347, 185-193. https://doi.org/10.3354/meps06977
  • Liu, W. and Cvekl, A. (2017). Six3 in a small population of progenitors at E8.5 is required for neuroretinal specification via regulating cell signaling and survival in mice. Developmental Biology, 428(1), 164-175. https://doi.org/10.1016/j.ydbio.2017.05.026
  • Ługowska, K. and Kondera, E. (2018). Early development of vimba (Vimba vimba) at different temperatures and temperature-related anomalies. Aquaculture Research, 49(6), 2336-2344. https://doi.org/10.1111/are.13670
  • Luo, G., Hofmann, C., Bronckers, A., Bradley, A., Karsenty, G. (1995). BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Development, 9(22), 2808-2820. https://doi.org/10.1101/gad.9.22.2808
  • Martins, M.L., Cardoso, L., Furtado, W., Tancredo, K.R. (2018) Histopathology guide for freshwater fish. Editora UFSC, Florianopolis
  • Milan, D., Jones, I., Ellinor, P., MacRae, C. (2006). In vivo recording of adult zebrafish electrocardiogram and assessment of drug-induced QT prolongation. American Journal of Physiology Heart and Circulatory Physiology, 291(1), H269-H273. https://doi.org/10.1152/ajpheart.00960.2005
  • Miquerol, L. and Kelly, R. (2012). Organogenesis of the vertebrate heart. Interdisciplinary Reviews Developmental Biology, 2(1), 17-29. https://doi.org/10.1002/wdev.68
  • Mohale. H.P., Sarang, N., Desai, A.Y. (2020) The common carp and its culture systeme management. Academia Publications, Delhi.
  • Morcillo, J., Martı́nez-Morales, J., Trousse, F., Fermin, Y., Sowden, J., Bovolenta, P. (2006). Proper patterning of the optic fissure requires the sequential activity of BMP7 and SHH. Development, 133(16), 3179-3190. https://doi.org/10.1242/dev.02493
  • Muthupriya, P., Sivakumar, K., Altaff, K. (2022). The Early Organogenesis of Carassius auratus (Cyprinidae): A Histological Perspectives. International Journal of Zoological Investigations, 8(1), 219-234. https://doi.org/10.33745/ijzi.2022.v08i01.025
  • Nebeker, A., Savonen, C., Stevens, D. (1985). Sensitivity of rainbow trout early life stages to nickel chloride. Environmental Toxicology and Chemistry, 4(2), 233. https://doi.org/10.1897/1552-8618(1985)4[233:sortel]2.0.co;2
  • Nowlin, W., Drenner, R. (2000). Context-dependent effects of bluegill in experimental mesocosm communities. Oecologia, 122(3), 421-426. https://doi.org/10.1007/s004420050048
  • Qin, J., Fast, A.W. (1997). Food selection and growth of young snakehead Channa striatus. Journal of Applied Ichthyology, 13, 21–25.
  • Ramcharitar, J., Higgs, D., Popper, A. (2006). Audition in sciaenid fishes with different swim bladder-inner ear configurations. The Journal of the Acoustical Society of America, 119(1), 439-443. https://doi.org/10.1121/1.2139068
  • Sakai, N., Insolera, R., Sillitoe, R., Shi, S., Kaprielian, Z. (2012). Axon sorting within the spinal cord marginal zone via robo-mediated inhibition of N-Cadherin controls spinocerebellar tract formation. Journal of Neuroscience, 32(44), 15377-15387. https://doi.org/10.1523/jneurosci.2225-12.2012
  • Saltys, H., Jonz, M., Nurse, C. (2005). Comparative study of gill neuroepithelial cells and their innervation in teleosts and Xenopus tadpoles. Cell and Tissue Research, 323(1), 1-10. https://doi.org/10.1007/s00441-005-0048-5
  • Schulz‐Mirbach, T., Metscher, B., Ladich, F. (2012). Relationship between swim bladder morphology and hearing abilities–a case study on Asian and African cichlids. Plos One, 7(8), e42292. https://doi.org/10.1371/journal.pone.0042292
  • Sivakumar, K. (2005). Freshwater fish and prawn larval rearing using indigenous live-feed. PhD thesis, University of Madras. India, 1-135.
  • Thorsen, D., Hale, M. (2007). Neural development of the zebrafish (Danio rerio) pectoral fin. The Journal of Comparative Neurology, 504(2), 168-184. https://doi.org/10.1002/cne.21425
  • Uemonsa, T., Sakagami, K., Yasuda, K., Araki, M. (2002). Development of dorsal–ventral polarity in the optic vesicle and its presumptive role in eye morphogenesis as shown by embryonic transplantation and in ovo explant culturing. Developmental Biology, 248(2), 319-330. https://doi.org/10.1006/dbio.2002.0737
  • Witeska, M., Sarnowski, P., Ługowska, K., Kowal, E. (2013). The effects of cadmium and copper on embryonic and larval development of ide Leuciscus idus l. Fish Physiology and Biochemistry, 40(1), 151-163. https://doi.org/10.1007/s10695-013-9832-4
  • Wu, G., Yang, Y., Zeng, L. (2007). Kinematics, hydrodynamics and energetic advantages of burst-and-coast swimming of koi carps (Cyprinus carpio koi). Journal of Experimental Biology, 210(12), 2181-2191. https://doi.org/10.1242/jeb.001842
  • Zhou, W., Boucher, R., Bollig, F., Englert, C., Hildebrandt, F. (2010). Characterization of mesonephric development and regeneration using transgenic zebrafish. American Journal Physiology Renal Physiology, 299(5), F1040-F1047. https://doi.org/10.1152/ajprenal.00394.2010
  • Zimmer, A., Wright, P., Wood, C. (2017). Ammonia and urea handling by early life stages of fishes. Journal of Experimental Biology, 220(21), 3843-3855. https://doi.org/10.1242/jeb.140210
There are 35 citations in total.

Details

Primary Language English
Subjects Fish Anatomy
Journal Section Research Articles
Authors

Sivakumar Kandhasamy 0000-0001-8971-869X

Muthupriya Palanichamy 0000-0002-7859-9290

Meenakshi Sivalingam Valliappan 0009-0007-7714-1732

Kareem Altaff 0000-0001-9178-2519

Early Pub Date December 11, 2024
Publication Date
Submission Date June 17, 2024
Acceptance Date August 14, 2024
Published in Issue Year 2025Volume: 8 Issue: 1

Cite

APA Kandhasamy, S., Palanichamy, M., Sivalingam Valliappan, M., Altaff, K. (2024). Studies on organogenesis of Cyprinus carpio var. koi with reference to histological perspectives. Aquatic Research, 8(1), 39-51.
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