Diem Tuong Dang , Randel Nyengaard Jens , Thi Thanh Huong Do * , Ngoc Hai Tran , Thanh Phuong Nguyen and Mark Bayley

* Corresponding author: Thi Thanh Huong Do (email: dtthuong@ctu.edu.vn)

Main Article Content

Abstract

Gill remodeling ability of clown knifefish exposed to different temperature levels (27°C and 33°C) and dissolved oxygen levels (hypoxia - 25% and 30% air saturation (at 27°C and 33°C), and normoxia - 95% air saturation) were performed applying vertical section to estimate lamellar surface area (SA), gill filament volume, lamellar volume, harmonic mean water blood thickness and calculate anatomic diffusion factor (ADF). The initial lamellar SA and harmonic mean water blood thickness of Chitala (33.12 ± 1.09 g) were 51.43 ± 3.10 mm2g-1 and 3.59 ± 0.15 µm in normoxia, respectively. The lamellae SA increased strongly after one month of exposure to elevated temperature and hypoxia. A significant reduction in the harmonic mean water–blood barrier thickness was observed following one month of hypoxia, whereas temperature effects were observed significantly after two months. The value of lamellar SA in the hypoxic group at 33°C (47.02 ± 2.44 mm2g-1) was twice as high as that of the normoxic group at 27°C (22.38 ± 1.06 mm2g-1) while the ADF in the hypoxic group at 33°C was nearly 4-fold higher than the normoxic group at 27°C. Findings in Chitala suggest that gill remodeling represents an ancient adaptation that has existed for over 300 million years.

Keywords: Clown knifefish, normoxia hypoxia, remodeling, temperature

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References

Baddeley, A., Gundersen, H.-J. G., & Cruz‐Orive, L. M. (1986). Estimation of surface area from vertical sections. Journal of Microscopy, 142(3), 259-276.

Boyd, C. E. (2015). Water quality (pp. 223-241). Springer International Publishing AG.

Brauner, C., Matey, V., Zhang, W., Richards, J., Dhillon, R., Cao, Z.-D., . . . & Fu, S.-J. (2011). Gill remodeling in crucian carp during sustained exercise and the effect on subsequent swimming performance. Physiological and Biochemical Zoology, 84(6), 535-542.

Da Costa, O. T., Pedretti, A. C. E., Schmitz, A., Perry, S. F., & Fernandes, M. N. (2007). Stereological estimation of surface area and barrier thickness of fish gills in vertical sections. Journal of Microscopy, 225(1), 1-9.

Dehadrai, P. V. (1962). Respiratory function of the swimbladder of Notopterus (Lacépède). Paper presented at the Proceedings of the Zoological Society of London.

Díaz, A. O., Castro, M. G., García, A. M., de Astarloa, J. M. D., & Figueroa, D. E. (2009). Gross morphology and surface ultrastructure of the gills of Odontesthes argentinensis (Actinopterygii, Atherinopsidae) from a Southwestern Atlantic coastal lagoon. Tissue and Cell, 41(3), 193-198.

Evans, D. H., Piermarini, P. M., & Choe, K. P. (2005). The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiological Reviews, 85(1), 97-177.

Fernandes, M. N., da Cruz, A. L., da Costa, O. T. F., & Perry, S. F. (2012). Morphometric partitioning of the respiratory surface area and diffusion capacity of the gills and swim bladder in juvenile Amazonian air-breathing fish, Arapaima gigas. Micron, 43(9), 961-970.

Fernandes, M. N., Rantin, F. T., Kalinin, A. L., & Moron, S. E. (1994). Comparative study of gill dimensions of three erythrinid species in relation to their respiratory function. Canadian Journal of Zoology, 72(1), 160-165.

Fu, S.-J., Brauner, C. J., Cao, Z.-D., Richards, J. G., Peng, J.-L., Dhillon, R., & Wang, Y.-X. (2011). The effect of acclimation to hypoxia and sustained exercise on subsequent hypoxia tolerance and swimming performance in goldfish (Carassius auratus). Journal of Experimental Biology, 214(12), 2080-2088.

Gundersen, H., Bagger, P., Bendtsen, T., Evans, S., Korbo, L., Marcussen, N., . . . & Pakkenberg, B. (1988). The new stereological tools: disector, fractionator, nucleator and point sampled intercept and their use in pathological research and diagnosis. Apmis, 96(7‐12), 857-881.

Hughes, G. M. (1972). Morphometrics of fish gills. Respiration Physiology, 14(1-2), 1-25.

Hughes, G. M., & Morgan, M. (1973). The structure of fish gills in relation to their respiratory function. Biological Reviews, 48(3), 419-475.

Hughes, G., Dube, S., & Munshi, J. (1973). Surface area of the respiratory organs of the climbing perch, Anabas testudineus (Pisces: Anabantidae). Journal of Zoology, 170(2), 227-243.

Hughes, G., & Munshi, J. (1973). Nature of the air‐breathing organs of the Indian fishes Channa, Amphipnous, Clarias and Saccobranchus as shown by electron microscopy. Journal of Zoology, 170(2), 245-270.

IPCC. (2014). Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II, and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, R.K. Pachauri and L.A. Meyer (eds.)]. IPCC, Geneva, Switzerland.

Li, S., Lu, X., & Bush, R. T. (2013). CO2 partial pressure and CO2 emission in the Lower Mekong River. Journal of Hydrology, 504, 40-56.

Matey, V., Richards, J. G., Wang, Y., Wood, C. M., Rogers, J., Davies, R., . . . & Brauner, C. J. (2008). The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii. Journal of Experimental Biology, 211(7), 1063-1074.

Metz, J. R., Van Den Burg, E. H., Bonga, S. E. W., & Flik, G. (2003). Regulation of branchial Na+/K+-ATPase in common carp Cyprinus carpio L. acclimated to different temperatures. Journal of Experimental Biology, 206(13), 2273-2280.

Mitrovic, D., Dymowska, A., Nilsson, G. E., & Perry, S. F. (2009). Physiological consequences of gill remodeling in goldfish (Carassius auratus) during exposure to long-term hypoxia. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 297(1), R224-R234.

Near, T. J., Eytan, R. I., Dornburg, A., Kuhn, K. L., Moore, J. A., Davis, M. P., . . . & Smith, W. L. (2012). Resolution of ray - finned fish phylogeny and timing of diversification. Proceedings of the National Academy of Sciences, 109(34), 13698-13703.

Nilsson, G. E. (2007). Gill remodeling in fish–a new fashion or an ancient secret? Journal of Experimental Biology, 210(14), 2403-2409.

Nilsson, G. E., Dymowska, A., & Stecyk, J. A. (2012). New insights into the plasticity of gill structure. Respiratory Physiology & Neurobiology, 184(3), 214-222.

Ong, K., Stevens, E., & Wright, P. (2007). Gill morphology of the mangrove killifish (Kryptolebias marmoratus) is plastic and changes in response to terrestrial air exposure. Journal of Experimental Biology, 210(7), 1109-1115.

Perry, S. F. (1978). Quantitative anatomy of the lungs of the red-eared turtle, Pseudemys scripta elegans. Respiration Physiology, 35(3), 245-262.

Perry, S. F., Fletcher, C., Bailey, S., Ting, J., Bradshaw, J., Tzaneva, V., & Gilmour, K. M. (2012). The interactive effects of exercise and gill remodeling in goldfish (Carassius auratus). Journal of Comparative Physiology B, 182 (7), 935-945.

Phuong, L. M., Malte, H., Nyengaard, J. R., & Bayley, M. (2018). Ontogeny and morphometrics of the gills and swim bladder of air-breathing striped catfish Pangasianodon hypophthalmus. Journal of Experimental Biology, 221(3), jeb168658.

Phuong, L. M., Nyengaard, J. R., & Bayley, M. (2017). Gill remodelling and growth rate of striped catfish Pangasianodon hypophthalmus under impacts of hypoxia and temperature. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 203, 288-296.

Poulsen, A. F., Hortle, K., Valbo-Jorgensen, J., Chan, S., Chhuon,C., Viravong, S., Nguyen, T. (2004). Distribution and ecology of some important riverine fish species of the Mekong River Basin. MRC Technical Paper, 10, 116.

Smith, H. M. (1945). The fresh-water fishes of Siam, or Thailand: Washington.

So, N. V., & Tuan, L. A. (2022). Assessment of the cultural situation and farming area management of Natopterus chitala in Hau Giang Province on the basis of GIS application. Vietnam Journal of Agriculture and Rural Development, 2, 81-88.

Sollid, J., De Angelis, P., Gundersen, K., & Nilsson, G. E. (2003). Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. Journal of Experimental Biology, 206(20), 3667-3673.

Sollid, J., & Nilsson, G. E. (2006). Plasticity of respiratory structures-adaptive remodeling of fish gills induced by ambient oxygen and temperature. Respiratory Physiology & Neurobiology, 154(1), 241-251.

Sollid, J., Weber, R. E., & Nilsson, G. E. (2005). Temperature alters the respiratory surface area of crucian carp Carassius carassius and goldfish Carassius auratus. Journal of Experimental Biology, 208(6), 1109-1116.

Tuong, D. D., Ngoc, T. B., Huynh, V. T. N., Phuong, N. T., Hai, T. N., Wang, T., & Bayley, M. (2018). Clown knifefish (Chitala ornata) oxygen uptake and its partitioning in present and future temperature environments. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 216, 52-59.

Tuurala, H., Egginton, S., & Soivio, A. (1998). Cold exposure increases branchial water–blood barrier thickness in the eel. Journal of Fish Biology, 53(2), 451-455.

Vidthayanon, C. (2012). Chitala ornata. The IUCN Red List of Threatened Species 2012: e.T181056A1693604. https://dx.doi.org/10.2305/IUCN.UK.2012-1.RLTS.T181056A1693604.en

Viet, T. V. (2015). Applications of GIS for evaluation the current culture status of Clown knife fish (Chitala ornata) in Phung Hiep District, Hau Giang Province. CTU Journal of Science, 38, 109-115.

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