ZnS nanoparticles persuade alterations in metabolic and hematological aspects in the cyprinid Labeo bata (Hamilton, 1822)

Nilanjana Chatterjee; Baibaswata Bhattacharjee

doi:10.7324/JABB.2018.60202

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Abstract

Due to increased surface photo-oxidation property associated with the nanocrystalline form of ZnS, the dissolved oxygen content in water gets reduced in a dose-dependent manner from their normal values when different concentrations of ZnS nanoparticles (NPs) with various sizes are exposed to the water. Therefore, the animals living in a habitat exposed to ZnS NPs are forced to live in a hypoxic atmosphere. The mechanism of acclimatization to this hypoxic atmosphere by an Indian minor carp Labeo bata, along with its liver morphology, hematological parameters, and metabolic responses are studied systematically. During progressive hypoxia, the liver histomorphology of L. bata shows salient alterations from its normal tissue layout. Furthermore, a significant increase in the number density of red blood corpuscles (RBC) is documented for relatively smaller time (<12 days) of ZnS NP exposure. Under hypoxia condition, hemoglobin and hematocrit concentrations are found to show a characteristic feature showing a peak value for an exposure time of 9 days. Blood glucose and blood lactate levels of L. bata are found to vary in accordance with the varied physiological behavior of the fish under ZnS NP exposure.

Keyword: ZnS nanoparticles Hypoxia Acclimatization Labeo bata.

Citation:

Chatterjee N, Bhattacharjee B. ZnS nanoparticles persuade alterations in metabolic and hematological aspects in the cyprinid Labeo bata (Hamilton, 1822). J App Biol Biotech. 2018;6(2):6-14. DOI: 10.7324/JABB.2018.60202

Copyright: Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike license.

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Reference

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[2]. Brody AL. Nano and food packaging technologies converge. Food Technol. 2006; 60:92-94.
[3]. Karnik BS, Davies SH., Baumann MJ, Masten SJ. Fabrication of catalytic membranes for the treatment of drinking water using combined ozonation and ultrafiltration. Environ Sci Technol. 2005; 39:7656-7661. https://doi.org/10.1021/es0503938
[4]. Carlson CS, Hussain MA, Schrand ML, Braydich-Stolle K, Hess KL, Jones RL. Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B. 2008; 112:13608–13619. https://doi.org/10.1021/jp712087m
[5]. Ispas C, Andreescu D, Patel A, Goia DV, Andreescu S, Wallace KN. Toxicity and developmental defects of different sizes and shape nickel nanoparticles in Zebrafish. Environ Sci Technol. 2009; 43:6349-6356. https://doi.org/10.1021/es9010543
[6]. Mironava T, Hadjiargyrou M, Simon M, Jurukovski V, Rafailovich MH. Gold nanoparticles cellular toxicity and recovery: effect of size, concentration and exposure time. Nanotoxicology. 2010; 4:120–137. https://doi.org/10.3109/17435390903471463
[7]. Pelkmans L, Helenius A. Envocytosis via caveolae. Traffic. 2002; 3:311-320. https://doi.org/10.1034/j.1600-0854.2002.30501.x
[8]. Reiman J, Oberle V, Zuhom IS, Hoekstra D. Size-dependant internalization of particles via the pathways of clathrin- and caveolaemediated endocytosis. Biochem J. 2004; 377:159-169. https://doi.org/10.1042/bj20031253
[9]. Moore MN. Lysosomal cytochemistry in marine environmental monitoring. Histochem J. 1990; 22:187-191. https://doi.org/10.1007/BF02386003
[10]. Adams LK, Lyon DY, Alvarez PJJ. Comparative ecotoxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. Water Research. 2006; 40 (19):3527–3532. https://doi.org/10.1016/j.watres.2006.08.004
[11]. Warheit D, Everitt J. Assessing the biological and environmental risks of nanoparticles. Proceedings of the 43rd Society of Toxicology Annual Meeting, 2004; p. 1850, Baltimore, Md, USA, March 2004.
[12]. Warheit DB, Laurence BR, Reed KL, Roach DH, Reynolds GAM, Webb TR. Comparative pulmonary toxicity assessment of single-wall carbon nanotubes in rats. Toxicological Sciences. 2004; 77 (1):117–125. https://doi.org/10.1093/toxsci/kfg228
[13]. Tong Z, Bischoff M, Nies L, Applegate B, Turco RF. Impact of fullerene (C60) on a soil microbial community. Environmental Science and Technology. 2007; 41(8):2985–2991. https://doi.org/10.1021/es061953l
[14]. Fang JD, Lyon Y, Wiesner MR, Dong J, Alvarez PJJ. Effect of a fullerene water suspension on bacterial phospholipids and membrane phase behaviour. Environmental Science and Technology. 2007; 41(7):2636–2642. https://doi.org/10.1021/es062181w
[15]. Smith, C. J., Shaw, B. J., & Handy, R. D. Toxicity of single walled carbon nanotubes to rainbow trout, (Oncorhynchus mykiss): respiratory toxicity, organ pathologies, and other physiological effects. Aquatic Toxicology. 2007; 82 (2):94–109. https://doi.org/10.1016/j.aquatox.2007.02.003
[16]. OberdÓ§rster E. Manufactured nanomaterials (fullerenes, C60) induce oxidative stress in the brain of juvenile largemouth bass. Environmental Health Perspectives. 2004; 112(10):1058–1062. https://doi.org/10.1289/ehp.7021
[17]. Koziara JM, Lockman PR, Allen DD, Mumper RJ. In situ blood-brain barrier transport of nanoparticles. Pharmaceutical Research, 2003; 20 (11):1772–1778. https://doi.org/10.1023/B:PHAM.0000003374.58641.62
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[19]. Lyon DY, Fortner JD, Sayes CM, Colvin VL, Hughes JB. Bacterial cell association and antimicrobial activity of a C60 water suspension. Environmental Toxicology and Chemistry. 2005; 24(11):2757–2762. https://doi.org/10.1897/04-649R.1
[20]. OberdÓ§rster E, Zhu S, Blickley TM, McClellan-Green P, Haasch ML. Ecotoxicology of carbon-based engineered nanoparticles: effects of fullerene (C60) on aquatic organisms. Carbon. 2006; 44 (6):1112–1120. https://doi.org/10.1016/j.carbon.2005.11.008
[21]. Zhu SQ, OberdÓ§rster E, Haasch ML. Toxicity of an engineered nanoparticle (fullerene, C60) in two aquatic species, Daphnia and fathead minnow. Marine Environmental Research. 2006; 62 (1), S5–S9. https://doi.org/10.1016/j.marenvres.2006.04.059
[22]. Griffitt RJ, Weil R, Hyndman KA. Exposure to copper nanoparticles causes gill injury and acute lethality in zebrafish (Danio rerio). Environmental Science and Technology. 2007; 41(23):8178–8186. https://doi.org/10.1021/es071235e
[23]. Federici G, Shaw BJ, Handy RD. Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects. Aquatic Toxicology. 2007; 84 (4):415–430. https://doi.org/10.1016/j.aquatox.2007.07.009
[24]. Bhattacharjee B, Chatterjee N, Lu, C-H. Harmful impact of ZnS nanoparticles on Daphnia sp. in the western part (districts of Bankura and Purulia) of West Bengal, India. ISRN Nanomaterials. 2013; 2013:Article ID 207239, 7 pages.
[25]. Chatterjee N, Bhattacharjee B, Lu, C–H. Hazardous effect of ZnS nanoparticles on the feeding behaviour, growth and maturation process of the Asian striped catfish, Mystus vittatus (Bloch, 1794). International Aquatic Research. 2014; 6:71-82. https://doi.org/10.1007/s40071-014-0071-9
[26]. Chatterjee N, Bhattacharjee B. Changing physicochemical properties of water due to exposure of ZnS nanoparticles and its detrimental effect on feeding behaviour and liver of a non-air breathing catfish Mystus vittatus. International Journal of Latest Research in Science and Technology. 2014; 3(4):199-204.
[27]. Chatterjee N, Bhattacharjee B. Salient alterations in hepatic and renal histomorphology of an Indian minor carp, Labeo bata (Hamilton, 1822) owing to ZnS nanoparticle induced hypoxia and environmental acidification. The International Journal of Earth & Environmental Sciences. 2015; 1(1):1-9.
[28]. Chatterjee N, Bhattacharjee, B. An analytic contemplation on the conspicuous vicissitudes in the histomorphology of corpuscles of Stannius of a fresh water catfish Mystus tengara (Hamilton, 1822) due to the exposure of ZnS nanoparticles. Scientifica. 2015; 2015: Article ID 697053, 7 pages.
[29]. Chatterjee N, Bhattacharjee B. ZnS nanoparticles affect hazardously the process of oogenesis in the dwarf Asian striped catfish Mystus vittatus (Bloch, 1794). Advanced Science Letters. 2016; 22 (1):126-131. https://doi.org/10.1166/asl.2016.6789
[30]. Chatterjee N, Bhattacharjee B. Revelation of ZnS nanoparticles induce follicular atresia and apoptosis in the ovarian preovulatory follicles in the catfish Mystus tengara (Hamilton, 1822). Scientifica. 2016; 2016: Article ID 3927340, 7 pages.
[31]. Bhattacharjee B, Chatterjee N. Perilous Effect of ZnS Nanoparticles on Testicular cell development and sperm morphology in the Asian striped catfish Mystus vittatus (Bloch, 1794). Advanced Science Letters. 2016; 22 (1):64-70. https://doi.org/10.1166/asl.2016.6787
[32]. Moulder JF, Stickle WF, Sobol PE, Bomren KD. Handbook of X-ray photoelectron spectroscopy, Physical Electronics, Inc., Minnesota, USA; 1995.
[33]. Guang M, Xiao C, Zhang J, Fan S, An R, Cheng Q, Xie J, Zhou M, Ye B, Xie Y. Vacancy Associates Promoting Solar-Driven Photocatalytic Activity of Ultrathin Bismuth Oxychloride Nanosheets. J. Am. Chem. Soc. 2013; 135 (28):10411-10417. https://doi.org/10.1021/ja402956f
[34]. Wang G, Huang B, Li Z, Lou Z, Wang Z, Dai Y, Whangbo M-H. Synthesis and characterization of ZnS with controlled amount of S vacancies for photocatalytic H2 production under visible light. Sci Rep. 2015; 5:8544. DOI: 10.1038/srep08544. https://doi.org/10.1038/srep08544
[35]. Becker WG, Bard A J. Photoluminescence and photoinduced oxygen adsorption of colloidal zinc sulphide dispersions. J Phys Chem. 1983; 87:4888–4893. https://doi.org/10.1021/j150642a026
[36]. Kobayashi A, Kawaji S. Adsorption and surface potential of semi-conductors. Part 1. Photo-enhanced adsorption of oxygen and change of contact potential of ZnS phosphors with illumination. J Phys Soc Jpn. 1955; 10: 270–273. https://doi.org/10.1143/JPSJ.10.270
[37]. Muminov MI, Kim G Ch, Zaitov FA, Kalamozov RU. Some features of the chemisorption of oxygen on semiconductors with different widths of the forbidden band. Dokl Akad Nauk Uzb SSR. 1975; 12:20–21.
[38]. Segner H, MÓ§ller H. Electron microscopical investigations on starvation induced liver pathology in flounders Platichthys flesus. Mar Ecol Prog Ser. 1984; 19:193-196. https://doi.org/10.3354/meps019193
[39]. Svobodova Z, Kroupova H, Modra H, Flajshans M, Randak T, Savina LV, Gela D. Haematological profile of common carp spawners of various breeds. Journal of Applied Ichthyology. 2008; 24:55–59. https://doi.org/10.1111/j.1439-0426.2007.01019.x
[40]. Rambhaskar B, Rao KS. Comparative haematology of ten species of marine fish from Visakhapatnam coast. Journal of Fish Biology. 1987; 30 (1):59–66. https://doi.org/10.1111/j.1095-8649.1987.tb05732.x
[41]. Heath AG, Pritchard AW. Changes in the metabolic rate and blood lactic acid of blue gill sun fish, Lepomis macrochirus following severe muscular activity. Physiological Zoology. 1962; 38: 767–776.
[42]. Brett JR. The metabolic demand for oxygen in fish, particularly salmonids, and a comparison with other vertebrates. Respiratory Physiology. 1972; 14:151–170. https://doi.org/10.1016/0034-5687(72)90025-4
[43]. Puckett KJ, Dill LM. Cost of sustained and burst swimming to juvenile Coho Salmon (Oncorhynchus kisutch). Canadian Journal of Fisheries and Aquatic Science. 1984; 41:1546–1551. https://doi.org/10.1139/f84-192
[44]. Puckett KJ, Dill LM. The energetics of feeding territorially in juvenile coho salmon (Oncorhynchus kisutch). Behaviour, 1985; 92:97–111. https://doi.org/10.1163/156853985X00398
[45]. Kauffman R. Respiratory cost of swimming in larval and juvenile cyprinids. Journal of Experimental Biology. 1990; 150:343–366.
[46]. Goolish EM. Aerobic and anaerobic scaling in fish. Biological Reviews of the Cambridge Philosophical Society. 1991; 66:33–56. https://doi.org/10.1111/j.1469-185X.1991.tb01134.x

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[1]. Aitken RJ, Chaudhry MQ, Boxall ABA, Hull M. Manufacture and use of nanomaterials: current status in the U. K. and global trends. Occup Med. 2006; 56:300-306. https://doi.org/10.1093/occmed/kql051

[2]. Brody AL. Nano and food packaging technologies converge. Food Technol. 2006; 60:92-94.

[3]. Karnik BS, Davies SH., Baumann MJ, Masten SJ. Fabrication of catalytic membranes for the treatment of drinking water using combined ozonation and ultrafiltration. Environ Sci Technol. 2005; 39:7656-7661. https://doi.org/10.1021/es0503938

[4]. Carlson CS, Hussain MA, Schrand ML, Braydich-Stolle K, Hess KL, Jones RL. Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B. 2008; 112:13608–13619. https://doi.org/10.1021/jp712087m

[5]. Ispas C, Andreescu D, Patel A, Goia DV, Andreescu S, Wallace KN. Toxicity and developmental defects of different sizes and shape nickel nanoparticles in Zebrafish. Environ Sci Technol. 2009; 43:6349-6356. https://doi.org/10.1021/es9010543

[6]. Mironava T, Hadjiargyrou M, Simon M, Jurukovski V, Rafailovich MH. Gold nanoparticles cellular toxicity and recovery: effect of size, concentration and exposure time. Nanotoxicology. 2010; 4:120–137. https://doi.org/10.3109/17435390903471463

[7]. Pelkmans L, Helenius A. Envocytosis via caveolae. Traffic. 2002; 3:311-320. https://doi.org/10.1034/j.1600-0854.2002.30501.x

[8]. Reiman J, Oberle V, Zuhom IS, Hoekstra D. Size-dependant internalization of particles via the pathways of clathrin- and caveolaemediated endocytosis. Biochem J. 2004; 377:159-169. https://doi.org/10.1042/bj20031253

[9]. Moore MN. Lysosomal cytochemistry in marine environmental monitoring. Histochem J. 1990; 22:187-191. https://doi.org/10.1007/BF02386003

[10]. Adams LK, Lyon DY, Alvarez PJJ. Comparative ecotoxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. Water Research. 2006; 40 (19):3527–3532. https://doi.org/10.1016/j.watres.2006.08.004

[11]. Warheit D, Everitt J. Assessing the biological and environmental risks of nanoparticles. Proceedings of the 43rd Society of Toxicology Annual Meeting, 2004; p. 1850, Baltimore, Md, USA, March 2004.

[12]. Warheit DB, Laurence BR, Reed KL, Roach DH, Reynolds GAM, Webb TR. Comparative pulmonary toxicity assessment of single-wall carbon nanotubes in rats. Toxicological Sciences. 2004; 77 (1):117–125. https://doi.org/10.1093/toxsci/kfg228

[13]. Tong Z, Bischoff M, Nies L, Applegate B, Turco RF. Impact of fullerene (C60) on a soil microbial community. Environmental Science and Technology. 2007; 41(8):2985–2991. https://doi.org/10.1021/es061953l

[14]. Fang JD, Lyon Y, Wiesner MR, Dong J, Alvarez PJJ. Effect of a fullerene water suspension on bacterial phospholipids and membrane phase behaviour. Environmental Science and Technology. 2007; 41(7):2636–2642. https://doi.org/10.1021/es062181w

[15]. Smith, C. J., Shaw, B. J., & Handy, R. D. Toxicity of single walled carbon nanotubes to rainbow trout, (Oncorhynchus mykiss): respiratory toxicity, organ pathologies, and other physiological effects. Aquatic Toxicology. 2007; 82 (2):94–109. https://doi.org/10.1016/j.aquatox.2007.02.003

[16]. OberdÓ§rster E. Manufactured nanomaterials (fullerenes, C60) induce oxidative stress in the brain of juvenile largemouth bass. Environmental Health Perspectives. 2004; 112(10):1058–1062. https://doi.org/10.1289/ehp.7021

[17]. Koziara JM, Lockman PR, Allen DD, Mumper RJ. In situ blood-brain barrier transport of nanoparticles. Pharmaceutical Research, 2003; 20 (11):1772–1778. https://doi.org/10.1023/B:PHAM.0000003374.58641.62

[18]. Lyon DY, Adams LK, Falkner JC, Alvarez, PJJ. Antibacterial activity of fullerene water suspensions: effects of preparation method and particle size. Environmental Science and Technology. 2006; 40 (14):4360–4366. https://doi.org/10.1021/es0603655

[19]. Lyon DY, Fortner JD, Sayes CM, Colvin VL, Hughes JB. Bacterial cell association and antimicrobial activity of a C60 water suspension. Environmental Toxicology and Chemistry. 2005; 24(11):2757–2762. https://doi.org/10.1897/04-649R.1

[20]. OberdÓ§rster E, Zhu S, Blickley TM, McClellan-Green P, Haasch ML. Ecotoxicology of carbon-based engineered nanoparticles: effects of fullerene (C60) on aquatic organisms. Carbon. 2006; 44 (6):1112–1120. https://doi.org/10.1016/j.carbon.2005.11.008

[21]. Zhu SQ, OberdÓ§rster E, Haasch ML. Toxicity of an engineered nanoparticle (fullerene, C60) in two aquatic species, Daphnia and fathead minnow. Marine Environmental Research. 2006; 62 (1), S5–S9. https://doi.org/10.1016/j.marenvres.2006.04.059

[22]. Griffitt RJ, Weil R, Hyndman KA. Exposure to copper nanoparticles causes gill injury and acute lethality in zebrafish (Danio rerio). Environmental Science and Technology. 2007; 41(23):8178–8186. https://doi.org/10.1021/es071235e

[23]. Federici G, Shaw BJ, Handy RD. Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects. Aquatic Toxicology. 2007; 84 (4):415–430. https://doi.org/10.1016/j.aquatox.2007.07.009

[24]. Bhattacharjee B, Chatterjee N, Lu, C-H. Harmful impact of ZnS nanoparticles on Daphnia sp. in the western part (districts of Bankura and Purulia) of West Bengal, India. ISRN Nanomaterials. 2013; 2013:Article ID 207239, 7 pages.

[25]. Chatterjee N, Bhattacharjee B, Lu, C–H. Hazardous effect of ZnS nanoparticles on the feeding behaviour, growth and maturation process of the Asian striped catfish, Mystus vittatus (Bloch, 1794). International Aquatic Research. 2014; 6:71-82. https://doi.org/10.1007/s40071-014-0071-9

[26]. Chatterjee N, Bhattacharjee B. Changing physicochemical properties of water due to exposure of ZnS nanoparticles and its detrimental effect on feeding behaviour and liver of a non-air breathing catfish Mystus vittatus. International Journal of Latest Research in Science and Technology. 2014; 3(4):199-204.

[27]. Chatterjee N, Bhattacharjee B. Salient alterations in hepatic and renal histomorphology of an Indian minor carp, Labeo bata (Hamilton, 1822) owing to ZnS nanoparticle induced hypoxia and environmental acidification. The International Journal of Earth & Environmental Sciences. 2015; 1(1):1-9.

[28]. Chatterjee N, Bhattacharjee, B. An analytic contemplation on the conspicuous vicissitudes in the histomorphology of corpuscles of Stannius of a fresh water catfish Mystus tengara (Hamilton, 1822) due to the exposure of ZnS nanoparticles. Scientifica. 2015; 2015: Article ID 697053, 7 pages.

[29]. Chatterjee N, Bhattacharjee B. ZnS nanoparticles affect hazardously the process of oogenesis in the dwarf Asian striped catfish Mystus vittatus (Bloch, 1794). Advanced Science Letters. 2016; 22 (1):126-131. https://doi.org/10.1166/asl.2016.6789

[30]. Chatterjee N, Bhattacharjee B. Revelation of ZnS nanoparticles induce follicular atresia and apoptosis in the ovarian preovulatory follicles in the catfish Mystus tengara (Hamilton, 1822). Scientifica. 2016; 2016: Article ID 3927340, 7 pages.

[31]. Bhattacharjee B, Chatterjee N. Perilous Effect of ZnS Nanoparticles on Testicular cell development and sperm morphology in the Asian striped catfish Mystus vittatus (Bloch, 1794). Advanced Science Letters. 2016; 22 (1):64-70. https://doi.org/10.1166/asl.2016.6787

[32]. Moulder JF, Stickle WF, Sobol PE, Bomren KD. Handbook of X-ray photoelectron spectroscopy, Physical Electronics, Inc., Minnesota, USA; 1995.

[33]. Guang M, Xiao C, Zhang J, Fan S, An R, Cheng Q, Xie J, Zhou M, Ye B, Xie Y. Vacancy Associates Promoting Solar-Driven Photocatalytic Activity of Ultrathin Bismuth Oxychloride Nanosheets. J. Am. Chem. Soc. 2013; 135 (28):10411-10417. https://doi.org/10.1021/ja402956f

[34]. Wang G, Huang B, Li Z, Lou Z, Wang Z, Dai Y, Whangbo M-H. Synthesis and characterization of ZnS with controlled amount of S vacancies for photocatalytic H2 production under visible light. Sci Rep. 2015; 5:8544. DOI: 10.1038/srep08544. https://doi.org/10.1038/srep08544

[35]. Becker WG, Bard A J. Photoluminescence and photoinduced oxygen adsorption of colloidal zinc sulphide dispersions. J Phys Chem. 1983; 87:4888–4893. https://doi.org/10.1021/j150642a026

[36]. Kobayashi A, Kawaji S. Adsorption and surface potential of semi-conductors. Part 1. Photo-enhanced adsorption of oxygen and change of contact potential of ZnS phosphors with illumination. J Phys Soc Jpn. 1955; 10: 270–273. https://doi.org/10.1143/JPSJ.10.270

[37]. Muminov MI, Kim G Ch, Zaitov FA, Kalamozov RU. Some features of the chemisorption of oxygen on semiconductors with different widths of the forbidden band. Dokl Akad Nauk Uzb SSR. 1975; 12:20–21.

[38]. Segner H, MÓ§ller H. Electron microscopical investigations on starvation induced liver pathology in flounders Platichthys flesus. Mar Ecol Prog Ser. 1984; 19:193-196. https://doi.org/10.3354/meps019193

[39]. Svobodova Z, Kroupova H, Modra H, Flajshans M, Randak T, Savina LV, Gela D. Haematological profile of common carp spawners of various breeds. Journal of Applied Ichthyology. 2008; 24:55–59. https://doi.org/10.1111/j.1439-0426.2007.01019.x

[40]. Rambhaskar B, Rao KS. Comparative haematology of ten species of marine fish from Visakhapatnam coast. Journal of Fish Biology. 1987; 30 (1):59–66. https://doi.org/10.1111/j.1095-8649.1987.tb05732.x

[41]. Heath AG, Pritchard AW. Changes in the metabolic rate and blood lactic acid of blue gill sun fish, Lepomis macrochirus following severe muscular activity. Physiological Zoology. 1962; 38: 767–776.

[42]. Brett JR. The metabolic demand for oxygen in fish, particularly salmonids, and a comparison with other vertebrates. Respiratory Physiology. 1972; 14:151–170. https://doi.org/10.1016/0034-5687(72)90025-4

[43]. Puckett KJ, Dill LM. Cost of sustained and burst swimming to juvenile Coho Salmon (Oncorhynchus kisutch). Canadian Journal of Fisheries and Aquatic Science. 1984; 41:1546–1551. https://doi.org/10.1139/f84-192

[44]. Puckett KJ, Dill LM. The energetics of feeding territorially in juvenile coho salmon (Oncorhynchus kisutch). Behaviour, 1985; 92:97–111. https://doi.org/10.1163/156853985X00398

[45]. Kauffman R. Respiratory cost of swimming in larval and juvenile cyprinids. Journal of Experimental Biology. 1990; 150:343–366.

[46]. Goolish EM. Aerobic and anaerobic scaling in fish. Biological Reviews of the Cambridge Philosophical Society. 1991; 66:33–56. https://doi.org/10.1111/j.1469-185X.1991.tb01134.x