Abstract
This study aimed to analyze the cold stress effects (in terms of hematology, energy reserves, and oxidative stress) in Piaractus mesopotamicus (pacú) and their mitigation by a Pyropia columbina red seaweed-supplemented diet. For this purpose, juvenile fish were fed with a control (CD) or a red seaweed-supplemented diet (RD) for 60 days, and then, the animals were exposed to a low temperature (14 °C) and a control temperature (24 °C) for 24 h. The cold shock generated an increase of hemoglobin levels in fish fed with both diets. In CD-fed fish, plasmatic triglycerides, cholesterol, and hepatic glycogen decreased after the thermal shock; meanwhile, the animals fed with RD showed decreased hepatic proteins, but increased cholesterol and hepatic glycogen. Regarding oxidative stress, antioxidant enzymes augmented their activity in the liver, intestine, and gills; meanwhile, lipid oxidative damage was observed in the liver and intestine of fish exposed to 14 °C and fed with both diets. Pacú was sensitive to cold shock, but no mitigation effects were observed in fish fed with the supplemented diet. Further research should target higher concentrations of P. columbina in supplemented diets to take advantage of this valuable resource.
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References
Ahmad SM, Shah FA, Bhat FA, Bhat JIA, Balkhi MH (2011) Thermal adaptability and disease association in common carp (Cyprinus carpio communis) acclimated to different (four) temperatures. J Therm Biol 36(8):492–497. https://doi.org/10.1016/j.jtherbio.2011.08.007
Bacchetta C, Rossi A, Ale A, Campana M, Parma MJ, Cazenave J (2014) Combined toxicological effects of pesticides: a fish multi-biomarker approach. Ecol Indic 36:532–538. https://doi.org/10.1016/j.ecolind.2013.09.016
Bacchetta C, Ale A, Rossi A, Karakachoff M, Cazenave J (2020) Effects of cold stress on juvenile Piaractus mesopotamicus and the mitigation by β-carotene. J Therm Biol 88:102497. https://doi.org/10.1016/j.jtherbio.2019.102497
Barbieri E (2009a) Effects of zinc and cadmium on oxygen consumption and ammonium excretion in pink shrimp (Farfantepenaeus paulensis, Pérez-Farfante, 1967, Crustacea). Ecotoxicology 18:312–318. https://doi.org/10.1007/s10646-008-0285-y
Barbieri E (2009b) Effect of 2, 4-D herbicide (2, 4-dichlorophenoxyacetic acid) on oxygen consumption and ammonium excretion of juveniles of Geophagus brasiliensis (Quoy & Gaimard, 1824) (Osteichthyes, Cichlidae). Ecotoxicology 18:55–60. https://doi.org/10.1007/s10646-008-0256-3
Barbieri E, Vigliar Bondioli AC (2013) Acute toxicity of ammonia in Pacu fish (Piaractus mesopotamicus, Holmberg, 1887) at different temperature levels. Aquac Res 46:1–7. https://doi.org/10.1111/are.12203
Beutler E (1982) Catalase. In: Beutler E (ed) Red cell metabolism, a manual of biochemical methods. Grune and Stratton Inc., New York, pp 105–106
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Burtin P (2003) Nutritional value of seaweeds. Elec J Env Agricult Food Chem Title 2:498–503
Castillo J, Castellana B, Acerete L, Planas JV, Goetz FW, Mackenzie S, Tort L (2008) Stress-induced regulation of steroidogenic acute regulatory protein expression in head kidney of Gilthead seabream (Sparus aurata). J Endocrinol 196:313–322. https://doi.org/10.1677/JOE-07-0440
Castro C, Pérez-Jiménez A, Guerreiro I, Peres H, Castro-Cunha M, Oliva-Teles A (2012) Effects of temperature and dietary protein level on hepatic oxidative status of Senegalese sole juveniles (Solea senegalensis). Comp Biochem Physiol B 163:372–378. https://doi.org/10.1016/j.cbpa.2012.07.003
Cazenave J, Wunderlin DA, Hued A, Bistoni MA (2005) Hematological characterization of a Neotropical fish, Corydoras paleatus (Pisces, Callichthyidae), captured from pristine and polluted water. Hydrobiologia 537:25–33
Chatzifotis S, Panagiotidou M, Papaioannou N (2010) Effect of dietary lipid levels on growth, feed utilization, body composition and serum metabolites of meager (Argyrosomus regius) juveniles. Aquaculture 307:65–70. https://doi.org/10.1016/j.aquaculture.2010.07.002
Cheng C-H, Guo Z-X, Wang A-L (2018) The protective effects of taurine on oxidative stress, cytoplasmic free-Ca2+ and apoptosis of pufferfish (Takifugu obscurus) under low temperature stress. Fish Shellfish Immunol 77:457–464. https://doi.org/10.1016/j.fsi.2018.04.022
Cian RE, Fajardo MA, Alaiz M, Vioque J, González RJ, Silvina R, Drago SR (2014) Chemical composition, nutritional and antioxidant properties of the red edible seaweed Porphyra columbina. Int J Food Sci Nutr 65(3):299–305. https://doi.org/10.3109/09637486.2013.854746
Cian RE, Garzón AG, Betancur Ancona D, Chel Guerrero L, Drago SR (2016) Chelating properties of peptides from red seaweed Pyropia columbina and its effect on iron bio-accessibility. Plant Foods Hum Nutr 71:96–101. https://doi.org/10.1007/s11130-016-0533-x
Cian RE, Bacchetta C, Rossi A, Cazenave J, Drago SR (2019) Red seaweed Pyropia columbina as antioxidant supplement in feed for cultured juvenile Pacú (Piaractus mesopotamicus). J Appl Phycol 31:1455–1465. https://doi.org/10.1007/s10811-018-1648-2
Claudiano GS, Yunis-Aguinaga J, Marinho-Neto FA, Miranda RL, Martins IM, Otani FS, Mundim AV, Marzocchi-Machado CM, Moraes JRE (2019) Hematological and immune changes in Piaractus mesopotamicus in the sepsis induced by Aeromonas hydrophila. Fish Shellfish Immunol 88:259–265. https://doi.org/10.1016/j.fsi.2019.01.044
CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas) (2005) Marco Ético de Referencia para las Investigaciones Biomédicas en Animales de laboratorio, de granja y obtenidos de la naturaleza, Buenos Aires, Argentina. Retrieved from www.conicet.gov.ar/wp-content/uploads/OCR-RD-20050701-1047.pdf
Donaldson MR, Cooke SJ, Patterson DA, MacDonald JS (2008) Cold shock and fish. J Fish Biol 73:1491–1530
Folch J, Sloane L, Stanley G (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509
Gasco L, Gai F, Maricchiolo G, Genovese L, Ragonese S, Bottari T, Caruso G (2018) Chapter 4: supplementation of vitamins, minerals, enzymes and antioxidant in fish feeds. In: Feeds for the aquaculture sector. Springer Briefs in Molecular Science. Springer, Cham. doi: https://doi.org/10.1007/978-3-319-77941-6_4
Geslin M, Benoit Auperin B (2004) Relationship between changes in mRNAs of the genes encoding steroidogenic acute regulatory protein and P450 cholesterol side chain cleavage in head kidney and plasma levels of cortisol in response to different kinds of acute stress in the rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 135:70–80
Goda AA, Sallam AE, Srour TM (2018) Evaluation of natural and synthetic carotenoid supplementation on growth, survival, total carotenoid content, fatty acids profile and stress resistance of European seabass, Dicentrarchus labrax, Fry. Aquac Stud 18(1):27–39. https://doi.org/10.4194/2618-6381-v18_1_04
Greene D, Selivonchick D (1987) Lipid metabolism in fish. Prog Lipid Res 26:53–85
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first step in mercapturic acid formation. J Biol Chem 249:7130–7139
Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine, 3rd ed., Oxford. University Press, Oxford, p. 936. In: The toxicology of fishes (Eds. Di Giulio RT y Hinton DE). 2008. CRC Press, Boca Raton, 273-326
Hassaan MS, El-Sayed AIM, Soltan MA, Iraqi MM, Goda AM, Davies SJ, El-Haroun ER, Ramadan HA (2019) Partial dietary fish meal replacement with cotton seed meal and supplementation with exogenous protease alters growth, feed performance, hematological indices and associated gene expression markers (GH, IGF-I) for Nile tilapia, Oreochromis niloticus. Aquaculture 503:282–292. https://doi.org/10.1016/j.aquaculture.2019.01.009
Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57:19–42
Hoseini SM, Yousefi M, Seyed Hoseinifar SH, Van Doan H (2019) Antioxidant, enzymatic and hematological responses of common carp (Cyprinus carpio) fed with myrcene- or menthol supplemented diets and exposed to ambient ammonia. Aquaculture 506:246–255. https://doi.org/10.1016/j.aquaculture.2019.03.048
Houston AH (1990) Blood and circulation. In: Schreck CB, Moyle PB (eds) Methods for fish biology. American Fisheries Society, Bethesda
Ibarz A, Martín-Pérez M, Blasco J, Bellido D, de Oliveira E, Jaume Fernández-Borras J (2010) Gilthead sea bream liver proteome altered at low temperatures by oxidative stress. Proteomics 10:963–975. https://doi.org/10.1002/pmic.200900528
Jager T, Barsi A, Hamda NT, Martin BT, Zimmer EI, Ducrot V (2014) Dynamic energy budgets in population ecotoxicology: applications and outlook. Ecol Model 280:140–147. https://doi.org/10.1016/j.ecolmodel.2013.06.024
Joy S, Alikunju AP, Jose J, Sudha HSH, Parambath PM, Puthiyedathu ST, Philip B (2017) Oxidative stress and antioxidant defense responses of Etroplus suratensis to acute temperature fluctuations. J Therm Biol 70:20–26. https://doi.org/10.1016/j.jtherbio.2017.10.010
Lermen CL, Lappe R, Crestani M, Vieira VP, Gioda CR, Schetinger MRC, Baldisserotto B, Moraes G, Morsch VM (2004) Effect of different temperature regimes on metabolic and blood parameters of silver catfish Rhamdia quelen. Aquaculture 239:497–507. https://doi.org/10.1016/j.aquaculture.2004.06.021
Logan M (2010) Biostatistical design and analysis using R: a practical guide. John Wiley and Sons
Lowry OH, Rosebrough MJ, Far AL, Randall RL (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Miller WL (1988) Molecular biology of steroid hormone synthesis. Endocr Rev 9:295–318
Milstein A, Zoran M, Peretz Y, Joseph D (2000) Low temperature tolerance of Pacu, Piaractus mesopotamicus. Environ Biol Fish 58:455–460
Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247(10):3170–3175
Muñoz LI, Wacyk J, Claudio Perez C, Carrasco J, Cortez-San Martin M (2018) Diets enriched in red seaweed (Pyropia columbina and Gracilaria chilensis) cryo concentrates modulate the immune-relevant gene encoding the Mx antiviral protein in salmon (Salmo salar) white blood cells. J Appl Phycol 31(2):1415–1424. https://doi.org/10.1007/s10811-018-1595-y
Nakagawa H (1997) Effect of dietary alga on improvement of lipid metabolisms in fish. Biomed Parmacother 51:345–348
Ngo D-H, Wijesekara I, Vo T-S, Ta QV, Kim S-K (2011) Marine food derived functional ingredients as potential antioxidants in the food industry: an overview. Food Res Int 44:523–529. https://doi.org/10.1016/j.foodres.2010.12.030
Nobrega RO, Batista RO, Corrêa CF, Mattioni B, Filer K, Pettigrew JE, Fracalossi DM (2019) Dietary supplementation of Aurantiochytrium sp. meal, a docosahexaenoic-acid source, promotes growth of Nile tilapia at a suboptimal low temperature. Aquaculture 507:500–509. https://doi.org/10.1016/j.aquaculture.2019.04.030
Panase P, Saenphet S, Saenphet K (2018) Biochemical and physiological responses of Nile tilapia Oreochromis niloticus Lin subjected to cold shock of water temperature. Aquac Rep 11:17–23. https://doi.org/10.1016/j.aqrep.2018.05.005
Parma de Croux MJ (1990) Benzocaine (ethyl-p-aminobenzoate) as an anaesthetic for Prochilodus lineatus, Valenciennes (Pisces, Curimatidae). J Appl Ichthyol 6:189–192. https://doi.org/10.1111/j.1439-0426.1990.tb00578.x
Pavlović SZ, Borković Mitić SS, Radovanović TB, Perendija BR, Despotović SG, Gavrić JP, Saičić ZS (2010) Seasonal variations of the activity of antioxidant defense enzymes in the Red mullet (Mullus barbatus l.) from the Adriatic Sea. Mar Drugs 8:413–428. https://doi.org/10.3390/md8030413
Pinto D, Pellegrin L, Fiori Nitz LF, da Costa ST, Monserrat JM, Garcia L (2019) Haematological and oxidative stress responses in Piaractus mesopotamicus under temperature variations in water. Aquac Res 00:1–11. https://doi.org/10.1111/are.14260
Reichenbach-Klinke HH (1980) Enfermedades de los peces. Acribia, Zaragoza
Rossi A, Bacchetta C, Cazenave J (2017) Effect of thermal stress on metabolic and oxidative stress biomarkers of Hoplosternum littorale (Teleostei, Callichthyidae). Ecol Indic 79:361–370. https://doi.org/10.1016/j.ecolind.2017.04.042
Rotllant J, Balm PH, Perez-Sanchez J, Wendelaar-Bonga SE, Tort L (2001) Pituitary and interrenal function in gilthead seabream (Sparus aurata L., Teleostei) after handling and confinement stress. Gen Comp Endocrinol 121:333–342. https://doi.org/10.1111/are.14260
Schlenk D, Handy R, Steinert S, Depledge MH, Benson W (2008) Biomarkers. In: The toxicology of fishes (Ed. Di Giulio RT, Hinton DE). CRC Press, Boca, 683-731 pp
Seifter S, Dayton S, Novic B, Montwyler E (1950) The estimation of glycogen with the anthrone reagent. Arch Biochem 25:191–200
Sørensen LE, Jeppesen PB, Christiansen CB, Hermansen K, Gregersen S (2019) Nordic seaweed and diabetes prevention: exploratory studies in KK-Ay mice. Nutrients 11(6):1435. https://doi.org/10.3390/nu11061435
Sotoudeh E, Mardani F (2017) Antioxidant-related parameters, digestive enzyme activity and intestinal morphology in rainbow trout (Oncorhynchus mykiss) fry fed graded levels of red seaweed, Gracilaria pygmaea. Aquac Nutr 24(2):1–7. https://doi.org/10.1111/anu.12606
Sun Z, Tan X, Liu Q, Ye H, Zou C, Xu M, Zhang Y, Ye C (2019) Physiological, immune responses and liver lipid metabolism of orange-spotted grouper (Epinephelus coioides) under cold stress. Aquaculture 498:545–555. https://doi.org/10.1016/j.aquaculture.2018.08.051
Tanaka K, Sano T, Ishizuka K, Kitta K, Kawamura Y (1994) Comparison of properties of leaf and root glutathione reductases from spinach. Physiol Plant 91:353–358. https://doi.org/10.1111/j.1399-3054.1994.tb02960.x
Teimouri M, Yeganeh S, Rahimi Mianji G, Najafi M, Mahjoub S (2019) The effect of Spirulina platensis meal on antioxidant gene expression, total antioxidant capacity, and lipid peroxidation of rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 45(3):977–986. https://doi.org/10.1007/s10695-019-0608-3
Turchini GM, Ng W-K, Tocher DR (2010) Fish oil replacement and alternative lipid sources in aquaculture feeds. 1st ed. Boca Raton, Taylor & Francis Group, CRC Press
Viant MR, Werner I, Rosenblum ES, Gantner AS, Tjeerdema RS, Johnson ML (2003) Correlation between heat-shock protein induction and reduced metabolic condition in juvenile steelhead trout (Oncorhynchus mykiss) chronically exposed to elevated temperature. Fish Physiol Biochem 29:159–171. https://doi.org/10.1023/B:FISH.0000035938.92027.81
Wang X, Wang L, Yao C, Qiu L, Zhang H, Zhi Z, Song L (2012) Alternation of immune parameters and cellular energy allocation of Chlamys farreri under ammonia-N exposure and Vibrio anguillarum challenge. Fish Shellfish Immunol 32(5):741–749. https://doi.org/10.1016/j.fsi.2012.01.025
Wang C, Hu W, Wang L, Qiao H, Wu H, Xu Z (2019) Effects of dietary supplementation with Sargassum horneri meal on growth performance, body composition, and immune response of juvenile turbot. J Appl Phycol 31(1):771–778. https://doi.org/10.1007/s10811-018-1590-3
Weiss RF (1970) The solubility of nitrogen, oxygen and argon in water and seawater. Deep-Sea Res Oceanogr Abstr 17:721–735
Wen B, Jin S-R, Chen Z-Z, Gao J-Z, Wang L, Liu Y, Liu H-P (2017) Plasticity of energy reserves and metabolic performance of discus fish (Symphysodon aequifasciatus) exposed to low-temperature stress. Aquaculture 481:169–176. https://doi.org/10.1016/j.aquaculture.2017.09.002
Wu SM, Liu J-H, Shu L-H, Chen CH (2015) Anti-oxidative responses of zebrafish (Danio rerio) gill, liver and brain tissues upon acute cold shock. Comp Biochem Phys A 187:202–213. https://doi.org/10.1016/j.cbpa.2015.05.016
Yagi K (1976) A simple fluorometric assay for lipoperoxide in blood plasma. Biochem Med 15(2):212–216. https://doi.org/10.1016/0006-2944(76)90049-1
Yoshinaga K, Nakai Y, Izumi H, Nagaosa K, Ishijima T, Nakano T, Abe K (2018) Oral administration of edible seaweed Undaria pinnatifida (Wakame) modifies glucose and lipid metabolism in rats: a DNA microarray analysis. Mol Nutr Food Res 62(12):e1700828. https://doi.org/10.1002/mnfr.201700828
Acknowledgements
Authors are thankful to the Área de Cereales y Oleaginosas of the Instituto de Tecnología de Alimentos (FIQ-UNL) for providing the control and supplemented extruded feed.
Funding
This work was supported by grants from Agencia Nacional de Promoción Científica y Tecnológica (PICT-2016 1911), Consejo Nacional de Investigaciones Científicas y Técnicas (PIP- 112 201501 00942 CO), and Universidad Nacional del Litoral (CAI+D 2016-50420150100016LI).
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AA: data curation, formal analysis, methodology, visualization, writing—original draft, writing—review and editing.
CB: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, project administration, resources, supervision, validation, visualization, writing—original draft, writing—review and editing.
AR: data curation, formal analysis, funding acquisition, project administration, investigation, methodology, supervision, validation, visualization.
PS: data curation, formal analysis, methodology, visualization, writing—review and editing.
JC: conceptualization, funding acquisition, investigation, methodology, project administration, resources, supervision, validation, visualization, writing—review and editing.
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Ale, A., Bacchetta, C., Rossi, A.S. et al. Low temperature stress in a cultured fish (Piaractus mesopotamicus) fed with Pyropia columbina red seaweed-supplemented diet. Fish Physiol Biochem 47, 829–839 (2021). https://doi.org/10.1007/s10695-021-00944-7
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DOI: https://doi.org/10.1007/s10695-021-00944-7