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ANIMAL SCIENCE • An. Acad. Bras. Ciênc. 97 (1) • 2025 • https://doi.org/10.1590/0001-3765202520240645 linkcopy

Open-access Physiological and oxidative responses of Colossoma macropomum and hybrid ♀ C. macropomum × ♂ Piaractus brachypomus subjected to different stressors in a recirculating aquaculture system (RAS)

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Abstract

The effects of acute handling stress on the physiological and antioxidant responses of tambaqui (Colossoma macropomum) and the hybrid tambatinga (C. macropomum × Piaractus brachypomus) raised in a recirculating aquaculture system were investigated. Thirty juveniles of tambaqui (27.8 ± 2.8 g) and thirty of tambatinga (26.2 ± 3.1 g) were used. Six fish/group were captured and subjected to the sample to determine basal parameters. The remaining animals were chased with hand net for 3 minutes, exposed to air for 2 minutes and subjected to biometry. Blood and oxidative parameters were determined immediately after stress (IAE) and after 1h (1hAE), 24h (24hAE) and 48h (48hAE). Stress caused an increase in the hematocrit of tambaqui at IAE, with reduction after 48hAE. For glycemia, there were differences between the fish groups and collections with higher values for tambatinga and after IAE and 1hAE. Cholesterol in tambaqui increased after 24hAE and 48hAE, decreasing in hybrid after 24hAE with return to basal after 48hAE. SOD increased in IAE while in tambaqui the response only occurred after 48hAE, resulting in an increase in lipid peroxidation. Conclude that biometric management resulted in hemodilution in tambatinga, without recovery of basal parameters. However, the antioxidant system prevented lipid peroxidation.

Key words
antioxidant enzymes; biometric procedure; freshwater fish; hybridization; reactive oxygen species

INTRODUCTION

Handling, classification and transportation are some of the routine practices of an aquaculture enterprise. Furthermore, monitoring zootechnical performance and animal health by biometric management is essential for maintaining production cycle efficiency (Almansa et al. 2015, Hasan et al. 2021, Tonachella et al. 2022). However, during its execution, animals are inevitably chased, captured, crowded and exposed to air (Abreu et al. 2009, Pereira-da-Silva & Oliveira 2017). These factors can represent a condition of acute stress and negatively affect animal growth (Urbinati & Carneiro 2004) and health (Sun et al. 2017) if carried out incorrectly.

Fish receive exposure to these stressful stimuli externally via sensory organs, followed by internal signaling through the action of the hypothalamus (Guo & Dixon 2021). Thus, in response to stress, the organism allows a neuroendocrine action of the hypothalamic-pituitary-interrenal (HPI) axis, which culminates in the secretion of cortisol in interrenal cells and the release of catecholamines (adrenaline and noradrenaline) in chromaffin cells located in the cephalic portion of the kidney (Tort 2011). After secretion into the bloodstream, these hormones are responsible for causing several changes in serum levels of hematological (Pagées et al. 1995, Castro et al. 2018), metabolic (Dias et al. 2023, Philippe et al. 2023), immunological (Dias et al. 2020) and osmoregulatory (Breves et al. 2010, Young et al. 2019) parameters.

Cellular respiration occurs primarily in the mitochondria (Biller-Takahashi et al. 2015), resulting in the production of reactive oxygen species (ROS). In response, fish have developed a complex antioxidant system composed of the enzymes superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx), glutathione reductase (GR), and glutathione S-transferase (GST), which work to eliminate the excess ROS produced during cellular respiration (Halliwell & Gutteridge 2015). However, activities that involve animal handling can also cause a transient or chronic imbalance to the antioxidant defense system, resulting in a condition known as oxidative stress (Sanchez-Muros et al. 2013, Castro et al. 2018, Monteiro et al. 2021). In such situations, the antioxidant defense system is not able to eliminate excess ROS, resulting in functional impairment of carbohydrates, proteins, lipids and nucleic acids (Jones 2006, Nimse & Pal 2015, Cadet & Davies 2017). Furthermore, oxidative stress can adversely affect zootechnical performance (Menon et al. 2023) and fish survival (Lu et al. 2019) during the production cycle. Therefore, the quantification of oxidative stress biomarkers becomes essential, with carbonyl proteins often used as indicators of protein degradation (Kantserova et al. 2022), while the quantification of thiobarbituric acid reactive substances (TBARS) used to determine the level of lipid peroxidation (Pinto et al. 2022).

Tambaqui, Colossoma macropomum (Cuvier 1818), is a freshwater fish of the family Characidade (order Characiformes), and the main fish species produced in some South American countries (Valladão et al. 2018). Tambaqui and its hybrids have also been introduced for aquaculture purposes in the United States, Mexico, China, Thailand and the Philippines (Amanajás et al. 2018, Hilsdorf et al. 2021). Tambatinga is a hybrid produced by crossing ♀ tambaqui (C. macropomum) and ♂ pirapitinga (P. brachypomus). Hybridization of these genera is generally performed to explore supposed heterosis for performance and carcass quality (Costa et al. 2019, 2020). However, hybridization can also result in different patterns of metabolic and biochemical responses linked to stress (Yang et al. 2021).

Therefore, in view of the above, this study aimed to investigate the effects of acute handling stress on the hematological, biochemical and antioxidant defense responses of juvenile tambaqui (C. macropomum) and juvenile tambatinga (♀ C. macropomum × ♂ P. brachypomus).

MATERIALS AND METHODS

Animals and conditions

The experimental procedures were conducted in accordance with the standards of the Comissão de Ética no Uso de Animais (protocol 25/2023, CEUA) at the facilities of the Laboratório de Aquacultura (LAQUA) of the Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Brazil.

Thirty juveniles of tambaqui (27.82 ± 2.83 g and 12.05 ± 0.81 cm) and thirty juveniles of tambatinga (26.27 ± 3.14 g and 11.83 ± 0.94 cm), were randomly distributed in 10 circular 28 L-1 tanks (density of 6 fish/tank; 5 tanks per fish group) in a recirculating aquaculture system with supplementary aeration.

The animals were acclimatized to experimental conditions for 14 days, with a photoperiod of 12L:12D (Key West DNI group, digital timer), water temperature of 27.20 ± 0.62 °C, salinity of 0.40 ± 0.10 g of salt L-1 and electrical conductivity of 0.81 ± 0.20 mS cm-1, all measured performed three times a week using multiparameter probe (Hanna Instruments HI98130, Hanna®, Barueri, SP, Brazil). Dissolved oxygen was maintained at 6.69 ± 0.41 mg L-1 (YSI, EcoSense® DO200A (Yellow Springs Instrument Co. Inc., Yellow Springs, OH, USA) and total ammonia below 0.5 mg L-1 (LabconTest, Alcon®, Camboriú, SC, Brazil) all measured performed two times a week. The animals were fed to apparent satiety twice a day (09:00 and 16:00) during this period, using an extruded commercial diet (Aquos Starter 2-3 mm, Descalvado, São Paulo, Brazil) containing 45% crude protein, 4% crude fiber, 15% maximum mineral matter, 8% and maximum ether extract, 2% minimum calcium, 0.8% minimum phosphorus).

Experimental protocol

Following fasting for 24 hours, fish from a circular tank of each group (n=6 fish) were quickly captured and immediately subjected to blood and tissue collection to determine basal parameters. The remaining animals (n=24 fish/group) were chased with hand net for 3 minutes, exposed to air for 2 minutes and subjected to biometrics to determine weight and total length. Immediately after biometrics, a group of animals of each species (n=6 fish/group) was selected and subjected to blood and tissue collection, thus constituting the immediately after stress group (IAE). The remaining animals were subjected to blood collection by caudal puncture, followed by euthanasia for tissue collection, at 1h (1hAE) (n=6 fish/group), 24h (24hAE) (n=6 fish/group) and 48h (48hAE) (n=6 fish/group). Survival rate was measured throughout the experimental period by direct observation of animals.

Hematological and biochemical analyses

Blood samples were collected with heparinized syringes and dispensed into microtubes containing sodium heparin (10%). Hemoglobin concentration was determined using a commercial colorimetric kit (Quibasa-Bioclin, Belo Horizonte, MG, Brazil). Hematocrit was measured using the method established by Goldenfarb et al. (1971). Total plasma protein was determined with an analog refractometer (Brix- RHB0-90; 0 to 90%). Erythrocyte number was determined by diluting 10 µL of whole blood in 2 mL of formaldehyde citrate and then counting cells in a Neubauer chamber using a binocular microscope. Erythrocyte, hemoglobin and hematocrit data were used to calculate mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH) and mean corpuscular hemoglobin concentration (MCHC), according to the formulae established by Wintrobe (1934).

Plasma obtained after blood centrifugation (4000 RPM for 10 min) was used to determine glucose, triglycerides, and cholesterol concentrations, and alanine aminotransferase (ALT) and aspartate aminotransferase (AST) enzymatic activities, using commercial colorimetric kits (Quibasa-Bioclin, Belo Horizonte, MG, Brazil) and spectrophotometer readings (Biochrom Libra S22 UV-VIS, Biochrom Instruments, Cambridge, United Kingdom).

Indicators of oxidative stress

After blood collection, fish were euthanized by eugenol (285 mg L-1) overdose (Mattioli et al. 2017) and had their liver quickly removed and frozen at -196°C. The liver was chosen as the target organ due to its significant role in the metabolism of carbohydrates, lipids, and proteins (Melo et al. 2024, Silva et al. 2023, Churova et al. 2014), as well as its status as the primary site for detoxification and the metabolism of xenobiotic compounds (Wolf & Wolfe 2005). Samples were subsequently weighed (Shimadzu AUW220D scale) and homogenized (Ultra Turrax T 18 Ika) in an ice-cold saline solution (NaCl 0.138 M; KCl-0.0027 M; pH 7.2) at the proportion of 1:10, and separated into two 500 μl aliquots for storage at -80°C until analysis on a microplate reader (Multiskan GO, Thermo Scientific, Waltham, Massachusetts, USA).

Superoxide dismutase (SOD) activity was determined according to Madesh & Balasubramanian (1997) based on the autooxidation of pyrogallol and absorbance reading at a wavelength of 570 nm. The method used to assesscatalase activity (CAT) was that proposed by Aebi (1984), with determination after H2O2 reduction. Glutathione peroxidase (GPx) concentration was measured using the rate of oxidation of nicotinamide adenine dinucleotide phosphate (NADPH) in the presence of H2O2, reduced glutathione (GSH) and glutathione reductase (GR) at 240 nm according to Flohé & Günzler (1984). Glutathione-S-transferase (GST) levels were determined according to Habig et al. (1974).

Protein carbonyl content (PCO) was measured according to Reznick & Packer (1994), based on the derivation of 2,4-dinitrophenylhydrazine (DNPH). Lipid peroxidation was determined through the quantification of substances reactive to thiobarbituric acid (TBARS) and measured at a wavelength of 530 nm (Gatta et al. 2000). Protein levels in extracts were determined by the Bradford method (1976). All enzymatic activities were expressed as specific activity in units per milligram of protein (U mg protein-1) of tissue.

Statistical analysis

Normality of residuals and homogeneity of variances were verified using Shapiro Wilk and Levene’s tests, respectively. Data not meeting the assumptions were transformed using the logarithmic function and evaluated again. Data were then subjected to a two-way ANOVA, comparing fish group (tambaqui or tambatinga), collection time (basal, IAE, 1hAE, 24hAE and 48hAE) and their interaction, followed by Tukey’s post-hoc test with a significance level of 5%. Analyses were performed using SAS statistical software, version 9.4 (SAS Institute Inc., Cary, NC, USA).

RESULTS

Survival

No mortality was observed during the experimental period.

Hematological parameters

Hematocrit showed effects of fish group (P <0.0001), collection time (P < 0.0001) and their interaction (P <0.0001) (Table I). The highest values were observed for tambaqui at 24hAE and for tambatinga at basal, IAE and 1hAE (Table II). Hematocrit did not differ between fish groups only at 1hAE, being lower at basal and IAE, and higher at 24hAE and 48hAE, for tambaqui in relation to tambatinga.

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Table I
Hematological parameters (mean ± standard error) of juveniles of tambaqui (C. macropomum) and tambatinga (♀ C. macropomum × ♂ P. brachypomus) subjected to capture and handling during biometric management.
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Table II
Detail of interactions between hematological parameters (mean ± standard error) of juveniles of tambaqui (C. macropomum) and tambatinga (♀ C. macropomum × ♂ P. brachypomus) subjected to capture and handling during biometric management.

Hemoglobin concentration also showed effects of fish group (P <0.0001), collection time (P <0.0001) and their interaction (P = 0.0125) (Table I). Management reduced the hemoglobin concentration of tambaqui at 24hAE and 48hAE (Table II), while tambatinga experienced increases at IAE and 1hAE, followed by decreases at 24hAE and 48hAE. Tambaqui had higher hemoglobin concentrations than did tambatinga at all collection times.

Erythrocyte number also showed effects of fish group (P <0.0001), collection time (P <0.0001) and their interaction (P = 0.0003) (Table I). The highest erythrocyte numbers for tambaqui were at IAE and 1hAE, with recovery of basal condition at 24hAE. The lowest numbers for tambatinga were at 24hAE, a condition that was maintained until 48hAE. The tambaqui and tambatinga showed similar erythrocyte numbers only in the basal condition, with the values for the tambaqui being higher at all the other collection times (Table II).

MCV showed effects of fish group (P = 0.0002), collection time (P <0.0001) and their interaction (P <0.0001) (Table I), with the highest values being observed for tambaqui at 24hAE and for tambatinga at IAE (Table II). Among collection times, tambatinga had higher MCV at IAE and 48hAE, while tambaqui was higher only at 24hAE.

MCH had no effects of fish group (P = 0.2189), collection time (P = 0.1220) or their interaction (P = 0.5230) (Table I). However, MCHC had an effect of fish group (P < 0.0001), collection time (P = 0.0235) and their interaction (P = 0.0478) (Table I). The tambaqui had the lowest MCHC only at 24hAE, while the tambatinga showed no variations throughout the collections (Table II). However, between collection times, the tambatinga showed lower values than the tambaqui at all collection times, except for 24hAE (Table II).

Blood biochemical parameters

Plasma protein levels had no effect of collection time (P = 0.1052), but there were effects of fish group (P <0.0001) and the interaction between factors (P =0.0020) (Table III). The lowest plasma protein level recorded for tambaqui was at basal, while for tambatinga the lowest levels were at 1hAE and 24hAE (Figure 1). Fish groups differed at basal, IAE and 48hAE, with higher values for tambatinga.

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Figure 1
Interaction breakdown (mean ± standard error) for total plasma protein for juveniles of tambaqui (C. macropomum) and tambatinga (♀ C. macropomum × ♂ P. brachypomus) subjected to capture and handling during biometric management. Different lowercase letters indicate significant differences between fish groups within collection times; different capital letters indicate significant differences for the same fish group among collection times.
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Table III
Blood biochemical parameters (mean ± standard error) for juveniles of tambaqui (C. macropomum) and tambatinga (♀ C. macropomum × ♂ P. brachypomus) subjected to capture and handling during biometric management.

Plasma glucose had effects of fish group (P < 0.0001) and collection time (P < 0.0001), but not for their interaction (P = 0.2098) (Table III). Tambatinga had higher glycemia than did tambaqui. The highest level recorded among collections was at IAE and 1hAE.

Cholesterol had no effect of fish group (P = 0.1668) but had an effect of collection time (P < 0.0001) and of their interaction (P < 0.0001). The highest concentration for tambaqui was at 48hAE. Stress caused a decrease in concentration for tambatinga at 1hAE and 24hAE but returned to basal condition at 48hAE (Figure 2). Tambatinga showed higher levels than tambaqui at basal and IAE, while at 24hAE there was a reduction in concentration.

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Figure 2
Interaction breakdown (mean ± standard error) for cholesterol level for juveniles of tambaqui (C. macropomum) and tambatinga (♀ C. macropomum × ♂ P. brachypomus) subjected to capture and handling during biometric management. Different lowercase letters indicate significant differences between fish groups within collection times; different capital letters indicate significant differences for the same fish group among collection times.

Triglyceride levels had no effect of fish group (P = 0.4298) but had an effect of collection time (P <0.0001) and of their interaction (P = 0.0343) (Table III). Triglyceride levels peaked at 24hAE for both fish groups. Among collection times, tambaqui and tambatinga differed only at 48hAE, with that of tambaqui being higher (Figure 3).

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Figure 3
Interaction breakdown (mean ± standard error) for triglyceride level for juveniles of tambaqui (C. macropomum) and tambatinga (♀ C. macropomum × ♂ P. brachypomus) subjected to capture and handling during biometric management. Different lowercase letters indicate significant differences between fish groups within collection times; different capital letters indicate significant differences for the same fish group among collection times.

ALT had an effect of fish group (P < 0.0001), but no effect of collection time (P = 0.5210) nor their interaction (P = 0.2911) (Table III). Results were similar for AST, with an effect of fish group (P <0.0001), but no effect of collection time (P = 0.0650) nor their interaction (P = 0.9958). Tambatinga had higher values than tambaqui for both ALT and AST.

Antioxidant defense

SOD had an effect of fish group (P = 0.0385) and of the interaction of factors (P = 0.0038), with no effect of collection time (P = 0.2308) (Table IV). Stress caused an increase in enzyme activity for tambatinga at IAE, 1hAE and 24hAE (Figure 4), while for tambaqui the increase in enzyme activity occurred at 1hAE and 48hAE. Fish groups differed at IAE, 24hAE and 48hAE, with tambatinga having the highest concentrations at all collection times, except the last at 48hAE.

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Figure 4
Interaction breakdown (mean ± standard error) for the enzyme superoxide dismutase (SOD) for juveniles of tambaqui (C. macropomum) and tambatinga (♀ C. macropomum × ♂ P. brachypomus) subjected to capture and handling during biometric management. Different lowercase letters indicate significant differences between fish groups within collection times; different capital letters indicate significant differences for the same fish group among collection times.
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Table IV
Oxidative parameters of (mean ± standard error) liver tissue for juveniles of tambaqui (C. macropomum) and tambatinga (♀ C. macropomum × ♂ P. brachypomus) subjected to capture and handling during biometric management.

CAT had no effect of collection (P = 0.7393) nor for the interaction of factors (P = 0.1205) (Table IV). However, when comparing groups of fish, the hybrid showed greater enzymatic activity compared to the pure species (P = 0.0432).

GPx had an effect of fish group (P = 0.0203) and collection time (P = 0.0317), but not for their interaction (P = 0.5491) (Table IV). Tambatinga had the highest concentration of GPx. Among collections, the lowest activity was at basal and the highest at 1hAE.

GR had no effect of fish group (P = 0.4977), of collection time (P = 0.0899) nor of their interaction (P = 0.6556) (Table IV). Likewise, GST also had no effect of fish group (P = 0.5463), of collection time (P = 0.7554) nor of their interaction (P = 0.3576).

Lipid peroxidation (TBARS) had an effect of fish group (P < 0.0001), collection time (P < 0.0001) and their interaction (P < 0.0001) (Table IV). The highest degree of lipid peroxidation for tambaqui was at 48hAE followed by 1hAE, with no differences among the other collection times for tambaqui (Figure 5). Tambaqui had higher peroxidation levels at 1hAE and 48hAE than did tambatinga.

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Figure 5
Interaction breakdown (mean ± standard error) for TBARS levels for juveniles of tambaqui (C. macropomum) and tambatinga (♀ C. macropomum × ♂ P. brachypomus) subjected to capture and handling during biometric management. Different lowercase letters indicate significant differences between fish groups within collection times; different capital letters indicate significant differences for the same fish group among collection times.

Protein degradation measured by carbonyl proteins (PC) did not have an effect of fish group (P = 0.5496) nor of the interaction of factors (P = 0.8998). However, protein degradation increased at 24hAE and 48hAE (Table IV).

DISCUSSION

Biometric handling did not result in any mortality in the present study, similar to what was observed for juvenile Arapaima gigas subjected to the stress of hand-net handling and air exposure (Dias et al. 2020). However, handling stress did cause changes to hematological, biochemical and oxidative responses, and evidenced different physiological responses for juveniles of tambaqui (C. macropomum) compared to juveniles of the hybrid tambatinga (♀ C. macropomum × ♂ P. brachypomus). Different response patterns between C. macropomum and its hybrid tambatinga were also observed by Santos-Silva et al. (2024) when the animals were subjected to thermal stress. Differences between the pure species and hybrids were also observed in the physiological responses of Acipenser baerii and its hybrid ♀ A. baerii × ♂ A. schrenckii (Yang et al. 2021), as well as O. niloticus and O. mossambicus and their hybrid (Yilmaz et al. 2021). Therefore, our results highlight that, despite being raised under the same conditions and subjected to the same type of stress, the pure species and the hybrid activate different physiological mechanisms to maintain homeostasis.

Hematological and biochemical parameters

Plasma glucose is considered an essential energy source and one of the most used secondary stress response indicators (Panase et al. 2018). The present study found blood glucose to increase immediately after stress and remain elevated after 1h, regardless of fish group. Hyperglycemia is an indication of increased energy metabolism to favor survival and maintenance of homeostasis, being mediated by the action of catecholamines and cortisol (Perry & Reid 1993). Furthermore, the similarity between glucose levels at basal and 48hAE for both fish groups reinforces that the time spent collecting blood from the animals need not be considered an additional stress factor in the study.

Increases in hematocrit, erythrocyte and hemoglobin levels are important indicators of additional oxygen transport, which is a physiological response responsible for ensuring energy supply and improving the capacity to deliver oxygen to tissues in stressful situations (Xie et al. 2023). Tambaqui showed an increase in hematocrit at 24hAE, but at 48hAE the values were lower than at other times for both fish groups. Changes in hematocrit depend on the number of circulating erythrocytes and cell size (Witeska et al. 2022), making this parameter an important indicator of blood viscosity. As a reduced erythrocyte number was accompanied increased MCV for tambaqui at 48hAE, the changes in hematocrit seem to reflect an increase in erythrocyte size. Still, according to Witeska et al. (2022), this change may also be a compensatory response to lower hemoglobin values, similar to what was observed in the present study for both groups. At 48hAE, the tambatinga exhibited hemodilution, with significant reductions in hematocrit, hemoglobin concentration, erythrocyte count, and MCHC, accompanied by an increase in MCV. In general, the release of catecholamines into the bloodstream causes ionic loss and osmoregulatory imbalance resulting in hemodilution, which can compromise the capacity to transport oxygen to tissues (Morgan & Iwama 1997).

Hemoglobin, the main oxygen-carrying blood protein (Tavares-Dias 2015), was also directly affected by handling stress. Stress caused increases in hemoglobin concentrations at IAE and 1hAE for tambatinga, while the levels remained similar to basal at these same sampling times for tambaqui. However, there was a reduction in hemoglobin concentration at 24hAE and 48hAE for only in the tambatinga. The increased hemoglobin levels observed here indicate a physiological response to the organism’s greater oxygen demand, similar to that observed for O. niloticus under acute stress conditions (Bao et al. 2018). However, this increase at the initial times may explain the loss of the ability of tambatinga to return to initial levels, as observed at 24hAE and 48hAE.

Hemoconcentration (Matsche 2011) and hemodilution (Stewart et al. 2019) can also affect plasma protein levels (albumin and globulin) in fish. The present study observed a reduction in plasma protein concentration in tambatinga from 1hAE onwards, without recovery of the initial condition. On the other hand, for tambaqui, there was an increase in levels at 24hAE, with recovery of osmoregulatory capacity at 48hAE. Therefore, these responses showed that biometric management can impact the mobilization and synthesis of plasma proteins in the liver in a different way, immediately after management. The significant reduction in plasma protein observed in tambatinga over 48 hours may indicate an increase in amino acid oxidation to meet the energy demands resulting from heightened physiological activity imposed by stress. This mechanism is consistent with the findings of Refaey et al. (2022) in hybrid red tilapia subjected to chronic stress. Another hypothesis is that the reduction in plasma protein synthesis may have been caused by alterations in hepatic and hematopoietic tissue, as suggested by Cheng et al. (2017).

ALT and AST are important enzymes that reflect the health status of fish, being concentrated in hepatocytes and released into plasma after damage or alteration of metabolic function (Cheng et al. 2017, Ghelichpour et al. 2017). The biometric procedure of the present study was not sufficient to cause changes in the concentrations of these enzymes, suggesting the absence of tissue damage. This finding is important because this type of management is common in fish farms. However, comparison of basal levels shows a difference between the two fish groups. Similarly, when investigating ALT and AST activity in cyprinids, Simkova et al. (2015) also found that hybridization can affect the levels of these enzymes.

The liver plays a fundamental role in metabolism and is the main organ for cholesterol synthesis and storage (Bera et al. 2020). In the body, cholesterol is a precursor of steroid hormones and is fundamental to the structure of several cell membranes (Pang et al. 2020). Here, stress resulted in an increase in cholesterol levels for tambaqui at 48hAE. However, this response does not seem to be a result of biometric management, but rather a possible effect of food deprivation. In general, it is known that cholesterol can be ingested via diet or obtained mainly through exogenous biosynthesis (Li et al. 2023). Therefore, the increase in cholesterol levels observed at 48hAE for tambaqui can only be explained by exogenous biosynthesis, being a biological response specific to the species and not observed for tambatinga. Still, according to Navarro et al. (1995), increased lipid metabolism during food deprivation is an attempt to preserve the different biological functions dependent on cholesterol because changes in cholesterol concentrations can cause changes in cell membranes and compromise energy balance (Kim et al. 2021). Another hypothesis is that hypercholesterolemia may have resulted from the release of damaged cells or from an increase in cholesterol synthesis by hepatic tissue and other organs (Mukherjee et al. 1991).

Similar to cholesterol, triglycerides play a fundamental role in providing cellular energy (Tammam et al. 2020). Both fish groups showed a peak in plasma triglyceride levels at 24hAE. It is generally known that acute or chronic stress can be associated with an increase in metabolic rate and result in changes in plasma metabolites (Dagoudo et al. 2023). Therefore, the results found here suggest that the increase observed in triglyceride levels for both fish groups may reflect a late physiological response of lipid metabolism in an attempt to provide energy to minimize the possible deleterious effects of stress and, thus, guarantee the survival of the animals. Interestingly, the elevation of cholesterol along with the increase in lipid peroxidation (TBARS) observed only in tambaqui at 48hAE suggests a metabolic and structural response to stress. The recovery of triglyceride levels in this group indicates an adaptive balance in tambaqui, where antioxidant mechanisms and lipid mobilization continue to respond to stress. However, tambaqui is simultaneously capable of promoting the recovery of essential energy reserves, thereby ensuring a long-term energy supply. Thus, our results highlight a difference in energy allocation between tambaqui and tambatinga during stress recovery, although the metabolic pathways involved in this process still require further investigation.

Antioxidant defense

Handling animals during the production cycle can result in excessive production of reactive oxygen species (ROS) and negatively affect the ability of the antioxidant defense system to deal with this increased production of ROS, and thus cause oxidative stress and cellular damage (Seifried et al. 2007, Monteiro et al. 2021). The biometric procedures of the present study increased SOD levels for tambatinga IAE, which returned to basal condition only at 48hAE. This response was contrary to what was observed in tambaqui, for which SOD activity remained similar to basal at all collection times, only increasing at 48hAE. SOD is an important antioxidant enzyme that acts in the body’s first line of defense and is responsible for catalyzing the superoxide radical (O2 -) into hydrogen peroxide (H2O2). Therefore, the increase in SOD activity immediately after biometric management highlights the ability of tambatinga to better deal with ROS accumulation and, thus, minimize the occurrence of cellular damage. For tambaqui, the increase in SOD at 48hAE was accompanied by an increase in lipid peroxidation, as assessed by TBARS, which can cause serious damage to cellular membrane integrity (Phrompanya et al. 2021).

Like SOD and CAT is also an important primary defense antioxidant enzyme that acts in the decomposition of hydrogen peroxide into water and oxygen, thus protecting cells from H2O2 attack (Yin et al. 2014, Zhang et al. 2020). However, unlike what was observed for SOD, CAT levels in this study remained unchanged throughout the experiment, with only fish group (hybridization) effects being identified. Furthermore, Liu et al. (2015) suggest that this behavior may be an adaptive response to the presence of ROS. Another hypothesis is that this enzyme is only activated under extreme stress conditions, in response to higher levels of peroxides, as observed by Atli & Canli (2007) when evaluating CAT gene expression in O. niloticus.

Protein oxidation and denaturation were evidenced by the higher carbonyl protein levels observed at 24hAE and 48hAE for both fish groups. The absence and/or inhibition of the antioxidant defense system may have contributed to the accumulation of ROS and thus increased the degree of protein degradation. Furthermore, the absence of changes in GR and GST concentrations helps to corroborate this hypothesis. According to Modesto & Martinez (2010), the inactivation of these enzymes in tambaqui may be in response to a high degree of lipid peroxidation and the accumulation of some products arising from protein carbonylation. Once in the body, an excess of these compounds can result in the loss of enzymatic function and result in the inactivation of antioxidant defenses by excess oxidants, even though this is the substrate itself.

CONCLUSIONS

Acute handling stress did not affect the survival of juveniles of tambaqui (C. macropomum) nor of juveniles of the hybrid tambatinga (♀ C. macropomum × ♂ P. brachypomus) within 48 hours after stress. However, handling stress caused hemodilution, with a reduction in hematocrit, hemoglobin concentration, erythrocyte number and MCHC being observed, accompanied by an increase in MCV in the tambatinga. Although, the antioxidant defense system showed a compensatory response to the effects of hemodilution and prevented the occurrence of lipid damage. In tambaqui, the antioxidant defense system was activated late and was unable to prevent lipid peroxidation. However, the tambaqui shows greater adaptation and resistance to biometric management when compared to tambatinga.

The results obtained in this study highlight the importance of carefully evaluating the methods used during biometric handling. It is recommended to evaluate other practices that prioritize animal welfare, such as careful handling, minimizing exposure time to air and the use of anesthetics to reduce excessive movement for both groups of fish, especially the tambatinga.

ACKNOWLEDGMENTS

This research was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Brasil – 402952/2021-9, 308547/2018-7); Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG-Brasill – APQ-01531-21); and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES-Brasil – finance code 001).

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Publication Dates

  • Publication in this collection
    17 Mar 2025
  • Date of issue
    2025

History

  • Received
    28 June 2024
  • Accepted
    15 Dec 2024
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