Fruit extract of Plinia trunciflora (O. Berg) Kausel reduces cortisol levels and exhibits antioxidant effects in Rhamdia quelen exposed to acute stressABSTRACT
Rhamdia quelen is a species native to the Americas that plays a significant role in extractive fishing and aquaculture in southern Brazil. It has been recognized as one of the most promising species for fish farming due to its resilience to management practices, rapid growth, and good feed efficiency. However, the intensification of farming systems exposes fish to stressful conditions, leading to diseases, reduced production yields, and negative environmental impacts. The jaboticaba tree (Plinia trunciflora), indigenous to Brazil, produces fruits rich in anthocyanins with high antioxidant activity. This study aimed to investigate the effects of jaboticaba fruit extract on oxidative stress parameters and whole-body cortisol levels in R. quelen under acute stress. A dried hydroalcoholic extract was incorporated into the fish diet and administered for 15 days. Afterward, the fish underwent an acute stress protocol using a net chase model. The effects of the treatment were evaluated by assessing superoxide dismutase, catalase (CAT), glutathione S-transferase (GST), lipid peroxidation (LPO), and non-protein thiol group levels in the liver of R. quelen. The results indicated that the extract effectively prevented oxidative damage and mitigated the stress-induced increase in cortisol levels. This study represents the first instance of demonstrating that adding an extract to fish diets can counteract the damage caused by acute stress by activating antioxidant systems and alleviating stress responses.
Keywords:
antioxidant activity; catfish; jaboticaba; jundiá; oxidative stress
Introduction
When an organism is exposed to stress caused by a stimulus (physical, chemical, biological, or psychosocial) that threatens homeostasis, it tends to respond in a uniform, non-specific, anatomical, and physiological manner. Although stress responses arise from efforts to adapt, intense reactions to external demands may lead to serious deleterious effects (McEwen and Akil, 2020). Stressors such as confinement, low levels of dissolved oxygen in water, capture, or changes in the physical environment have significantly contributed to economic losses in fish farming because they affect the metabolism and, consequently, fish growth (Daskalova, 2019).
Rhamdia quelen (Quoy & Gaimard, 1824), also known as jundiá or catfish, is a freshwater fish species found from central Argentina to southern Mexico (Gomes et al., 2000). The species is recognized for its excellent growth performance and yield in intensive farming and demonstrates adaptability to reproductive management (Santos and Meurer, 2020). Its ease of handling, omnivorous feeding habits, early feed acceptance, flavorful meat, absence of intramuscular bones, and ability to grow in winter make jundiá a species of great interest for aquaculture (Garcia et al., 2008).
As cropping systems intensify, fish are exposed to increasingly stressful conditions, leading to diseases and environmental deterioration problems (Banerjee et al., 2019; Zhu et al., 2021). Fish stress responses initially manifest as endocrinological changes, including increased corticosteroid concentrations; subsequently, metabolic changes can also influence antibody production. Ultimately, whole-organism changes may impact growth, behavioral patterns, and disease resistance (Barton, 2002).
Natural products may help animals endure adverse conditions in a healthy manner and without harm, enabling them to resist standard aquaculture management practices. Plant extracts can contribute to sustainable aquaculture by facilitating disease control with biodegradable products, thereby reducing the reliance on harmful chemicals that pose risks to humans and the environment (Reverter et al., 2014; Xavier et al., 2021).
In this context, Plinia trunciflora (O. Berg) Kausel has been the subject of several studies highlighting the high antioxidant activity of species such as Myrciaria cauliflora (Mart.) Kausel and Myrciaria jaboticaba (Vell.) Kausel. This biological effect is primarily attributed to their significant anthocyanin content. Jaboticaba anthocyanins have been shown to reduce oxidative stress and prevent inflammatory, cardiovascular, and neoplastic diseases (Inada et al., 2021; Nascimento et al., 2023; Rigolon et al., 2020). Although the biological activity of some jaboticaba species has been described, relatively little attention has been dedicated to P. trunciflora (Sacchet et al., 2015). Therefore, this work aimed to investigate the effects of P. trunciflora fruit extract on oxidative stress parameters and whole-body cortisol in R. quelen submitted to acute stress.
Materials and Methods
Plant material and extraction
Plinia trunciflora fruits were collected in the municipality of Alpestre, Rio Grande do Sul, Brazil (27°10’56.82" S, 53°7’19.55" W, altitude 224 m) and identified by botanist Marcos Eduardo Guerra Sobral. The plant voucher specimen is housed in the herbarium of the Universidade Comunitária da Região de Chapecó (Unochapecó), in the city of Chapecó, Santa Catarina, Brazil (Voucher 3302). The fruit peels were removed and dried to a constant weight at 40 °C.
The dried fruit peels of P. trunciflora were ground and mixed with absolute ethanol (analytical grade) and ultrapure water (70:30 v/v) in a 1:2 ratio for 72 h at room temperature. Subsequently, the macerate was filtered, and the solvent was removed by evaporation and lyophilization.
Chemical analysis
All chemicals were of analytical grade. Acetonitrile and formic acid were purchased from Merck. The anthocyanins cyanidin chloride, malvidin chloride, cyanidin 3-O-glucoside chloride, malvidin 3-O-glucoside chloride, and delphinidin 3-O-glucoside chloride were acquired from ChromaDex.
High-performance liquid chromatography (HPLC) was conducted using a Shimadzu Prominence Auto Sampler (SIL-20A) HPLC system, which included an SPD-M20A diode array detector and LC solution software (version 1.22 SP1).
The analyses used a C18 column (4.6 mm × 150 mm × 5 μm). The mobile phase comprised 1 % formic acid (water) and acetonitrile, following the compositional gradient outlined by Kamdem et al. (2013), with slight modifications. Stock solutions of standard references were prepared at a concentration range of 0.030-0.250 mg mL–1. Chromatography peaks were validated by comparing their retention times with those of anthocyanins reference standards and by their diode array detector spectra.
Calibration curves were obtained for compound quantification with a correlation coefficient greater than 0.999. The limit of detection (LD) and the limit of quantification (LQ) were calculated based on the standard deviation of the responses and the slope from three independent analytical curves (Boligon et al., 2013). All chromatography operations were conducted at room temperature and performed in triplicate.
Animals
The experiment involved 64 catfish (R. quelen, three months old, 50:50 male:female ratio, average weight of 6.12 ± 0.86 g and 7.15 ± 1.22 cm in length) obtained from a fish farm in the municipality of Ajuricaba, Rio Grande do Sul, Brazil (28°13’17" S, 53°41’36" W, altitude 336 m). The Comitê de Ética no Uso de Animais (CEUA) of Unochapecó approved the experimental protocol (#002/2012).
Eight fish per group were used (n = 8). The animals were acclimated to 15 L tanks containing 4 g of NaCl. The NaCl was added to the tanks to help prevent the emergence of ich (Ichthyophthirius multifiliis), a parasite that commonly infects catfish, causing lesions and, consequently, fish mortality.
Experimental design
The animals were divided into two major groups: non-stressed and stressed. These groups were further subdivided as follows: TC = animals fed only with commercial diet; T-1 % = animals fed with rations containing 1 % P. trunciflora fruit extract (PTE); T-3 % = animals fed with rations containing 3 % PTE; and T-10 % = animals fed with rations containing 10 % PTE.
The final fish density in the tanks was approximately 3.26 g L–1, which is not considered stressful for R. quelen (Barcellos et al., 2001). Water physicochemical parameters were monitored daily: temperature 22 ± 2 °C, pH 7.57 ± 0.15, dissolved oxygen 6.92 ± 0.56 mg L–1, and ammonia levels at 0.83 ± 0.15 mg L–1. The animals were subjected to a 10/14 (light/dark) cycle and fed twice a day (9h00 and 16h00) for 15 days with commercial feed (Supra) (0.03 kg kg–1 ration) containing 0.42 kg kg–1 crude protein. In this feed, different concentrations of PTE were adsorbed.
Acute stress protocol
After the feeding period, the stressed groups underwent a stress protocol that involved a chase net for 8 min. This model is an adaptation of what Barcellos et al. (2011) used. Subsequently, the animals were euthanized using the anesthetic MS 222 (tricaine) at 0.1 g L–1. The liver samples were soaked in phosphate-buffered saline (PBS, pH 7.2), centrifuged at 377 rad s–1 for 15 min, and the supernatants subjected to ex vivo assays. Animals in the non-stressed group were euthanized and sampled using the same procedure.
Cortisol assay
Cortisol levels were assessed using the methods outlined by Sink et al. (2007) and Barcellos et al. (2009). After the stress protocol, the fish were captured and immediately frozen at –20.0 °C until cortisol extraction. Once the animals were weighed and crushed, a 0.5 g sample was macerated with 3 mL of PBS (pH 7.2) until complete homogenization was achieved. A 1 mL aliquot of this homogenate was combined with 3 mL of ethyl ether. The sample tubes were then placed in a container with liquid nitrogen, where the ethyl ether containing cortisol was decanted. When transferred to a new tube, the ethyl ether was wholly evaporated, yielding a lipid extract containing cortisol. The extract was analyzed using an ELISA kit (enzyme-linked immunosorbent assay, EIAgen Cortisol Test™, BioChem ImmunoSystems).
Oxidative stress assays
Lipid peroxidation (LPO) was assessed by measuring the levels of thiobarbituric acid-reactive species (TBARS) through their reaction with malondialdehyde (MDA). To prepare a sample, 250 µL of liver homogenate supernatant was mixed with 10 % trichloroacetic acid (TCA), 0.67 % thiobarbituric acid, and ultrapure water to achieve a final volume of 2.0 mL. The mixture was then incubated for 60 min at 95 °C. Following this, 1.5 mL of n-butanol was added, stirred for 40 s by vortexing, and centrifuged at 377 rad s–1 for 20 min. The optical density of the supernatant was measured by spectrophotometry at 535 nm (Buege and Aust, 1978).
The activity of the superoxide dismutase enzyme (SOD) in the liver was measured by assessing the inhibition of the superoxide radical reaction with epinephrine as described by Misra and Fridovich (1972). One unit of SOD is defined as the amount of enzyme that inhibits the rate of adrenaline oxidation by 50 %. SOD activity was determined by measuring the formation rate of adrenochrome at 480 nm in a reaction medium containing glycine-NaOH (50 mM, pH 10.2) and adrenaline (60 mM, pH 1.7).
The activity of glutathione S-transferase (GST) in the liver was measured using the method described by Habig et al. (1974), which utilizes 1-chloro-2,4-dinitrobenzene (CDNB) as a substrate. The enzyme activity was calculated based on changes in absorbance at 340 nm, utilizing a molar extinction coefficient of 9.6 mmol–1 cm–1. A unit of GST activity is defined as the amount of enzyme needed to catalyze the conjugation of CDNB with 1 mol reduced glutathione per minute at 25 °C.
Catalase (CAT) activity was measured by the rate of H2O2 consumption during the first minute of the reaction at 240 nm, as described by Aebi (1984). The enzymatic assay was performed in a potassium phosphate buffer (50 mM, pH 7.0) containing 30 µL of liver homogenate. A total of 70 µL 0.3 M H2O2 primer was used as substrate.
The analysis of non-protein thiols (NPSH) followed the methodology described by Ellman (1959) with some modifications. An aliquot of 150 µL of the supernatant (liver homogenate) was initially homogenized with 150 µL of 10 % TCA. Next, 100 µL of the homogenate was mixed with 10 mM 5,5’-dithiobis (2-nitrobenzoic acid), 0.5 M phosphate buffer at pH 7.0, ultrapure water, and 1.0 M Tris. After 10 min, the samples were read by spectrophotometry at 412 nm.
The total protein concentration was measured using the Lowry method, with albumin as the standard (Lowry et al., 1951).
Statistical analyses
The data are expressed as the mean ± standard error of the mean. The normal distribution of the data was confirmed using Kolmogorov-Smirnov and Levene tests, and results were analyzed by two-way Analysis of Variance (ANOVA), followed by Tukey's multiple range tests. Differences were considered significant at p < 0.05.
Results
The analysis of anthocyanins by HPLC revealed that the PTE yielded a high amount of these compounds, including cyanidin, which comprised 34.35 % of the total quantified anthocyanins, followed by cyanidin 3-0-glucoside at 21.97 % and malvidin at 21.03 % (Table 1).
After 15 days of treatment with varying doses of PTE and exposure to a stress factor, the cortisol levels in animal tissues were measured. The acute stress protocol applied to the fish proved effective, resulting in significantly higher cortisol levels in the fish subjected to the stress protocol compared to the control group. For the fish in the non-stress protocol, an evaluation of the treatments with varying doses of PTE revealed no difference (p > 0.05) from the control group, demonstrating that the extract does not alter hormone levels. However, in the stressed groups, the treatments at 1 % and 3 % extract concentrations showed a significant difference from the control stressed treatment. These treatments were comparable to the fish group not subjected to the stress protocol (Figure 1).
Cortisol levels in juvenile Rhamdia quelen treated with Plinia trunciflora fruit extract. Values are expressed as the mean ± standard deviation (n = 8). Distinct letters represent statistical differences (p < 0.05).
It was noted that LPO levels in the liver of R. quelen were not significantly influenced by either PTE supplementation or stress (Figure 2). In animals subjected to the stress protocol through net chase, an increase in SOD activity was observed, which was inhibited by treatment with PTE at a 1 % dose and partially prevented by the extract at 10 %. However, at the 3 % extract dose, SOD activity was higher compared to the control group, as shown in Figure 3A. CAT activity in the stressed group was similar to that in non-stressed groups at 1 and 10 % extract concentrations. However, at 3 %, there was a significant increase in CAT activity (Figure 3B). The GST enzymatic activity results showed reduced activity in the stressed group. Treatment with 1 % PTE restored GST levels in the stressed group to levels like those in the non-stressed group (Figure 3C).
Thiobarbituric-acid reactive species (TBARS) levels in juvenile Rhamdia quelen treated with Plinia trunciflora fruit extract. Values are expressed as the mean ± standard deviation (n = 8). MDA = malondialdehyde.
A) Superoxide dismutase enzyme (SOD) activity, U = enzyme concentration required to inhibit the oxidation rate of adrenaline by 50 %; B) Catalase (CAT), U = micromole H2O2 decomposed per minute; C) Glutathione S-transferase (GST); D) Non-protein thiols (NPSH) in juvenile Rhamdia quelen treated with Plinia trunciflora fruit extract. Values are expressed as the mean ± standard deviation (n = 8). Distinct letters represent statistical differences (p < 0.05). CDNB = 1-chloro-2,4-dinitrobenzene.
The non-enzymatic antioxidant defense system, indicated by non-protein thiol levels, increased in the stressed group. However, he extract did not alter this effect, as no significant differences were observed between the stressed groups treated with any PTE concentrations (Figure 3D).
Discussion
The PTE demonstrated a high concentration of anthocyanins, which are phenolic compounds derived from the secondary metabolism of plants and are responsible for the purple pigmentation in some fruit species (He and Giusti, 2010), such as P. trunciflora. Anthocyanins are polar compounds, and adding water as a solvent facilitates the extraction of more hydrophilic anthocyanins, particularly those belonging to the glycosylated chemical class. Compounds such as cyanidin and delphinidin 3-0-glucoside have also been described in the fruits and barks of M. cauliflora and M. jaboticaba (Abe et al., 2012; Lima et al., 2011; Mattos et al., 2022; Santos et al., 2010), with cyanidin 3-0-glucoside likely being the primary anthocyanin present in various jaboticaba species, including P. trunciflora, as indicated in the present study. These compounds are primarily responsible for the biological effects observed in jaboticaba, including the reduction of oxidative stress and the prevention of inflammatory, cardiovascular, and neoplastic diseases (Inada et al., 2021; Nascimento et al., 2023; Rigolon et al., 2020).
Whole-body cortisol levels have served as indicators of stress in animals (Sadoul and Geffroy, 2019). Cortisol is the primary glucocorticoid released during stress responses in most fish. When left unchecked, these responses may disrupt the homeostatic state and cause alterations that lead to functional impairment in organisms, such as changes in growth, disease resistance, and altered behavioral patterns (Lemos et al., 2023). The increased whole-body cortisol levels in the stressed group after 8 min suggest that R. quelen rapidly produces cortisol in response to net stress. Studies demonstrate that whole-tissue homogenates are reliable alternatives for hormone quantification when plasma volume is insufficient, yielding results equivalent to plasma concentrations in small fish (Nouri et al., 2020).
The results indicate that PTE positively affected cortisol levels in R. quelen under stress. Stressed fish treated with a 10 % extract showed no significant reduction in cortisol levels compared to the control group. The high dose of 10 % may have impacted the feed's palatability, decreased consumption, and reduced the extract's effectiveness. It is important to note that this study evaluated the response to a physical stressor, leading to a significant increase in cortisol levels. Chemical stressors, such as agrochemicals, may have varying effects depending on the specific stressor and the stress intensity to which the fish are exposed.
Lipid peroxidation is associated with oxidative stress. The production of elevated TBARS levels, particularly in the liver, clearly indicates LPO, as measured by MDA (Lushchak et al., 2009).
Lipid peroxidation levels remained largely unchanged in both groups, suggesting that the employed stress model was inadequate to induce changes in LPO (Figure 2). Previous studies have reported higher TBARS levels in catfish subjected to chemical stressors such as Roundup and Tebuconazole pesticides for 96 h (Ferreira et al., 2010; Menezes et al., 2011). The enzymatic antioxidant defense system encompasses the enzymes SOD, CAT, and GST. SOD catalyzes the dismutation of the superoxide anion to H2O2 and oxygen, while CAT converts H2O2 into water and oxygen. Consequently, the observed increase in SOD activity, along with a decrease in CAT activity in the stressed group without extract, may indicate an accumulation of H2O2. Cyanidins are recognized for their potent antioxidant and radical-scavenging properties (Jung et al., 2014; Merecz-Sadowska et al., 2023; Yang et al., 2023). The effects observed in this study are likely attributable to cyanidin, cyanidin 3-glucoside, and malvidin in the extract.
Glutathione S-transferase facilitates the binding of toxic xenobiotics and reactive products to itself (Allocati et al., 2018). In this study, GST activity was lower in the stressed group. However, treatment with 1 % PTE effectively restored GST activity to levels comparable to those of the non-stressed group, an effect that was not observed with 3 or 10 % PTE.
The increase in thiol levels in the groups exposed to oxidative stress may indicate an adaptive response to producing reactive oxygen species during stress. NPSH, primarily composed of the tripeptide glutathione, are important non-enzymatic antioxidants that help maintain intracellular redox homeostasis (Chai and Mieyal, 2023). The increased NPSH levels in the stressed group are likely linked to the antioxidant action mechanism, which involves these thiols competing to eliminate free radicals generated during the stress response (Maltez et al., 2018). However, it is important to note that this increase is not directly related to PTE.
The potential of plant extracts in aquaculture has emerged as a sustainable alternative for managing various diseases. These extracts exhibit a range of beneficial activities, including growth promotion, immunostimulation, antimicrobial and more (Awad and Awaad, 2017; Diler et al., 2017). This study focuses on jaboticaba, a plant renowned for its high antioxidant content, which has been validated by several studies. Additionally, jaboticaba is a native species commonly found in southern Brazil. Notably, the use of this plant in fish farming presents a sustainable alternative to chemical treatments. This strategy can help maintain fish health when faced with stressors such as confinement, capture, or changes in their physical environment. The incorporation of PTE into the diet of R. quelen, particularly at a dosage of 1 %, demonstrated its ability to inhibit the increase of cortisol levels during acute stress. Although there was no observed oxidative damage to lipids or an increase in NPSH levels in stressed fish, the impact on antioxidant enzyme activity contributed to improving the antioxidant status in these animals under stress.
Data availability statement
All data generated and analyzed during this study are included in this publication article. All datasets are made available by the corresponding author upon reasonable request.
Acknowledgments
The authors thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Universidade Comunitária da Região de Chapecó (Unochapecó) for the financial support and the granted scholarships.
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Edited by:
Renata Guimarães Moreira Whitton
