Lamiaceae as Feed Additives in Fish Aquaculture

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This entry is adapted from the peer-reviewed paper 10.3390/fishes7060349

Aquaculture products represent an important source of high-quality animal proteins, as well as essential macro- and micronutrients. The growing demand for fish, both salty and freshwater, has prompted the aquaculture industry to adopt intensive and even ultra-intensive farming systems to increase productivity. However, intensive practices are responsible for numerous problems, such as poor water quality, overcrowding, high temperature, and poor nutrition, that contribute to lowering the growth performances of fish health and immune competence, with consequently increased stress and high susceptibility to diseases. Although aquaculture plays an important role today, it is a sector that must overcome numerous challenges that hinder its expansion, such as the spreading of infectious diseases, fish health problems, and consequent economic damage.

Lamiaceae fish health growth performance antioxidant

1. Lamiaceae Family

Lamiaceae are distributed all over the world, although the best environmental conditions for their growth were found in the Mediterranean basin ^[1]. The Lamiaceae family includes 245 genera and approximately 8000 species ^[2]. Since ancient times, the dried herb, leaves, and essential oils of Lamiaceae plants have been used in humans to treat various respiratory diseases, rheumatoid arthritis, gastrointestinal disorders, and urinary tract infections ^[2]. Plants of the Lamiaceae family represent a natural, economical, sustainable, and safe source of feed integrators capable of enhancing the growth performance, immune system, and antioxidant status of farmed fish ^[3]^[4]^[5]. Such beneficial effects are attributable to the bioactive molecules present in Lamiaceae plants, such as terpenes, terpenoids, alkaloids, and flavonoids ^[6]. For example, the immunomodulatory properties of the Lamiaceae plants are mediated by the predominant terpenes, carvacrol, and thymol, which are capable of modulating inflammatory processes through the activation of ion channels, such as TRP (Transient Receptor Potential) channels, and consequently activate the NFkB pathway ^[7]. Moreover, carvacrol and thymol show strong antioxidant activity due to their ability to neutralize the oxygen free radicals (ROS) in tissues and cells ^[7].

Lamiaceae, as feed additives, can be administered in different forms, as a whole plant or parts (leaves or seeds), as active compounds extracted from the plant, and individually or as a combination of extracted compounds ^[6]. It should be emphasized that the efficacy of Lamiaceae plants as feed additives depends on several crucial factors such as dose, duration, time schedule of administration, and fish species ^[6]. In particular, the most important factor is represented by the dose which, if suitable, can induce beneficial effects, while if too low or too high, may induce either no response or even be toxic ^[8]. As reported in a meta-analysis study on fish diets enriched with plants, the dosages used in aquaculture vary according to the plant species used. The higher dosages are used with powdered plants (0.1–420 mg/100 g of fish × day), followed by ethanolic and aqueous extracts (0.2–160 mg/100 g of fish × day; 0.03–200 mg/100 g of fish × day, respectively), while the lower doses are used with essential oils (0.005–30 mg/100 g of fish × day) ^[9]. Thus, to improve the growth performances and health of a specific fish species, the challenge for researchers is to identify the optimal conditions in terms of the part of the plant to be used, doses, duration, and time schedule.

2. Oregano

2.1. Oregano’s Effects on Growth Performance

Great attention has been paid by researchers to the use of oregano essential oil (OEO) in farmed fish (Table 1). OEO feed inclusion stimulates the growth performance of fish, primarily by improving the feed utilization rate and by acting on metabolic processes. Zhang et al. ^[10] reported that 0.15 and 0.45% of OEO supplementation, for 56 days, stimulated digestive enzymes in koi carp juveniles (Cyprinus carpio), increasing the activation of proteases, amylases and lipases. The same beneficial effects on intestinal enzymes have been reported for the hydroalcoholic extract of oregano (at a dose of 3% in 85 days feeding trial) in rainbow trout (Oncorynchus mykiss) ^[11]. In addition, OEO dietary supplementation may promote growth due to its beneficial effects on intestinal health. The inclusion of 1.5% of OEO in the diet for 60 days significantly improved growth performance and intestinal histomorphometry (villous height and width) in common carp fry ^[12]. Similarly, the addition of 0.05% of OEO to the diet of yellow-tailed (Astyanax altiparanae) for 90 days increased the absorption area of the intestine ^[13]. The study by Huley et al. ^[14] showed that the inclusion of different OEO concentrations (0.075, 0.15, 0.225, and 0.3%) in Nile tilapia (Oreochromis niloticus) juveniles for 64 days acted as a developmental stimulant of intestinal villi and, consequently, as a growth promoter.

The beneficial effects of OEO supplementation on growth performance are also, most likely, linked to the improvement of the gut microbial community ^[10]. Fish gut microbiota serves crucial functions in host health, growth, and development, aiding digestive functions and protecting against intestinal infections ^[15]. Dietary supplementation with the major monoterpenes of oregano (thymol and carvacrol) positively altered the gut microbiota of Nile tilapia ^[16], and resulted in improved nutrient digestibility and absorption, as well as protein conversion ^[17]^[18]. The OEO inhibited some pathogenic bacterial groups and increased commensal beneficial communities of Corynebacterium, Brevinema, and Propionibacterium in koi carp juveniles ^[10].

In contrast to the beneficial effects of OEO, Santo et al. ^[19] reported no significant improvement in growth performances and no significant alterations in intestinal villous height in Nile Tilapia juveniles fed with different percentages (0.025, 0.05, 0.075, 0.1, 0.125, and 0.15%) of dried oregano leaves for 30 days. Similarly, weight gain (WG) and specific growth rate (SGR) did not significantly differ in seabream juveniles (Sparus aurata) fed with 0.5 and 1% oregano leaves powder for 15 or 30 days ^[20].

The hydroalcoholic oregano leaf extract also appeared to counteract the toxic effects of Diazinon, an organophosphate pesticide, on growth and liver metabolic enzymes (aspartate aminotransferase (AST), alanine aminotransferase (ALT) and lactate dehydrogenase (LDH) in rainbow trout juveniles; in fact, doses between 0.2 and 1%, but not higher, of oregano hydroalcoholic extract dietary inclusion significantly increased the body weight index (BWI) and the SGR compared to the standard diet in a 60 day feeding trial ^[21].

Based on these results, the best forms of oregano feed supplement for fish to stimulate growth rate and feed conversion parameters are essential oils and hydroalcoholic extracts, while powdered oregano leaves have no beneficial effects. A possible explanation may reside in the similar percentage of bioactive constituents (carvacrol 63%; thymol 4.7%; ρ-cimene 12.8%; γ-terpinene 8.4%) in essential oils and hydroalcoholic extracts ^[13]^[19]^[22].

2.2. Oregano’s Effects on Oxidative Stress

Oregano essential oil or hydroalcoholic extracts administered in the diet reduced the oxidative stress in different fish species, including common carp ^[10]^[23]^[24], rainbow trout ^[4]^[17]^[18]^[25], Nile tilapia ^[26]^[27], and catfish ^[28]. Oregano acted as an antioxidant activity enhancer, promoting the activities of serum and hepatic superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPX) enzymes accompanied by a reduction in malonaldehyde (MDA) levels ^[10]^[23].

The choice of the administered dose plays an important role in the antioxidant effect of oregano when used as a feed additive. For example, in rainbow trout juveniles, after a 60 day feeding trial with 0.6 and 1% doses of hydroalcoholic oregano leaf extract, the activity of antioxidant enzymes SOD, CAT, and glutathione peroxidase (GPX) increased, while high doses (1.4%) caused a decrease in their activities ^[17]. Similarly, the particular part of the plant being used appears to play an important role in determining its antioxidant effect. The use of 0.5 and 1% of oregano leaf powder for 30 days in sea bream juveniles, for example, did not cause any significant effects on liver antioxidant enzymes activities ^[20]; this is likely a result of the lower number of bioactive components with respect to the essential oil and the hydroalcholic extract. Further, the presence of the bioactive molecules within the vegetable matrix, as it occurs in the leaves, makes their extraction and absorption during the digestive processes difficult, with a consequent limited action. Indeed, the level of bioactive molecule uptake in the intestine represents only a limited percentage of the total quantity.

2.3. Oregano’s Effects on Immune Response

The effects of dietary oregano supplementation on the immune status of farmed fish have been widely reported. The results of numerous studies carried out on rainbow trout ^[4]^[25]^[29], Nile tilapia ^[27], and koi carp ^[10] reported that both oregano essential oil and hydroalcoholic extract increased the non-specific immune response, mainly via improving lysozyme, protease and complement system activities. In comparison to mammals, the innate immune system represents a fundamental defense weapon in fish ^[30]. For example, lysozyme is capable of destroying the bacterial cell, by splitting the β-1,4 glycosidic bonds of the peptidoglycan, providing protection against fish pathogens ^[31]. The use of 0.02% of hydroalcoholic oregano (O. majorana) leaf extract for 56 days enhanced the activity of lysozyme in common carp juveniles ^[24]. In another study, dietary integration of 0.1% of OEO in red-bellied tilapia (Tilapia zillii) improved lysozyme activity levels, accompanied by the increase in proteases, antiproteases, and bactericidal activities ^[32].

The supplementation with immunostimulants in fish diets also beneficially improved the expression of specific immune elements, such as IgM ^[20] and pro-inflammatory cytokyne Interleukin-1β (IL-1β) ^[32]. In particular, in sea bream juveniles, supplementation with oregano leaf powder at 0.5 and 1% for 30 days improved both the innate (complement system and antibacterial activity) and adaptive (IgM) responses of skin mucus immunity compared to the control group, while the oregano leaf powder integration did not alter the humoral immune response in the serum ^[20]. From this difference in the results, it was suggested that the immune defense against pathogens resides in the antibody response of the skin mucus, which increases proportionally with the concentration of oregano leaf powder in the diet (resulting highest at the dose of 1%).

2.4. Oregano’s Effects on Hemato-Biochemical Parameters

Hemato-biochemical parameters are reliable biomarkers of the health and immunity conditions of farmed fish species ^[33]. The incorporation of hydroalcoholic extract of the oregano aerial part into fish feed had no effect on red and white blood cell counts (RBC and WBC, respectively), leukocytes count (monocyte, lymphocyte and neutrophile), hematocrit (Hct), and hemoglobin (Hb) in rainbow trout juveniles treated with a dose of 1% ^[25]^[29] and in Nile tilapia treated with 0.2 and 0.5% ^[27]. On the contrary, the hematological parameters were significantly enhanced in red-bellied tilapia fed with 0.1% of OEO for 15 days ^[32]. Similar augmentation of RBC, WBC, thrombocytes, and hemoglobin was recorded in common carp juveniles fed a diet containing 0.02% of oregano (O. majorana) leaf hydroalcoholic extract for 56 days ^[24]. It has been suggested that the increase in the hematological parameters RBC, Hct, and Hb, may favor the tissue oxygenation and the elimination of carbon dioxide, contributing to growth ^[34]. Moreover, homeostasis, or the increase in such hematological parameters, indicates that the oregano supplementation had no negative effects on erythrocytes production and the destruction of mature RBC, therefore indicating that it is non-toxic ^[35]. Serum biochemical parameters, such as total protein, albumin, and globulin values, were enhanced by hydroalcoholic oregano leaf extract, added to the diet at the dose of 1% in rainbow trout juveniles ^[25]^[29]. Similarly, in sea bass (Dicentrarchus labrax) juveniles fed with 0.01% of OEO for 150 days, the improvement of total protein, glucose, triglycerides, and cholesterol occurred ^[36].

2.5. Oregano’s Effects against Pathogen Infections

Several studies have revealed that the use of OEO, in addition to increasing growth and feed utilization, improves resistance to pathogens in common carp ^[10]^[23]^[24], channel catfish (Ictalurus punctatus) ^[28], zebrafish (Danio rerio) ^[37], Nile Tilapia ^[27], rainbow trout ^[4], and red-bellied tilapia ^[32]. Carvacrol and thymol, the most abundant phenolic components, are likely responsible for the antimicrobial activities of oregano, being able to alter the bacterial outer membrane and consequently its permeability ^[38]. Carvacrol, in particular, is involved in the disintegration of bacterial cells by altering the synthesis and mobility of the flagella, the fatty acid composition of the membranes, membrane proteins, and periplasmic enzymes ^[27]^[39]. The flavonoids and terpenoids contained in the oregano also contribute to the antimicrobial power, as demonstrated by the terpenoids, ρ-cymene ^[39].

3. Rosemary

3.1. Rosemary’s Effects on Growth Performance

Several studies have confirmed that the oral administration of rosemary could enhance growth performances in farmed fish, such as common carp ^[40]^[41], Nile tilapia ^[42]^[43]^[44], and sea bream ^[45]. Among the rosemary-based products, rosemary leaf powder is the most commonly investigated as a fish feed additive. In common carp fingerlings, different doses (1, 2, and 3%) of rosemary leaf powder positively increased, in a dose-dependent manner, the growth performances and feed conversion parameters (WG, SGR, final weight (FG), feed conversion ratio (FCR) levels) after a trial of 65 days ^[40].

The same findings with rosemary leaf powder supplementation were also obtained in Nile tilapia fingerlings ^[42]^[44]; in particular, Naiel et al. ^[44] recorded better growth performance in fish fed on 0.5 and 1% of rosemary leaf powder for 60 days. Similarly, in a 65-day feeding trial, common carp juveniles fed on hydroalcoholic rosemary leaf extract (0.01, 0.25, 0.5, and 1%) showed an increase in growth performances ^[41]. Various studies have shown that herbal plants not only improved fish growth and nutrition, but also enhanced appetite and modified the gut microbiota composition, increasing the diversity and activity of the beneficial bacteria, while inhibiting pathogenic bacteria ^[6]^[46]^[47]. In agreement with these findings, rosemary leaf powder also showed a positive role in controlling nutrient uptake and enhancing the intestinal mucosal condition in rats (^[48]. On the contrary, in Nile tilapia juveniles fed 90-day diets with different amounts (0.1, 0.25, and 0.5%) of commercial rosemary extract, Yilmaz et al. ^[43] did not report significant changes in growth performances. In addition, in gilthead seabream, growth performances and feed intake were not modified by the inclusion of different doses (0.06, 0.12, 0.18, 0.24%) of commercial rosemary extract for 84 days ^[45]. Such differences could be attributed to different fish species, feeding trial length, source and rosemary doses. In this regard, it is necessary to emphasize that, in the experiment conducted by Hernández et al. ^[45], a commercial rosemary extract powder made of a blend at the ratio 1:1 of two diterpenes (carnosic acid and carnosol) was used. Similarly, Yilmaz et al. ^[43] used a commercial rosemary extract composed of rosmarinic acid at 5.32%. Therefore, the lack of results may be associated with the small amount of the chemical active principles in the feed additive used. In contrast to the inclusion of powder or fresh leaf extract, it is also interesting to underline that rosemary oil did not result in an increase in growth performance, as well as growth rate (GR) and FCR in sturgeon juveniles (Huso huso) ^[49] and seabass ^[50].

3.2. Rosemary’s Effects on Oxidative Stress

The beneficial effects of rosemary dietary-inclusion also resulted in the improvement of the antioxidant status in common carp ^[40] and in Nile tilapia ^[44]. Rosemary leaf powder supplementation at the doses of 0.5 and 1% in the diet of Nile tilapia fingerlings for 60 days significantly improved the antioxidant status via an increase in CAT activity ^[44]. Similarly, in a 65-day feeding trial in common carp juveniles, different doses (1, 2, and 3%) of rosemary leaf powder induced an increase, in a dose-dependent manner, of blood CAT activity, but the higher dose (3%) led to a decrease in blood SOD activity ^[51].

The effect of powdered rosemary leaves as antioxidant defense enhancers could be linked to its several beneficial compounds, such as rosmarinic and carnosic acids ^[52].

3.3. Rosemary’s Effects on Immune Response

Dietary supplement with rosemary products showed an enhancement of the immune system in fish. The elevation of total immunoglobulin (Ig) levels, lysozyme and alternative complement activities of common carp juveniles fed on diets containing rosemary leaf powder in various doses (1, 2, and 3%), for 65 days, was reported ^[40]. The findings of Dezfoulnejad and Molayemraftar ^[41] confirmed the potential of oral administration of hydroalcoholic rosemary leaf extract as a stimulatory agent of the non-specific immune system in common carp juveniles. Similarly, in tilapia (O. mossambicus) fingerlings, the inclusion of 0.25 and 0.5% hydroalcoholic rosemary extracts for 60 days led to an improvement in the principal non-specific immunity elements (lysozyme, immunoglobulin and alternative complement) ^[53]. In addition, in Nile tilapia fingerlings, the oral administration of 1% of rosemary leaf powder for 60 days induced a significant increase in the expression of the immune genes related to innate and adaptive immune response, such as lysozyme, complement and immunoglobulin M (IgM) ^[44].

3.4. Rosemary’s Effects on Hemato-Biochemical Parameters

It has been reported that rosemary bioactive compounds, such as rosmarinic acid, could positively affect thymus and spleen activities, leading to a significant increase in the WBC counts (lymphocytes T and B, monocytes and neutrophils) ^[54]. In fact, after 65 days of oral administration of 2 and 3% of rosemary leaf powder, WBC markedly increased in common carp juveniles ^[40]. Similarly, tilapia fingerlings treated with 1% of rosemary leaf powder showed a significant increase in both haematological (WBC, haematocrit and leukocrit levels) and serum biochemical (total protein, albumin and globulin levels) parameters ^[42]. Serum biochemical parameters are good fish health indicators ^[34]. Several studies have suggested the possible correlation between enhanced fish growth performance and the simultaneous increase in total protein, albumin and globulin levels due to dietary herbal inclusion ^[34]^[55]. Findings on the oral supplementation of rosemary in common carp ^[40]^[41] and in Nile tilapia ^[42]^[44] confirmed the hypothesis of the combination effects of health and growth performance in fish treated with herbal supplementation. Moreover, several vitamins (A, B, and C) and minerals (K, Ca, and Fe) present in significant quantities in rosemary could positively modulate other blood biochemical parameters due to their hypocholesterolaemic effects ^[56]. For example, the levels of triglycerides and LDL (low-density lipoprotein cholesterol) diminished, while HDL (high-density lipoprotein cholesterol) augmented in common carp juveniles fed on hydroalcoholic extract of rosemary at 1% in a 65-day feeding trial ^[41].

3.5. Rosemary’s Effects against Pathogen’s Infections

Some studies have evaluated the effects of rosemary as an alternative antimicrobial agent in aquaculture. The dietary application of dried rosemary leaves for 20 days improved the resistance against Streptococcus iniae at the 8% dose and against Streptococcus agalactiae at 16% dose in tilapia fingerlings ^[57]. Similarly, the 60-day feeding supplementation of 1% of rosemary leaf powder provided adequate protection to Nile tilapia fingerlings against the infection of Aeromonas hydrophila ^[44]. Numerous in vitro studies demonstrated that rosemary possessed antibacterial properties against Gram-positive and Gram-negative bacteria, mainly linked to its composition in phenolic compounds ^[58]^[59].

4. Sage

4.1. Sage’s Effects on Growth Performance

As reported for O. vulgare L. and R. officinalis L., Salvia officinalis has also been studied in several experiments in farmed fish ^[3]^[60]^[61]. One study by Sönmez et al. ^[3] reported the positive effects of a 60-day dietary supplementation of sage oil (0.05, 0.1, and 0.15%) on growth performance and parameters such as SGR and FCR in rainbow trout juveniles. The same results were shown in beluga after 42 days of dietary inclusion of sage ethanolic extract (3, 6, and 12%) ^[61]. This growth-promoting action could be partially attributed to the sage polyphenolic compounds, such as ursolic acid, a pentacyclic triterpenoid carboxylic acid, which induces muscular hypertrophy in rainbow trout ^[62]. An increase in growth performance was also reported in gilthead seabream juveniles fed for 92 days with 0.01% of a combined extract of sage and lemon verbena (Lippia citriodora) leaf ^[60].

4.2. Sage’s Effects on Oxidative Stress

The dietary inclusion of sage protects against reactive oxygen species (ROS) by stimulating the antioxidant defenses in farmed fish ^[3]^[60]. In rainbow trout juveniles, different concentrations (0.05, 0.1, and 0.15%) of sage oil added to the diet for 30 days significantly increased liver enzyme SOD, glucose-6-phosphate dehydrogenase (G6PD) and glutathione peroxidase (GPx) activities, while an extension of the feeding trial to 60 days induced a reduction in the antioxidant enzymes activities ^[3]. A positive modulation on the antioxidant defense system was also reported in gilthead seabream ^[60]. The findings of Salomón et al. ^[60] have shown that a 92-day administration of 0.1% dietary additives made of sage and lemon verbena hydroethanolic leaf extract stimulated SOD and CAT gene expression in gilthead seabream fingerlings.Herein, the up-regulation of SOD and CAT genes could be linked to the triterpenic and polyphenolic compounds, mainly ursolic acid, present in the sage ^[60].

4.3. Sage’s Effects on Immune Response

Great attention has been given to the utilization of the dietary inclusion of sage to fortify innate immunity in farmed fish. In beluga juveniles, the immunomodulation through the oral administration of sage ethanolic extract for 42 days (3, 6, and 12%) enhanced lysozyme and alternative complement activities, and serum immunoglobulin levels ^[61]. In addition, in rainbow trout juveniles, 30 days of dietary supplementation of 0.5, 1, and 1.5% of hydroethanolic extracts of sage positively affected the immune system indices (lysozyme and complement activities and total immunoglobulin levels) in a dose-dependent manner ^[63].

In fish, the immunomodulatory properties of the dietary supplementation of sage combined with other medicinal herbs have also been demonstrated. After a feeding trial of 28 days, the combination of sage and Spirulina platensis (Arthrospira platensis) increased the non-specific (lysozyme, IgM and complement) and specific (IL-1β and TNFα cytokines) immune response in Nile tilapia juveniles ^[64]. In sea bream fingerlings, the dietary administration of 0.1% sage and verbena hydroethanolic leaf extract stimulated the expression of lysozyme, IgM, Il-1β and TNFα, and also increased the anti-inflammatory cytokines TGF-1β and IL-10 levels ^[60].

4.4. Sage’s Effects on Hemato-Biochemical Parameters

The dietary inclusion of sage leads to the improvement of the hemato-biochemical parameters in beluga ^[61] and seabream ^[60]. Sage ethanolic extract (3, 6, and 12%), administered for 42 days, stimulated RBC, Hct, Hb, total protein, albumin, and globulin levels in beluga juveniles ^[61]. Moreover, Dadras et al. ^[61] reported that the dietary inclusion of sage ethanolic extract decreased the serum ALT and AST levels, supporting the beneficial effect of sage on the physiological status of fish. In fact, AST and ALT enzyme activities are used as stress indicators and the increase in their blood levels indicates liver impairment and hepatocellular damage ^[35].

4.5. Sage’s Effects against Pathogen’s Infections

The positive impact of the dietary inclusion of 0.5, 1, and 1.5% hydroethanolic extracts of sage for 30 days on the non-specific and specific immune responses led to an increase in rainbow trout juveniles’ resistance against infection with S. iniae ^[63]. The 28-day dietary treatment with sage leaf inclusion protected Nile tilapia juveniles against infection with Pseudomonas aeruginosa, causing a significant elevation of the expression of lysozyme, IgM, and pro-inflammatory cytokines (IL-1β and TNFα) ^[64].

5. Thyme

5.1. Thyme’s Effects on Growth Performance

Several studies have investigated the effect of dietary thyme inclusion on fish growth parameters ^[42]^[65]^[66]^[67]^[68]. These scientific findings have shown that thyme does not possess adverse or toxic effects and is able to maintain the physiological conditions of the alimentary tract in fish ^[5]^[69]. As for the other herbal products, the optimal concentration of thyme is a critically important factor. Rainbow trout juveniles fed on 0.05, 0.1, and 0.2% of thyme essential oil for 60 days showed the best growth performance and parameters (weight gain, SGR, and feed intake) with the dose of 0.05% ^[3]^[67]. In common carp fingerlings, the dietary administration of 1.5% of thyme leaf led to the improvement of growth performances after a 56-day feeding trial when compared to the other experimental dietary concentrations tested (0.5, 1, and 2%) ^[65]. In sturgeon (Acipenser stellatus) juveniles, 58 days of feed thyme application improved fish growth at the concentration of 2% ^[70] compared to the 1% inclusion dose ^[71].

5.2. Thyme’s Effects on Oxidative Stress

The positive role of thyme in enhancing antioxidant capacity has been demonstrated in rainbow trout juveniles ^[3]^[66]. For example, 0.05 and 0.1% of thyme essential oil supplementation provided enhanced antioxidant protection, improving liver CAT, SOD, GPx, and glutathione reductase (GR) activities and decreasing MDA production after 30 days of the feeding trial ^[3]. Thyme essential oil or water extract could successfully mitigate oxidative stress, likely due to their high concentrations of thymol and carvacrol ^[5]. The antioxidant effects of thymol and its isomer carvacrol have been well documented in several in vitro and in vivo studies, including cell lines ^[72] and animal models, such as weaning piglets ^[73].

5.3. Thyme’s Effects on Immune Response

Several studies have been carried out to understand the immunomodulatory effects of thyme in fish. Thyme dietary inclusion is capable of stimulating the non-specific immune response in rainbow trout, including lysozyme, alternative complement and total immunoglobulin levels ^[66]^[67]. Furthermore, dietary 1% of thyme essential oil counteracted the negative effects on immunity and intestinal inflammation induced by aflatoxin B1 in rainbow trout juveniles, significantly lowering the expression levels of TNFα, IL-8 and TGF-β ^[68]. The immunomodulatory effects of thyme are linked to its major bioactive components, such as carvacrol, thymol, eugenol, and cymene ^[67]. Thymol feed supplementation, for example, improved the immunoglobulin levels in broiler chickens ^[74] and in pigs’ guts ^[75].

On the contrary, the feeding inclusion of 0.1, 0.5, and 1% of thyme essential oil for a short period (15 days) did not alter respiratory burst activity, lysozyme concentration, or alternative complement activity in Nile tilapia juveniles ^[69]. These results confirm the importance of the optimal choice of the duration of immunostimulant administration.

5.4. Thyme’s Effects on Hemato-Biochemical Parameters

In farmed fish, the increase in blood parameters (Hb, RBC, and WBC counts) and the improvement of biochemical profile (total protein, albumin and globulin levels) suggest that the dietary inclusion of thyme products are safe feed additives able to enhance fish health and welfare. In Nile tilapia juveniles, 0.1, 0.5, and 1% of thyme essential oil for 15 days led to a significant increase in total leukocytes (monocytes, neutrophils, basophils and lymphocytes), especially at the highest dose (1%) ^[69]. The safety of thyme as a fish feed additive is also confirmed by the absence of negative or toxic effects on ALT and AST levels ^[67]^[69]. For example, the inclusion of up to 0.2% of thyme oils over 2 months did not alter the activity of these enzymes in rainbow trout juveniles, suggesting that thyme oils at up to 0.2% in feed can be considered as a safe additive for trout ^[67].

5.5. Thyme’s Effects against Pathogen’s Infections

Thyme also improves fish disease resistance against several bacteria and fungi, such as Saprolegnia spp. ^[65], A. hydrophila ^[67], Yersinia ruckeri ^[76], and S. iniae ^[77]. The efficacy of thyme essential oil or leaf powder could be a consequence of the increasing levels of the main immunity factors (lysozyme, alternative complement, immunoglobulin and cytokynes) and hemato-biochemical parameters. Feed supplementation of 0.05% thyme essential oil improved the resistance of rainbow trout juveniles against motile Aeromonas septicemia caused by A. hydrophila via the upregulation of the C3 and CD4 immune genes and the increase in IL-1β cytokine gene expression ^[67]. In fish, CD4 T helper cells provide a protective response against bacteria, fungi, and protozoa and C3 protein is crucial for the activation of both classical and alternative complement pathways ^[78].

6. Mint

Another aromatic plant belonging to the family Laminaceae that captured the attention of researchers for its use in aquaculture is mint, also known as mentha or peppermint (Mentha piperita). Mint is a perennial herbaceous plant and is widely cultivated ^[79]. Peppermint is a crucial medicinal and aromatic plant, used in food since ancient times, and more recently in sanitary and cosmetic industries ^[80]. Several studies have confirmed its antimicrobial, antioxidant, and immunomodulatory effects ^[79]. The beneficial activities of mint, especially its antimicrobial effect, are due to its major compounds, such as menthol (33.8%), menthone (15.8%) and pulegone (8.3%) ^[80]^[81]. Used in perfumery and aromatherapy, pulegone and menthol are potentially toxic compounds when administered in large amount, causing liver damage in rats ^[82]. On the contrary, menthone has a digestive favoring effect and is non-toxic ^[81]. Mint also presents a high polyphenolic content (19–23%), primarily characterized by rosmarinic acid, luteolin, hesperidin and apigenin ^[83].

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