Elsevier

Fish & Shellfish Immunology

Volume 106, November 2020, Pages 959-966
Fish & Shellfish Immunology

Full length article
Effects of dietary fern (Adiantum capillus-veneris) leaves powder on serum and mucus antioxidant defence, immunological responses, antimicrobial activity and growth performance of common carp (Cyprinus carpio) juveniles

https://doi.org/10.1016/j.fsi.2020.09.001Get rights and content

Highlights

  • Dietary administration of fern improved serum immune responses.

  • Carp fed with fern showed modulated antioxidant enzymes activity.

  • Feeding on fern affected skin mucus and serum antibacterial activity.

Abstract

A 56-day research was performed to examine the influence of graded levels (0 (control), 0.5, 1 and 2%) of Fern (Adiantum capillus-veneris) leaves powder (FLP) in diet on immune competence and growth of common carp (Cyprinus carpio, initial weight = 20 g). The serum total immunoglobulins content and lysozyme activity in the 1 and 2% FLP groups remarkably increased compared to the other groups (P < 0.05). The skin mucosal lysozyme activity enhanced with increasing dietary FLP level in a dose-response manner. Fish fed on the FLP-supplemented diets had higher skin-mucosal superoxide dismutase activity than the control (P < 0.05). However, serum antioxidant enzymes were not affected by dietary fern (P > 0.05). The serum bactericidal activity against human and fish pathogens increased with enhancing the FLP level in diet against Staphylococcus aureus, Escherichia coli (EHEC ATCC 43895), Escherichia coli (CI), Pseudomonas aeruginosa, Klebsiella pneumonia and Aeromonas hydrophila. The serum antibacterial activity against Yersinia ruckeri in the 2% FLP group was higher than the other treatments. Furthermore, the serum bactericidal activity against P. aeruginosa (ATCC 27853) only observed in fish fed on the 1 and 2% FLP-supplemented diets. The skin mucosal bactericidal activity and inhibitory effects increased with enhancing the FLP level in diet against E. coli, K. pneumonia, Y. ruckeri and A. hydrophila in a dose response manner. Moreover, the skin mucosal bactericidal activity against S. aureus only observed in fish fed on 1 and 2% FLP-supplemented diets. The weight gain values in the 1 and 2% FLP groups were higher than the other treatments (P < 0.05). Feed conversion ratio (FCR) improved with increasing FLP level in diet in a dose-response manner (P < 0.05). By considering serum and mucosal bactericidal activities against different pathogenic bacteria, the supplementation of 2% FLP in diet is recommended for C. carpio during grow-out phase.

Introduction

Common carp (Cyprinus carpio) is a worldwide warm freshwater species and its sustainable production by intensification is pivotal to meet its increasing global demand [1]. It is widely cultured fish and contribute 7.7% (ca. 4.2 million tons) of the world's total finfish aquaculture production [1]. But, the intensification of aquaculture production along with other general activities during grow-out phase (e.g. handling, grading and transportation) may induce stressful condition that result in growth retardation and may compromise fish welfare. Furthermore, chronic or even acute stress under intensive culture may lead to weakening of immune system of fish that could trigger contagious infectious disease, which finally result in financial harm [2]. On the other hand, the use of chemotherapeutic drugs for controlling disease outbreaks appears to be unsustainable as these chemotherapeutic agents may depress immune system of farmed aquatic species and accumulate in the final production that would be unsafe for public health [3]. In addition, the misuse of antibiotics and chemicals may threat wildlife and may induce the emergence of multi-drug resistant pathogens [3,4]. Nowadays, huge attention is focused on herbal therapy scenarios by applying phytochemicals and herbal extracts as a promising, environmentally friendly and sustainable alternatives to chemotherapeutic drugs to achieve “green aquaculture” goal through strengthening fish immune system [[5], [6], [7], [8]]. In addition, herbal extracts are more accessible, cost-effective, and environmentally safe compared to chemotherapeutic agents [6]. During past decade a plethora of studies have been evaluated a great range of herbal extracts on farmed fish species with promising beneficial effects that mainly attributed to their bioactive constituents including essential oils, phytoandrogens, triterpenoids, alkaloids, saponins, phenols, flavonoids and polysaccharides among the others [8]. In this sense, herbal extracts have been highly recommended as an additive in aquaculture due to the bioactive components and secondary metabolites that have a broad-spectrum medicinal properties such as immunostimulation [[9], [10], [11], [12]], growth promoter and antioxidant effects [[13], [14], [15], [16]]. Moreover, It has been confirmed that the use of herbal extract can promote health status in fish by stimulating humoral [17,18], cellular [18] and skin-mucosal [[18], [19], [20]] immune components, immune-related genes [[21], [22], [23]], secretion of cytokines [16], gut-related immune parameters [24,25] and disease resistance [26,27] in different fish species. Furthermore, the antioxidant characteristics of herbal extracts mostly related to phytochemicals (e.g. phenol/polyphenols, vitamins, flavonoids) that can inhibit oxidation process in body by enhancing the antioxidant enzymes activities (e.g. catalase, superoxide dismutase) [28] or by incrementing the bioavailability of antioxidant vitamins (E and C) [29]. Also, the growth promoting effects of herbal extract attributed to appetite stimulation, enhancement of digestive enzymes activities, providing bioactive components, vitamins and minerals for animal or by providing beneficial substrates for guts' healthy microbiome [8,20].

Maidenhair Fern, Adiantum capillus-veneris is a perennial plant that grows in humid and organic material-rich environments [30]. Maidenhair fern exhibited a wide range of medical effects such as antibacterial, antifungal, wound healing, anti-inflammatory, antioxidant as well as diuretic, and detoxifying effects among the other medical effects [31]. Ancient physicians declared some of the confirmed pharmacological effects. It has been reported that Adiantum-capillus veneris leaves contains phenolics and terpenoids, alkaloids, quaternary and N-oxides, fiber and elements (e.g. Zn and Cu) indicating the presence of wide range of immuno-nutritional constituents in this herb [32]. This plant has been confirmed to have inhibitory influence (in vitro) on some human bacterial pathogens such as Streptococcus pyogenus, Corynebacterium ovis, Bacillus spp, and Aspergillus flavus. In this context, Omidi et al. [33] demonstrated antibacterial activity of silver nanoparticles with Adiantum capillus-veneris leaf extract (used as a reducing agent) against E. coli and S. aureus. Therefore, the current research was aimed to examine the medical effects of Fern leaves powder (FLP) on immune responses, bactericidal activity and growth performance in C. carpio juveniles.

Section snippets

Experimental condition

This research was performed at Gorgan University of Agricultural and Natural Resources, Gorgan, Iran. A husbandry system including 12 fiberglass 250-L tanks that filled with 200-L filtered fresh water was used for feeding trial and each tank equipped with an aquarium bubbler for continuous aeration. One hundred and forty four juvenile common carp with mean weight of 20.0 ± 0.5 g were stocked in the husbandry system (12 fish per tank) and for a 14-days period were acclimatized to the

Results

The findings of the current research showed that serum total protein content did not change among different groups (Fig. 1a); however, serum total Ig content (Fig. 1b) and lysozyme activity in the 1 and 2% FLP groups were pronouncedly higher than the others (P < 0.05). Regarding skin mucosal immune parameters, total Ig level (Fig. 2a) in the skin mucus did not affect by dietary treatments, whereas the skin mucosal lysozyme activity (Fig. 2b) linearly increased with augmentation of dietary FLP

Discussion

The findings of this study clearly demonstrated the positive impacts of dietary FLP on humoral and skin mucosal immunity of C. carpio juveniles. Total serum proteins content are considered as a broad clinical index of health, stress status as well as nutritional condition in fish because this index include a wide spectrum of proteic components (e.g. albumin, Ig, the complement proteins, acute phase proteins, cytokines, lysozyme, transferrin and lectins) [40]. In this research serum total

Credit author contribution statement

Seyed Hossein Hoseinifar: Supervision, Conceptualization, Funding acquisition, Project administration, Resources. Amin Jahazi: Investigation, Methodology. Roghieh Mohseni: Investigation, Methodology. Mojtaba Raeisi: Conceptualization, Data curation, Formal analysis. Mahsan Bayani: Investigation, Methodology, Visualization. Mohammad Mazandarani: Investigation, Resources. Morteza Yousefi: Investigation, Resources. Hien Van Doan: Conceptualization, Data curation, Formal analysis. Mansour Torfi

Acknowledgment

The authors would like thanks the research affairs of GUASNR for their financial supports. This research work was partially supported by Chiang Mai University. The publication has been prepared with the support of the “RUDN University program 5–100” dedicated to Morteza Yousefi.

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