Recent Advances of Phytobiotic Utilization in Carp Farming: A Review

use, distribution, and reproduction in any medium, provided the original work is properly cited. Carp farming is a popular aquaculture activity that provides a ﬀ ordable protein sources and job opportunities to many people worldwide. As carp farming intensi ﬁ es, farmers face major issues such as rising feed costs and excessive antibiotic usage. Thus, there is an urgent need to explore alternative resources to ensure the sustainability of the carp farming industry. One of the most promising resources is phytobiotics that possess various properties bene ﬁ cial for carp production. Furthermore, most phytobiotics are derived from agricultural waste that is abundant and cheap, but some phytobiotics are produced commercially and available in the market. The main topics of this review are highlighted sources, characteristics of phytobiotics, and the usefulness of phytobiotics in improving growth performance, feed utilization e ﬃ ciency, antioxidant activity, and health of carps against diseases. Furthermore, in this review, recent methods of administration of phytobiotics such as through feeding, bathing, and intraperitoneal injection in carp farming are also discussed and summarised.


Introduction
Carp, alongside tilapia and shrimp, are the main aquaculture species that made up 50% of the total world aquaculture production in 2018 [1]. The first carp farming was recorded 2500 years ago, and carp continues to be cultured in 123 countries today, with 28.9 million tons of production valued at USD 61.6 billion in 2018 [2]. The common carp production alone exceeded 4000 tons or 7.7% of the world's aquaculture production in 2018 [2]. China has remained the leading carp producer in the world since 1997, with 5.7 million tons of carp production in 2018, followed by India and Bangladesh [2]. The major carp species farmed worldwide are grass carp, silver carp, common carp, bighead carp, and catla. Furthermore, carp production is expected to increase in the coming years due to the rising global market demand. However, there are several issues in carp farming that have limited the expansion of carp production.
Carp farming is susceptible to huge losses due to disease outbreaks. When carp production is affected, it will lead to loss of income and unemployment among farmers [1,3]. Traditionally, fish farmers depend on antibiotics to mitigate disease outbreaks, but this practice has led to overreliance and antibiotic resistance of pathogenic bacteria in aquaculture sites [4]. Therefore, it is essential to identify an alternative antimicrobial agent for aquaculture species health management. In addition, many European countries have banned aquaculture products containing antibiotic residues [4]. Phytobiotic is a potential solution in improving aquaculture species' health and function while minimizing antibiotic dependence.
Carp farming has also become increasingly expensive due to the rising cost of conventional raw materials for feed formulation [3]. Prices of feed ingredients such as soybean meal and fish meal continue to rise since these conventional raw materials are also utilized in the feed formulation of other livestock. Thus, an alternative to the current raw materials for feed formulation is urgently needed to maintain the cost of carp production and ensure the stability and sustainability of the carp farming industry. Currently, farmers are looking at phytobiotics as an alternative resource to the conventional raw materials for carp farming for safe and sustainable carp production.
Phytobiotics refer to plant-based extracts, derivatives, bioactive compounds, whole plant, or part of a plant utilized 2 Aquaculture Nutrition as feed additives or raw materials for feed formulation to improve livestock production [5][6][7]. Feeding, intraperitoneal injection, and bath immersion are available options to deliver these polysaccharides to the fish. Various studies have revealed the potential of phytobiotics in improving carp growth performance, feed utilization efficiency, antioxidant activities, innate immune response, and carps' health against diseases, which will be further discussed in this review.

Phytobiotic Sources and Characteristics
What are phytobiotics? Phytobiotics are referred to as a group of plant-based products or compounds that can benefit animal farming including humans [6]. Phytobiotics can be found naturally and abundant in vegetables, fruits, herbs, legumes, and essential oils [8]. They can be used as whole plants or through extracting their bioactive compounds such as phenolic compounds, carotenoids, alkaloids, and many more [8]. The presence of bioactive compounds in phytobiotics will determine the characteristics of the phytobiotics. For example, the presence of phenolic compounds in phytobiotics can contribute to the antioxidant property of phytobiotics [9]. Besides, phytobiotics were reported to possess other huge characteristics such as anti-inflammatory and antimicrobial. Therefore, phytobiotics were widely used in animal production as growth promoters and prophylactic agents to increase animal production.

The Role of Phytobiotics in Improving Carp Growth Performance
Phytobiotic is a growth promoter and a protein replacement for conventional raw materials like fish and soybean meals. This plant-based material positively impacts the gut microflora and encourages digestive enzyme secretion [7]. Examples of phytobiotics include rapeseed cake [10], defatted rubber seed meal [11], and a combination of rapeseed and Chlorella meal [12]. These alternative and protein-rich feed-stuffs can help reduce operational costs in carp farming by using as fish meal protein replacement in fish feed formulation.
However, not all plant-based products are beneficial in fish farming. Fish feed high in starch content has adverse effects on fish growth performance. For example, Tan et al. [13] reported that fish feed with high starch concentration (32-40%) negatively affected the growth performance of gibel carp (Carassius auratus). Thus, fish farmers must select the appropriate plant-based product as phytobiotics for their aquaculture species.
Many studies reported on the role of phytobiotic in enhancing carp growth performance as shown in Table 1. For example, Lin et al. [14] claimed that fish feed consisting of 40% wheat meal could promote fish growth since it is rich in the amino acid leucine. Meanwhile, Amirkhani and Firouzbakhsh [15] revealed that a 400 mg/kg diet of the basil (Ocimum basilicum) ethanolic extract could improve the growth performance of the common carp (Cyprinus carpio). In addition, other phytobiotics that positively influenced aquaculture species growth performances are fenugreek seed meal [16], date palm (Phoenix dactylifera) seed extract [17], Chlorella [18], juniper berry oil [19], white button mushroom powder [20], curcumin [21], and wheat meal [14]. Moreover, certain phytobiotics such as fenugreek seed meal exhibited additional benefits by reducing stress and improving growth performance [16]. On top of that, phytobiotics such as fenugreek seed meal, Chlorella, juniper berry oil, and curcumin are abundant, making them accessible to most farmers.

The Role of Phytobiotics in Promoting Carp Feed Utilization Efficiency
Feed utilization efficiency is crucial in determining the success of carp farming. Phytobiotic application improves nutrient availability and digestibility, contributing to enhanced feed conversion and protein synthesis [7]. Various phytobiotics like oregano essential oil [40], curcumin [21], 3 Aquaculture Nutrition grape pomace flour (GPF) [34], and savory (Satureja hortensis) essential oil [38] are easily applicable in carp farming as shown in Table 2. Nevertheless, these phytobiotics are only useful when the aquaculture species nutritional requirements are fulfilled. High feed utilization efficiency will result in a low feed conversion rate (FCR), thus boosting the income of carp farmers.

The Role of Phytobiotics in Enhancing Carp Antioxidant Activities
Numerous studies have revealed the potential of phytobiotics in enhancing antioxidant activities in carps as shown in Table 3. Antioxidants are essential for protection against free radicals and oxidative stress [42]. Moreover, some phytobiotics are inexpensive in the market, making them accessible to most carp farmers. Examples of phytobiotics that promote antioxidant activities in carps are Chlorella [18], garlic [43], ulvan [44], and grape pomace flour (GPF) [34]. Nonetheless, inadequate resources and the high processing cost of the current technology are limitations to the phytobiotic application in carp farming [3,5].

The Role of Phytobiotics in
Activating an Innate Immune Response in Carps. Like higher vertebrates, the fish immune system consists of two components: (1) innate immunity and (2) adaptive immunity. The first line of defence in fish is the innate immune system during the pathogenic invasion. In aquaculture, the most reliable disease management is through immunostimulant administration [51]. Some phytobiotics act as immunostimulants and promote antioxidant activities in carps but do not contribute to their growth performance. For example, Paray et al. [47] revealed that oak (Quercus castaneifolia) leaf extract-medicated feed for 60 days in common carp (Cyprinus carpio) enhanced antioxidant activities and promoted their immune system but did not influence carps' growth rate. Generally, phytobiotics with high antioxidant properties can stimulate the fish immune system [52]. Some phytobiotics are low cost and easy to access such as garlic [43], grape pomace flour (GPF) [34], ulvan [44], and turmeric powder [53], which can be used to boost carps' immune response and increase fish production as shown in Table 4. However, certain plant-based products must be processed before they can be used as an aquaculture feed additive, such as Psidium guajava leaf [54] and dried lemon (Citrus limon) peel [48]. These agricultural wastes are subjected to drying and converted into powder form before being used as phytobiotics to enhance the immune system of carps. 4 Aquaculture Nutrition

Antioxidant Activities of Phytobiotics.
Plant-based phytobiotics are rich in antioxidants with different total antioxidant capacities, which will determine the potential of the plant as a source of antioxidants. Bioactive compounds such as phenols, phenolic acids, coumarins, flavonoids, stilbenes, tannin, lignans, and lignin determine the plants' total antioxidant capacity [64]. Many scientific approaches have been developed to quantify the total antioxidant capacity of plant extracts [65]. The main attraction of phytobiotics is their abundance and low cost, making them a source of antioxidant feed additive for aquaculture to enhance aquaculture species health and production [66]. Nevertheless, fish farmers prefer nontoxic materials for their aquaculture species, high antioxidant activity at low dosage, and inexpensive fish feed formulation.

The Role of Phytobiotics in Stimulating Carps' Health against Diseases
Motile Aeromonas Septicemia (MAS) caused by Aeromonas hydrophila and spring viraemia of carp virus (SVCV) are two diseases that pose a major threat and lead to significant economic losses in carp farming. Various studies have attempted the search for potential treatments or phytobiotics against these diseases. Traditionally, fish farmers use antibiotics in carp farming health management, but recent discoveries suggested phytobiotics as potential antimicrobial agents to stimulate carp resistance against diseases like MAS and SVCV. Furthermore, some of the proposed phytobiotics are commercially available in the market, thus highly accessible to fish farmers to be applied instantly in their farms to prevent disease outbreaks. Examples of potential phytobiotics against diseases are garlic, Allium sativum [67], tapioca [68], spirulina, Arthrospira platensis [69], and curcumin [70] as shown in Table 5. Other phytobiotics were also found effective in disease control but not readily available in the market. Based on a literature survey, only one study was using dipping to expose phytobiotics to carp species [71]. Although the study showed promising result, it is not practical to use in a large scale such as in an earthen pond. Hence, exposure phytobiotics to carp fish via feeding is the most cost-effective way.    [81] as shown in Table 6. Therefore, more synergistic studies involving phytobiotics with other supplements should be carried out to enhance carp farming production in the future.

Conclusion and Recommendation
The study of application of phytobiotics in carp farming is well documented in the literature. Phytobiotics are abundant and inexpensive where some can be found from agricultural wastes and some are commercially available in the market. Phytobiotics can help to improve growth performance of carp farming as protein source replacement and served as prebiotic to increase digestibility of the fish. This will reduce reliance on conventional protein sources such as fishmeal and soymeal in carp farming. Recent studies revealed the huge potential of phytobiotics in modulating the immune system and disease resistance of carp against various diseases. The novel findings showed that phytobiotics are ready to replace antibiotic as a prophylactic agent in carp farming health management. Application of these less ecological footprint prophylactic agents in carp farming can gain confidence of consumer to the aquaculture products. However, dosage and duration effects were the problems in administration of phytobiotics in carp farming. Different dosages and durations of phytobiotic application in carp farming will generate variable results. Besides, experimental conditions and the sources of phytobiotics may also play roles in determining the effectiveness of phytobiotics in carp farming. The administration of phytobiotics in carp farming can be applied orally and through intraperitoneal injection or bathing. Although the intraperitoneal method and bathing were found more effective, the methods need high labour work. Hence, most of studies recommended using phytobiotics as a feed additive in carp farming. Furthermore, oral administration of phytobiotics is a nonstressful method and practical and suitable to all sizes of fish. In conclusion, phytobiotics are rich in nutrients and bioactive compounds that help promote fish growth, digestibility, antioxidant activities, immunity, and resistance to diseases. Thus, this plant-based feed is a promising raw material for the future of aquaculture. Furthermore, most phytobiotics are derived from agricultural wastes; thus, utilizing these materials improves agricultural management and sustainability. Further study needs to be carried out on the potential phytobiotics by screening their toxicity as a prerequisite for their application in carp farming in order to produce a database on appropriate dosage as a usage guideline to the carp fish farmer.

Data Availability
This paper only reviews published literatures, and no data was collected.

Conflicts of Interest
The authors declare that they have no known competing financial interests or personal relationships that could influence the work reported in this paper.