1. Introduction
The improvement of aquaculture sustainability is an issue of increasing importance. The lack of fish meal has forced the aquaculture sector to seek a more reliable solution for the environment and fishery resources. Advances in aquaculture sustainability are gradually reducing the amount of wild fishmeal used in aquafeeds. These advances have manifested in various ways, such as creating standards and regulations for protecting the environment or creating or caring for the environment in production processes and reducing and managing waste [
1]. Organic aquaculture is a term usually understood as synonymous with ecological aquaculture and is a comprehensive method of farming fish and other marine species that adheres to organic principles [
2]. The exact definition of organic may vary depending on the certification system with specific rules regarding production methods, and only products that follow the guidelines are allowed to use certified organic labels.
In most organic systems, such as EU regulatory processes, the preference for organic consideration of the raw ingredients is for the use of by-products coming from certified organic farms [
3]. Organic aquaculture is a relatively new food-producing sector [
4]. The first common carp (
Cyprinus carpio) standard was established in Austria in 1994 [
5]. According to the European Market Observatory for Fisheries and Aquaculture (EUMOFA) [
6], overall organic aquaculture output in the EU 27 was estimated at 74,032 tonnes in 2020, accounting for 6.4% of the total EU aquaculture production. Production has grown by 60% from 2015 (46,341 tonnes at the EU 27 level in 2015), while European nations represent approximately 20% of the world’s organic aquaculture. However, some European nations have decreased production lately [
7]. The fundamental organically produced species, arranged by significance, are salmon, mussels, carp, trout, seabass, and seabream [
8]. Specifically, for organic aquaculture, the Regulation mentions that it is a relatively new production sector, and the number of aquaculture production units converting to organic production is expected to rise. This will generate new experience, technical knowledge, and advances in ecological aquaculture that must be reflected in production standards [
9]. The scope of organic farming is still minimal regarding the primary Mediterranean-farmed species: seabass and seabream [
10]. Organic feeds result from a farming system that does not use synthetic fertilizers, pesticides, growth regulators, or livestock feed additives. Organic legislation generally prohibits irradiation and using genetically modified organisms (GMOs) or products derived from or containing GMOs [
11].
Organic seabream production has been hampered mainly by economic concerns, such as the higher cost of production feed prices, which have deterred consumers and producers [
10]. According to recent consumer preference studies, the Mediterranean has much potential for organic seabream production [
12,
13]. Furthermore, expanding organic aquaculture production is limited by the need for more organic feed, particularly for carnivorous species. Indeed, the EU organic legislation imposes minimums on the source of organic ingredients for the formulation of nutritionally balanced diets [
14,
15]. Only some ingredients must be organically certified (60% in the EU); only the plant ingredients must be organic. The limitations of the protein ingredients that can be used for organic feeds are one of the main challenges. Currently, most organic labels are allowed to use non-organic fishmeal, although the use of fishmeal from sustainable fisheries is required. However, according to the regulation (EU) 2018/848 [
16], transformed animal proteins (TAPs) can be used, and TAPs of organic origin would be considered organic. To reduce reliance on conventional fishmeal and fish oil, fisheries and aquaculture by-products are an excellent sustainable aquafeed option [
17,
18]. Using by-products from organic production would open the door to an increase in the percentage of the minimum organic raw ingredients used in the organic formulation. There are few studies in which organic feed has been used in carnivorous fish species. The regulatory limitations are summarised as all vegetable ingredients must be organic, a maximum of 60% of vegetable ingredients are allowed, and the absence of synthetic amino acids. Fish meal can be used as long as it comes from sustainability-certified fisheries or organic production. The use of non-synthetic amino acids is allowed. Therefore, the fundamental protein source with the scope of sustainability should be fishmeal from organic aquaculture or sustainable fisheries, and, due to the lack of availability, it is different. With these limitations, the availability of good ecological protein sources suitable for carnivorous fish is complicated. The main challenges for the supply of feed ingredients for the organic production of carnivorous fish are to increase the diversity of ingredients available to balance the amino acid profile without synthetic amino acids and to identify new sources suitable for the supply of eicosapentaenoic acid (EPA, 20:5n3) and docosahexaenoic acid (DHA, 22:6n3) [
14].
Even fewer studies compare conventional feeding with organic feeding. Sardinha et al. [
19] in sea bream, Pascoli et al. [
20] in seabass, or Di Marco et al. [
21] in seabass (
Dicentrarchus labrax) and sea bream (
Sparus aurata) compare organic with conventional feeding. However, in these studies, organic feeds have conventional fishmeal as a protein source. The stress and immunological markers in the fish were similar [
20], while the fillet fatty acid composition varied depending on the diet [
22]. The by-product meals used in this study need to be better studied. More protein sources from organic sources must be prioritised in research. The main alternatives are using TAPs from organic cattle and generating a circular economy, using the remains of other species of organic fish, and avoiding cannibalism to generate organic meals with nutritionally optimal fatty acids and amino acid profiles. The purpose of this research was to specifically determine the effect that organic feeds have on the growth of gilthead seabream and to see how new organic raw materials, such as poultry, remains of trout, and remains of seabass, affect growth and nutritional and biometric parameters. The goal was to better understand organic feeds as alternative ecological sources for gilthead seabream. These products may have a role in developing organic aquaculture in the Mediterranean to make it more sustainable.
4. Discussion
According to Craig and McLean, the need for certified protein sources significantly hinders the growth of organic aquaculture [
29]. There is still much discussion about the certifiability of by-catch from commercial fisheries, by-products, and processing wastes from aquaculture, fish, and meat processing industries as ingredients for organic aquafeed. The acceptability and availability of amino acids in these products are also questionable [
30]. Vegetable protein sources pose challenges, especially for feeding higher-level carnivores such as seabream. They contain antinutritional factors and have low biological value due to essential amino acid deficiencies and poor digestibility [
31]. Furthermore, including non-organic certified plant ingredients instead of fish ingredients in fish feeds also brings about the presence of undesirable substances [
32]. Some commonly used pesticides in land-based agriculture have been identified in aquatic feeds. For instance, a recent extensive analysis of aquafeeds has revealed the potential presence of chlorpyrifos-methyl (CPM) [
33]. A survey of commercially available aquatic feeds conducted in 2017 reported CPM levels ranging from 11 to 26 μg/kg [
34]. On average, approximately 5–10% of the examined feed samples had CPM levels exceeding the detection limit.
This study observed the highest final weight in fish fed the CONT and ORG diets without significant differences (
p > 0.05). In these diets, 30% of commercial fishmeal was used as a protein source. These high-quality fish meals are known to be the best protein source for fish thanks to their high digestibility and because their amino acid composition is very close to the need profile of most carnivorous aquaculture species [
35,
36]. Regarding the amino acid profile, in both the CONT and ORG diets, there is a greater quantity of essential amino acids compared to other diets, which also must impact the final growth results.
For the organic diets without a commercial fish meal, the TRO and SBS diets exhibited better growth compared to MIX and POU diets. However, previous studies of diets produced with the remains of the rest of the seabass and trout cannot be found. The growth results observed in the fish fed the TRO and SBS diets can be explained by the nature of the diet. Fish protein has an amino acid profile that closely matches the nutritional needs of the fish, which likely contributes to their improved growth compared to the control diet. The differences between the control diet and the TRO and SBS meal diets can be attributed to the fact that the raw materials used are the remains of these species. The remains may affect factors such as protein availability or the processing of these raw materials, leading to variations in growth outcomes. Using trout meal and seabass meal by-products promotes resource efficiency, waste reduction, and the establishment of a circular economy. One of the key advantages of using these by-products is their positive environmental impact. Instead of discarding them, incorporating them into other products or processes minimises the need for additional resources and waste disposal. This approach fosters a more sustainable production cycle and contributes to environmental conservation [
37]. There is currently no commercial organic supply chain for trout and seabass. These certified organic meal products should be manufactured in dedicated organic meal factories. The current availability of organic seabass and trout is insufficient to justify these factories’ existence. However, if such products were established, it could greatly enhance the profitability of organic production.
It is worth noting that the fish from the MIX treatment, which included poultry meal in its composition, obtained a lower final weight than those containing organic ingredients and aquaculture proteins (TRO and SBS). The presence of poultry meal in the MIX treatment affected the growth of the gilthead seabream and may have impacted protein availability. Moreover, the lowest final weight was obtained with the POU treatment.
According to Regulation (EU) 2018/848 [
16], Part III, paragraph (e) of
Section 3.1 regarding feeding aquaculture animals, it dictates that “growth factors and synthetic amino acids will not be used.” Consequently, using amino acids is not allowed commercially in organic aquaculture. Its application in diet formulation at the production level would not be feasible unless sustainable plant amino acids are used, such as vegetable methionine, in the present work, even though its efficiency is lower (at the time of the design of the experiment, when the commercial company that provided the diet-only had vegetable methionine).
Concerning the fatty acids in the diet, they do not seem to be the determining factor in the present study, given the amount of fish oil in this diet. Likewise, it depends on the percentage of inclusion in the diet and its quality, as mentioned above. In the present study, the feed intake was numerically higher in the organic diet groups than in the control group. However, the differences were not statistically significant. The fact that the FI and FCR were higher in the organic diet groups may indicate that the organic diets’ nutrients were unbalanced. Hence, the animals needed to increase their feed intake to compensate for deficient nutrients, such as essential amino acids. This may be the result of the origin of the raw materials. Regarding the FCR, the highest values and those statistically different from the rest of the treatments were registered in the fish fed the POU diet. Because of the above and in agreement with the study by Karapanagiotidis et al. [
38], a 100% replacement of fishmeal for poultry meal significantly increased the FCR and reduced the efficiency of feed utilisation. However, if the ECR is observed, the ORG and POU diets resulted in a higher investment of money to produce fish. The higher price of the ORG diet and the high FCR of the POU diet causes this worsening of the ECR. On the other hand, the growth of the CONT, TRO, SBS, and MIX diets entails a similar ECR: the better FCR of the CONT diet is compensated by the lower prices of the organic diets made with by-products. In addition, mortality was higher in the POU treatment than in other studies [
38], where no difference in mortality was evident between the treatments. This was possibly a consequence of the lower appetite of these fish, providing justification for their worse growth.
Some studies on seabream and seabass have been published that compare conventional diets with organic diets, obtaining better growth in organic diets [
21,
39] since these diets were formulated with a higher percentage of fish meal (63 and 56%) than the conventional ones (50 and 20%).
Regarding body composition and nutrient retention efficiencies, the fat was significantly lower in the poultry treatment diets (POU and MIX) compared to the ORG diet, which differs from the study by Sabbagh et al. [
40,
41], where no differences were found. However, it agrees with the findings of other studies in which a higher inclusion of poultry meal led to a decrease in body fat [
38], possibly due to the lower growth obtained with this diet.
The CONT and ORG treatments show higher percentages for protein retention efficiency (PPV) and fat retention efficiency (PFV). This means that they use a higher proportion of proteins and lipids in their diet for their growth, and consequently, more significant growth is manifested. On the other hand, the PPV was significantly lower in the POU treatment and was similar to the MIX treatment, which is related to the low growth of the fish fed these types of diets. The essential amino acid profile in the diet can also explain differences in amino acid retention efficiency. Some authors [
42,
43] noticed that protein retention efficiency decreases with the intake. Consequently, it seems logical that the efficiency retention of a single amino acid could be influenced by the feed composition, increasing the efficiency when the composition is lower. Some of the increased efficiencies observed in
Figure 2 could be explained by observing the TRO diet, which is a low amount of histidine (9.70 g/kg), but has the highest retention efficiency for this EAA (16.98%). The same trend is evident in the diet SBS with phenylalanine, where there is a low amount of this amino acid (18.90 g/kg), and the retention efficiency is the highest (16.56%). In general, many of the high retention efficiencies of gilthead seabream could be due to a lower amino acid content. The fact that EAAs with higher concentrations in the organic diets have lower retentions in fish suggests that the EAA profile needs to be well balanced. Instead of being used for protein synthesis, these excessive dietary EAAs were catabolised. This results in the lower retention of EAAs with high concentrations in the organic diets.
The retention efficiency of fatty acids in seabream fed experimental diets is directly related to the fatty acid profile in different diets, as has been seen in other species such as
Salmo salar [
44,
45] or
Dicentrarchus labrax [
46]. Even though the dietary profile of fatty acids differs by the type of feeding of the fish, the results agree with the studies carried out by other authors, where saturated fatty acids are represented mainly by C16: 0 and C18: 0, and those monounsaturated by C: 18: 1n9 [
47]. The literature reports that those species that include significant amounts of linoleic acid (C18: 2n-6) or linolenic acid (C18: 3n-3) in their diet present lower concentrations of the C18: 1n-9t and C18: 1n-9 acids in their tissues [
48]. The variations of these acids in the analysed species are probably multiple factors, among them the feeding of the fish, a determining element for their composition [
49,
50].
It is essential not to ignore the effect of lipid composition on the fatty acid composition of fish fed organic feed. From the data in
Table 3 and
Table 7, the retention efficiency of n-6 and n-3 of fish lipids is greatly affected by the n-6 and n-3 of dietary lipids. When the dietary ratio is very high in n-6 fatty acids, fish tend to alter the proportion of PUFAs incorporated in favour of n-3 fatty acids [
48]. It is common to see changes in fatty acid profiles by substituting fishmeal for other lipid sources. However, there needs to be more information on the effects of changes in the retention efficiency of fatty acids. A study carried out in
Seriola dumerili [
26] fed fish with high levels of substitution of fish oils for a mixture of vegetable oils; however, in this case, such high differences were not obtained in terms of efficiency and retention, since the differences in growth concerning the control feed were not so relevant. On the other hand, it can be stated that they are closely related to the productive values obtained for fat, which was significantly lower in fish fed POU, as well as the low retention of EPA and DHA, which, together with the lower levels of these fatty acids in the diet, could have been the trigger for mortality observed in this group.
The highest productive values of FA were observed in the fish fed the CONT diet. In these diets, commercial fish oil was used as a lipid source. These high-quality fish oils are known to be the best lipid source for fish thanks to their high digestibility and their fatty acid composition availability [
51]. These results agree with other studies that show that the dietary fatty acid compositions reflect FA compositions in marine fish [
52]. It is perceived that variations in the fatty acid profile of meals are primarily reflected in the fish composition [
53]. The productive values of the FA of the gilthead seabream show that when an FA is at a lower dietary level, its retention efficiency will increase; the opposite occurs when there is a higher level of FA.
This study found that the best growth occurred in the two control diets containing 30% fishmeal, regardless of whether the rest of the ingredients were organic. Regarding the experimental diets, the fish fed the TRO diet showed the highest growth, followed by the SBS and MIX diets; finally, the POU diet showed the lowest growth. The fish fed the POU diet exhibited the highest mortality, while those fed the CONT, ORG, TRO, SBS, and MIX diets presented similar mortality rates. Regarding nutrient retention efficiency, different organic ingredients in the diets showed significant changes in the retention efficiency of several fatty acids between the treatments. However, no significant differences were found in eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA). Using trout meal and seabass meal by-products in production offers various benefits, including resource efficiency, waste reduction, and promoting a circular economy. Incorporating these by-products into other products or processes minimises environmental impacts and conserves resources. The availability of these raw materials depends on factors related to fish farming, fisheries management, and market demand. Implementing sustainable practices and establishing collaborations within the industry is crucial for maintaining a reliable supply chain. However, the specific growth outcomes can be influenced by factors such as the composition of the diets and the presence of certain raw materials such as poultry meal.
One of the main factors impeding organic production growth is the higher cost of organic feed. However, this does not have to be the case. The present study demonstrates that organic feed can be obtained at competitive prices by utilising by-products from other organic farms. Based on economic indices, completely replacing fishmeal with more organic alternatives containing organic fish by-products is a promising alternative to feeding farmed fish organically. Total replacement and some efficiency parameters appear to affect growth, but slightly enough to still be economically convenient. The findings provide insights into the potential benefits of using organic ingredients in aquaculture diets. Therefore, it is recommended to continue increasing the knowledge in this sector to mitigate the impact of extractive fishing and more aquaculture sustainability, as well as the experimental conclusions that can be drawn.