Elsevier

Aquaculture

Volume 530, 15 January 2021, 735879
Aquaculture

Effect of dietary poultry meal and oil on growth, digestive capacity, and gut microbiota of gilthead seabream (Sparus aurata) juveniles

https://doi.org/10.1016/j.aquaculture.2020.735879Get rights and content

Highlights

  • Poultry by-products replaced fishmeal up to 83% without impair growth performance and feed efficiency of gilthead seabream.

  • Poultry by-product meal did not affect gut microbiota.

  • The fishmeal replacement by poultry by-product improves economic efficiency

Abstract

This study aimed to evaluate the effect of replacing fish meal by poultry by-product meal (PBM) in actual commercial standard diets for gilthead seabream juveniles on growth performance, diet digestibility, digestive function, intestinal microbiota, and provide an economic analysis of using PBM in practical diets.

Six isoproteic and isolipidic diets were formulated including increasing levels (from 0 to 37.5%) of PBM in replacement of fish meal, corresponding to a fish meal protein replacement in the diets up to 83%. Each diet was randomly assigned to triplicate groups of fish (IBW 63 g) and the growth trial lasted 70 days. No differences between groups were observed on growth performance, voluntary feed intake, feed efficiency, nitrogen utilization, and whole-body composition. Digestive enzymes activity and the ADC of protein, phosphorus, and energy were also not affected by dietary treatment. Regarding gut microbiota, fish fed diet PBM22.5 showed higher species richness and diversity of digesta microbiota, but no differences between groups were observed in mucosa OTUs, richness, and diversity indices. The cost of diet formulation decreased with the dietary replacement of FM by PBM, highlighting the potential of poultry by-products inclusion in commercial diets.

Overall, this study indicates that dietary FM could be replaced at least up to 83% with PBM in diets for gilthead seabream juveniles without affecting growth performance and feed utilization while improving the economic efficiency of these diets.

Introduction

Aquaculture is recognized as a crucial player for the blue growth economy and food security for the human population, a central point of the United Nations Agenda 2030 for sustainable development goals (UN General Assembly, 2015). However, to support aquaculture blue growth, resilient and sustainable ingredients have to be used in aquafeeds as an alternative to the traditional fisheries products.

Plant ingredients have been extensively used as major dietary alternative protein sources, due to their relatively low market price and high availability (Gatlin et al., 2007). Nevertheless, high dietary levels of plant feedstuffs still pose problems due to the presence of antinutritional factors and potential amino acid imbalances that may impair fish growth and feed intake and compromise intestinal health and function (Oliva-Teles, 2012; Espe et al., 2012; Krogdahl et al., 2010).

Since the re-authorization of the use of non-ruminant processed animal proteins (PAP) in aquafeeds in Europe (EC Regulation No 56/201), these ingredients have received increased interest as an alternative to fishmeal (FM) and plant protein concentrates. PAP are cost-effective and sustainable feedstuffs, have relatively high protein content, generally more balanced amino acid profile, and a lower carbon footprint than the majority of plant feedstuffs (Hatlen et al., 2013; Hill et al., 2018).

Poultry by-product meal (PBM) is a highly palatable PAP, made from by-products of poultry slaughterhouses and poultry processing plants, with a high protein content (58–65%) and an essential amino acid profile similar to that of FM, except for the lower levels of lysine and methionine (Hill et al., 2018; Galkanda-Arachchige et al., 2020). The potential of PBM to replace dietary FM has been studied in several fish species with different results. The maximum dietary incorporation level was lower than 30% for tench, Tinca tinca (González-Rodríguez et al., 2016); chinook salmon, Oncorhynchus tshawytscha (Fowler, 1991); sunshine bass, Morone chrysops x M. saxatilis (Webster et al., 1999); or golden pompano, Trachinotus ovatus (Ma et al., 2014); circa 40% for the Japanese sea bass, Lateolabrax japonicus (Wang et al., 2015) and red sea bream, Chrysophrys major (Takagi et al., 2000); 50–60% for rainbow trout, Oncorhynchus mykiss (Steffens, 1994; Parés-Sierra et al., 2014) and cobia, Rachycentron canadum (Watson et al., 2014); and as high as 67% for Florida pompano, Trachinotus carolinus (Riche, 2015) and red drum, Sciaenops ocellatus (Kureshy et al., 2000).

For gilthead seabream, utilization of PBM in aquafeeds was already the object of a few studies. In a first study, performed before the interdiction of using PBM in Europe, Nengas et al. (1999) concluded that using a high-quality PBM total dietary replacement of FM by PBM could be achieved, while with a low-quality PBM reduced growth performance was observed with a dietary FM replacement higher than 50%. Modern technological processes, used after the EU re-authorization of using PAP in aquafeeds, have guaranteed the production of more stable and high-quality PBM. New technological processes have to ensure feed safety, by heat-treating raw materials to kill microbes and have to ensure the chemical quality, by for example guarantee the quality and freshness of raw material, delivering a high standard final product (Jędrejek et al., 2016). Davies et al. (2019) showed that up to 75% of FM protein could be replaced by PBM without negatively affecting growth performance, though feed intake and feed and protein utilization efficiency were reduced. Similarly, Karapanagiotidis et al. (2019) showed that 50% and 100% FM replacement by PBM reduced body weight gain and feed utilization of gilthead seabream, which the authors attributed to lower feed intake and lower methionine and lysine. The authors further confirmed that if the diets were supplemented with lysine and methionine a 50% FM replacement (the highest level tested) was possible without negative effects in fish performance. Yet in another study, it was shown that if adequately supplemented with methionine and lysine, PBM could completely replace dietary FM without compromising growth, digestive enzymes activities, and fish welfare (Sabbagh et al., 2019).

Adding to zootechnical and digestive performances, replacement of FM by alternative protein sources can also affect fish gut health, including its microbial population or microbiota (Nayak, 2010; Perez et al., 2010; Estruch et al., 2015; Ringø et al., 2016; Egerton et al., 2018). The gut microbiota has a key role in fish nutrition, immunity, and health, and its imbalance or dysbiosis can promote immune suppression and contribute to the development of fish diseases (Estruch et al., 2015; Perez et al., 2010; Egerton et al., 2018). Maintenance of well-balanced gut microbiota is thus of critical importance for fish (Estruch et al., 2015; Ringø et al., 2016). Being largely dependent on host-diet composition, gut microbiota modulation upon nutritional changes has been a focus on most recent studies, in particular, those testing alternative protein and lipid sources to fish meal or fish oil (Hartviksen et al., 2014). The effect of dietary inclusion of PBM on the gut microbiota is, however, largely underexplored in animal nutrition in general, and in fish nutrition in particular. The few studies available were done in the salmonids Atlantic salmon, Salmo salar, and rainbow trout with somehow contradictory results. For instance, in Atlantic salmon, the dietary inclusion of poultry by-products led to a microbiota modulation when compared to the control diet (Hartviksen et al., 2014), On the contrary, in rainbow trout, such inclusion did not affect microbiota (Rimoldi et al. (2018).

Following the recent evidence of the good acceptance of high PBM inclusion levels in diets for gilthead seabream, this study further aimed to evaluate the effect of replacing FM by PBM in diets formulated according to actual commercial standards on gilthead seabream performance, diet digestibility, digestive function, and intestinal microbiota, and to perform an economic analysis of dietary PMP incorporation in practical diets.

Section snippets

Material and methods

The present study was conducted according to the Directive 2010/63/EU of the European

Parliament and of the Council on the protection of animals for scientific purposes and was performed by accredited scientists in laboratory animal science by the

Portuguese Veterinary Authority (DGAV-Portugal), following FELASA category C

recommendations.

Results

Fish promptly accepted all diets and neither pathological signs nor mortality were observed during the trial. Growth performance, expressed as final body weight, weight gain, and daily growth index, was unaffected by the dietary inclusion of PBM (Table 2). Similarly, voluntary feed intake, feed efficiency, protein efficiency ratio, and protein retention (as a percentage of protein intake) were also unaffected by the dietary PBM inclusion level.

At the end of the growth trial, the whole-body

Discussion

PAPs, including PBM, have high protein content, lack of anti-nutritional factors, are highly palatable and have high potential as a dietary protein source for aquaculture fish (Oliva-Teles et al., 2015). Contrary to plant protein sources, PAPs have however high variable composition, depending on the quality of raw materials and processing methods and maybe limiting in essential amino acids, such as methionine and lysine (Galkanda-Arachchige et al., 2020). The optimum dietary replacement level

Author statement

All authors declare that they have contributed to the conception and design of the study or acquisition of data, and analysis including interpretation of data, drafting of the article, and finally approval of the submitted version. All authors agree to authorship and submission of this manuscript for peer review.

Declaration of Competing Interest

The authors declare that they have no conflict of interest.

Acknowledgments

F·F was supported by grant-funded by ALGALUP project (ref:0558-ALGALUP-6). RM was supported by grant-funded by FCT (ref: SRH/BD/115870/2016). This work was supported by the R&D&I project “Development of innovative sustainable protein and omega-3 rich feedstuffs for aquafeeds, from local agro-industrial by-products”, reference POCI-010145-FEDER-030377, funded by European Regional Development Fund (ERDF) and Portuguese Foundation for Science and Technology (FCT); by the InovFeed project (ref.

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      The PCoA plot showed no clear clustering of microbial samples, and the α-diversity evaluated by Shannon and Simpson index was not significantly different between the FM group and treatment groups, indicating the overall microbial community structure was not altered by PBM replacement. However, dietary incorporation of PBM remarkably increased diversity indices in digesta but not in the mucosa samples of gilthead seabream [60]. It has also been found that microbiota richness was significantly increased both in intestinal digesta and mucosa samples of Atlantic salmon upon PBM incorporation in the diet [61].

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