Nutritional evaluation of shrimp waste and its inclusion in laying diet for meat-type quailsAbstract
The research aimed to evaluate the shrimp waste meal (SWM1) in the diet of European quails in the production phase. A metabolism trial was performed with 96 quails of 28 days of age distributed in a completely randomized design with three treatments (reference diet and two test diets in which SWM replaced 20% and 40% of the reference diet) and four replications of eight birds. There was no difference in metabolizable energy values. In the performance trial 200 quails of 28 weeks of age were distributed in a completely randomized design with four treatments (0, 50 100 and 150 g/kg of inclusion of SWM) and five replications of ten birds. There was reduction in the nitrogen metabolization coefficient with the inclusion of 150 g/kg SWM. The feed intake, production and egg mass worsened with 150 g/kg inclusion. The inclusion of SWM at all levels reduced the values of specific gravity and Hugh units, and the level 150 g/kg promoted reduction in shell percentage and shell thickness. It was concluded that the metabolizable energy of SWM is 2,377 MJ/kg and that the inclusion of SWM in the diet of quails in production can be up to 100 g/kg.
Key words
Alternative feed; chitin; Coturnix coturnix coturnix; shrimp farming waste
INTRODUCTION
Feed cost is one of the main factors that impact poultry production, basically due to the dependence on the use of conventional ingredients (corn and soybean meal) and the constant variation of their prices. In this scenario, the search for alternative ingredients is a solution to reduce production costs and improve competitiveness (Farahat et al. 2013, Abd El-Moneim & Sabic 2019). Several agro-industry wastes have shown promise as alternative ingredients, and research is needed to evaluate the impact of their inclusion in poultry feed as well as the use recommendation.
The residue generated from the processing of shrimp for the separation of the filet has been the subject of study by various segments of the chemical, pharmaceutical, and animal nutrition industries. The interest in this waste comes from the significant volume generated and its chemical composition, whose inappropriate disposal presents high environmental risk (Ogawa et al. 2007).
According to data from IBGE (2021), 63.169.853 tons of shrimp were produced in Brazil in 2020. Considering that the waste generated from the processing to obtain the fillet is composed of the cephalothorax, shell, fillet remains, as well as, small shrimp, and represents approximately 50% of the total weight of the animal (Shahidi et al. 1999, Jeon et al. 2000, Sachindra & Mahendrakar 2005), it was estimated that the volume produced of this waste was 31.584.93 tons.
Regarding the chemical composition, the high content of protein (326.0 to 527.0 0 g/kg), energy value (9.97 to 19.78 MJ of gross energy/kg) and the presence of minerals especially calcium (47.0 to 122.2 g/kg), phosphorus (14.4 to 23.1 g/kg) and sodium (13.3 g/kg) (Rosenfeld et al. 1997, Carranco-Jáuregui et al. 2006, Fanimo et al. 2000, Gernat 2001, Khempaka et al. 2006a, Lima et al. 2007, Brito et al. 2020a, b) are characteristics that make the product feasible to be used in animal feeding.
The possibility of including shrimp waste in poultry feed may result in the reduction of the dependence on the use of soybean meal, which is the main source of protein, coming from a commodity, whose grains, products and by-products present price oscillations depending on market conditions (Cunha et al. 2006). Moreover, the presence of astaxanthin in shrimp waste is an attribute that makes it very attractive for use in poultry farming, since this substance has high pigment power (Lima et al. 2007), which may be a strategy to avoid the use of synthetic pigmenting agents in the feed as a way to improve yolk color, adapting the production system and the final product to the consumers who seek eggs with more intense yolk color without the use of synthetic ingredients for this purpose (Fonseca et al. 2006).
On the other hand, the use of shrimp waste in poultry feed may be limited by its fiber content (153.8 g/kg). Freitas et al. (2002) found a high content of dietary fiber in the shrimp shell meal, attributing it to chitin, normally present in the shells of crustaceans, and these fibers were not digested in the analysis process. Unlike the dietary fiber present in ingredients of vegetable origin, the fiber in shrimp waste is composed of chitin, a polysaccharide of chemical structure very similar to cellulose, whose concentration varies from 17.0 to 32.0 g/kg, depending on processing conditions and species (Shahidi & Synowiecki 1991, Synowiecki & Al-Khateeb 2000). Fanimo et al. (2000) and Khempaka et al. (2011) found that the analyzed shrimp waste had 98.2 and 189.9 g/kg chitin, respectively. Due to the structural similarity with cellulose, chitin has analogous functionality, presenting insolubility to most solvents and low chemical reactivity, as well as resistance to degradation by hydrolytic enzymes (Singla & Chawla 2001) and not being digested by digestive enzymes of animals (Muzzarelli 1986). Thus, it is possible that the nutrients and energy of the rations will be used up, depending on the level of inclusion of this ingredient.
However, the sodium incorporated into the waste during the salting process of shrimp processing may be a technical limit to the inclusion of this ingredient in the formulation of diets when it is chosen not to exceed the minimum recommendation of the nutritional requirements guides. Some reports in the literature have suggested a negative effect of excess sodium in poultry diets on egg laying, performance and egg quality (Fassani et al. 2002, Pizzolante et al. 2006, Barreto et al. 2007), but in many cases the levels adopted exceed the recommendations.
In this context, the present research aimed to determine the energy value of shrimp waste meal and evaluate its inclusion in diets for European quails in the laying phase.
MATERIALS AND METHODS
This study was conducted in a manner that avoided unnecessary discomfort to the animals using proper management and laboratory techniques, and experimental procedures were approved by the Ethics Committee on the Use of Animals - CEUA/UFC (protocol No. 9648290319), according to the ethical principles adopted by the Brazilian Council for the Control of Animal Experimentation.
Two trials were carried out in the poultry sector owned by the Animal Science Department of the Universidade Federal do Ceará, in the city of Fortaleza, Ceará, Brazil, one for metabolism and the other for performance.
The shrimp waste used was obtained in the town of Quixelô, Ceará, Brazil, from manual shrimp fishing. It was generated after the process of shrimp capture, boiling in water and salt, drying at sun, and separation of the fillet from the shell and cephalothorax, through the beating method. The residue was composed of cephalothorax, shell and tail, as well as small shrimps.
After obtaining the residue, it was milled, forming the shrimp waste meal (SWM) that was used in this research.
Determination of chemical composition and metabolizable energy of shrimp waste meal
To determine the value of apparent metabolizable energy (AME) and apparent metabolizable energy corrected for nitrogen balance (AMEn) a metabolism trial was performed using the total excreta collection method. Ninety-six 28-day-old European quails (Coturnix coturnix) were housed in battery metal cages of dimensions 50x50x50 cm (length x width x height), equipped with a trough feeder, pressure drinker and metal trays for excreta collection. The birds were weighed and distributed, according to their weight, in a completely randomized design consisting of three treatments of four replications of eight birds per experimental unit.
The treatments consisted of a reference diet (Table I), formulated according to the nutritional recommendations proposed by Silva & Costa (2009) for growing European quails, considering the feed composition values proposed by Rostagno et al. (2017) and two test diets in which the levels of 20 and 40% replacement of the basal diet by SWM were used.
Composition and nutritional levels of the of the reference diet used in the metabolism assay with quails in the growth phase and of the experimental diets for laying quails.
The trial lasted for seven days, three days for adaptation of the birds to the cages and four days for collection of the excreta. Throughout the trial period, feed and water were provided at will.
For the collection of excreta, the aluminum trays were previously covered with plastic, in order to collect the whole content excreted by the birds. One percent (10 g/kg) ferric oxide was added to the feed as a marker to identify the beginning and the end of the collection period. Two daily collections were performed, at 8am and 4pm, and the excreta were weighed, packed in plastic containers and stored in a freezer at -10 °C for further laboratory analysis.
At the end of the collection period the excreta were thawed, homogenized, weighed, and dried in a forced ventilation oven (55 °C) for a period of 72 hours. Then, samples of pre-dried excreta, diet and SWM were sent to the animal nutrition laboratory, where they were ground in a knife mill with a 16 mesh sieve of 1mm and then subjected to laboratory analysis for determination of dry matter (method 934.01), nitrogen (method 976.05), ether extract (method 920.39), mineral matter (method 942.05), calcium (method 968.08), phosphorus (method 965.17) and sodium (method 985.01) according to the methodology described by AOAC International (2005) and neutral and acid detergent fibers according to the methodology proposed by Van Soest et al. (1991), being determination of the neutral detergent fibre performed in assay with a heat stable amylase and expressed inclusive of residual ash and the acid detergent fibre expressed inclusive of residual ash. The energy was determined in a calorimetric pump (C200, IKA®, Stauten, Germany). The value of apparent metabolizable energy corrected for nitrogen balance (AMEn) was determined using the equations proposed by Matterson et al. (1965).
Shrimp waste meal in the laying diet for quails
The bird performance trial was performed in a conventional shed for laying quails, equipped with galvanized wire cages 35x25x20 cm (length x width x height) with capacity to house five quails per cage, which were arranged in a pyramidal system with linear trough feeder, nipple drinker and egg collection tray.
To carry out the trial, 200 European quails (Coturnix coturnix coturnix) in the production phase at 28 weeks of age were used. The birds were selected based on weight and egg production, then distributed uniformly in cages so that all replications were composed of birds with similar weight and egg production. The quails were then distributed in the cages following a completely randomized design composed of four treatments and five replications of ten birds, with the experimental unit consisting of eight females and two males. The treatments were the control diet and three other diets with the inclusion of 50, 100 and 150 g/kg of SWM.
For the formulation of the diets (Table I) the chemical composition values of the feeds indicated by Rostagno et al. (2017) were used, except for the shrimp waste meal, to which it was considered the values determined in the laboratory, as well as, the ones obtained in the literature. For the nutritional requirements, the recommendations proposed by Silva & Costa (2009) for quails in the laying phase were considered, and the diets were formulated to be isoenergetic in all levels and isonutrient, except for the level of sodium that was relaxed to allow greater inclusion of the evaluated feed.
Metabolization of nutrients and energy from experimental diets
To evaluate the effect of the inclusion of SWM on the metabolization of nutrients and energy in the feed, it was used the total excreta collection method with the 10 g/kg ferric oxide as a marker in the feed. In the fourth experimental period, plastic-coated aluminum trays were placed under the cages. The collection period lasted four days and there was no adaptation period, because the birds were already used to the feed and cages. At the end of the collection period, total feed intake and excreta production of each experimental unit were quantified for subsequent determination of dry matter, nitrogen and energy metabolization coefficients as well as metabolizable energy values of the diets.
For this purpose, excreta samples were dried in a forced ventilation oven at 55 °C, ground in a knife mill with a 16-mesh sieve of 1 mm and then subjected together with the feed samples to laboratory analysis for determination of dry matter (method 934.01), and nitrogen (method 976.05) according to the methodology described by AOAC International (2005). The energy was determined in a calorimetric pump (C200, IKA®, Stauten, Germany). To calculate the metabolizability coefficients of dry matter, nitrogen and gross energy and the values of apparent metabolizable energy corrected by nitrogen balance, it was used the laboratory data applying the equations proposed by Matterson et al. (1965).
Productive performance
The following performance variables were evaluated: feed intake (g/quail/day), eggs production (%), egg weight (g), egg mass (g/quail/day) and feed conversion ratio (g of feed/g of egg). Feed intake was calculated by the difference between the amount of feed offered and the remaining feed at the end of each period. Egg production was recorded daily and the laying percentages were calculated at the end of each period per replicate. To determine the egg weight, once a week, all eggs from each plot were collected and weighed on an electronic scale (sensitivity 0.01g), whose egg weight was obtained by arithmetic mean. The egg mass was calculated by multiplying the average egg weight by the laying percentage of each replication in the period. Fed conversion ratio was calculated from the ratio of feed intake data and the egg mass produced by each replication per period.
Egg quality
The egg quality was evaluated through specific gravity (g/cm3), Haugh units, albumen percentage (%), yolk percentage (%), eggshell percentage (%), yolk color and shell thickness (mm). For the determination of those parameters, all eggs from each plot were collected, identified and taken to the egg quality assessment laboratory, in the Poultry Sector of the Universidade Federal do Ceará, once a week throughout the experimental period, where the eggs were individually weighed on a semi-analytical scale with sensitivity of 0.01 g, to determine the average egg weight. After weighing the eggs, 3 eggs per plot were selected (avoiding broken, cracked or dirty eggs), according to the average weight of each plot, and submitted, in sequence, to the other determinations according to the steps described below.
Initially, the specific gravity (g/cm3) of the eggs was determined according to procedures described by Freitas et al. (2004). Then, the evaluation of the albumen quality was carried out with the determination of the Haugh units, where the eggs were broken on a flat glass surface and had the height (mm) of the dense albumen measured by a depth micrometer (Baxlo Haugh®), that along with the egg weight were applied in the equation: HU = 100 xlog(H−1.7 x W 0.37+7.6), where: HU = Haugh units; H = albumen height in mm and W = egg weight in g.
Following, the yolk was separated from the albumen and weighed on a semi-analytical scale with sensitivity of 0.01 g, and its percentage was obtained by dividing the yolk weight (g) by the egg weight (g) and multiplying by 100. The measurement of the yolk color was performed using a digital yolk colorimeter (Digital YolkFanTM). After breaking, the eggshells were washed and put to dry for 72 hours and weighed on a semi-analytical scale with sensitivity of 0.01 g, with the shell percentage (%) being obtained by dividing the shell weight by the egg weight, and multiplying by 100. The percentage of albumen (%) was obtained by difference, where: % albumen = 100 - (% yolk + % shell).
In order to determine the shell thickness (mm), measurements were taken in three regions: greater and lesser poles and equatorial region of the eggs, using a digital micrometer (Mitutoyo Company, Kawasaki, Japan) with 0.01mm divisions, and calculating the average of the obtained values.
Economic viability
To determine the economic viability of the inclusion of SWM in the diets, the cost of the diets was determined based on the prices of the ingredients in the city of Fortaleza - CE in the experimental period. The cost of the feed per egg mass produced was calculated according to the equation proposed by Bellaver et al. (1985), considering Yi = (Qi x Pi) / Mi, where Yi = amount spent on feed per kilogram of egg in the ith treatment; Pi = price of kilogram of the feed used in the ith treatment; Mi = amount of feed consumed in the ith treatment, and Mi = egg mass in the ith treatment. The economic efficiency index (EEI) and the cost index (CI) proposed by Fialho et al. (1992) were calculated as follows: EEI = (LCei/CTei)x 100 and CI = (CTei/LCei)x 100, where L Cei = lowest feed cost per egg mass, observed among treatments, and CTei = cost of treatment i considered.
Statistical analysis
The statistical analysis was performed using the software Statistical Analysis System, version 9.2 (SAS 2000). The data obtained in the two experiments were subjected to analysis of variance, through the SAS ANOVA procedure. Diet digestibility, quail performance, egg quality and economic viability data were compared with the averages by Dunnett’s test at 5% probability. Additionally, the degrees of freedom referring to the treatments were submitted to polynomial regression, through the SAS GLM procedure, to establish the curve that best described the data behavior and to determine the best level of inclusion of SWM.
RESULTS
Determination of chemical composition and metabolizable energy of shrimp waste meal
The determined chemical composition of the shrimp waste meal (Table II) showed 883.4 g/kg dry matter, 414.1 g/kg crude protein, 246.7 g/kg mineral matter, 51.4 g/kg calcium, 14.5 g/kg total phosphorus, 577.3 and 340.5 g/kg neutral and acid detergent fiber, respectively, and 55.5 g/kg ether extract.
In the results of the assay to determine the metabolizable energy of shrimp waste meal for European quails (Table III), it was found that there was no significant difference between the values of apparent metabolizable energy (AME) and apparent metabolizable energy corrected by nitrogen balance (AMEn) determined in the levels of 20 and 40% replacement of the reference diet, both on as fed and dry matter basis.
Table III. Average values of apparent metabolizable energy (AME), and corrected apparent metabolizable energy (AMEn) of shrimp waste meal determined for European quails expressed on as fed (AF) and dry matter (DM) basis.
Metabolization of nutrients and energy from experimental diets
The metabolization coefficients of nutrients and the metabolizable energy values of the diets during the experiments are presented in Table IV. When comparing the treatments that included SWM and the control treatment, there was a significant effect only for the metabolization coefficient of nitrogen, which was lower in the diet with the inclusion of 150 g/kg of SWM, without effect on the dry matter and gross energy metabolization coefficient, apparent metabolizable energy, apparent metabolizable energy corrected by nitrogen balance on natural matter basis and apparent metabolizable energy corrected by nitrogen balance on dry matter basis. Furthermore, there was a linear decreasing effect for the nitrogen metabolization coefficient (y = 30.4420 – 0.5794x; R2 0.88), apparent metabolizable energy (y = 3.4699 – 0.007x; R2 0.74) and Apparent metabolizable energy corrected by nitrogen balance on dry matter basis (y = 3.3690 – 0.0047x; R2 0.65), without effect of linear or quadratic regression for dry matter metabolism coefficient, gross energy metabolism coefficient and apparent metabolizable energy corrected by nitrogen balance on natural matter basis.
Metabolizability coefficients and metabolizable energy values of the diets for European quails in the laying phase containing shrimp waste meal.
Productive performance
In the results for the performance variables (Table V), a significant reduction in feed intake, production and egg mass was observed only for birds that were fed diets containing 150 g/kg inclusion of SWM when compared to birds that received the control treatment, and no significant effect was detected for average egg weight and feed conversion per egg mass.
However, in the regression analysis, it was observed that with the increasing inclusion of SWM there was quadratic effect in feed intake (y = 31.3312 + 0,4204x – 0,0370x2; R2 0.86), whose highest feed intake was estimated for a diet including 56.8 g/kg of SWM, and linear reduction in egg production (y = 88.4870 – 0.9157x; R2 0.66) and in egg mass (y = 11.8852 – 0.1280x; R2 0.62), without effect of linear or quadratic regression for egg weight and feed conversion.
Egg quality
Regarding the egg quality results (Table VI), significant differences were observed among treatments for specific gravity, Haugh unit, shell percentage, shell thickness and yolk color. When compared to the control treatment, eggs from quails fed the diets containing 5, 10 and 150 g/kg of SWM showed lower values of specific gravity and Haugh unit, while the percentage and shell thickness were lower only in eggs from birds fed the diet with 150 g/kg of inclusion of SWM. On the other hand, the inclusion of SWM improves yolk coloration, with significantly better results obtained when birds were fed the diets containing 100 and 150 g/kg of SWM. In the regression analysis, linear worsening was observed for specific gravity (y = 1.0761 - 0.0007x; R2 0.97), unit Haugh (y = 94.4292 - 94.4292x; R2 0.73), shell percentage (y = 8.0763 - 8.0763x; R2 0.94) and shell thickness (y = 0.2284 - 0.0007x; R2 0.85) and linear improvement for yolk color (y = 6.2094 + 0.0462x; R2 0.88).
Egg quality from European quails in the laying phase fed diets containing shrimp waste meal.
Economic viability
Regarding the results of the economic feasibility analysis (Table VII) it was observed that, in comparison to the control treatment, the cost with feed and the economic efficiency index and cost index were statically identical in all treatments that had the inclusion of SWM. Also, no significant effect was observed in the regression analyses on any of the variables.
Economic evaluation of the inclusion of shrimp waste meal in the feeding of European quails in the production phase.
DISCUSSION
Determination of chemical composition and metabolizable energy of shrimp waste meal
The shrimp waste meal presented values of dry matter, crude protein, mineral matter, calcium, total phosphorus, neutral and acid detergent fiber and ether extract similar to those found by other authors (Rosenfeld et al. 1997, Gernat 2001, Carranco-Jáuregui et al. 2006, Khempaka et al. 2006a, Brito et al. 2020a, b), with the exception of sodium content, which has not been reported in the literature, and showed a high value in the residue used in the present study, which was already expected, considering that the shrimp processing involves salting.
In the determination of the metabolizable energy, it was found no significant difference between the values of AME and AMEn, both on as fed and dry matter basis. Differences between metabolizable energy values for a feed determined in metabolism trials with substitution levels are usually correlated to the characteristics of the feed under study, the main factors being those that affect intake, such as palatability, physical aspect, and fiber content and type that interfere with the passage rate and enzymatic degradation (Sakomura & Rostagno 2016). However, the high concentration of sodium and non-starch polysaccharides, characterized by neutral and acid detergent insoluble fibers present in the evaluated SWM, did not compromise the determination of metabolizable energy at the two levels tested (20 and 40%). Therefore, the average of the AMEn values obtained at the two levels of substitution in the trial can be adopted to characterize the shrimp waste meal, which are 9.95 MJ/kg in dry matter and 8,76 MJ/kg on as fed.
Rosenfeld et al. (1997) and Gernat (2001), both applying the method of Sibbald (1976) for the determination of the corrected apparent metabolizable energy of shrimp waste meal replacing part of the feed for broilers and layers, respectively, obtained values of 10.03 MJ/kg and 9.77 MJ/kg in dry matter, corroborating with the values found in the present study.
Metabolization of nutrients and energy from experimental diets
The lower metabolization coefficient of nitrogen in the diet with the inclusion of 150 g/kg of may be associated to the property of chitin to strongly bind to proteins (Campana-Filho et al. 2007) making this nitrogen unavailable during the digestive and absorptive process, since apparent digestibility of chitin in bird is low betwen 18-24% (Khempaka et al. 2006b). Acording to Gooday (1990) at least two enzymes, such as chitinase and N-acetyl-β-Dglucosaminidase are needed for the digestion and assimilation of chitin. However, Koh & Iwamae (2013) observed that the chitinolytic enzymes activity are limited, with lower activity in the duodenum than in the proventiculus, and that appears not to be stimulated by dietary chitin. Although the metabolizable energy values of the treatment with the inclusion of SWM did not differ from the control treatment, the data on apparent metabolizable energy and apparent metabolizable energy corrected by nitrogen balance based on dry matter had a linear decreasing behavior, which occurred as a function of lower nitrogen retention as there was an increase in the inclusion of SWM, indicated by the worsening of the nitrogen metabolization coefficient.
On the other hand, the high sodium content in the diet with 150g/kg of SWM, may also have had a negative effect on the absorption of amino acids. Although sodium is essential for the absorption of amino acids, due to its participation in sodium-dependent transporters, excess sodium in the diet can lead to imbalances that alter homeostasis and the normal function of intestinal transporters. These changes are associated with disturbances in the sodium gradient, which can trigger negative feedback mechanisms, where the body can adjust the expression or activity of sodium-coupled transporters to maintain electrolyte balance, which can compromise the efficiency of amino acid absorption. Excess sodium can also cause fluid retention and changes in gastrointestinal motility, which can affect the luminal environment of the intestine, influencing the absorption of several nutrients, including amino acids. Furthermore, high levels of sodium in the diet can interfere with the absorption of other nutrients that compete for the same transport mechanisms or that are affected by changes in the intestinal environment.
Considering the composition of the evaluated feed, the initial hypothesis was that the inclusion of this residue could compromise the use of nutrients and energy of the feed, because the high content of animal fiber present in SWM used in this study (340.5 g/kg of acid detergent fiber and 547.3 g/kg of neutral detergent fiber) could compromise the digestibility of nutrients, mainly because most of this fiber is represented by chitin, whose concentration in shrimp waste varies from 170 to 320 g/kg, depending on the processing conditions and shrimp species (Shahidi & Synowiecki 1991, Synowiecki & Al-Khateeb 2000). However, the absence of a significant effect in the test comparing the means of the control treatment with those that included SWM for dry matter metabolization coefficients and gross energy and metabolizable energy values indicate that the inclusion of up to 150 g/kg of SWM does not affect their utilization.
Productive performance
The inclusion of SWM had a negative effect on quail performance, specifically on feed intake, laying and egg mass for birds fed the diet containing 150 g/kg of SWM. The effect on feed intake may be associated to the characteristics of the feed under study. The high fiber content of the diet with higher inclusion of SWM (82.4 g/kg of of acid detergent fiber and 170,9 g/kg of of neutral detergent fiber) may have interfered with the passage rate and enzymatic degradation of the feed (Sakomura & Rostagno 2016), increasing the stay time in the gastrointestinal tract and, consequently, increasing the feeling of satiety which, in turn, reduced feed intake.
On the other hand, the high sodium content of SWM caused the diet with 150 g/kg of SWM inclusion to have increased level of this mineral by 80.4% of the nutritional requirement. The higher level of sodium in the diet may induce reduction in feed intake and increase in water consumption in an attempt not to compromise the osmotic balance and acid-base balance of the body (Lima et al. 2011). Furthermore, the high water intake associated with the higher level of sodium in the diet and the higher presence of fiber may have acted synergistically and caused a feeling of satiety in the birds decreasing feed intake.
Several studies have shown that birds fed diets with excess sodium, increase water intake and excretion of this mineral as a regulatory mechanism of water homeostasis and maintenance of acid-base balance, to the detriment of feed intake, which may explain the reduction found in this parameter, besides the fact that levels above 5.0 g/kg promote toxicity and decrease performance variables (Leeson & Summers 2001).
It is important to consider that although the sodium requirement (Silva & Costa 2009) is 2.3 g/kg for laying quails, in the literature there is divergence for the recommendation of the ideal sodium level, which can be associated to genetics, bird age and environmental conditions, as well as the levels tested in each study. This suggests that it is possible to maintain bird performance within normal parameters when they are fed diets containing sodium levels above the recommendation between 2.4 and 2.8 g/kg (Barreto et al. 2007, Ribeiro et al. 2008), which is proven in this study, considering that the diet with inclusion of 100 g/kg of SWM had 2.8 g/kg of sodium and the performance results were similar to the control treatment.
Regarding the effects on egg production, it can be inferred that this parameter was negatively affected by the reduction in feed intake associated with the tendency of reduction metabolizable energy values observed in the diet metabolism assay of the diets for European quails in the laying phase, which compromised the energy intake of the birds. According to Leeson & Summers (1997) meeting the metabolizable energy requirement of the laying bird is directly related to egg production. Thus, a reduction in the daily energy intake will promote a reduction in production, which was observed for the quails in this study.
Considering that the level of protein and especially of amino acids in the feed are two important factors for egg size or weight, since they influence the availability of amino acids for metabolic processes (Leeson & Summers 1997), it was observed that the average egg weight did not vary significantly between treatments, although nitrogen metabolization and feed intake reduced as the SWM was included. However, it should be considered that there was a reduction in egg production and, consequently, in the amino acid requirements for egg formation, which may have ensured that eggs with similar egg weights were produced. Furthermore, the diets were calculated to maintain synthetic amino acid supplementation, which may have contributed to a better amino acid profile for the birds since the reduction was in the metabolization of total nitrogen in the diet, which includes protein and non-protein nitrogen. In the context, is important to consider that chitin is a polysaccharide that contains non-protein nitrogen, so that the reduction in the nitrogen metabolism coefficient was probably due to an increase in the excretion of chitin, whose degradation is less than 30% (Jeuniaux & Cornelius 1978)
In turn, considering that egg mass depends on egg production and average egg weight, and that egg weight did not vary between treatments, the effects on egg production were reflected directly in egg mass.
For feed conversion, it was observed that although the numbers indicate a worsening of that variable between the results obtained for the different levels of SWM and the control group, there was no significant difference. This type of result can be associated with the proportionality between intake and production values, since the reduction in performance was a reflection of the lower feed intake by the birds fed with SWM.
The effects of inclusion of SWM in the diet on quail performance observed in the present study differ, in part, from some reports for the use of shrimp waste as feed for laying hens. Gernat (2001) reported increased feed intake without influence on egg production and consequently poorer feed conversion when SWM replaced soybean meal from 40% (94 g/kg SWM in the diet), Carranco et al. (2003) and Carranco-Jáuregui et al. (2006) observed no significant differences in production variables when including up to 250 g/kg of SWM. However, it is worth noting that the authors do not report, in the characterization of the product tested in the feed, the excess of sodium, this characteristic being inherent to the type of processing from which the residue is obtained.
Egg quality
The negative effect of the inclusion of SWM on the Haugh unit may reflect the reduction of the nitrogen metabolization coefficient observed in this study, considering that this parameter is directly related to the quality of the protein secreted in the oviduct. Thus, the unavailability of amino acids linked to chitin from SWM did not provide the contribution to the formation of albumen with quality compatible with that obtained in the control treatment. However, it should be considered that although there was a reduction in the values found in all treatments with inclusion of SWM, they are within excellent standards of albumen quality (value greater than 72) according to the United States Department of Agriculture (USDA 2000). Moreover, it is known that blood pH must remain stable for the proper functioning of physiological processes, occurring changes in acid-base balance when there is excess of some ion in the diet such as sodium and chloride, influencing the homeostasis and thus, failures may occur in maintaining this electrolyte balance forcing the animal organism to divert part of its resources to achieve homeostasis at the expense of other functions such as growth and production, (Ribeiro et al. 2008, Lima et al. 2015).
The effects on albumen quality observed, differ from some studies with laying hens. Carranco et al. (2003) and Carranco-Jáuregui et al. (2006) found no significant differences for Haugh unit using up to 250 g/kg of SWM in laying hens feed, as well as Chacón-Villalobos et al. (2016) who included SWM at the level of up to 150 g/kg. However, even though there was a worsening in the parameters of albumen quality, the percentage of albumen among treatments containing SWM did not differ from the control treatment, showing that even with lower quality, protein deposition in the albumen occurred. Similarly, the percentage of yolk did not differ in the treatments containing SWM when compared to the control treatment, which may be associated to the non-commitment of energy utilization of the feed, since the values of metabolizable energy corrected by the nitrogen balance were not affected, maintaining the deposition of lipids for yolk formation.
Whereas the worsening observed in the shell quality parameters can be associated not only to the presence of chitin in SWM, which possibly hindered the absorption of nutrients, especially minerals, due to its characteristics similar to those of fibers found in vegetables, but also to the presence of common salt in the SWM, added during shrimp processing. Composed of 397 g/kg sodium and 596 g/kg chlorine (Rostagno et al. 2017), common salt increased the concentration of these minerals in the diets with higher inclusion of SWM, whose sodium content determined was 26. 6 g/kg. Thus, the inclusion of SWM inevitably promoted increase in the concentration of sodium in the ration that was already above the recommendation (2,3 g/kg), starting at the level of 100 k/kg. Besides sodium, the amount of chloride certainly also increased in the rations.
According to Mongin (1968) the eggshell is the variable most affected by the variation in the levels of sodium and chloride in the rations, due to changes in the acid-base balance, which is an important factor in eggshell formation. Hall & Helbacka (1959) suggested that the deposition of calcium carbonate in eggshell depends on blood pH, where sodium and chloride ions are the main regulators, and therefore the proportion of these minerals in the diet can result in metabolic acidosis or alkalosis (Cohen et al. 1972).
The maintenance of acid-base balance is important because during shell formation, there is a reduction in the pH of the uterine fluid, resulting in an acidosis condition, which is aggravated by carbonate formation by the shell gland, and under normal conditions, can be partially compensated by hyperventilation and the formation of acidic urine. This compensation is necessary because the optimal activity of carbonic anhydrase is found in a slightly alkaline environment (Chen & Balnave 2001). However, under acidosis conditions, due to excessive chloride intake, there is a limitation of calcium transport to the shell gland and a reduction in the concentration of bicarbonate in the lumen, worsening the shell quality (Leeson & Summers 2001).
Furthermore, according to Gal-Garber et al. (2003) and Costa et al. (2012) under conditions of electrolyte imbalance, caused by the ingestion of feed rich in chloride and especially sodium, there is an alteration in the kinetic behavior of the small intestine of birds, possibly with the reduction of nutrient absorption by the sodium and potassium pump, especially calcium. With the reduction in absorbed calcium, a smaller amount of this mineral will be available for eggshell formation, producing eggs with a more fragile shell.
The results obtained for shell quality differed from those found by Gernat (2001), who tested soybean meal replacement up to 80% by SWM and observed no significant effect on the specific density of eggs from laying hens, and Carranco et al. (2003) who found no significant differences in egg shell thickness of eggs from hens fed levels up to 250 g/kg of inclusion of SWM. On the other hand, the results observed in the present study corroborate with those found by Chacón-Villalobos et al. (2016) who observed decreasing values for eggshell thickness when the inclusion levels of SWM increased up to 150 g/kg of in the diets. However, it should be considered that the divergence of the results can be attributed to the type of shrimp processing, in which the salting process is not always used.
Whereas the values obtained for yolk coloration show that the presence of astaxanthin in shrimp waste, a highly pigmenting carotenoid compound (Lima et al. 2007), resulted in improved yolk pigmentation when SWM was included at levels of 100 and 150 g/kg. As carotenoids are not synthesized by the animals their addition is used as a feed supplement providing pigmentation characteristics in these animals, and in poultry, aiming to increase the color of the egg yolk, increasing its quality and acceptance by the consumer market (Fonseca et al. 2006).
Other authors have reported a significant increase in yolk coloration with the use of SWM both as a replacement for soybean meal and for inclusion in commercial laying hens diets, observing an improvement in this parameter at 20% replacement and 150 g/kg of inclusion levels (Gernat 2001, Carranco-Jáuregui et al. 2006). The inclusion of SWM in the diet of laying hens at up to 250 g/kg, significantly increased the color of the egg yolk and the concentration of astaxanthin in them (Carranco et al. 2003), proving that this pigment is transferred to the egg.
Economic viability
Regarding the economic analysis, it was found that the cost of the kilogram of the tested diets gradually reduced with the inclusion of SWM, from $0.23 for the control diet to $0.19 for the diet with 150 g/kg of SWM, which is approximately 170 g/kg. However, the reduction in the cost per kilogram of feed did not influence the feasibility results, since the level of SWM did not affect the feed conversion rate of the birds, as the economic feasibility variables are a reflection of the efficiency of the birds in each treatment in converting the feed intake into egg mass.
However, it should be considered that, although the economic viability was statistically similar among treatments, the performance of birds fed with 150 g/kg of SWM was inferior to the other treatments, due to the low intake, which negatively affected production and egg mass. Although from the point of view of economic evaluation this reduction has been compensated by the lower cost of the feed consumed, from the technical point of view, the results obtained for this treatment cannot be considered viable, since it impairs the achievement of an expected standard of egg production for the birds, which is important to obtain the number of eggs to be made available to the market.
Therefore, it is concluded that for European quails, the corrected apparent metabolizable energy of shrimp waste meal is 9.95MJ/kg of dry matter and the inclusion of shrimp waste meal in the diet for European quails in production can be up to 100 g/kg of.
ACKNOWLEDGMENTS
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brasil) - Finance Code 001 and by Conselho Nacional de Desenvolvimento Científico (CNPq, Brasil).
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