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Latin american journal of aquatic research

versión On-line ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.47 no.3 Valparaíso jul. 2019

http://dx.doi.org/10.3856/vol47-issue3-fulltext-8 

Research Article

Effects of dietary fatty acids on the reproduction of South American female catfish Rhamdia quelen (Quoy & Gaimard, 1824)

Cleonice Cristina Hilbig1  2 

Nivaldo Ferreira do Nascimento2 

Adriano Luis Heinen3 

Aldo Tovo Neto2 

Jackson Pablo Funghetto3 

Robie Allan Bombardelli3 

Fábio Meurer4 

Laura Satiko Okada Nakaghi2 

1Universidade Federal da Grande Dourados, Dourados, MS, Brasil

2Centro de Aquicultura da UNESP (CAUNESP), Universidade Estadual Paulista, São Paulo, Brasil

3Universidade Estadual do Oeste do Paraná, Toledo, PR, Brasil

4Universidade Federal do Paraná, Jandaia do Sul, PR, Brasil

ABSTRACT

The effects of a diet supplemented with 5% marine fish oil, 5% refined palm oil, 5% soybean oil, and a combination of the three on reproductive parameters of females Rhamdia quelen was investigated. Spawning was artificially induced to evaluate rates of fertilization, hatching and larvae normality. Fatty acid profiles of the diets, ovaries and oocytes were determined. A higher spawning rate (%) was observed for diets containing fish oil (78.65 ± 3.60) and palm oil (77.15 ± 3.97), followed by oil mix (65.46 ± 4.57). The diet containing soybean oil was associated with significantly lower fertilization (60.14 ± 5.66; P < 0.05) than the palm and fish oil diets. Lower fertilization may be explained by a high level of n-6 fatty acids in the diet, which possibly accelerate the oocyte maturation. Satisfactory fecundity (P > 0.05) were observed for all tested diets, whit 289.77 ± 23.90 (palm oil) until 323.31 ± 38.45 oocytes g-1 body weight (fish oil). The treatments were not shown to influence oocyte size, larval size or rate of larva deformity. Oocyte fatty acid composition was like that of gonads. Docosahexaenoic (DHA; C22:6 n-3) fatty acid was preferentially deposited in ovaries and oocytes. Ratios of n3/n6, DHA/EPA, EPA/ARA, did not affect the reproductive performance of females. Therefore, regarding female reproductive performance, the vegetable lipid sources tested are suitable for being used in R. quelen diet, and palm oil, in particular, is considered an excellent alternative to fish oil.

Keywords: broodstock; lipid sources; puberty; fecundity; spawning; aquaculture

INTRODUCTION

Fish oil is considered the best source of fatty acids for commercial aquaculture feeds, but its financial and environmental costs challenge its use for nutrition and production of freshwater fish (Turchini et al., 2009). Vegetable oil has been used for sustainable partial or complete replacement of fish oil in some fish diets, including for broodstock nutrition (Babalola et al., 2011).

Marine fish oils have high concentrations of docosahexaenoic (DHA; C22:6 n-3) and eicosapentaenoic (EPA; C20:5 n-3) acids as well as considerable levels of arachidonic acid (ARA; C20:4 n-6), none of which are present in vegetable oils (Bell & Sargent, 2003). These long-chain poly-unsaturated fatty acids (PUFAs) are necessary for normal fish growth (Izquierdo et al., 2001) and regulate responses to the steroid hormones that influence gonad development, sexual maturation and the reproductive cycle (Navas et al., 1998; Zhang et al., 2013).

Although not present in vegetable oils, ARA, EPA and DHA can be produced by freshwater fish from their fatty acid precursors, linoleic (LA, C18:2n-6) and linolenic (LNA, C18:3n-3) acids. Most freshwater fish can convert LA into ARA, and LNA into EPA and, subsequently, DHA, through a series of elongations and desaturations (Sargent et al., 2002; Turchini et al., 2006). However, competitive interactions can occur between LA and LNA, because they compete for the enzymes involved in the biosynthesis of ARA, EPA and DHA (Sargent et al., 1999). The ratio of n3/n6 fatty acids in broodstock diet must also be considered (Furuita et al., 2007), as fatty acid ratios (EPA/ARA/DHA, n3/n6) directly affect the composition and quality of eggs in a species-specific manner (Ng & Wang, 2011).

Palm oil is considered a potential alternative to fish oil (Aysi & Zhao, 2014). It has been reported that tilapia Oreochromis niloticus receiving palm oil diets showed earlier first spawning, a shorter inter-spawning interval, a more extended period of broodfish fertility, higher total egg production, higher hatching rates and reduced larval deformities compared to broodfish fed a fish oil based diet (Ng & Wang, 2011). Soybean oil, on the other hand, is the world's second most commonly produced oil (Aysi & Zhao, 2014). Liang et al. (2014), mixing fish and soybean oil, proportions of 2.2:1, respectively, in diets for tongue sole Cynoglossus semilaevis obtained higher rates of fertilization, higher survival and lower larva abnormalities. The ready availability and low cost of palm and soybean oil make them promising alternatives to fish oil.

The South American catfish Rhamdia quelen (Quoy & Gaimard, 1824) is an important aquaculture species in temperate and subtropical South America (Ittzés et al., 2014). It can efficiently convert C18 n-3 and n-6 fatty acids into the long-chain PUFAs ARA, EPA and DHA when fed vegetable oil (Vargas et al., 2014). R. quelen reaches sexual maturity at 12 months, and oocyte development is asynchronous, with fractional spawning (Ghiraldelli et al., 2007). The natural breeding period is August to March in southern Brazil (Gomes et al., 2000).

Few studies (Coldebella et al., 2013) focusing on fatty acids profiles of ovaries and eggs of R. quelen have been conducted using soybean oil at different levels of inclusion. The present study compared the effects of diets based on fish oil and those supplemented with soybean or palm lipids, alone and in combination with fish oil, on the growth, reproductive performance, and the fatty acid composition of ovaries and oocytes in South American catfish in their first reproductive cycle.

MATERIALS AND METHODS

Ethics

The ethics committee on the use of animals of the Paulista State University approved the experimental protocol no 6728/12. The study took place at the Instituto de Pesquisa em Aquicultura Ambiental (INPAA), Universidade Estadual do Oeste do Paraná, Toledo, Paraná, Brasil (24°46’S, 53°43’W) from May 2013 to April 2014.

Experimental diets

Four isoproteic and isocaloric diets containing 38% crude protein and 5% lipids were formulated: 5% of marine fish oil, 5% palm oil, 5% soybean oil, and a combination of the three (MIX) (Table 1). Experimental diets were extruded in an Exteec extruder and dried under forced ventilation at 55°C for 12 h, producing 4 mm pellets. After weighing, oils were gradually added over 30 min using a rotating mixer. The fatty acid composition of the diets was analysed at the Instituto de Tecnologia de Alimentos, ITAL- Campinas/São Paulo, using the methods of Zenebon & Pascuet (2005) for total lipid extraction, and Horwitz et al. (2005) and Firestone (2014) for fatty acid profile (Table 2).

Table 1 Formulation and mean values of the composition of experimental diets (dry matter). 

Ingredients g kg-1 Experimental diets
SO PO FO MIX
Soybean meal 300.00 300.00 300.00 300.00
Maize (ground grain) 255.60 255.60 255.60 255.60
Salmon meal 200.00 200.00 200.00 200.00
Wheat gluten 93.60 93.60 93.60 93.60
Dicalcium phosphate 75.71 75.71 75.71 75.71
Soybean oil 50.00 16.60
Refined palm oil 50.00 16.60
Fish oil 50.00 16.60
Premix1 20.00 20.00 20.00 20.00
Salt (NaCl) 5.00 5.00 5.00 5.00
BHT (antioxidant) 0.20 0.20 0.20 0.20
Fungicide (propionic acid) 0.01 0.01 0.01 0.01
Nutrients (%)2
Dry matter 95.62 95.11 93.49 96.35
Crude protein 38.46 38.51 37.92 38.84
Ether extract 6.36 7.74 7.20 6.07
Crude fiber 1.72 2.61 2.19 2.27
Ash 12.93 12.93 12.81 13.20
Nitrogen-free extract 36.15 33.32 33.37 35.97

1Basic composition: vitamin A: 1,000,000 UI kg-1, vitamin D3: 500,000 UI kg-1; vitamin E: 20,000 UI kg-1; vitamin K3: 500 mg kg-1; vitamin B1: 1,900 mg kg-1; vitamin B2: 2,000 mg kg-1; vitamin B6: 2,400 mg kg-1; vitamin B12: 3,500 mg kg-1; vitamin C 50 g kg-1; Niacin: 5,000 mg kg-1; Pantothenic acid: 4,000 mg kg-1; Folic acid: 200 mg kg-1; Biotin: 40 mg kg-1; Manganese: 7,500 mg kg-1; Zinc: 25 g kg-1; Iron: 12.5 g kg-1; Copper sulphate: 2,000 mg kg-1; Iodine: 200 mg kg-1; Selenium: 70 mg kg-1 BHT 300 mg kg-1.

2Weende analysis carried in Laboratório de nutrição Animal (LANA-Unesp Jaboticabal-SP).

SO: diet containing soybean oil; PO: diet containing refined palm oil; FO: diet containing marine fish oil; MIX: diet containing a combination of the three oils.

Table 2 Fatty acid profile (% of total FA) of the diet containing different lipid sources fed to Rhamdia quelen females. 

Fatty acid (%)1 Diets
SO PO FO MIX
C12:0 0.00 0.21 0.11 0.11
C14:0 0.45 0.97 2.13 1.20
C15:0 0.00 0.11 0.34 0.11
C16:0 13.86 29.43 18.61 21.24
C17:0 0.11 0.11 0.34 0.22
C18:0 3.98 4.19 3.92 4.03
C 20:0 0.34 0.32 0.34 0.33
C22:0 0.34 0.11 0.11 0.22
C24:0 0.00 0.75 0.00 0.00
Σ Saturated 19.09 36.20 25.90 27.45
C16:1n7 0.57 0.64 4.15 1.74
C 17:1 0.00 0.00 0.22 0.11
C18:1n9 28.30 37.92 28.48 31.37
C20:1n11 0.45 0.43 0.90 0.54
C22:1 0.00 0.00 0.11 0.00
C24:1 0.34 0.21 0.34 0.22
Σ Mono-unsaturated 29.66 39.21 34.19 33.99
C18:2n6 43.18 20.62 23.21 28.87
C18:3n3 3.86 1.50 2.91 2.83
C20:2n6 0.23 0.21 0.45 0.33
C20:3n6 0.11 0.11 0.22 0.11
C20:3n3 0.00 0.00 0.11 0.11
C20:5n3 (EPA) 0.68 0.00 2.58 1.31
C 22:6n3 (DHA) 1.02 0.97 3.81 1.85
C22:5n3 0.23 0.32 0.90 0.44
Σ Poly-unsaturated 49.32 23.74 34.19 35.84
Σ Omega 3 5.80 2.79 10.31 6.54
Σ Omega 6 43.41 20.84 23.65 29.19
n-3/n-6 0.13 0.13 0.44 0.22
Total lipids (g 100-1 g) 9.17 9.73 9.33 9.61

1Analyzes carried out in the Centro de Ciência e Qualidade de Alimentos-ITAL, Campinas/São Paulo.

SO: diet containing soybean oil, PO: diet containing refined palm oil, FO: diet containing marine fish oil, MIX: diet containing a combination of the three oils.

Fish and experimental design

Two-thousand juveniles of Rhamdia quelen at 60 days post-hatching (dph) of mixed-sex obtained from a commercial fishery were distributed among 20 outdoor 12 m2 concrete tanks (water volume of approximately 9.3 m3 and depth of 100 cm), 100 fish/tank. The mean ± SE (standard error) initial weight of the fish was 24.50 ± 0.78 g, total length 14.10 ± 0.41 cm and standard length 11.54 ± 0.26 cm, with no significant differences (P > 0.05) among tanks.

The fish were randomly assigned to one of the four diet groups, five tanks per diet. Fish were fed twice daily, at 10:00 and 16:00 h, and were weighed and measured monthly to adjust the feeding rate to 2% of body weight d-1. In October 2013, ~270 dph, sexual dimorphism was evident from external features and the ease with which sperm could be obtained through hand stripping. Twenty females from each tank (total 400) were randomly selected, weighed, measured (total length) and transferred (keeping treatments units) to each of 20 4×2×1 m cages in 800 m2 tanks (20 females/cage) with good water circulation, which not required artificial aeration. Feeding continued at 2% of body weight d-1 for another six months.

Water temperature was monitored twice daily, morning (17.45 ± 1.82°C) and afternoon (27.20 ± 1.16°C) with the YSI 550 A. The dissolved oxygen (YSI 550 A) and pH levels (Tecnal® Tec 5) were recorded weekly, at 06:00 h: 5.64 ± 0.15 mg L-1 and 7.11 ± 0.04; and at 16:00 h: 6.67 ± 0.16 mg L-1 and 7.37 ± 0.08, respectively. Ammonia levels were checked monthly (0.03 ± 0.01 mg L-1) by colorimetry (Koroleff, 1976).

Spawning and sampling

In February 2014, five females exhibiting a rounded abdomen, reddish protruding urogenital papillae and uniform oocyte size, indicating reproductive maturity, were selected from each cage and transferred to 20 fiberglass tanks of 500 L for artificial insemination (n = 100, 5 tank-1). Tanks were maintained in a recirculation system with mean water temperature of 26.5 ± 1.5°C and dissolved oxygen of 5.5 ± 1.0 mg L-1.

Ovulation was synchronized with carp pituitary extract (CPE) in an initial injection of 0.5 mg kg-1 body weight, followed by a second injection of 5.0 mg kg-1 body weight 12 h later (Bombardelli et al., 2006). Oocytes were collected by gently squeezing the female abdomen at 240 degree-h (10 h with water temperature at 24°C) after the second injection. The oocyte mass released by each female was weighed to 0.01 g using an analytic scale (Marte® AS2000C), and an aliquot of 0.1 g (analytic scale Marte® AY220, 0.0001 g accuracy) was fixed in Karnovisky solution to determine the number of oocytes g-1, absolute fecundity (total number of oocytes released), relative fecundity (number of oocytes released relative to body weight) and size of oocytes.

Fifty-gram samples of oocytes released by the females (n = 5) in each cage were combined, placed in plastic bags, labeled and stored at −18°C until analysis of fatty acids.

One year old South American catfish males, obtained from the Instituto de Pesquisa em Aquicultura Ambiental, were stocked separately from the females into 200 m2 excavated masonry-lined ponds (water volume of approximately 300 m3) with an earth bottom and fed a commercial diet (28% crude protein). The males were injected with a single dose of 3.0 mg kg-1 bodyweight CPE at the time of the second female hormone injection. Semen was stripped from 20 males by gentle abdominal pressure and collected into graduated test tubes (± 0.1 mL). Approximately 2 mL of semen from each male was used to create five pools, each comprising semen of four males. A sample of each pool was used to determine spermatozoon concentration (Neubauer chamber, 1:1,000 semen: formalin), and spermatozoon motility (Computer-Assisted Sperm Analysis) according to Sanches et al. (2010).

The quality of the semen pools was satisfactory concerning mean volume, spermatozoon concentration and motility (Table 3). Each semen pool (n = 5) was used to fertilize eggs of females of four tanks, each one from a different treatment. A standard insemination dose of 100 μL of semen was used to fertilize 2 mL (3,496.96 ± 115.38) of oocytes from each female. Gamete activation was conducted in 150 mL plastic containers with 20 mL of water. After activation, eggs were hydrated for 1 min during fertilization and, subsequently, incubated in 100 conical incubators of 2.5 L each, in a recirculating water system equipped with mechanical and biological filtration at a water temperature of 27 ± 1.0°C maintained by electrical heating.

Table 3 Characteristics of Rhamdia quelen sperm pools used for fertilization. 

Pool
n = 4
Weight (g) Volume (mL) Concentration
(SPZ mL-1)
Motility (%)
1 132.52 ± 20.51 6.42 ± 3.00 8.50×109 60.53
2 113.80 ± 17.20 5.50 ± 0.57 1.85×1010 81.79
3 86.67 ± 27.94 2.57 ± 0.94 1.96×1010 87.81
4 123.57 ± 20.52 6.52 ± 4.03 1.83×1010 69.38
5 85.00 ± 25.67 5.07 ± 0.97 6.20×109 84.50

SPZ mL-1: spermatozoa per millilitre.

Eleven hours post-fertilization (hpf), after blastopore closure, fertilized eggs (translucent with apparent normal embryonic development) and non-fertilized eggs (white and opaque) were counted. The fertilization rate (FR) was determined in three sub-samples of ~135 eggs from each incubator using the equation: FR(%)=number of viable oocytes×100/total number of eggs .

At 36 hpf, all larvae were removed from the incubators and fixed in Karnovisky solution. Larval deformity rate was determined by examining 300 larvae with a stereomicroscope (Leica DMZ 180) and classifying them as normal according to De Amorim et al. (2009), or abnormal. All fixed larvae were counted to determine the hatching rate (HR) using the equation: HR=[number of hatched larvae/(number of eggs in2mLthe number of eggs used for calculating FR)×100] .

A stereomicroscope (Nikon, SMZ 1500, Tokyo, Japan) equipped with a camera (DS-Fi, Nikon, Japan) was used to obtain digital images of oocytes and fixed larva, and size was determined using Nis-elements Advanced Research software (Nikon, Japan). The diameter of 10 oocytes and the total length of 10 larvae from each female were recorded. Before spawning, two females from each cage sacrificed in benzocaine at 0.75 mg L-1. After the samples of the ovaries were labeled and immediately frozen at −18°C for fatty acids analysis.

Fatty acid analysis

The fatty acid composition of the ovaries and oocytes was analyzed at the Laboratório de Bioquímica de Microorganismos e plantas da Universidade Estadual Paulista, Jaboticabal-SP. The fatty acids were measured using the total lipid extraction method of Bligh & Dyer (1959) and the official methylation method Ce2-66: Preparation of methyl esters of long chain fatty acids firestone (2009).

The fatty acid profiles were analyzed using a gas chromatograph CG-14B (Shimadzu) with fused silica capillary column OMEGAWAX250 (30 m × 0.25 mm × 0.25 um, catalog N°24136-SUPELCO). The column temperature was set at 100°C for 2 min and heated at a rate of 4°C min-1 to 220°C, and held for 25 min. The injector and detector temperatures were 250 and 280°C, respectively. The carrier gas (H2) flow rate was 1 mL min-1 (SPLIT: 1/100), the volume injected was 1 μL, using a flame ionization detector. The standard used for fatty acid identification was the Sigma fatty acid standard, catalog N°189-19, and 47015-U.

Statistical analysis

The study employed a completely randomized design, and data were checked for homogeneity using the Levene's test (Brown & Forsythe, 1974) and for normality using the Cramer-von Mises test (Darling, 1957). Afterward, the data were analyzed by ANOVA, followed by Tukey's test for multiple comparisons, using Statistica v.10.0 (Statsoft, Tulsa, USA). Significance was considered at P < 0.05.

RESULTS

Reproductive performance

All the females subjected to hormone treatment released oocytes. In 25 per diet group, spawning with successful development was observed in 23 fish in the palm oil group (92%), 17 in the soybean (68%) and 15 for mixed and fish oil groups (60%) (Table 4).

Table 4 Reproductive and larval characteristics of female Rhamdia quelen fed diets containing different lipid sources, soybean, palm, marine fish and a blend of three oils (MIX). 

Parameters Diets
SO PO FO MIX
Spawning (%)* 68.00 92.00 60.00 60.00
Weight (g)1 333.21 ± 37.44a 318.91 ± 11.85a 297.05 ± 21.90a 300.47 ± 26.35a
Absolute fecundity2 1.11 ± 0.21×105a 0.92 ± 0.06×105a 0.94 ± 0.16×105 0.98 ± 0.12×105a
Relative fecundity3 319.55 ± 35.21a 289.77 ± 23.90a 323.31 ± 38.45a 312.68 ± 13.76a
Oocyte size (μm) 880.28 ± 5.32a 881.81 ± 7.04a 892.01 ± 4.37a 889.64 ± 18.29a
Fertilization (%) 60.14 ± 5.66b 77.15 ± 3.97a 78.65 ± 3.60a 65.46 ± 4.57ab
Hatching (%) 45.68 ± 7.71a 61.00 ± 5.40a 61.29 ± 6.72a 45.22 ± 6.23a
Larva size (μm) 3,766.77 ± 55.26a 3,842.58 ± 50.55a 3,830.13 ± 54.12a 3,814.88 ± 70.50a
Larva deformity (%) 13.81 ± 4.59a 8.73 ± 2.72a 13.85 ± 3.45a 9.45 ± 1.35a

1Mean weight of spawning females

2number of oocytes female-1

3oocytes g-1 body weight. Different letters in a row indicate a significant difference (P < 0.05).

SO: diet containing soybean oil; PO: diet containing refined palm oil; FO: diet containing marine fish oil; MIX: diet containing a combination of the three oils.

*No statistical analysis was performed.

Diets showed a significant effect only on the fertilization rate. The best results were obtained for diets containing fish oil (78.65 ± 3.60) and palm oil (77.15 ± 3.97), followed by oil mix (65.46 ± 4.57). The diet containing soybean oil was associated with significantly lower fertilization (60.14 ± 5.66; P < 0.05) than the palm and fish oil diets. Diet had no significant effect (P > 0.05) on absolute and relative fecundity, hatching rate, oocyte and larval size, or deformity rate (Table 4).

The total fatty acid composition of gonads and oocytes

The diet of South American catfish females (Table 2) was reflected in the fatty acid composition of ovary and oocytes, which varied significantly (P < 0.05) among diet groups (Tables 5-6).

Table 5 Mean ± standard error of the fatty acid content (% of total FA) in ovaries of Rhamdia quelen, fed with diets containing different lipid sources, soybean, palm, marine fish and the blend of three oils (MIX), obtained from ovaries from two females per cage (material collected in February). 

Fatty acid (%) Diets
SO PO FO MIX
C14:0 0.92 ± 0.06c 1.07 ± 0.06bc 1.73 ± 0.04a 1.15 ± 0.02a
C15:0 0.18 ± 0.00bc 0.15 ± 0.01c 0.33 ± 0.02a 0.23 ± 0.01b
C16:0 4.70 ± 0.28c 29.32 ± 0.38a 27. 91 ± 0.20b 27.59 ± 0.26b
C17:0 0.23 ± 0.02b 0.16 ± 0.00c 0.38 ± 0.04a 0.26 ± 0.01b
C18:0 9.99 ± 0.27a 9.44 ± 0.40a 9.29 ± 0.31a 9.20 ± 0.24a
C 20:0 0.10 ± 0.01ab 0.08 ± 0.00b 0.11 ± 0.01a 0.09 ± 0.00ab
Σ Saturated 36.14 ± 0.41c 40.24 ± 0.40a 39.77 ± 0.27ab 38.54 ± 0.25b
C16:1 1.07 ± 0.15b 1.55 ± 0.01b 2.74 ± 0.21a 1.68 ± 0.11b
C 17:1 0.06 ± 0.00c 0.06 ± 0.00c 0.22 ± 0.01a 0.10 ± 0.00b
C18:1n7 2.53 ± 0.11bc 2.36 ± 0.17c 3.54 ± 0.13a 2.94 ± 0.09b
C18:1n9 20.57 ± 0.36bc 25.58 ± 0.34a 19.67 ± 0.38c 21.55 ± 0.17b
C20:1n9 0.77 ± 0.44b 1.13 ± 0.06a 1.10 ± 0.06a 1.05 ± 0.03a
C24:1n9 1.35 ± 0.04ab 1.06 ± 0.04c 1.40 ± 0.06a 1.25 ± 0.04b
Σ Mono-unsaturated 26.37 ± 0.53c 31.77 ± 0.27a 28.67 ± 0.62b 28.57 ± 0.17b
C18:3n3 0.45 ± 0.07a 0.19 ± 0.01c 0.36 ± 0.04b 0.31 ± 0.02b
C20:3n3 0.34 ± 0.02a 0.20 ± 0.01b 0.29 ± 0.01a 0.30 ± 0.02a
C20:5n3 (EPA) 0.52 ± 0.04c 0.51 ± 0.04c 1.30 ± 0.05a 0.77 ± 0.03b
C22:6n3 (DHA) 9.25 ± 0.36c 8.89 ± 0.30c 13.86 ± 0.43a 11.53 ± 0.09b
C18:2n6 12.09 ± 0.55a 6.77 ± 0.24c 7.31 ± 0.38bc 8.79 ± 0.31b
C18:3n6 2.31 ± 0.29a 1.05 ± 0.08b 0.68 ± 0.06b 1.11 ± 0.09b
C20:2 2.39 ± 0.19a 1.58 ± 0.05b 1.60 ± 0.09b 2.07 ± 0.08a
C20:3n6 5.65 ± 0.27a 4.86 ± 0.07b 3.17 ± 0.08c 4.46 ± 0.10b
C20:4n6 (ARA) 3.06 ± 0.14a 2.61 ± 0.03ab 1.78 ± 0.10c 2.32 ± 0.12b
C22:4n6 0.53 ± 0.06a 0.38 ± 0.02b 0.53 ± 0.02a 0.44 ± 0.02a
C 22:5n6 0.95 ± 0.10a 0.85 ± 0.04ab 0.54 ± 0.01c 0.66 ± 0.04bc
Σ C18 14.85 ± 0.82a 8.00 ± 0.25c 8.36 ± 0.42bc 10.21 ± 0.39b
Σ C20-22 22.70 ± 0.80a 19.90 ± 0.24b 23.07 ± 0.53a 22.57 ± 0.23a
Σ Poly-unsaturated 37.56 ± 0.08a 27.91 ± 0.38c 31.43 ± 0.86b 32.78 ± 0.21b
n3 10.57 ± 0.40c 9.80 ± 0.30c 15.82 ± 0.46a 12.92 ± 0.10b
+n6 24.59 ± 0.54a 16.53 ± 0.24b 14.01 ± 0.47c 17.79 ± 0.24b
n3/n6 0.43 ± 0.02d 0.59 ± 0.02c 1.13 ± 0.03a 0.73 ± 0.01b
DHA/EPA 18.07 ± 1.74a 17.56 ± 1.03a 10.70 ± 0.31b 14.98 ± 0.54a
EPA/ARA 0.17 ± 0.01c 0.20 ± 0.03c 0.73 ± 0.03a 0.34 ± 0.02b

Different letters in a row indicate significant difference (P < 0.05).

SO: diet containing soybean oil; PO: diet containing refined palm oil; FO: diet containing marine fish oil; MIX: diet containing a combination of the three oils.

Table 6 Fatty acid profile (%) in oocytes of Rhamdia quelen females fed diets containing different lipid sources, soybean, palm, marine fish and the blend of three oils (MIX). 

Fatty acid (%) Diets
SO PO FO MIX
C14:0 1.1 ± 0.03c 1.37 ± 0.04b 1.76 ± 0.04a 1.39 ± 0.08b
C15:0 0.18 ± 0.01bc 0.15 ± 0.00c 0.33 ± 0.01a 0.22 ± 0.01b
C16:0 25.18 ± 0.16c 30.08 ± 0.10a 27.91 ± 0.39b 27.93 ± 0.38b
C17:0 0.22 ± 0.00c 0.16 ± 0.00d 0.37 ± 0.01a 0.26 ± 0.01b
C18:0 9.83 ± 0.22a 9.81 ± 0.23a 9.09 ± 0.17a 9.80 ± 0.43a
C 20:0 0.09 ± 0.00a 0.07 ± 0.01a 0.09 ± 0.00a 0.08 ± 0.00a
Σ Saturated 36.61 ± 0.31c 41.67 ± 0.24a 39.56 ± 0.37b 39.69 ± 0.62b
C16:1 1.17 ± 0.05c 1.80 ± 0.09b 2.67 ± 0.14a 1.76 ± 0.18b
C 17:1 0.07 ± 0.00c 0.07 ± 0.01c 0.18 ± 0.01a 0.11 ± 0.01b
C18:1n7 2.44 ± 0.09a 2.24 ± 0.06b 3.64 ± 0.11a 2.65 ± 0.14b
C18:1n9 21.42 ± 0.32b 25.98 ± 0.29a 20.20 ± 0.33c 22.05 ± 0.19b
C20:1n9 0.79 ± 0.03b 1.18 ± 0.04a 1.13 ± 0.03 a 1.02 ± 0.04a
C24:1n9 1.18 ± 0.02b 1.05 ± 0.02b 1.47 ± 0.09 a 1.23 ± 0.02b
Σ Mon-unsaturated 27.08 ± 0.39c 32.33 ± 0.37a 29.32 ± 0.44b 28.85 ± 0.27b
C18:2n6 12.21 ± 0.27a 6.18 ± 0.12d 7.28 ± 0.14c 8.47 ± 0.20b
C18:3n6 2.65 ± 0.26a 1.10 ± 0.07b 0.74 ± 0.05b 1.34 ± 0.06b
C18:3n3 0.46 ± 0.02a 0.18 ± 0.01c 0.33 ± 0.01b 0.32 ± 0.01b
C20:2 2.40 ± 0.13a 1.45 ± 0.03c 1.67 ± 0.09bc 1.84 ± 0.04b
C20:3n6 5.50 ± 0.11a 4.57 ± 0.05b 3.29 ± 0.09c 4.58 ± 0.06b
C20:4n6 (ARA) 2.74 ± 0.08a 2.53 ± 0.05ab 1.81 ± 0.10c 2.39 ± 0.04b
C20:3n3 0.35 ± 0.02a 0.20 ± 0.01c 0.28 ± 0.01b 0.28 ± 0.01b
C20:5n3 (EPA) 0.49 ± 0.04c 0.42 ± 0.01c 1.24 ± 0.07a 0.69 ± 0.04b
C22:4n6 0.43 ± 0.02a 0.40 ± 0.01a 0.50 ± 0.01a 0.47 ± 0.06a
C 22:5n6 0.79 ± 0.07a 0.96 ± 0.05a 0.54 ± 0.02b 0.72 ± 0.05ab
C22:6n3 (DHA) 8.05 ± 0.33c 7.93 ± 0.14c 13.32 ± 0.39a 10.18 ± 0.31b
9.25 ± 0.36 c 8.89 ± 0.30c 13.86 ± 0.43a 11.53 ± 0.09b 9.25 ± 0.36c
A C18 15.33 ± 0.48a 7.46 ± 0.17c 8.35 ± 0.17c 10.13 ± 0.24b
Σ C20-22 20.76 ± 0.68ab 18.46 ± 0.23b 22.64 ± 0.71 19.88 ± 0.65b
Σ Poly-unsaturated 36.08 ± 0.33a 25.92 ± 0.21c 30.99 ± 0.80b 31.32 ± 0.50b
n3 9.35 ± 0.34c 8.72 ± 0.13c 15.17 ± 0.47a 11.47 ± 0.34b
n6 24.33 ± 0.27a 15.74 ± 0.15c 14.16 ± 0.30d 18.00 ± 0.16b
n3/n6 0.39 ± 0.02d 0.55 ± 0.01c 1.07 ± 0.02a 0.64 ± 0.02b
DHA/EPA 16.91 ± 1.29ab 18.93 ± 0.55a 10.82 ± 0.35c 14.78 ± 0.50b
EPA/ARA 0.18 ± 0.01c 0.17 ± 0.01c 0.68 ± 0.02a 0.29 ± 0.01b

Mean ± standard error of results obtained from a pool of oocytes from five females per treatment. Different letters in a row indicate significant difference (P < 0.05).

SO: diet containing soybean oil; PO: diet containing refined palm oil; FO: diet containing marine fish oil; MIX: diet containing a combination of the three oils.

Oocyte fatty acid composition was like that of gonads. There were significant differences among diets (P < 0.05) in the total levels of saturated, mono- and poly-unsaturated fatty acids. Fish receiving the palm oil diet had significantly higher (P < 0.05) levels of saturated and monounsaturated fatty acids in gonads and oocytes, with palmitic acid, C16:0, and oleic acid, 18:1n-9, being the most prevalent. The highest levels of total n-3 fatty acids were observed in the ovaries and oocytes of the fish oil groups at 15.8 and 15.2%, respectively, and, consequently, higher levels of EPA and DHA were also present. Arachidonic acid was present in significantly higher quantities in the ovaries and oocytes of the soybean oil group (P < 0.05) than in the fish and mixed oil groups. Total n-6 fatty acids (24.6% in the ovary and 24.3% in oocytes) were significantly higher (P < 0.05) in the soybean oil group.

The lowest n3/n6 ratio was observed in the liver, ovaries and oocytes of the soybean oil group. The mixed oil diet resulted in a balance of the fatty acids. Fish oil was associated with an increase in EPA, DHA, and n-3 acids and soybean oil increased the level of n– 6 fatty acids (18%).

DISCUSSION

A diet containing vegetable oils was effective and resulted in satisfactory reproductive indices in Rhamdia quelen females, which suggests vegetable oils are effective and sustainable alternatives to fish oil in diets for this species. The diet containing palm oil was associated with the highest spawning rate. This positive influence may be due to the presence of tocopherol and tocotrienol in palm oil, which are potent anti-oxidants acting against the free radicals that catalyse lipid peroxidation thus protecting the cell membranes (Ng & Wang, 2011; Abozaid et al., 2012; Aysi & Zhao, 2014) and reducing the oxidative stress after hormone induction.

The relative and absolute fecundity observed in this study were superior to those reported by Tessaro et al. (2014), who analyzed various digestible energy levels for South American catfish females fed soybean oil at the same age of our study. Tessaro et al. (2014) reported means of 51,000 to 71,000 oocytes released per female and a relative fecundity rate of 246-301 oocytes g-1. In the present study, the mean number of oocytes released per female was 92,000 (palm oil) to 111,000 (soybean oil), and relative fecundity rate was 289 at 323 oocytes g-1.

The lower fertilization and hatching rates of females fed soybean oil may be due to the more advanced stage of maturation of these females at the time of hormone induction, resulting in over-ripening. This process can be seen when oocytes remain too long in the abdominal cavity and thus lack oxygen, leading to tissue degeneration and metabolic changes (Lahnsteiner et al., 2008). This process of super-maturation is commonly observed in native Brazilian species, as in hormone-induced South American catfish (Romagosa et al., 2012). In super-maturation, fertilization rates are compromised, and fish may be infertile (Lahnsteiner et al, 2008).

The higher quantity of oleic acid observed in the ovaries and oocytes of the palm oil group may explain the fertilization rate similar to that obtained with the fish oil diet, as this fatty acid is essential for normal embryo development in fish (Fernandez-Palacios et al., 1997). This energy came from the mitochondrial β- oxidation of saturated (16:0) and monosaturated (18: 1n-9) fatty acids, which are preferred substrates for energy production in fish (Henderson, 1996). In general, evidence indicates that β-oxidation of fatty acids in units is essential for oocyte maturation and early stages of embryo development (Dunning & Robker, 2012).

Similar results have been reported by Sink & Lochmann (2008), who used poultry fat in the diet of channel catfish Ictalurus punctatus and recommended it as a source of saturated fat to increase production and quality of eggs and larvae. In South American catfish, higher levels of saturated fatty acid in the diet (pork fat) resulted in normal embryo and larval development (Parra et al., 2008).

Although some studies suggest that the levels of n– 3 fatty acids should be lower than n-6 fatty acids in diets of freshwater fish. Sargent et al. (2002) observed greater conversion for n-3 production, especially DHA, than for n-6 in ovary and oocyte. This is in agreement with Coldebella et al. (2013) and corroborates the potential for fatty acids to be mobilized from the tissues to the oocytes (Tocher, 2003).

Although the palm oil diet resulted in low levels of linolenic acid (18:3n-3), South American catfish females converted this into poly-unsaturated fatty acids including EPA and DHA, stored primarily in the gonads and oocytes. Anido et al. (2015) reported a higher quantity of EPA (2.3%) and DHA (7.3%) observed in mature ovaries of wild R. quelen than those observed in this study.

Despite low levels of linoleic acid in palm oil diets, females of this group appeared to efficiently convert it to ARA, as the quantity of this fatty acid in ovary and oocytes was similar to that of females fed soybean oil. The conversion may have been enhanced by lower levels of linolenic acid, enabling the Δ-6 desaturase enzyme to convert linoleic acid into ARA (Ng & Wang, 2011). This variable ability of desaturation and elongation in fish may be related to different age stages (Bell et al., 2001) and water temperature (Agaba et al., 2005). However, Coldebella et al. (2013) observed lower levels of EPA and DHA in the ovaries of R. quelen, compared with the present study. Such difference could be explained by our use of salmon meal in the diet, with higher levels of C18: 3n-3, while Coldebella et al. (2013) used pork meat and bone meal in their diet.

As observed by several authors, adequate ARA concentrations in the diet are important to stimulate oocyte maturation (Pérez et al., 2007; Norambuena et al., 2013). Linoleic acid is a precursor of ARA via the action of the Δ-6-desaturase. However, high levels of ARA may cause harmful effects in some species, as verified by Furuita et al. (2007), who found the hatching rate and larval development of Anguilla japónica were compromised.

Ovaries and eggs varied in DHA/EPA, EPA/ARA and n3/n6 ratios among treatments. Liang et al. (2014) suggested that optimum dietary ratios of these fatty acids are necessary to ensure the quality of the eggs and larvae but can be species-dependent. We found ovaries and eggs to have low proportions of EPA/ARA, which did not affect the reproductive performance of R. quelen females.

Hormone treatment may affect the synthesis of vitellogenin and fatty acid of R. quelen oocytes (Żarski et al., 2012). In the present study, the fatty acid profile of ovaries and oocytes was similar; however, oocyte DHA levels were lower than was observed in the ovaries, also reported in hormonally induced milkfish Chanos chanos (Ako et al., 1994).

Research on broodstock nutrition has highlighted the use of palm oil as a potential partial or complete replacement for fish oil. Although it does not provide high quantities of poly-unsaturated fatty acids, especially n-3, it provides a superior source of energy for reproductive success (Ng & Wang, 2011).

The diets containing vegetable oils alone and in combination with fish oil, fed to females for eleven months produced satisfactory rates of fecundity and fertilization in the first reproductive cycle. The higher quantity of n-6 fatty acids soybean oil possibly accelerated ovarian development, resulting in lower fertilization, although accurate prediction of the spawning period could resolve it. Fatty acids in the diet influenced the profile of gonads and oocytes, with higher concentrations of DHA observed, indicating that R. quelen can be synthesized and deposit LC-PUFAS in the ovaries and eggs from the 18-carbon precursor. Such deposition could be related to the salmon meal (20%), which contains high amounts of these fatty acids, in the formulated diet. The vegetable sources used are suitable for broodstock nutrition and, as reported by other authors (Shiranee & Natarajan, 1996; Ng & Wang, 2011) palm oil could be used as a replacement to fish oil.

ACKNOWLEDGMENTS

This study was funded by the Research Aid (Auxílio à Pesquisa) from FAPESP (2012/23089-4) and CNPq through a Ph.D. grant (142751/2011-1). The authors would like to thank the Instituto de Pesquisa em Aquicultura Ambiental-Unioeste/PR for providing the infrastructure, Nicoluzzi and Agropalma industries for donating the marine fish oil and the refined palm oil.

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Received: August 14, 2018; Accepted: January 23, 2019

Corresponding author: Cleonice Cristina Hilbig (cleonicehUbig@ufgd.edu.br)

Corresponding editor: Jesús Ponce Palafox

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