Abstract:
The purpose of this study was to assess the effect of different carbohydrate and lipid (CHO/L) ratios on the performance and energy metabolism of hybrid catfish (♂Pseudoplatystoma corruscans × ♀ Pseudoplatystoma fasciatum). One hundred and sixty-eight fish (104.9±16.5 g BW) were distributed into 24 100-L tanks. The experiment was performed using a randomised block design with four CHO/L ratios (0.45, 1.00, 1.66 and 2.85) and six replications. Growth performance, protein content, glucose and triglycerides in plasma, muscle and liver, and the hepatic activity of the malic and glucose-6-phosphate dehydrogenase (G6PD) enzymes were measured after 60 feeding days. No significant differences were observed in growth performance, protein and triglycerides of plasma and muscle, hepatic protein or malic enzyme activity. CHO/L: 2.85 provided the highest plasma and liver glucose, while CHO/L: 0.45 showed high liver triglycerides. A linear effect was found for the hepatic activity of G6PD and dietary starch levels (R2=0.93). The hepatic activity of G6PD was greater in CHO/L=2.85 than for CHO/L: 0.45. In conclusion, the limit of dietary starch inclusion and lipids were 15% and 9.00%, respectively (CHO/L: 1.66), and this level did not affect the energy metabolism of the juvenile hybrid catfish.
Key words
enzymes activity; hepatic function; intermediary metabolism; hybrid catfish; Surubim
INTRODUCTION
Carbohydrate-containing feedstuffs are less expensive than other nutrients in diet and directly influence economic fish production viability (PapoutsoglouPAPOUTSOGLOU ES and LYNDON AR. 2006. Digestive enzymes along the alimentary tract of the parrotfish Sparisoma cretense. J Fish Biol 69: 130-140. and Lyndon 2006, KamalamKAMALAM BS, MEDALE F and PANSERAT S. 2017. Utilisation of dietary carbohydrates in farmed fishes: New insights on influencing factors, biological limitations and future strategies. Aquaculture 467: 3-27. et al. 2017). Although no nutritional requirements of carbohydrates exist in these animals’ diets, their inclusion at appropriate levels can ensure better efficiency in utilising other nutrients by contributing positively in the diet extrusion process, and acting as an abundant energy source for lipids and proteins (KrogdahlKROGDAHL Å, HEMRE GI and MOMMSEN TP. 2005. Carbohydrates in fish nutrition: digestion and absorption in postlarval stages. Aquacult Nutr 11: 103-122. et al. 2005, NRCNRC. 2011. Nutrient Requirements of Fish and Shrimp. Washington, DC: The National Academies Press, 392 p. 2011, ZhouZHOU C, GE X, NIU J, LIN H, HUANG Z and TAN X. 2015. Effect of dietary carbohydrate levels on growth performance, body composition, intestinal and hepatic enzyme activities, and growth hormone gene expression of juvenile golden pompano, Trachinotus ovatus. Aquaculture 437: 390-397. et al. 2015, Kamalam et al. 2017). However, carbohydrate use in a carnivorous fish diet is complex and not well-known for digestion, absorption and metabolism processes (Krogdahl et al. 2005). Such processes depend on the relationships between fish species and carbohydrate type or content (Krogdahl et al. 2005, Kamalam et al. 2017). These species are more efficient in using lipids as an energy source given their metabolism’s limited capacity to reduce glycaemia (CaserasCASERAS A, METÓN I, VIVES C, EGEA M, FERNÁNDEZ F and BAANANTE IV. 2007. Nutritional regulation of glucose-6-phosphatase gene expression in liver of the gilthead sea bream (Sparus aurata). Brit J Nutr 88: 607-614. et al. 2007, HemreHEMRE GI, MOMMSEN TP and KROGDAHL Å. 2002. Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquacult Nutr 8: 175-194. et al. 2002).
The metabolic profile and its pathways are the reflex from diet, regardless of performance or muscle and liver function. Carbohydrate/ lipids (CHO/L) ratios of around 1.3:1 produce the best growth performance in hybrid catfish (Pseudoplatystoma reticulatumxLeiarius marmoratus) (BernardesBERNARDES CL, NAVARRO RD, GUERRA-SANTOS B and FORTES-SILVA R. 2016. Effects of dietary carbohydrate/lipid ratios on growth, body composition, and nutrient utilization of hybrid catfish (Pseudoplatystoma reticulatum x Leiarius marmoratus). Rev Colom Cienc Pecua 29: 58-65. et al. 2016). One of the statements about fish growth variation is the relation between carbohydrate levels and their effects on diet viscosity and digestion which can, in turn, lead to a change in nutrient use (TranTRAN-TU LC, HIEN TTT, BOSMA RH, HEINSBROEK LTN, VERRETH JAJ and SCHRAMA JW. 2017. Effect of ingredient particle sizes and dietary viscosity on digestion and faecal waste of striped catfish (Pangasianodon hypophthalmus). Aquacult Nutr 24: 961-969.-Tu et al. 2017). Moreover, increased dietary protein and fewer carbohydrates and lipids attenuate glycolytic activity and induce hepatic gluconeogenesis in South American catfish (Rhamdia quelen) (MeloMELO JFB, LUNDSTEDT LM, INOUE LAK, METÓN I, BAANANTE IV and MORAES G. 2016. Glycolysis and gluconeogenesis in the liver of catfish fed with different concentrations of proteins, lipids and carbohydrates. Arq Bras Med Vet Zoo 68: 1251-1258. et al. 2016). The liver histology was normal in the yellow catfish (Pelteobagrus fulvidraco) fed the 2.45, 3.63 and 5.58 CHO/L diets. The hepatic steatosis and hepatocyte apoptosis rates increased in the yellow catfish fed with 1.11 and 1.67 CHO/L than 2.45, 3.63 and 5.58 CHO/L (WangWANG L-N, LIU W-B, LU K-L, XU W-N, CAI D-S, ZHANG C-N and QIAN Y. 2014. Effects of dietary carbohydrate/lipid ratios on non-specific immune responses, oxidative status and liver histology of juvenile yellow catfish Pelteobagrus fulvidraco. Aquaculture 426-427: 41-48. et al. 2014). Thus it is imperative for modern aquaculture to define the optimum dietary ratio between non-protein energy sources such as carbohydrates and lipids (Wang et al. 2016WANG JT, JIANG YD, HAN T, LI XY, WANG Y and LIU YJ. 2016. Effects of Dietary Carbohydrate-to-Lipid Ratios on Growth and Body Composition of Orange-spotted Grouper Epinephelus coioides. N Am J Aquacult 79: 1-7.).
Pseudoplatystoma corruscans and Pseudoplatystoma fasciatum are carnivorous fish and important species with commercial characteristics produced in South America (MartinoMARTINO RC, CYRINO JEP, PORTZ L and TRUGO LC. 2002a. Effect of dietary lipid level on nutritional performance of the surubim, Pseudoplatystoma coruscans. Aquaculture 209: 209-218. et al. 2002a, LeonardoLEONARDO AFG, ROMAGOSA E, BORELLA MI and BATLOUNI SR. 2004. Induced spawning of hatchery-raised Brazilian catfish, cachara Pseudoplatystoma fasciatum (Linnaeus, 1766). Aquaculture 240: 451-461. et al. 2004), along with their hybrids (♂P. corruscans×♀P. fasciatum) (BeelenBEELEN R, BOYD B, GARAVELLO JC, PAVANELLI GC and AINSWORTH AJ. 2003. A cytochemical, light and electron microscopic study of the peripheral blood leucocytes of hybrid surubim catfish (Pseudoplatystoma corruscans x Pseudoplatystoma fasciatum). Comp Clin Path 12: 61-68. et al. 2003). Pseudoplatystoma spp. is able to adjust amylase activity in accordance with dietary carbohydrate levels (LundstedtLUNDSTEDT LM, MELO JFB and MORAES G. 2004. Digestive enzymes and metabolic profile of Pseudoplatystoma corruscans (Teleostei: Siluriformes) in response to diet composition. Comp Biochem Phys B 137: 331-339. et al. 2004). Both plasma glucose and plasma protein concentrations lower when corn gluten meal levels increase in P.fasciatum (BicudoBICUDO ÁJDA, BORGHESI R, DAIRIKI JK, SADO RY and CYRINO JEP. 2012. Performance of juveniles of Pseudoplatystoma fasciatum fed graded levels of corn gluten meal. Pesq Agropec Bras 47: 838-845. et al. 2012). All these South American catfish are species of the same family (Pimelodidae). However, very little is known about this hybrid metabolism function in relation to the nutrition effect. In some carnivorous species, e.g. Oncorhynchus mykiss, Rachycentron canadum and Mystus nemurus, glucose stimulates glucose-6-phosphate dehydrogenase (G6PD) and malic enzyme (ME) activities (AlvarezALVAREZ MJ, DÍEZ A, LÓPEZ-BOTE C, GALLEGO M and BAUTISTA JM. 2000. Short-term modulation of lipogenesis by macronutrients in rainbow trout (Oncorhynchus mykiss) hepatocytes. Brit J Nutr 84: 619-628. et al. 2000, CuiCUI XJ, ZHOU QC, LIANG HO, YANG J and ZHAO LM. 2010. Effects of dietary carbohydrate sources on the growth performance and hepatic carbohydrate metabolic enzyme activities of juvenile cobia (Rachycentron canadum Linnaeus.). Aquaculture Research 42: 99-107. et al. 2010, HamidHAMID NKA, MAHAYAT M and HASHIM R. 2011. Utilization of different carbohydrate sources and starch forms by bagrid catfish (Mystus nemurus) (Cuv & Val). Aquacult Nutr 17: e10-e18. et al. 2011), which are the main enzymes responsible for producing NADPH, which is required for lipid synthesis. Thus, the quantification of metabolites in different tissues and enzyme activity in relation to energy metabolism are important for understanding the use of dietary carbohydrates to optimise growth, spare proteins and avoid economical waste while farming species.
The present work was conducted to assess the influence of different CHO/L ratio on the energy metabolism of hybrids ♂Pseudoplatystoma corruscans×♀Pseudoplatystoma fasciatum by estimating performance, protein concentration, glucose and triglycerides in plasma, muscle and liver, and the hepatic activity of both ME and G6PD.
MATERIALS AND METHODS
ANIMAL HOUSING
The growth trial was performed at the Aquaculture Station of the Federal University of Lavras - UFLA, Minas Gerais (Brazil), and was approved by the UFLA’s Ethics Committee on Animal Use, and was certified by Protocol 028/12. Juvenile catfish (Pseudoplatystoma spp.) were obtained from a farm in Minas Gerais, Brazil. One hundred and sixty-eight fish (initial body weight of 104.9±16.5 g; mean±S.D) were distributed into 24 100-L tanks (7 fish per tank). Fish were fed twice until apparent satiation. The system comprised a 5-μm particle sand filter, an ultraviolet filter and a biological filter. The water flux in the experimental boxes was sufficient to renew water 3 times/hour. During the experiment, the water temperature was maintained at 28±0.1oC. Dissolved oxygen was measured daily by a portable digital oxymeter (F-1550A, Bernauer®, Indaial, SC, Brazil), with average values of 5.1±0.9 mg L-1. Ammonia, nitrite and pH were measured weekly using a commercial kit (Labcon Test, Alcon®, Camboriú, SC, Brazil), with average values of 0.009±0.002 ppm, 0.01±0.001 ppm, and 7.3±0.1, respectively. Fish were submitted to a 15-day adaptation period before the experiment began.
EXPERIMENTAL DIETS
Four isoproteic (460 g kg-1 crude protein) and isoenergetic (3,500 kcal kg-1) diets were formulated to contain the dietary carbohydrate and lipid ratios (CHO/L: 0.45, 1.00, 1.66 and 2.85) (Table I). Canola oil was considered herein because the parietal P. fasciatumis well able to use plant oils than fish oil to transform linoleate into arachidonate (ArslanARSLAN M, RINCHARD J, DABROWSKI K and PORTELLA MARIA C. 2008. Effects of Different Dietary Lipid Sources on the Survival, Growth, and Fatty Acid Composition of South American Catfish, Pseudoplatystoma fasciatum, Surubim, Juveniles. J World Aquacult Soc 39: 51-61. et al. 2008). Moreover, plant oil is used by P. coruscans (MartinoMARTINO RC, CYRINO JEP, PORTZ L and TRUGO LC. 2002b. Performance and fatty acid composition of surubim (Pseudoplatystoma coruscans) fed diets with animal and plant lipids. Aquaculture 209: 233-246. et al. 2002b). Dietary ingredients were mixed in a paddle mixer (Inbramaq®, São Paulo, Brazil) with 20% of water, pelletized (4 mm) and dried for 12 h in an oven at 50°C. Diets were stored in a freezer (5°C) until used.
EXPERIMENTAL DESIGN
After the adaptation period, fish were fed the experimental diets (4 CHO/L ratios and 6 replies) twice a day at 08:00h and 18:00h. The amount of diet was provided according to apparent animal satiety. The delivered amount of diets was quantified daily by weighing before and after the feeding process. The trial lasted 60 days. At the end of the experimental period, fish were starved for 24h, weighed and then kept in anaesthetic solution until opercular movement had completely ceased (0.8 ml.l-1 2-phenoxyethanol). One millilitre of blood per cardiac punch was also sampled using a heparinised syringe (1 ml; needle size of 21G 1/2” 0.8x40). Blood was centrifuged at 3,000 rpm for 10 minutes before isolating plasma by a Pasteur micropipette. After this procedure, fish were decapitated at the skull insertion point. Then the liver and white dorsal muscle samples (approximately 3g) were collectedfrom each juvenile. The liver was weighed to calculate the hepatossomatic index. Samples were stored at -80oC for further analyses.
The following parameters were calculated: Hepatosomatic Index (HSI) = [(liver weight/fish weight)×100]; weight gain (WG) = final weight - first weight; feed conversion ratio (FCR) = ingested rate/weight gain; protein efficiency rate (PER) = weight gain/ingested crude protein, and energy efficiency rate (EER) = weight gain/ingested crude energy.
Muscle and liver assessments
The liver and muscle homogenates were obtained according to PaulinoPAULINO RR, PEREIRA RT, FONTES TV, OLIVA-TELES A, PERES H, CARNEIRO DJ and ROSA PV. 2018. Optimal dietary linoleic acid to linolenic acid ratio improved fatty acid profile of the juvenile tambaqui (Colossoma macropomum). Aquaculture 488: 9-16. et al. (2018) with slight modifications. The white muscle and liver samples were homogenized in ice-cold deionised water and centrifuged (13,400 × g, 10 min; 4ºC).The resultant supernatant was collected and stored at -80ºC. Glucose and triglyceride levels were measured with commercial kits (Glucose HK Liquiform, Cat. 85 and Triglycerides Liquiform, Cat. 87). Soluble protein content was determined according to BradfordBRADFORD MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254. (1976), with bovine serum albumin solution (Sigma) used as a standard.
The specific activity of both malic enzyme (ME, E.C.1.1.1.40) and glucose-6-phosphate dehydrogenase (G6PD, E.C.1.1.1.49) was estimated following the methodology outlined in GraeveGRAEVE K, SCHAEWEN A and SCHEIBE R. 1994. Purification, characterization, and cDNA sequence of glucose-6-phosphate dehydrogenase from potato (Solatium tuberosum L.). Plant J 5: 353-361. et al. (1994) and SpinaSPINA J, BRIGHT HJ and ROSENBLOOM J. 1970. Purification and properties of L-malic enzyme from Escherichia coli. Biochemistry 9: 3794-3801. et al. (1970), respectively. Hepatic tissue was macerated with a pistil in an ice-bath. After maceration, the sample was put in an ultrasonic bath for 10 minutes before being centrifuged at 10,000 g and 4oC for 30 minutes before collecting the supernatant. The homogenate of supernatants was used to estimate specific G6PD activity. All the enzymatic activities are shown as U.mg-1 protein.
STATISTICAL ANALYSIS
All the obtained data were analyzed using the SAEG statistical package proposed by EuclydesEUCLYDES RF. 1997. Manual de utilização do programa SAEG: Sistema para análises estatísticas e genéticas. 2ª ed., Universidade Federal de Viçosa, Viçosa. (1997). A data analysis was done by a one-way analysis of variance (ANOVA) after testing for normality and homogeneity of variances with the Shapiro-Wilk test and the Levene test, respectively. Significant differences among the means were determined by a Student-Newman-Keuls test. A regression equation was obtained to describe the glucose-6-phosphate dehydrogenase pattern.
RESULTS
No fish mortality was recorded during the experimental period. After the 60 days that the trial lasted, no growth performance parameter, e.g. weight gain, feed conversion rate, Hepatosomatic Index, protein efficiency rate and energy efficiency rate, was significantly affected (P>0.05) by the dietary carbohydrate/lipid (CHO/L) ratio (Table II).
Growth performance, feed utilisation and Hepatosomatic Index of the juvenile Pseudoplatystoma ssp fed the experimental diets for 60 days. Lack of superscript letters in the same line implies no differences in data at (P<0.05).
The concentrations of glucose, triglycerides and protein in the white muscle of juveniles did not change (P>0.05) (Table III). However, CHO/L had an effect on glucose in both plasma and the liver, as did triglycerides on hepatic tissue (P<0.05). The highest plasma and liver glucose contents were found in the fish fed the diet (CHO/L =2.85). The catfish juveniles fed the diet (CHO/L=0.45) showed higher concentrations of hepatic triglycerides compared to other CHO/L ratios (P<0.05). The plasma and liver protein concentrations were not affected by diet (P>0.05).
The plasma (mg.dL-1), liver (mg.g-1) and white muscle (mg.g-1) compositions of the juvenile Pseudoplatystoma ssp fed the experimental diets for 60 days. The means in the same row with different superscripts are significantly different at (P<0.05).
No significant differences were observed for the hepatic activity of ME (P>0.05). However, G6PD activity was greater in the treatment (CHO/L =2.85) compared to CHO/L=0.45 (P<0.05) (Table IV). A linear effect was found for G6PD activity, which increased with a rising carbohydrate concentration in diet (Figure 1).
Hepatic enzyme activity of the juvenile Pseudoplatystoma ssp. fed the experimental diets for 60 days. The means in the same row with different superscripts are significantly different at (P<0.05).
Linear regression of the hepatic glucose-6-phosphate dehydrogenase activity of the juvenile Pseudoplatystoma ssp. fed the experimental diets for 60 days (n=18).
DISCUSSION
In this study, the fish fed different CHO/L ratio in their diet did not show any significant differences in their performance. The range within which dietary carbohydrates can be used to meet energy requirements vastly varies between, and even within, species, depending on many factors which have been categorised into those also related to biology and experimental conditions (Kamalam et al. 2017). For example, the inclusion of dietary soluble polysaccharides does not affect growth performance, nor the feed conversion ratio, in African catfish (Clarias gariepinus). MartinoMARTINO RC, CYRINO JEP, PORTZ L and TRUGO LC. 2005. Performance, carcass composition and nutrient utilization of surubim Pseudoplatystoma coruscans (Agassiz) fed diets with varying carbohydrate and lipid levels. Aquacult Nutr 11: 131-137. et al. (2005) found that replacing the energy obtained from soya bean oil in diet with corn flour did not affect the specific growth rate, the feed conversion rate, total consumption, protein and the hepatosomatic index of the parietal Pseudoplatystoma ssp. On the other hand, the 4%, 8% and 12% increases in soya bean oil led to enhanced nitrogen fixation in a P. coruscans carcass (CamposCAMPOS P, MARTINO RC and TRUGO LC. 2006. Amino acid composition of Brazilian surubim fish (Pseudoplatystoma coruscans) fed diets with different levels and sources of fat. Food Chem 96: 126-130. et al. 2006). The feed conversion ratio and daily feed consumption showed a marked drop in the inverse proportion to the lipid level in diet in P. coruscans (Martino et al. 2002b). In short, the present study revealed that the hybrid (♂P. corruscans×♀P. fasciatum) was efficient in using different dietary amounts of carbohydrate or lipid ratios as energy sources when considering growth parameters.
In the hybrid catfish, the CHO/L ratios had an effect in energy metabolism terms. The low lipid and high carbohydrateratios increased plasma and hepatic glucose, and also the hepatic triglyceride levels in the studied hybrid. Lundstedt et al. (2004) obtained similar results for P. corruscans, according to which the incorporation of corn flour into diet significantly increased glycaemia and hepatic glucose. The liver is the central organ that controls glycaemia via enzymes that exert the main catabolism and synthesis of energy substrates. The metabolic capacity of reducing glycaemia is limited in carnivorous fish (Caseras et al. 2007, Hemre et al. 2002), which can lead to poor carbohydrate absorption, and also to an inefficient metabolism and energy profit from glucose. No influence of the CHO/L ratios was found on the protein content in white muscle, liver and plasma. However, the highest glycaemia and plasma protein rates were low at 0.33, with a high 1.24 protein/CHO ratio, respectively, in the P. fasciatum (♀) X L. marmoratus (♂)hybrids (SouzaSOUZA SA, SOUZA RC, CAMPECHE DFB, CAMPOS RML and MELO JFB. 2014. Relação proteína:carboidrato no desempenho e no metabolismo de híbridos de Pseudoplatystoma fasciatum (fêmea) X Leiarius marmoratus (macho). Arq Bras Med Vet Zoo 66: 879-886. et al. 2014). In our study, although the fish fed the diet containing 15% of corn starch (CHO/L: 1.66) showed high hepatic glucose values, this concentration did not influence glycaemia. The livers of the fish fed this diet were probably able to metabolize circulating glucose after 24 h of fasting. This effect was not found for the treatment that contained 20% corn starch (CHO/L: 2.85), which probably characterises a liver capacity limit to recover glycaemia homeostasis.
Our findings revealed no differences in ME when hybrid catfish were fed at different CHO/L ratios. In agreement with our result, lipogenic enzyme (G6PD) activity was more pronounced than the gluconeogenic enzyme (ME) in catfish (Mystus nemurus) (Hamid et al. 2011). G6PD activity was greater at a high CHO/L ratio. JinJIN J, MÉDALE F, KAMALAM BS, AGUIRRE P, VÉRON V and PANSERAT S. 2014. Comparison of Glucose and Lipid Metabolic Gene Expressions between Fat and Lean Lines of Rainbow Trout after a Glucose Load. PLOS ONE 9: e105548. et al. (2014) reported an increase in both the G6PD enzyme expression and hepatic glycaemia levels after an intraperitoneal injection of glucose in rainbow trout of a weak lineage. It is the main enzyme in the pentose phosphate pathway to generate NADPH as a reducing power for biosynthesis, such as lipid synthesis, and has been widely assessed to describe animals’ adaptation capacity to diets containing a high carbohydrate concentration. G6PD and 6PGDH in the catfish liver did not respond to the dietary concentrations of protein, carbohydrates and lipids. Indeed the only response to be obtained has been found in fasted freshwater South America catfish (Randia quelen) (Melo et al. 2016). However, this fish is considered an omnivorous species, which means that the carbohydrate type appeared to influence the activities of liver enzymes to a greater extent. Greater G6PD activity has been observed in freshwater blunt snout breams, Megalobrama amblycephala, fed a glucose diet than those fed a dextrin or wheat starch diet at 2 h postprandial (Ren et al. 2015REN M, HABTE-TSION H-M, XIE J, LIU B, ZHOU Q, GE X, PAN L and CHEN R. 2015. Effects of dietary carbohydrate source on growth performance, diet digestibility and liver glucose enzyme activity in blunt snout bream, Megalobrama amblycephala. Aquaculture 438: 75-81.). Thus, our findings suggest that carnivorous hybrid hepatic cells appear to use carbohydrate properly at lower CHO/L ratios. The increased metabolism activity for glucose at the cell level may lead to a drop in not only hepatic G6PD, the rate-limiting enzyme in the pentose-phosphate-pathway, but also in the production of both NADPH and ribose-5-phosphates, the building blocks of nucleic acids, via an initial breakdown of glucose in channel catfish (Ictalurus punctatus) (SchroeterSCHROETER JC, PETERSON BC, BLEDSOE J, LI M and SMALL BC. 2018. Targeted gene expression panels and microbiota analysis provide insight into the effects of alternative production diet formulations on channel catfish nutritional physiology. Aquaculture 489: 46-55. et al. 2018).
CONCLUSIONS
By way of conclusion, the present study suggests that a rise in the carbohydrate/lipid ratio (2.85) might lead to increasing glycaemia, but does not improve either growth or the protein efficiency rate in hybrid catfish. However, the glycaemia effect was not observed in the diet with a CHO/L of 1.66, which may be the most suitable carbohydrate and lipid inclusion level for this species. CHO/L=2.85 also affected G6PD activities, which somehow suggests that ♂Pseudoplatystoma corruscans×♀Pseudoplatystoma fasciatum is unable to efficiently cope with high dietary carbohydrate levels. The authors declare that there is no conflict of interest.
REFERENCES
- ALVAREZ MJ, DÍEZ A, LÓPEZ-BOTE C, GALLEGO M and BAUTISTA JM. 2000. Short-term modulation of lipogenesis by macronutrients in rainbow trout (Oncorhynchus mykiss) hepatocytes. Brit J Nutr 84: 619-628.
- ARSLAN M, RINCHARD J, DABROWSKI K and PORTELLA MARIA C. 2008. Effects of Different Dietary Lipid Sources on the Survival, Growth, and Fatty Acid Composition of South American Catfish, Pseudoplatystoma fasciatum, Surubim, Juveniles. J World Aquacult Soc 39: 51-61.
- BEELEN R, BOYD B, GARAVELLO JC, PAVANELLI GC and AINSWORTH AJ. 2003. A cytochemical, light and electron microscopic study of the peripheral blood leucocytes of hybrid surubim catfish (Pseudoplatystoma corruscans x Pseudoplatystoma fasciatum). Comp Clin Path 12: 61-68.
- BERNARDES CL, NAVARRO RD, GUERRA-SANTOS B and FORTES-SILVA R. 2016. Effects of dietary carbohydrate/lipid ratios on growth, body composition, and nutrient utilization of hybrid catfish (Pseudoplatystoma reticulatum x Leiarius marmoratus). Rev Colom Cienc Pecua 29: 58-65.
- BICUDO ÁJDA, BORGHESI R, DAIRIKI JK, SADO RY and CYRINO JEP. 2012. Performance of juveniles of Pseudoplatystoma fasciatum fed graded levels of corn gluten meal. Pesq Agropec Bras 47: 838-845.
- BRADFORD MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
- CAMPOS P, MARTINO RC and TRUGO LC. 2006. Amino acid composition of Brazilian surubim fish (Pseudoplatystoma coruscans) fed diets with different levels and sources of fat. Food Chem 96: 126-130.
- CASERAS A, METÓN I, VIVES C, EGEA M, FERNÁNDEZ F and BAANANTE IV. 2007. Nutritional regulation of glucose-6-phosphatase gene expression in liver of the gilthead sea bream (Sparus aurata). Brit J Nutr 88: 607-614.
- CUI XJ, ZHOU QC, LIANG HO, YANG J and ZHAO LM. 2010. Effects of dietary carbohydrate sources on the growth performance and hepatic carbohydrate metabolic enzyme activities of juvenile cobia (Rachycentron canadum Linnaeus.). Aquaculture Research 42: 99-107.
- EUCLYDES RF. 1997. Manual de utilização do programa SAEG: Sistema para análises estatísticas e genéticas. 2ª ed., Universidade Federal de Viçosa, Viçosa.
- GRAEVE K, SCHAEWEN A and SCHEIBE R. 1994. Purification, characterization, and cDNA sequence of glucose-6-phosphate dehydrogenase from potato (Solatium tuberosum L.). Plant J 5: 353-361.
- HAMID NKA, MAHAYAT M and HASHIM R. 2011. Utilization of different carbohydrate sources and starch forms by bagrid catfish (Mystus nemurus) (Cuv & Val). Aquacult Nutr 17: e10-e18.
- HEMRE GI, MOMMSEN TP and KROGDAHL Å. 2002. Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquacult Nutr 8: 175-194.
- JIN J, MÉDALE F, KAMALAM BS, AGUIRRE P, VÉRON V and PANSERAT S. 2014. Comparison of Glucose and Lipid Metabolic Gene Expressions between Fat and Lean Lines of Rainbow Trout after a Glucose Load. PLOS ONE 9: e105548.
- KAMALAM BS, MEDALE F and PANSERAT S. 2017. Utilisation of dietary carbohydrates in farmed fishes: New insights on influencing factors, biological limitations and future strategies. Aquaculture 467: 3-27.
- KROGDAHL Å, HEMRE GI and MOMMSEN TP. 2005. Carbohydrates in fish nutrition: digestion and absorption in postlarval stages. Aquacult Nutr 11: 103-122.
- LEONARDO AFG, ROMAGOSA E, BORELLA MI and BATLOUNI SR. 2004. Induced spawning of hatchery-raised Brazilian catfish, cachara Pseudoplatystoma fasciatum (Linnaeus, 1766). Aquaculture 240: 451-461.
- LUNDSTEDT LM, MELO JFB and MORAES G. 2004. Digestive enzymes and metabolic profile of Pseudoplatystoma corruscans (Teleostei: Siluriformes) in response to diet composition. Comp Biochem Phys B 137: 331-339.
- MARTINO RC, CYRINO JEP, PORTZ L and TRUGO LC. 2002a. Effect of dietary lipid level on nutritional performance of the surubim, Pseudoplatystoma coruscans. Aquaculture 209: 209-218.
- MARTINO RC, CYRINO JEP, PORTZ L and TRUGO LC. 2002b. Performance and fatty acid composition of surubim (Pseudoplatystoma coruscans) fed diets with animal and plant lipids. Aquaculture 209: 233-246.
- MARTINO RC, CYRINO JEP, PORTZ L and TRUGO LC. 2005. Performance, carcass composition and nutrient utilization of surubim Pseudoplatystoma coruscans (Agassiz) fed diets with varying carbohydrate and lipid levels. Aquacult Nutr 11: 131-137.
- MELO JFB, LUNDSTEDT LM, INOUE LAK, METÓN I, BAANANTE IV and MORAES G. 2016. Glycolysis and gluconeogenesis in the liver of catfish fed with different concentrations of proteins, lipids and carbohydrates. Arq Bras Med Vet Zoo 68: 1251-1258.
- NRC. 2011. Nutrient Requirements of Fish and Shrimp. Washington, DC: The National Academies Press, 392 p.
- PAPOUTSOGLOU ES and LYNDON AR. 2006. Digestive enzymes along the alimentary tract of the parrotfish Sparisoma cretense. J Fish Biol 69: 130-140.
- PAULINO RR, PEREIRA RT, FONTES TV, OLIVA-TELES A, PERES H, CARNEIRO DJ and ROSA PV. 2018. Optimal dietary linoleic acid to linolenic acid ratio improved fatty acid profile of the juvenile tambaqui (Colossoma macropomum). Aquaculture 488: 9-16.
- REN M, HABTE-TSION H-M, XIE J, LIU B, ZHOU Q, GE X, PAN L and CHEN R. 2015. Effects of dietary carbohydrate source on growth performance, diet digestibility and liver glucose enzyme activity in blunt snout bream, Megalobrama amblycephala. Aquaculture 438: 75-81.
- SCHROETER JC, PETERSON BC, BLEDSOE J, LI M and SMALL BC. 2018. Targeted gene expression panels and microbiota analysis provide insight into the effects of alternative production diet formulations on channel catfish nutritional physiology. Aquaculture 489: 46-55.
- SOUZA SA, SOUZA RC, CAMPECHE DFB, CAMPOS RML and MELO JFB. 2014. Relação proteína:carboidrato no desempenho e no metabolismo de híbridos de Pseudoplatystoma fasciatum (fêmea) X Leiarius marmoratus (macho). Arq Bras Med Vet Zoo 66: 879-886.
- SPINA J, BRIGHT HJ and ROSENBLOOM J. 1970. Purification and properties of L-malic enzyme from Escherichia coli. Biochemistry 9: 3794-3801.
- TRAN-TU LC, HIEN TTT, BOSMA RH, HEINSBROEK LTN, VERRETH JAJ and SCHRAMA JW. 2017. Effect of ingredient particle sizes and dietary viscosity on digestion and faecal waste of striped catfish (Pangasianodon hypophthalmus). Aquacult Nutr 24: 961-969.
- WANG JT, JIANG YD, HAN T, LI XY, WANG Y and LIU YJ. 2016. Effects of Dietary Carbohydrate-to-Lipid Ratios on Growth and Body Composition of Orange-spotted Grouper Epinephelus coioides. N Am J Aquacult 79: 1-7.
- WANG L-N, LIU W-B, LU K-L, XU W-N, CAI D-S, ZHANG C-N and QIAN Y. 2014. Effects of dietary carbohydrate/lipid ratios on non-specific immune responses, oxidative status and liver histology of juvenile yellow catfish Pelteobagrus fulvidraco. Aquaculture 426-427: 41-48.
- ZHOU C, GE X, NIU J, LIN H, HUANG Z and TAN X. 2015. Effect of dietary carbohydrate levels on growth performance, body composition, intestinal and hepatic enzyme activities, and growth hormone gene expression of juvenile golden pompano, Trachinotus ovatus. Aquaculture 437: 390-397.
Publication Dates
-
Publication in this collection
25 Nov 2019 -
Date of issue
2019
History
-
Received
24 Jan 2019 -
Accepted
10 May 2019