Antinutritional Factors Present in Plant-Derived Alternate Fish Feed Ingredients and Their Effects in Fish

Aquaculture 199 2001. 197227 www.elsevier.
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Review article
Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish
George Francis a , Harinder P.S. Makkar b, Klaus Becker a, )
Department of Animal Nutrition and Aquaculture, Institute for Animal Production in the Tropics and Subtropics, Uniersity of Hohenheim (480), D 70593 Stuttgart, Germany b Animal Production and Health Section, International Atomic Energy Agency, P.O. Box 100, Wagramerstr. 5, A-1400 Vienna, Austria
a
Abstract The use of plant-derived materials such as legume seeds, different types of oilseed cake, leaf meals, leaf protein concentrates, and root tuber meals as fish feed ingredients is limited by the presence of a wide variety of antinutritional substances. Important among these are protease inhibitors, phytates, glucosinolates, saponins tannins, lectins, oligosaccharides and non-starch polysaccharides, phytoestrogens, alkaloids, antigenic compounds, gossypols, cyanogens, mimosine, cyclopropenoid fatty acids, canavanine, antivitamins, and phorbol esters. The effects of these substances on finfish are reviewed. Evidently, little unanimity exists between the results of different studies as to the specific effects of antinutrients, since most studies have been conducted using an ingredient rich in one particular factor and the observed effects have been attributed to this factor without considering other antinutrients present in the ingredient, or interactions between them. Tentatively, protease inhibitors, phytates, antigenic compounds, and alkaloids, at levels usually present in fish diets containing commercially available plant-derived protein sources, are unlikely to affect fish growth performance. In contrast, glucosinolates, saponins, tannins, soluble non-starch polysaccharides, gossypol, and phorbol esters, are more important from a practical point of view. The effectiveness of common processing techniques such as dry and wet heating, solvent extraction and enzyme treatment in removing the deleterious effects of antinutrients from feed materials is discussed. More insights into the nutritional, physiological and ecological effects of antinutrients on fish need to be accumulated through studies using purified individual antinutrients and their mixtures in proportions similar to those in alternative nutritional sources in fish feeds. Such studies would provide data useful for designing optimum inclusion levels of
Corresponding author. Tel.: q 49-711-4593158; fax: q 49-711-4593702. E-mail address: kbecker@uni-hohenheim.de K. Becker..
0044-8486r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 0 1 . 0 0 5 2 6 - 9
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G. Francis et al. r Aquaculture 199 (2001) 197227
plant-derived materials and treatment methods that would neutralise the negative effects of the antinutritional factors. q 2001 Elsevier Science B.V. All rights reserved.
Keywords: Aquaculture; Plant-derived nutritional sources; Antinutrients
1. Introduction As estimated by FAO, the human demand for food fish will climb from the current level of consumption of about 90 million metric tonnes Mtn. to about 110 Mtn by the year 2010. The share of aquaculture in the total world food fish production is set to increase from 29% in 1996 to 38% by the year 2010. In fact, aquaculture has become the fastest growing food production sector of the world, with an average annual increase of about 10% since 1984 as compared to 3% increase for livestock meat and 1.6% increase for capture fisheries FAO, 1997.. To sustain such high rates of increase in aquaculture production, a matching increase in the levels of production of fish feeds is required. Aqua-feed production is currently one of the fastest expanding agricultural industries of the world, with annual growth rates in excess of 30% per year. Estimates of the global levels of aqua-feed production for the year 2000 vary widely from 16.8 to 4.5 Mtn FAO, 1997.. Almost one third of the 122 Mtn of fish harvested in the year 1997 was converted into fishmeal or fish oil to be used in producing animal feed, including aquaculture feed. Of the total global production of fishmeal in 1996, 2 Mtn was used in fish farming, with farming of shrimp accounting for 20.3%, of salmon 18.8%, carp 18.3%, marine fish 13.9%, trout 10.9%, eel 10.7%, milkfish 1.6% and catfish farming 1.3% of that tonnage Sargent and Tacon, 1999.. FAO 1999. estimates that about 40% of the total aqua-feed production was for carnivorous finfish species, 35% for noncarnivorous species, and 25% for shrimp. Thus, although the bulk of fishmeal is used in salmon, trout and marine fish farming in western countries, freshwater fish farming, largely that of carp, also consumes a substantial proportion. Given the current very rapid increase in the intensification of fresh-water farming in Asia, particularly in China, intense future competition for limited global supplies of fishmeal and fish oil are likely Sargent and Tacon, 1999; Naylor et al., 2000.. This predicted strong demand from Asia for available feed resources will have a considerable impact on the world commodity markets and feed prices in general FAO, 1999.. Fishmeal production is also rather localised in some regions of the world, as a result of which it is becoming more expensive and difficult to obtain in many countries practising aquaculture. The need for alternative protein sources to replace fishmeal in aqua-feeds is therefore obvious and was strongly recommended by the Second International Symposium on Sustainable Aquaculture 1998. in Oslo, Norway. The very sustainability of the growing aquaculture industry depends on the progressive reduction of wild fish inputs into fish feed Naylor et al., 2000.. 2. Antinutritional factors Most of the potential, alternative, plant-derived nutrient sources are known to contain a wide variety of antinutritional substances Table 1.. Hundreds of studies have been
G. Francis et al. r Aquaculture 199 (2001) 197227 Table 1 Important antinutrients present in some commonly used alternative fish feed ingredients Plant-derived nutrient source Soybean meal Rapeseed meal Lupin seed meal Pea seed meal Sunflower oil cake Cottonseed meal Leucaena leaf meal Alfalfa leaf meal Mustard oil cake Sesame meal Antinutrients present Protease inhibitors, lectins, phytic acid, saponins, phytoestrogens, antivitamins, allergens Protease inhibitors, glucosinolates, phytic acid, tannins Protease inhibitors, saponins, phytoestrogens, alkaloids Protease inhibitors, lectins, tannins, cyanogens, phytic acid, saponins, antivitamins Protease inhibitors, saponins, arginase inhibitor Phytic acid, phytoestrogens, gossypol, antivitamins, cyclopropenoic acid Mimosine Protease inhibitors, saponins, phytoestrogens, antivitamins Glucosinolates, tannins Phytic acid, protease inhibitors
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published where the effects of inclusion of these materials in the diets of common culture fish are reported. A few studies in which plant-derived materials containing antinutrients have been included in fish diets and the effect of this inclusion on fish growth are summarised in Table 2. The main observations from various experiments that studied the effects of purified antinutritional factors in fish are listed in Table 3. Antinutrients have been defined as substances which by themselves, or through their metabolic products arising in living systems, interfere with food utilisation and affect the health and production of animals Makkar, 1993.. They could be broadly divided into four groups: 1. factors affecting protein utilisation and digestion, such as protease inhibitors, tannins, lectins; 2. factors affecting mineral utilisation, which include phytates, gossypol pigments, oxalates, glucosinolates; 3. antivitamins; 4. miscellaneous substances such as mycotoxins, mimosine, cyanogens, nitrate, alkaloids, photosensitizing agents, phytooestrogens and saponins. Antinutrients may also be classified according to their ability to withstand thermal processing, the most commonly employed treatment for destroying them. Heat labile factors include protease inhibitors, phytates, lectins, goitrogens and antivitamins, whereas heat stable factors are represented by saponins, non-starch polysaccharides, antigenic proteins, estrogens and some phenolic compounds van der Peol, 1989; Rumsey et al., 1993.. Oligosaccharides become somewhat more digestible after heat treatment, whereas the effect of thermal treatment on substances such as tannins remains uncertain. An overview on the effects of some antinutrients present in oilseeds and pulses on fish has been presented by Tacon 1997.. The present review takes into account additional information provided by experiments conducted in recent years, particularly those in which the effects of purified antinutrients such as saponins, tannins and phorbol esters have been studied on different species of fish. Our endeavour is to provide information on the nature, possible mode of action and effects of antinutrients, and known methods to eliminate potent antinutrients in conventional and unconventional plant resources. It is hoped that the information collated in
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Table 2 An overview of the results of selected studies where plant-derived ingredients were used to replace fishmeal in fish diets Plant material Fish species Grass carp fry Carp Inclusion rate %. 40 to 60 Crude protein level %. 29 to 46 Percentage of fishmeal replaced 100 Biological effects References
Commercial soybean meal
Thermally and hydrothermally treated full-fat soybean meal
50
44 to 50
50
Commercial hexane extracted soybean meal
Tilapia O. niloticus = O. aureus .
17 or 23
24 or 32
30
Raw R. or boiled B. or mixture of R and B RqB. or defatted D. soybean meal Commercial soybean meal
Nile tilapia
Rainbow trout
55 R. or 56 to 58 RqB. or 58 B. or 52 D. 13, 25 and 50
30
83
38
25 to 100
Full-fat soybean meal SBM. or soy protein concentrate SPC.
Atlantic salmon
30 SBM. or 28 SPC.
43
30 or 48
Growth performance lower than fish fed fishmeal based diet and it declined with increasing soybean content. Fishmeal based control fish showed best performance, among the soybean meals the hydrothermally treated and the intensely thermally treated meals supported better growth performance At 24% protein level inclusion of soybean meal did no affect growth, but at the 32% level groth was significantly reduced if methionine was not supplied additionally Fish fed diet with boiled or defatted soybean diet grew better than control while increasing levels of raw meal progressively depressed growth The 13% group showed performance as control, depression of growth in 25% group; growth arrestment and high mortality in the 50% group; decrease in amino acid absorption in all soy fed groups Abnormal intestinal morphology in SBM fed fish; no abnormality in the SPC group
Dabrowski and Kozack, 1979 Abel et al., 1984
Shiau et al., 1987
Wee and Shu, 1989
Dabrowski et al., 1989
van den Ingh et al., 1991
Solvent extracted soybean meal
Fingerling red drum
71, 53, 35.5, 18
34
25 to 100
Solvent extracted 1., special processed solvent extracted 2., enzyme-treated solvent extracted 3., ethanol-treated solvent extracted 4. and alkali-treated 5. solvent extracted soybean meal Full-fat FF., full-fat extruded FFE., solvent extracted FFSE., and solvent extracted and infrared radiation-treated FFR. soybean meal Soybean meal
Rainbow trout
33 to 44
50
70
Supression of feed intake, growth and high mortality at the highest level; lower feed consumption, higher feed efficiency and lower growth at the inclusion level of 53.2%; no significant difference between the other two groups and the control fed a diet based on fishmeal alone. Growth of group 2 was similar to control; other groups had lower growth; protein utilisation was comparable in all groups except 3, which had significantly lower values for protein utilisation and carcass protein Growth rates of soybean fed groups except FFE better than control; FFE group had significantly lower growth
Reigh and Ellis, 1992
Rumsey et al., 1993
Rainbow trout
21 to 30
40
30
Oliva-Teles et al., 1994
Rainbow trout Hybrid striped bass
32
41
40
Methionine supplemented soybean meal
15.7, 34 or 44
35
24 to 64
No differences in weight gain and growth rate, feed intake was higher in fish fed thesoybean meal diet With small fish 5 g. there were no difference in performance at the lowest and highest levels but growth was significantly lower at the 34% level; in bigger fish there was no differences in growth
Sanz et al., 1994 Gallagher, 1994
(continued on next page)
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Table 2 continued . Plant material Fish species Rainbow trout Inclusion rate %. 22 to 62 SPC. or 24 to 42 SF. Crude protein level %. 46 Percentage of fishmeal replaced 33 to 100 or 25 to 50 Biological effects References
Soy protein concentrate SPC. or commercial soy flour SF.
Soybean meal
Gilthead seabream
10, 20 or 30 each
55 to 57
10 to 30
Commercial soy concentrate SC. or phytase-treated SC A 1:4 mixture of defatted soybean meal and soy protein concentrate Raw or heated lupin seed meal Lupin seed meal Extruded lupin flour
Atlantic salmon Rainbow trout Rainbow trout Gilthead seabream Rainbow trout
48
43 to 45.7
75
44
35
73
10, 20, 30 or 40 10, 20 or 30 each 30, 50 or 70
44 to 46
10 to 40
53 to 56 40 to 46
10 to 30 33 to 88
Colzapro coextruded rapeseed and peas.
Rainbow trout
8, 16, 24 or 45
34 to 42
5 to 48
No significant difference in growth performances between the different groups, an insignificant decline in growth when soy flour was used, significant reduction in protein retention when soy flour replaced fishmeal Growth performance similar to control; trypsin activity retarded at 30% levels; deposition of lipid in the liver at high soybean level Growth performance similar to control; treatment of SC with phytase further improved protein utilisation Fish on the test diet grew significantly better than control; supplementation by phytase did not affect weight gain of fish Performance similar to control up to a level of 30% inclusion; heating did not improve performance Growth performance similar to control; trypsin activity retarded at 30% level Growth performance similar to control up to the 50% level, lipid deposition in the liver; significantly lower performance at 70% level of inclusion Growth slightly better than control at the first 3 levels and significantly lower growth rate but higher protein efficiency ratio and feed to body mass gain ratio at 45% level.
Kaushik et al., 1995
Robaina et al., 1995
Storebakken et al., 1998 Vielma et al., 2000
de la Higuera et al., 1988 Robaina et al., 1995 Burel et al., 1998
Gomes et al., 1993
Undephytinized rapeseed protein concentrate Dephytinized rapeseed protein concentrate
Juvenile rainbow trout Juvenile rainbow trout Rainbow trout Rainbow trout
12, 24, 36
42 to 45
33 to 100
13, 26 or 39
42 to 45
33 to 100
Low and high glucosinolate rapeseed RM. meal Raw R., commercial C., low heated LH., heated H. or glandless G. cottonseed meal Cottonseed cake Decorticated DC. or corticated CC. cottonseed meal
30 or 50 each 25 each
40 50
18 and 33 26 to 40 of casein was replaced here
Growth was depressed only when fishmeal was totally replaced, feed consumption was highest at this level Growth was depressed only when fishmeal was totally replaced, feed consumption was highest at this level, dephytinisation lowered protein quality. Significant decrease in growth performance in all RM based diets Growth depression in the R and LH groups, LH being the worst
Teskeredzic et al., 1995 Teskeredzic et al., 1995
Burel et al., 2000b Herman, 1970 G. Francis et al. r Aquaculture 199 (2001) 197227
Tilapia Nile tilapia
16.4 to 19.4 65 or 80
18 to 32 30
100 100 or 86
Growth depression at all levels Significant depression in growth rate and other food utilisation parameters at both levels; DC was better than CC as far as growth was concerned; supplementation with L-lysine did not improve the nutritiponal quality of cottonseed meal No differences in weight gain and growth rate The 45% carbohydrate diets led to the greatest weight increases, best food utilisation and protein sparing Performance not significantly different from control
Ofojekwu and Ejike, 1984 El-Sayed, 1990
Sunflower meal Cassava or rice meal
Rainbow trout Carp
42.5 15 to 45
41 30
40 15 to 45
Sanz et al., 1994 Ufodike and Matty, 1983 Fagbenro, 1999
Autoclaved or roasted winged bean
African catfish
50
40
80
(continued on next page)
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Table 2 continued . Plant material Fish species Nile tilapia Inclusion rate %. 31 to 90 Crude Percentage Biological effects protein of fishmeal level %. replaced 21 to 30 26 to 100 Significant decline in growth at all levels of inclusion; the soaked leaf meal performed better than the other leaf meal diets Up to 40% leucaena meal was tolerated without negative effects on growth by males; but growth was affected at all levels for females; fry production significantly reduced beyond the 40% level Cassava leaf meal significantly reduced growth performance with growth reduction increasing linearly with increasing leaf meal inclusion; the treatment of the cassava leaf meal did not improve fish performance. Fish fed lowest level of 1 and up to 20% of 2 showed significant improvement in growth from control; others showed negative effects Negative effects on growth at all levels of inclusion and these increased with increasing levels Depressed feed intake and increased mortality with increased use of autoclaved jack bean seed meal; the treatments resulted removal of non-themolabile toxins so that replacement of 26% of fishmeal protein by treated meal did not reduce growth performance References
Soaked, sundried or commercial leucaena leaf meal Leucaena leaf meal
Wee and Wang, 1987 G. Francis et al. r Aquaculture 199 (2001) 197227 Santiago et al., 1988
Nile tilapia
20 to 80
20
19 to 78
Soaked sun dried or sun dried cassava leaf meal
Nile tilapia
20 to 100
30
20 to 100
Ng and Wee, 1989
Chloroplastic CH. and cytoplastic CY. alfalfa leaf protein Dehydrated alfalfa DA. or saltbush Artiplex . SB. leaves Autoclaved A. or otherwise treated, OT, chopped soaked and boiled; chopped and autoclaved; chopped and soaked in ethanol sulphuric acid 1:1. and autoclaved. jack bean meal
Tilapia O. mossambicus.
11 to 41 CH. or 9 to 32 CY.
40
15 to 55
Olvera-Novoa et al., 1990
Tilapia O. aureus L.. Tilapia
6 to 34 DA. 40 or 6 to 38 SB. 13 to 47 A. or 33 OT. 39
5 to 30
Yousif et al., 1994 Martinez-Palacios et al., 1988
10 to 35 or 26
Autoclaved A. or raw R. or differently treated with water DT. Sesbania grandiflora seed meal Pea seed meal Unheated or heat-treated J. curcas meal Copra, groundnut, soy, sunflower, rapeseed, cottonseed or leucaena meal
Tilapia
9 to 33 A. or 24 R. or 25 DT.
38
10 to 36
Depressed feed intake with increased mortality with increased use of sesbania seed meal; fish fed the water-treated meal performed better but still was not as good as control No significant differences in performance from control Growth lower than control, heat treatment had no significant effect Leucaena meal at 25% level; copra, groundnut and soy at 50% levels produced poor growth, sunflower produced comparable and rapeseed and cottonseed better growth than control at the 50% level; at 75% level all induced growth depression All ingredients had significantly lower nutrient digestibility coefficients than control Growth significantly lower than control in all cases, among the various treatments 25% MC and 25% LM gave best results for growth Growth performance was significantly better in the control fish, aqueous extraction and autoclaving improved the nutritional value of the meals to carp but not to the level of fishmeal Fish fed the sunflower meal and cottonseed meal showed slightly better performance than control, but the soybean meal fed fish had inferior growth performance and feed conversion
Olvera-Novoa et al., 1988
Juvenile European 20 or 40 sea bass Common carp 23 Tilapia S. Mossambicus. 17.4 to 69.4
48 35 30
9 to 18 46 25, 50 or 75
Gouveia and Davies, 1998 Makkar and Becker, 1999 Jackson et al., 1982
Mustard oil cake, linseed meal or sesame meal Mustard oil cake MC., linseed meal LM. or sesame meal SM. Linseed meal LM. or sesame meal SM.
Common carp
70 to 88
30
100
Hossain and Jauncey, 1989a Hossain and Jauncey, 1989b
Common carp
Common carp
30 or 61 MC., 40 30 or 59 or 23LM., 47 or 70 SM. 30 LM. or 40 27 SM.
25 to 75
25
Hossain and Jauncey, 1990
Commercial soybean meal, Tilapia cottonseed meal or sunflower seed meal
21 to 34
28.5
32
Sintayehu et al., 1996
205
206
Table 3 Effects of purified antinutritional chemicals occuring in plant material on fish Substance tested Gossypol acetate Fish species Fingerling trout Inclusion rate %. 0.025, 0.1 or 0.2 Biological effect At the first two levels, fish accepted the feeds well but accumulated gossypol in the vascular tissues; complete suppression of feed intake at 2000 ppm level Growth depression and high mortality; thickening of the glomerular basement membrane and fatty degeneration of the liver No significant differences in growth or feed conversion Growth inhibition; alterations in liver fatty acid composition and abnormal glycogen deposition in liver Depression in growth and food conversion efficiency The 25.8 grkg group showed depressed growth, food and protein conversion and thyroid function. Depression of growth, food utilization and protein dogestibility; effect was exacerbated by simultaneous increases in dietary calcium and magnesium levels. Intestinal epithelium showed abnormalities. Except formononetin, all induced hepatic synthesis of vitellogenin References Roehm et al., 1967
Gossypol acetate
Rainbow trout
0.1
Herman, 1970
Gossypol acetate Sterculic acid
Fingerling tilapia Rainbow trout
0.1 or 0.2 0.01 or 0.02
Robinson et al., 1984 Roehm et al., 1970
Phytic acid Sodium phytate Sodium phytate
Rainbow trout Juvenile chinook salmon Common carp
0.5 0.16, 0.65 or 2.58 5 or 10 mg per g
Spinelli et al., 1983 Richardson et al., 1985 Hossain and Jauncey, 1990
Phytoestrogens-formononetin, daidezin, genistein and equol
Yearling Siberian sturgeon
Administered at rates of 0.05 to 0.5 mg per g body weight
Pelissero et al., 1991a
Soybean protease inhibitors
Rainbow trout
0.37, 0.74, 1.11 or 1.48
Quillaja bark saponin Quillaja bark saponin Purified alcohol extract of soybean meal PAES. or soy protein isolate SPI. active principle being soy saponins PAES 1. or SPI 2., active principle being soy saponins Phorbol esters Tannic acid hydrolysable tannin. and quebracho tannin condensed tannin.
Chinook salmon Rainbow trout Chinook salmon
0.15 or 0.30 0.15 or 0.30 1 or 0.3
Increased trypsin inhibition with increased inclusion; this was partly compensated by increased enzyme secretion and absorption by the intestine; the compensation was complete at lower levels of the inhibitor Growth depression only at the higher level; abnormal intestinal morphology at both levels Growth depression only at the higher level; abnormal intestinal morphology at both levels Suppression of feed intake and growth in both cases
Krogdahl et al., 1994
Bureau et al., 1998 Bureau et al., 1998 Bureau et al., 1998 G. Francis et al. r Aquaculture 199 (2001) 197227
Rainbow trout
1 or 0.3
Common carp Common carp
03.75 to 1000 ppm 2
Depression in growth and moderate intestinal damage when fed 1; No significant effect when fed 2 only 2 weeks duration. Feed rejection, faecal mucus production, significant suppression in growth starting from 31 ppm onwards Condensed tannin did not affect the performance of fish but hydrolysable tannin had adverse effects after 28 days when it completely supressed feeding
Bureau et al., 1998
Becker and Makkar, 1998 Becker and Makkar, 1999
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this review will provide an impetus to further research in this area, enabling better utilisation of plant resources as sources of protein and carbohydrate for sustaining the current growth rate of aquaculture production.
3. Protease inhibitors Protease inhibitors are widespread antinutrient substances in many plant-derived nutritional ingredients that could be used in fish feed, particularly the legumes Norton, 1991.. Their potency depends on their origin and the target enzyme. In soybean, for example, there are two groups of protease inhibitors: the Kunitz soybean trypsin inhibitor that is relatively heat- and acid-sensitive, and the more stable BowmanBirk protease inhibitor. One molecule of the former blocks either one trypsin or one chymotrypsin molecule, while one molecule of the latter blocks either two trypsin or chymotrypsin molecule or one trypsin and one chymotrypsin molecule at the same time Norton, 1991.. Commercial soybean products mostly show trypsin inhibitors TI. in the range of 26 mgrg, averaging 4 mgrg Synder and Kwon, 1987.. TI have a wide distribution in the plant kingdom and is present in most legume seeds and cereals. The common culture fish species differ in their ability to tolerate dietary TI. Tilapia Jackson et al., 1982; Shiau et al., 1987, 1989; Wee and Shu, 1989., carp Abel et al., 1984; Makkar and Becker, 1999., rainbow trout Dabrowski et al., 1989; Rumsey et al., 1993; Krogdahl et al., 1994., channel catfish Wilson and Poe, 1985., salmon Higgs et al., 1982; Olli et al., 1994a. and seabream Robaina et al., 1995. are able to maintain growth rates comparable to fish-meal based controls see Table 2. after the inclusion of varying levels of soybean meal, lupin seed meal, rapeseed meal and Jatropha seed meal, all of which are known to contain TI. TI levels of 1.6 mgrg or higher in the diet retarded Nile tilapia growth, but the fish tolerated and grew well at dietary levels of 0.6 mg TIrg diet Wee and Shu, 1989.. Makkar and Becker 1999. found that carp fed diets containing meal of J. curcas seeds of non-toxic provenance, with 24.8 mg TIrg and heat-treated meal with 1.3 to 8.3 mg TIrg, showed no differences in growth performance implying that the fish were able to tolerate the high levels of TI. The reduction in growth of carps and tilapia Oreochromis aureus = O. niloticus . fed diets containing TI as compared to the controls Dabrowski and Kozak, 1979; Viola et al., 1983; Abel et al., 1984; Shiau et al., 1987. may have been caused by amino acid imbalance in the soybean of experimental diets. Rainbow trout has been found to be highly sensitive to the soybean protease inhibitors and a direct relation was observed between the amount of TI in the diet and the availability of protein and energy for trout Sandholm et al., 1976; Krogdahl et al., 1994.. Dabrowski et al. 1989. suggested that the impairment of chymotrypsin secretion in rainbow trout fed soybean-supplemented diets is caused by the suppression of the pancreatic feedback mechanism. Trypsin production in Atlantic salmon peaked when the TI level in the diet was around 4.8 mgrg Olli et al., 1994a.. Juvenile channel catfish showed the best growth performance in this trial when the TI level was 2.2 mgrg of the diet Wilson and Poe, 1985.. The negative effect of TI on growth in fingerling channel
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catfish at higher levels in this experiment was less pronounced when dietary protein was also high. Krogdahl et al. 1994. observed that rainbow trout were able to partly compensate for TI action by increased enzyme secretion and enhanced absorption of protein in the distal parts of the intestine. Rumsey 1991. found little effect on growth or feed intake at TI levels below 5 mgrg, when feeding trout at levels of TI ranging from 2.6 to 51.0 mgrg. It seems that below the 5 mgrg level, most cultured fish are able to compensate for the presence of TI by increasing trypsin production. At the usual levels at which the materials containing protease inhibitors such as commercially available soybean meal are included in fish diets, other antinutritional factors or interactions between them may be more important. For other materials, moist heat treatment autoclaving for 1530 min; Norton, 1991. is recommended as a means of reducing the amount of trypsin inhibitors below the critical levels. This heating process should be carefully regulated to minimise the loss of nutritional quality of the feed material, such as the loss of availability of amino acids like lysine and the decrease in protein degradability due to excessive heat denaturation.
4. Phytates Phytate hexaphosphates of myo-inositol. is common in plant seeds. They can chelate with di- and trivalent mineral ions such as Ca2q, Mg 2q, Zn2q, Cu3q and Fe 3q resulting in these ions becoming unavailable for consumers Duffus and Duffus, 1991.. Since phytates cannot be broken down by non-ruminants, their occurrence in feed reduces the availability of phosphorus to these animals Liener, 1989.. Phytates also form sparingly digestible phytateprotein complexes, thus reducing the availability of dietary protein Richardson et al., 1985.. Commonly used and potentially usable plant-derived fish feed ingredients such as soybean meal, rapeseed meal, and sesame meal contain 1015, 5075 and 24 grkg phytate, respectively. Growth in commonly cultured fish species, such as carp, tilapia, trout and salmon, is negatively affected by inclusion of phytate containing ingredients in the diet see Table 2.. The involvement of phytates in inducing the negative effects has been corroborated by feeding studies where synthetic phytate was added to fish diets. Spinelli et al. 1983. observed decreased growth rates in rainbow trout fed a diet containing 5 grkg synthetic phytic acid. Formation of sparingly digestible phytic acidprotein complexes was found to be the main reason for growth depression in this study. High dietary phytic acid synthetic, 25.8 grkg. dramatically depressed the rate of growth in Chinook salmon Richardson et al., 1985.. The lowered feed and protein conversion ratios observed here were partly due to diminished zinc bio-availability, as supplementation of the high phytate diets with zinc 0.35 to 0.4 grkg. partially improved the food and protein conversion when dietary calcium was also high. The authors also found abnormalities in thyroid, kidney and alimentary tract morphology of the fish. Furthermore, the pyloric caecae were found to be abnormally hypertrophied and showing cytoplasmic vacuolation. Phytate obviously had a toxic effect on the epithelial layer of the pyloric caecae. In juvenile Chinook salmon fed high
210
phytate and low zinc diets, the same authors observed incidence of cataract, indicating mineral-chelating action of phytic acid. Pure synthetic phytic acid 5 and 10 grkg feed. resulted in lower growth performance in common carp Hossain and Jauncey, 1993.. The effects of phytic acid were exacerbated by the simultaneous addition of calcium and magnesium to the diet. Dietary phytate in this experiment caused hypertrophy and vacuolization of the cytoplasm of the intestinal epithelium. A significant depression of zinc levels in the carcass was observed in juvenile rainbow trout fed a diet containing undephytinised rapeseed protein concentrate Teskeredzic et al., 1995.. The rapeseed protein concentrate used in this study contained 53 to 75 grkg phytic acid. Feeding trials by Sugiura et al. 1999. demonstrated that apparent availability of phosphorus was significantly higher when mutant varieties of corn and barley, low in phytic acid content, were used in rainbow trout diets. Supplementation of phytate-containing diets with the enzyme phytase neutralised the negative effects of phytate. True P availability to rainbow trout from various plant foodstuffs, which ranged between 9.7% and 48.4%, significantly increased to 46.2% to 75.6% on supplementation with phytase Riche and Brown, 1996.. Soy concentrate, previously incubated with phytase, when included in the diet, improved protein utilisation parameters, apparent digestibility coefficients, and body levels of Ca, Mg and Zn and retention of P in Atlantic salmon Storebakken et al., 1998; Vielma et al., 1998.. The lowered growth performance of fish fed high phytate diets can be attributed to various factors, namely reduced bio-availability of minerals, impaired protein digestibility caused by formation of phytic acidprotein complexes, and depressed absorption of nutrients due to damage to the pyloric cecal region of the intestine. Phytates, particularly in cereals, are concentrated in the outer endosperm. Milling to remove the outer layer of seeds therefore reduces the phytate content of the seed considerably. Fermentation has also been shown to reduce the phytic acid content of grains because of the action of phytases produced by yeast or lactic acid bacteria Duffus and Duffus, 1991; Mukhopadhyay and Ray, 1999a.. Heat treatment autoclaving. was also found to reduce phytic acid in linseed and sesame meals by up to 72% and 74%, respectively Hossain and Jauncey, 1990.. Salmonids seem to be able to tolerate dietary levels of phytate in the range of 56 grkg, while carp appears to be sensitive to these levels. It seems to be advisable to maintain the level of phytates below 5 grkg in fish feeds. The addition of minerals such as Zn has been shown to be only partially capable of counteracting the negative effects of dietary phytate.
5. Glucosinolates Glucosinolates are thioglucosides commonly found in plants belonging to the family Cruciferae. They are always accompanied by thioglucosidase enzymes in plants but the two are kept separated in different cell compartments. When the contents of these two components come together by cellular damage, breakdown products like isothiocyanates and nitriles, capable of causing potentially harmful effects to animals, are released Duncan, 1991.. The presence of intact glucosinolates has been correlated with the
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occurrence of liver haemorrhage in laying hens while nitriles have been shown to cause tissue damage in liver and kidney and increased organ weights and isothiocyanates affect thyroid function see Duncan, 1991.. Glucosinolates are the main antinutrients present in rapeseed Brassica spp.. meal and mustard oil cake see Duncan, 1991. which are potentially attractive protein sources in fish feeds. Plant geneticists have developed improved varieties of both of the common species, Brassica napus and B. campestris, with low glucosinolate content less than 3 mgrg. in the seed; such varieties are known as canola. Higgs et al. 1982. found that dietary rapeseed meal 16%. affected the thyroid structure in juvenile Chinook salmon whereas dietary canola meal did not. Growth performance was comparable to control in both cases. The thyroids of the affected fish were characterised by the presence of clear hyperplasia and follicular hypertrophy, indicating higher than normal thyroid activity. The thyroid follicles in these fish had little colloid, numerous mitotic figures and significantly taller epithelial cells when compared to control fish; symptoms of an obvious effort by the fish to maintain blood thyroid hormone levels through increased thyroid gland activity. Similar thyroid abnormalities were found in carp Cyprinus carpio . fed a diet containing 3.3 g purified glucosinolaterkg Hossain and Jauncey, 1989b. and tilapia O. mossambicus. fed a diet containing 2.5 g glucosinolaterkg, Davies et al., 1990.. Increased thyroid activity was observed in juvenile rainbow trout fed undephytinised rapeseed protein concentrate containing glucosinolates Teskeredzic et al., 1995.. Trout and turbot Psetta maxima. were found to compensate for decreased thyroid functioning caused by dietary glucosinolates through higher activity of the deiodinases, which convert thyroxine into the active component, triiodothyronine Burel et al., 1998, 2000a,c.. It is interesting that turbot fed a high glucosinolate 11.6 m molrg., rapeseed meal-based diet had normal thyroxine and triiodotyronine contents in plasma even though higher deiodinase activity was observed Burel et al., 2000c.. This might have been due to lack of breakdown of glucosinolates into toxic by-products in untreated rapeseed meal. The ingestion of very low amounts of glucosinolates 1.4 m molrg diet. led to a decrease of both growth rate and feed efficiency in rainbow trout, but this effect was not exacerbated when dietary glucosinolate was increased to 11.6 m molrg. Stronger depression of growth was observed when the level of glucosinolates went up to 19.3 m molrg in the diet. Thyroid activity in trout was already affected at the lowest level of glucosinolate Burel et al., 2000b.. Heat treatment is effective in reducing the glucosinolate content of feed materials in rapeseed meal from 40 to 26 m molrg after wet pressure-cooking; Burel et al., 2000a.. Extracting with water was found to be a cost-effective method of removing glucosinolates from full-fat and fat-free Moringa oleifera kernels Makkar and Becker, 1997.. Colzapro, a co-extruded product of rapeseed and peas, did not affect thyroid morphology in rainbow trout, indicating the effectiveness of this treatment in minimising the negative effects of glucosinolates Gomes et al., 1993.. Over the long term, thyroid dysfunction induced by continuous consumption of glucosinolate containing feed is certain to affect metabolism and growth in fish. Setting a threshold level of glucosinolates in fish diets is, however, difficult because of inadequacies of data available on the quantities of its toxic derivatives, such as isothiocyanates and nitriles, which are mainly responsible for the negative effects.
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6. Saponins Saponins are steroid or triterpenoid glycosides found in many of the potential, alternate plant-derived feed ingredients for fish, like legumes ranging between 18 and 41 mgrkg in various legume seeds; 67 mgrkg in defatted roasted soybean flour; Fenwick et al., 1991.. When added to water, they are highly toxic to fish because of the damage caused to the respiratory epithelium of the gills by the detergent action of the saponins. Tea Camellia sinensis . seed cake, containing about 78% saponins, when added to water at a dose of 100 ppm resulted in the death of tilapia within 5 to 6 h De et al., 1987.. They are also considered to be the active components of many traditionally used fish poisons, like mahua oil cake. Saponins in lupin seed meal 1.1%. and alfalfa Medicago satia, - 0.30% in low saponin varieties to ) 1.5% in high saponin varieties. could have been important contributing factors for the lower growth performance of rainbow trout de la Higuera et al., 1988., and tilapia Olvera-Novoa et al., 1990; Yousif et al., 1994. fed diets containing high levels of these ingredients. Krogdahl et al. 1995. however did not find any negative effects of saponins included in the diet of Atlantic salmon at levels similar to that expected to be found in a soybean meal 3040%. based diet. In the same study, an alcohol extract of soybean meal caused growth retardation, altered intestinal morphology and depressed mucosal enzyme activity in the distal intestine. Bureau et al. 1998. observed that rainbow trout was more tolerant to inclusion of purified alcohol extracts of soybean meal extracted to isolate soy saponins. in the diet than Chinook salmon. Chinook salmon fed this diet had an intestinal morphology resembling that of a fasting fish, probably caused by the deterrent action of the saponin on feeding. Extensive damage to the intestinal mucosa was observed in both fish species at a dietary level of 1.5 grkg Quillaja bark saponin. The condition of the intestine of these fish was similar to that of fish fed the raw soybean meal diet, indicating the role of the saponins in causing the damage. The negative effects of saponins could be caused by the well-known effects of these surface-active components on biological membranes. Ingested soy saponins do not seem to be absorbed either as saponins or even as constituent sapogenins in chickens, rats and mice Gestener et al., 1968.. In these animals, hind gut microorganisms break down the saponins into sapogenins and sugars. The fate of saponins in the alimentary tract of fish has not been studied. Some saponins readily increase the permeability of small intestinal mucosal cells and inhibit active nutrient transport, although different saponins might differ in effectiveness. For example, soy saponin was less effective compared to Gypsophylla saponins in reducing transmural potential difference, the main driving force for active hexose transport across the brush border membrane in the small intestine of rats Johnson et al., 1986.. Other properties of saponins may also play a role in its growth depressing action. Endogenous saponins have been shown to reduce the protein digestibility of soybean by chymotrypsin Shimoyamada et al., 1998., probably by the formation of sparingly digestible saponinprotein complexes Potter et al., 1993.. Complex formation between saponins and other antinutrients could, however, lead to the inactivation of the toxic effects of both the substances Makkar et al., 1995a.. Simultaneous consumption of saponin and tannin resulted in the loss of their individual
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toxicity to rats Freeland et al., 1985.. This is considered to be due to chemical reactions between them, leading to the formation of tanninsaponin complexes, inactivating the biological activity of both tannins and saponins. Soy saponins have been found to actually stimulate feeding in oriental clouded yellow larva, Coliaserate poliographus Matsuda et al., 1998.. Saponins might also increase the digestibility of carbohydrate-rich foods because of their detergent-like activity, which reduces viscosity and thus prevents the normal obstructing action of such foods against movement of digesta in the intestine. Because of the high solubility of most saponins in water, aqueous extraction would remove most saponins from feed ingredients and this could be recommended for removing saponins provided it does not otherwise affect the nutritional quality of the material. Levels below 1 grkg of diet are unlikely to affect growth performance of common culture fish. More investigations are required on the effects and tolerance limits of this widely present factor in plants to fish.
7. Tannins Tannins are secondary compounds of various chemical structures widely occurring in plant kingdom and are generally divided into hydrolysable and condensed tannins. Their antinutritional effects include interference with the digestive processes either by binding the enzymes or by binding to feed components like proteins or minerals Liener, 1989.. Tannins also reduce the absorption of vitamin B12 . Some materials tested as alternative nutrient sources for fish do contain this substance Table 1.. Common carp has been shown to be able to tolerate a 2% addition of quebracho tannin powder a condensed tannin. without any effect on growth while a similar level of hydrolysable tannin tannic acid. induced feed rejection after 28 days of feeding Becker and Makkar, 1999.. Contrary to condensed tannins, the hydrolysable tannins are easily degraded in biological systems, forming smaller compounds that can enter the blood stream and over a period of time cause toxicity to the organs e.g., liver and kidney.. How far the purified commercially available tannins simulate those naturally occurring in plant products needs to be investigated. Condensed tannins present in copra at a level of approximately 2.4% could have been the cause of growth depression in tilapia and rohu Labeo rohita. fingerlings even at such low levels of inclusion as 25% or 20% Jackson et al., 1982; Mukhopadhyay and Ray, 1999b.. Other tannin containing feeds, like rapeseed and pea seed meal, have reportedly been tolerated by different fish species at moderate to high levels of inclusion see Table 2.. Broad bean Vicia faba. meal, with a high condensed tannin content, had lower protein digestibility than soybean in in vitro experiments Grabner and Hofer, 1985.. The differences in digestibility were more pronounced after digestion under the simulated conditions of the carp gut than those of the rainbow trout gut. These differences probably indicate the differences in tolerances of different fish species and differences in the structure of the tannins or their interactions with other components in the diet. Tannins are also known to interact with other antinutrients. For example, interaction between tannins and lectins removed the inhibitory action of tannins on amylase Fish and Thompson, 1991., and interactions between tannins and
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cyanogenic glycosides reduced the deleterious effects of the latter Goldstein and Spencer, 1985.. Recommended methods for the removal of condensed tannins include de-hulling the seeds to remove the tannin rich outer layer, autoclaving or treatment with alkali Griffiths, 1991.. Mukhopadhyay and Ray 1999a. observed a reduction in the tannin content of sesame seed meal from 20 to 10 grkg after fermentation with lactic acid bacteria. The treatment of tannin-containing feeds with oxidising agents and supplementation with a tannin-complexing agent, polyethylene glycol, could mitigate their negative effects on animals Makkar et al., 1995b; Makkar and Becker, 1996.. Limited literature on the effects of purified tannins on fish suggest that fish are sensitive to tannins and caution should be exercised in incorporating seeds and agroindustrial byproducts containing high amounts of tannins.
8. Lectins Plant lectins or phytohaemagglutinins are found in many legume seeds and are able to bind reversibly to carbohydrate moieties of complex glyco-conjugates present on membranes. Even though they are proteins, they are at least partially resistant to proteolytic degradation in the intestine. Their common biological effects include disruption of the small intestinal metabolism and morphological damage to the villi Grant, 1991.. Soybean lectins 60 haemagglutinating unitsrmg protein., otherwise known as soybean agglutinin SBA., have been shown to be able to bind extensively to the brush border surfaces, particularly in the distal part of the small intestine of Atlantic salmon and may contribute to the toxic effect of full-fat soybeans and soybean products in diets for salmonids Hendriks et al., 1990.. van der Ingh et al. 1991. observed distinct effects of full-fat soybean meal FFSB. on the mucosa of the distal intestine in the Atlantic salmon as compared to a standard herring meal diet HM. fed control. In the FFSB group, the epithelium had an increased density of goblet cells and a marked decrease or absence of absorptive vacuoles; the microvilli of the enterocytes were shortened with increased microvillar vesicle formation. These effects are similar to those observed after SBA was given to other animals see Grant, 1991.. The increase in goblet cell density may have been the result of hypertrophic mucus production in the intestine when subjected to irritation by lectins. Carp growth was similar when fed diets containing high 51 haemagglutination units. or low lectin - 1.2 haemagglutination units. activity Makkar and Becker, 1999.. Other effects of lectins, such as muscle wastage and depletion of lipids in the adipose tissue and liver enlargement Grant, 1991., have not been observed in fish so far. Lectins can be removed by aqueous heat treatment 1008C for 10 min. or autoclaving Grant, 1991.. Aregheore et al. 1998. reduced the lectin content in Jatropha seed meal from 102 to 1.17 haemagglutination units by moist heating at 1008C for 10 min. Irritation caused by lectins to the intestinal membrane resulting in over secretion of
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mucus may impair the enzymatic and absorptive capacity of the intestinal wall. Their deleterious effect may be more potent when present along with other antinutrients.
9. Oligosaccharides and non-starch polysaccharides Oligosaccharides of the raffinose family and non-starch polysaccharides NSPs. are important constituents of a wide variety of grain legumes and cereals Saini, 1989.. In fish, their negative effects may be either due to binding to bile acids or obstructing action against action of digestive enzymes and movement of substrates in the intestine Storebakken et al., 1998.. Arnesen et al. 1989. found a decrease in nutrient utilisation caused by soybean carbohydrates in Atlantic salmon. They, however, found little effect of soy oligosaccharides on protein utilisation in rainbow trout. The main oligosaccharides of defatted soybean meal are sucrose 67%., raffinose 12%. and stachyose 56%., accounting for a total soluble carbohydrate content of 1215%. Decreased feed intake in hybrid striped bass Gallagher, 1994. and rainbow trout de la Higuera et al., 1988., and lower feed digestibility in trout Sanz et al., 1994. fed diets containing soybean, lupin, and sunflower meal, were attributed to the presence of high proportions of NSPs such as pectins, galactans, cellulose and lignin. High fecal water content, probably induced by the presence of osmotically active NSPs, was observed when soy products were included in diets of salmonid fish Olli and Krogdahl, 1994; Olli et al., 1994b; Refstie et al., 1997.. NSPs such as arabinan, arabinogalactan and acid polysaccharides, which form about 14% to 18% of the total carbohydrate content of defatted soybean meal might also bind minerals in the intestine and reduce the digestibility of fat Storebakken et al., 1998.. The addition of soybean oligosacccharides to a fishmeal based diet did not cause morphological changes in the intestinal tract van der Ingh et al., 1991. or affect nutrient digestibility or growth Krogdahl et al., 1995. in Atlantic salmon. It must be added that trout have been shown to be able to satisfactorily utilise diets containing sunflower meal Tacon et al., 1984; Sanz et al., 1994. and soybean meal Rumsey et al., 1993; Sanz et al., 1994; Kaushik et al., 1995.. Feed containing high levels of carbohydrates was also shown to be well tolerated by tilapia Jackson et al., 1982. and carp Ufodike and Matty, 1983.. Erfanullah and Jafri 1998. observed that steam cooking improved the digestibility coefficients of yellow corn and potato in these fish species. However, heat-treated lupin seed meal, abundant in galactans that were made more digestible by the treatment, reduced the feed intake of rainbow trout, probably by inducing hyperglycaemia de la Higuera et al., 1988.. Extrusion at high temperature has the potential to improve the carbohydrate digestibility in legume seeds Bangoula et al., 1993; Burel et al., 2000a. because of a higher break up of cell walls andror a partial degradation of a-galactosides. There are discrepancies among different studies as to the level of tolerance and utilisation of feed carbohydrates by fish species such as trout. This could be because of the different origins of the carbohydrates and the different treatment methods employed in different studies. It could be concluded that NSPs, particularly the soluble NSPs, are more detrimental to growth of fish than the oligosaccharides Refstie et al., 1999.. They trap water and form gum-like masses in the intestine, increase the viscosity of intestinal
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contents, and obstruct the digestive enzyme activity, thus exerting potent antinutritional activity when present in fish diets.
10. Phytoestrogens Non-steroidal estrogenic substances are widely distributed among potential plant-derived feeds Farnsworth et al., 1975a,b.. Estrogenic activity has been reported to be present in soybeans, cottonseed, linseed, safflower etc. Chemically, plant estrogens are mostly isoflavones that occur in the form of glycosides. The sugar moiety is attached to one or more of the hydroxyl groups located at various positions of the isoflavone nucleus Liener, 1980.. For example, soybean contains estrogenic isoflavones and derivatives such as coumestrol, formononetin, diadzein, biochanin A, genistein and equol about 0.25% in defatted meal; Pelissero et al., 1991a.. Studies with sturgeon indicated that dietary phytoestrogens were estrogenic in fish and induced vitellogenesis Pelissero et al., 1991b.. Coumsterol, and isoflavonic compounds such as genistein and daidzein had estrogenic properties when administered intraperitoneally in the pure form to the same fish species. These compounds act either by binding direct to oestrogen receptors or getting converted into compounds that have estrogenic effects, like equol. Dietary estrogenic effects of plant-derived materials can have wide ranging consequences, as oestrogen is known to have wide ranging effects on various physiological processes in animals. Siberian sturgeon fed a commercial trout diet containing estradiol also had hypertrophic and hyperlipidemic livers, features which disappeared when fish were fed a diet free of any steroids Pelissero et al., 1991a.. Kaushik et al. 1995. detected daidzein and genistein in the bile of trout fed soy flour rich diets and attributed the slightly poor growth rates to these substances. Plasma vitellogenin levels of the treated group in this study tended to be higher compared to the levels in the control group. Mambrini et al. 1999. postulates that the presence of isoflavones could only be considered as one of the reasons for reduced growth of trout fed a soy protein concentrate diet. Additional fish studies are required to evaluate the significance of observed effects of phytoestrogens Mambrini et al., 1999.. The presence of these substances, however, need to be kept in mind when fish diets are formulated Pelissero and Sumpter, 1992.
11. Alkaloids Alkaloids are secondary metabolites widely found in plants. With few exceptions, true alkaloids are basic, contain nitrogen in the heterocyclic ring, and are derived from amino acid precursors Petterson et al., 1991.. Alkaloid-containing grain legumes, such as lupins Lupinus albinus ., are otherwise ideally suited as feed ingredients in aquaculture because of their high digestible protein content 3050%.. The presence of quinolizadine alkaloids, which interfere with nerve functioning, makes them unsuitable for human consumption.
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The organoleptic properties of alkaloid-containing diets may lower the feed intake in rainbow trout de la Higuera et al., 1988.. According to Bangoula et al. 1993., rainbow trout fed a diet containing crude lupin seed meal showed lower feed efficiency. In more recent studies, rainbow trout and turbot were found to be tolerant to high inclusion levels of lupin seed meal in their feed, probably because extruded meal of a variety with low alkaloid content - 20 mgrkg. was used Burel et al., 1998, 2000a.. Breeding for low alkaloid varieties has been successful in the case of lupin and is the obvious solution to reduce the alkaloid content in alternative nutritional sources. Aqueous extraction also removes alkaloids from some materials. Bangoula et al. 1993. observed that extrusion at 1458C led to higher digestive utilisation, and higher growth performance in trout than the same lupin seed meal extruded at 1208C. Few studies are available on the effects of alkaloid-containing feeds in other species of fish. The mechanism of action of alkaloids in fish and their metabolic fate in the fish body are not properly understood. It is reasonable to assume that fish would be capable of tolerating lupin meal with a low alkaloid content at moderate levels of dietary inclusion.
12. Antigenic compounds A few protein components of some legume seeds and cereals elicit antigenic effects in animals; these compounds are capable of inducing intestinal mucosal lesions, abnormalities in the villi, specific and non-specific immune responses and abnormal movement of digesta through the gut DMello, 1991a.. Soybean protein contains compounds such as glycinin G. and beta conglycinin b C., which act as allergens to several animals. Rumsey et al. 1993. reported that high levels of immunologically active G and b C in different soy preparations seemed to negatively affect growth performance in rainbow trout. They assumed that the comparatively under-investigated effects of allergens may provide answers to why conventionally processed soybean, in which the protease inhibitors and lectins have been largely inactivated, results in poor growth of salmonid fish. Haemagglutination inhibition assays HIA. by the same authors showed that normal processing measures like toasting and de-fatting did not significantly reduce antigenicity levels in soybean meal. Krogdahl et al. 2000. observed enteritis-like changes in the distal intestine of Atlantic salmon Salmo salar L.. fed diets containing solvent-extracted soybean meal or an alcohol extract of soybean meal. The antigenic compounds present in feed may trigger a variety of non-specific and specific immune responses in the fish body and this might lead to a reduction in growth. Their presence in common plant-derived feed ingredients, however, remains a matter of controversy. Kaushik et al. 1995. failed to detect any antigenic proteins in the soy protein concentrate, nor was there any agglutinating activity against soybean protein in the sera of rainbow trout fed with diets containing soy protein concentrate. It may be safe to conclude that at those levels at which they are likely to be present in practical fish feeds, the allergen content does not cause any serious growth reduction in cultured fish species.
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13. Gossypols Gossypols are polyphenols, contained in the pigment glands of plants of the genus Gossypium and in certain other members of the order Malvales. Feeding diets containing gossypols cause negative effects such as growth depression and intestinal and other internal organ abnormalities Berardi and Goldblatt, 1980.. The formation of indigestible gossypolprotein complexes may produce deficiencies of some amino acids, such as methionine, which are essential for the normal fat metabolism Herman, 1970.. Commercially available cottonseed meal has gossypol levels ranging from - 0.01% in glandless cottonseed meals to an average of about 1.3% in glanded varieties, levels that may cause toxicity in fish. Raw cottonseed meal supplementation in the diet the diet contained 0.029% free gossypol. caused a reduction in growth and tissue pathology in rainbow trout Herman, 1970.. Necrotic changes in the liver cells, thickening of the glomerular basement membrane, and accumulation of ceroid pigment granules in the liver in this study were all attributed to the presence of gossypol. A dietary level of 0.1% gossypol resulted in quick development of severe focal fatty degeneration in the liver and extensive kidney damage in the same study. At the end of this study, an extremely unbalanced sex ratio 1 male:4 female. in fish fed a diet containing a moderate level 0.0531%. of gossypol was also observed. Gossypol is known to cause problems to the reproductive system in mammals by affecting the reproductive tissues directly or pituitary and gonadal hormone secretion Randel et al., 1992.. Cottonseed meal at levels above 8% in the diet resulted in alterations in spermatic activity, increase in abnormal spermatozoids, and abnormalities in the histology of the testes Salaro et al., 2000.. Yellow perch Perca flaescens. sperm cells were immobilised in vitro by a level of 200 m M gossypol Ciereszko and Dabrowski, 2000.. The growth rate of fingerling carp was depressed to half of that of the control on a 1% dietary inclusion of gossypolacetate Roehm et al., 1967.. A 2% gossypol level resulted in feed rejection in the same study. Significant amounts of gossypol became bound to liver, kidney and spleen tissue. This bound gossypol remained in the liver which is the main organ responsible for metabolising these compounds. even after fish were fed a gossypol-free control diet for 10 weeks. Tilapia O. aureus . growth was affected at a dietary free gossypol content of 0.012% Robinson et al., 1984.. Tilapia and catfish fed diets containing full-fat cottonseed meal had higher levels of palmitic acid and linoleic acid, and lower levels of oleic acid in their carcass. O. niloticus niloticus exhibited a poor growth response when fed cottonseed meal based diets, even when the crude protein level of these diets was higher than that of the fishmeal based control diet Ofojekwu and Ejike, 1984.. Lysine unavailability caused by gossypol cannot be the only reason for the negative effect of cottonseed meal, as lysine supplementation failed to improve the growth performance of tilapia O. niloticus . fed diets containing cottonseed meal El-Sayed, 1990.. It is, however, notable that the use of cottonseed meal was calculated to be more profitable even with lower growth rates in this study. It is not evident from these studies whether gossypol toxicity was the only reason for reduced fish growth even though toxicity of this compound to fish seems to be high even at low levels ; 0.05%.. High levels of inclusion of cottonseed meal resulted in a growth performance comparable to a control fed a
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fishmeal diet in channel catfish Reigh, 1999. and tilapia Jackson et al., 1982; Sintayehu et al., 1996; Mbahinzireki et al., 2000.. Different treatments undergone by the cottonseed meal used in the different trials may have been the reason for the erratic growth performance of the fish in different studies. Pre-pressed and solvent extracted glandless cottonseed meal should be able to support good growth even at high inclusion levels in the range of 50%. in most cultured fish species, if supplemented with the deficient amino acids such as cystine, lysine and methionine.
14. Miscellaneous antinutrient substances Cyanogens are compounds found in high concentrations in a number of pulses, root crops, such as cassava, and some oil seeds, such as linseed, which have been tried as fish feed ingredients. Cyanogens, when hydrolysed, produce toxic products such as hydrogen cyanide and probably other carbonyl compounds that suppress natural respiration and cause cardiac arrest Davies, 1991.. The enzyme required for this conversion is usually found in extracellular spaces in the plant tissues. Thiocyanate, a detoxication product of cyanide, acts as an antithyroid agent. Fish fed cyanogen-containing feed materials, such as linseed and cassava, have generally shown reduced growth when compared to the respective controls Hossain and Jauncey, 1989b; Ufodike and Matty, 1983.. However, dietary cyanide did not depress growth in Nile tilapia, as fish fed diets containing soaked sun-dried cassava leaf meal 9.9 ppm total cyanide. and sun-dried cassava meal 71.1 ppm. showed similar growth at similar levels of inclusion Ng and Wee, 1989.. More studies are required to determine the level of tolerance of different species of cultured fish to this substance and whether there are any long-term effects at low ingestion levels. Mimosine is an unusual amino acid present in Leucaena leucocephala and comprises about 35% of the dry weight of total protein Liener, 1980.. It has extensive deleterious properties in animals including disruption of reproductive processes and teratogenic effects DMello, 1991b.. Dietary Leuceana leaf meal does not seem to be well tolerated by fish. Studies in tilapia indicate that Leucaena leaf proteins are poorly digested and hence it is arguable whether enough mimosine enters the body to cause its physiological effects. Difference in the growth response of male and female tilapia has been observed when fed a diet containing leucaena meal; males seemed to tolerate it better than females Santiago et al., 1988.. Production of fry was significantly reduced beyond the 40% inclusion level in this study. It would be interesting to see if these effects could be reproduced using pure mimosine, and if so, what the mechanism of its action is. Cyclopropenoid fatty acids, like sterculic and malvalic acid present in cottonseed oil and meal, are known to cause abnormalities in the reproductive processes and alterations in the lipid metabolism in mammals. These substances, together with other toxins, such as aflatoxins, are suspected to be carcinogenic to fish. In rainbow trout, they have been shown to interfere with the long chain fatty acid metabolism and with stearic and palmitic dehydrogenation. Negative effects in rainbow trout recorded at 100 ppm methyl sterculate in the diet did not increase when its concentration was increased to 200 ppm
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Roehm et al., 1970.. Negative effects on growth were strongest initially, later the fish seemed to adapt, but the final weight after 87 days was still lower than the control. Tilapia fed a diet containing full-fat cottonseed meal tended to show lower growth compared to those fed the diet containing the defatted flour, which indicated adverse effects of cyclopropenoid fatty acid Robinson et al., 1984.. Canaanine is a thermoresistant-free amino acid present in many legume species DMello, 1991b.. It is an antagonist of arginine. Jack bean Canaalia ensiformis. meal treated for removal of canavanine was as efficient a feed ingredient for tilapia as fishmeal Martinez-Palacios et al., 1988.. Tilapia fed diets containing toxic jack seed meal exhibited depressed appetite, lethargic movements and subsequent high mortality. There is little information on effects in other fish. Antiitamin factors. Many of the alternative protein sources tested in fish like soybeans, alfalfa and oilseed meals are known to contain a variety of antivitamin factors Liener, 1980. that might affect their efficiency as nutrient sources. Antivitamins are heat labile so these substances should not be of much physiological significance in fish, provided the plant-derived resources being incorporated in diets are properly heat-treated. Most commercially available seed meals are heat-treated to inactivate trypsin inhibitors and lectins, and hence these are also free from antivitamins. Phorbol esters, toxic substances found in J. curcas physic nut. meal, act as a co-carcinogen and have a wide range of adverse biochemical and cellular effects in animals. Common carp was found to be extremely sensitive to these compounds. At a level of 31 ppm in feed, they induced depression in feed intake, growth and production of faecal mucus Becker and Makkar, 1998.. Use of non-toxic varieties of J. curcas in which phorbol esters are absent is an obvious solution. Oxycarotenoids such as zeaxanthin and lutein present in corn gluten meal reduce the market acceptance of white fleshed fish in certain regions by giving the fillet a yellow pigmentation Skonberg et al., 1998.. Park et al. 1997. showed that bleaching with soy flour was a practical method of removing carotenoids from corn gluten meal.
15. Conclusions The fish feeding studies reviewed in our paper used plant-derived materials that contain more than one antinutritional substance, and because of this it is difficult to pinpoint any one factor as the culprit for the adverse effects that these feed ingredients produced when fed to fish. Understandably, there is little agreement among the results of different studies as to the specific effects of individual antinutrients. Most of the antinutrients, at levels present as a result of incorporating alternate protein sources in fish feeds, do not lead to mortality, but could produce adverse effects and decrease productivity. However, it is difficult to make firm conclusions regarding specific plant secondary metabolites causing deleterious effects and their threshold levels in fish diets. Tentatively, protease inhibitors, phytates, and antigenic compounds, at levels likely to be present in fish diets containing commercially available plant-derived protein sources, are unlikely to affect fish growth performance. In contrast, glucosinolates, saponins, tannins, phorbol esters, soluble non-starch polysaccharides and gossypol seem to be more
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important in practical aquaculture nutrition. Information available on substances like lectins, phytoestrogens and alkaloids is too scarce to arrive at any conclusion. More insights into the nutritional, physiological and ecological effects of these substances on fish need to be accumulated. The common processing techniques, like dry and especially wet heating, extracting with water, and addition of feed supplements have been widely and successfully used to reduce the concentration of antinutrients in plant feeds. Caution needs to be exercised when resorting to treatment methods because they sometimes have unintended adverse effects on the nutritional quality of the feed material, e.g., heat treatment reportedly alters the chemical nature and decreases the nutritional quality of proteins and carbohydrates van der Poel, 1989.. The different tolerance limits of individual fish species to the presence of antinutrients also need to be considered before deciding on treatment procedures to reduce their levels. Tilapia species, for example, seem to be more tolerant than carp to the increased presence of antinutrients in general. Feeding experiments using purified individual antinutrients are needed to determine the threshold limits that will not affect the productivity of common culture fish. Another important factor to be considered is the interactions between various antinutritional factors in a particular substance as these interactions in some instances lead to a decrease in the toxic effect of the interacting antinutrients. For example, saponintannin Freeland et al., 1985., tanninlectin Fish and Thompson, 1991. and tannincyanogen Goldstein and Spencer, 1985. interactions have all been shown to result in a reduction in the individual toxicity of the antinutrients. A more detailed study of such interactions would be particularly useful, as many of the plant-derived materials that have the potential to be used as fish feed ingredients contain more than one of the antinutrients. Studies are also needed to expose the effects of mixtures of antinutrients in proportions similar to those in plant-derived nutritional sources.
Acknowledgements G. Francis is thankful to the Katholischer Akademischer Auslander Dienst, Bonn, for providing a stipend for doing PhD in Germany.
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Antinutritional Factors Present in Plant-Derived Alternate Fish Feed Ingredients and Their Effects in Fish

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Aquaculture 199 2001. 197227 www.elsevier.

G. Francis et al. r Aquaculture 199 (2001) 197227

G. Francis et al. r Aquaculture 199 (2001) 197227

Commercial soybean meal

Thermally and hydrothermally treated full-fat soybean meal

Commercial hexane extracted soybean meal

Tilapia O. niloticus = O. aureus .

55 R. or 56 to 58 RqB. or 58 B. or 52 D. 13, 25 and 50

Full-fat soybean meal SBM. or soy protein concentrate SPC.

Dabrowski and Kozack, 1979 Abel et al., 1984

Shiau et al., 1987

Wee and Shu, 1989

Dabrowski et al., 1989

van den Ingh et al., 1991

Solvent extracted soybean meal

Fingerling red drum

71, 53, 35.5, 18

Reigh and Ellis, 1992

Rumsey et al., 1993

G. Francis et al. r Aquaculture 199 (2001) 197227

Oliva-Teles et al., 1994

Rainbow trout Hybrid striped bass

Methionine supplemented soybean meal

Sanz et al., 1994 Gallagher, 1994

(continued on next page)

Soy protein concentrate SPC. or commercial soy flour SF.

10, 20, 30 or 40 10, 20 or 30 each 30, 50 or 70

Colzapro coextruded rapeseed and peas.

Kaushik et al., 1995

G. Francis et al. r Aquaculture 199 (2001) 197227

Robaina et al., 1995

Storebakken et al., 1998 Vielma et al., 2000

de la Higuera et al., 1988 Robaina et al., 1995 Burel et al., 1998

Gomes et al., 1993

Undephytinized rapeseed protein concentrate Dephytinized rapeseed protein concentrate

18 and 33 26 to 40 of casein was replaced here

Teskeredzic et al., 1995 Teskeredzic et al., 1995

Tilapia Nile tilapia

Ofojekwu and Ejike, 1984 El-Sayed, 1990

Sunflower meal Cassava or rice meal

Rainbow trout Carp

Sanz et al., 1994 Ufodike and Matty, 1983 Fagbenro, 1999

Autoclaved or roasted winged bean

(continued on next page)

Soaked, sundried or commercial leucaena leaf meal Leucaena leaf meal

Soaked sun dried or sun dried cassava leaf meal

Ng and Wee, 1989

Olvera-Novoa et al., 1990

Tilapia O. aureus L.. Tilapia

6 to 34 DA. 40 or 6 to 38 SB. 13 to 47 A. or 33 OT. 39

Yousif et al., 1994 Martinez-Palacios et al., 1988

Olvera-Novoa et al., 1988

G. Francis et al. r Aquaculture 199 (2001) 197227

Hossain and Jauncey, 1989a Hossain and Jauncey, 1989b

30 or 61 MC., 40 30 or 59 or 23LM., 47 or 70 SM. 30 LM. or 40 27 SM.

Hossain and Jauncey, 1990

Commercial soybean meal, Tilapia cottonseed meal or sunflower seed meal

Sintayehu et al., 1996

G. Francis et al. r Aquaculture 199 (2001) 197227

Gossypol acetate Sterculic acid

Fingerling tilapia Rainbow trout

0.1 or 0.2 0.01 or 0.02

Robinson et al., 1984 Roehm et al., 1970

Phytic acid Sodium phytate Sodium phytate