Download Growth and intestinal morphology in cobia (Rachycentron canadum

Aquaculture Nutrition 2008 14; 174–180
doi: 10.1111/j.1365-2095.2007.00517.x
..............................................................................................
Growth and intestinal morphology in cobia (Rachycentron
canadum) fed extruded diets with two types of soybean meal
partly replacing fish meal
O.H. ROMARHEIM1,2, C. ZHANG2, M. PENN1,3, Y.-J. LIU4, L.-X. TIAN4, A. SKREDE1,2,
Å. KROGDAHL1,3 & T. STOREBAKKEN1,2
1
Aquaculture Protein Centre, CoE, Norway; 2 Department of Animal and Aquacultural Sciences, Norwegian University of Life
Sciences, Ås, Norway; 3 Department of Basic Sciences and Aquatic Medicine, Norwegian School of Veterinary Science, Oslo,
Norway; 4 School of Life Sciences, Institute of Aquatic Economic Animals, Sun Yat-Sen University, Guanzhou, Guangdong,
China
Abstract
Juvenile cobias, Rachycentron canadum, were fed extruded
diets containing toasted defatted soybean meal (SBM) or
untoasted defatted SBM [white flakes (WF)] to study
growth and feed conversion, and to study if SBM induces
morphological changes in the gastrointestinal (GI) tract.
Three diets were produced: a fish meal-based control diet
(FM diet) with 558 g FM kg)1, and two diets with 335 g
FM and either 285 g SBM kg)1 (SBM diet) or 285 g WF
kg)1 (WF diet). The diets were extruded at approximately
120C with 280 g kg)1 moisture. Triplicate groups of
cobias (mean weight: 25.9 g) were fed the diets during
6 weeks. Feed intake of the FM and SBM diets were not
significantly different, whereas the cumulative feed intake
of cobias fed the WF diet was lower (P < 0.05) than
that of cobias fed the FM and SBM diets after the first 21day period. Specific growth rate and feed conversion ratio
were not significantly different between cobias fed the FM
and SBM diets, but significantly poorer results were obtained in cobias fed the WF diet. No morphological differences in the GI tract could be attributed to the diets,
and cobias fed soy did not develop enteritis in the distal
intestine.
KEY WORDS: cobia Rachycentron canadum, distal intestine,
growth, histology, soybean meal, white flakes
Received 15 September 2006, accepted 10 April 2007
Correspondence: Dr Trond Storebakken, Aquaculture Protein Centre, PO
Box 5003, N-1432 Ås, Norway. E-mail: [email protected]
Introduction
The cobia, Rachycentron canadum, is a warm-water pelagic
fish widely distributed in tropical/subtropical waters, except
in the central and eastern Pacific Ocean. It is recognized for
its fast growth and good meat quality, and has been intensively farmed since the 1990s (Liao et al. 2004). World fish
meal (FM) production has been relatively stable during the
past 20 years, except in El Niño years, whereas fish feed
production has grown rapidly (Tacon 2004; Shepherd et al.
2005). Therefore, access to a stable supply of suitable, lowpriced dietary protein sources is a major challenge for further
expansion of intensive fish farming. Commercial feeds for
growing cobias contain approximately 450 g kg)1 protein
(Liao et al. 2004) and recent studies have concluded that
approximately 400 g kg)1 of the FM can be replaced by
soybean meal (SBM) in diets for juvenile cobias without a
reduction in growth (Chou et al. 2004; Zhou et al. 2005).
Furthermore, Zhou et al. (2004) found that the apparent
digestibility of protein from SBM was above 90% in juvenile
cobias determined with feces collected in settling columns,
which also reflected high apparent digestibility values of the
individual amino acids. However, neither Chou et al. (2004)
nor Zhou et al. (2004, 2005) have included measurements of
antinutritional factors present in the soybean-containing
diets, which may cause problems for carnivorous fishes (reviewed by Storebakken et al. 2000; Francis et al. 2001).
Toasting or extrusion may inactivate most of the heat labile
antinutrients in soybeans (Björck & Asp 1983; Qin et al.
1998; Clarke & Wiseman 1999; Romarheim et al. 2005).
Even small amounts of protease inhibitors have been shown
..............................................................................................
174
2007 Blackwell Publishing Ltd
Cobia fed two types of soybean meal
to influence protein digestibility and intestinal proteolytic
activities in rainbow trout, Oncorhynchus mykiss (Krogdahl
et al. 1994), and work should therefore be carried out to
establish the acceptance level of protease inhibitors in the
cobia. In salmonid fish, another major concern with soybean
products are the morphological alterations found in the distal
intestine (DI) (van den Ingh et al. 1991; Rumsey et al. 1994;
Baeverfjord & Krogdahl 1996). The morphological changes
in salmonids are probably caused by alcohol-soluble components (van den Ingh et al. 1996; Bureau et al. 1998) that
have yet to be conclusively identified.
The main objectives of the present study were to: (1)
evaluate performance of juvenile cobias fed extruded high-fat
diets with inclusion of either SBM or white flakes (WF), and
(2) find out if inclusion of soybean products induces morphological changes in the intestine of the cobia.
Materials and methods
Diets
The protein feedstuffs utilized in this study were FM (Norse
LT-94; Norsildmel, Bergen, Norway), conventional defatted and toasted SBM (Deno-Soy F; Denofa, Fredrikstad,
Norway) and untoasted defatted SBM (WF, Prosam F; The
Solae Company LLC, Esteio, Brazil). The control diet (FM
diet) contained high-quality FM as the only protein feedstuff.
In the two other diets, 400 g kg)1 of the total amino acids
from FM were replaced by either SBM (SBM diet) or WF
(WF diet) (Table 1). Substitution was made on the basis of
the analysed total amino acid contents of the FM, SBM and
Table 1 Formulation and analysed chemical composition of diets
FM diet SBM diet WF diet
)1
Main ingredients, g kg
Fish meal
Soybean meal
White flakes
Wheat
Fish oil
Vitamin and mineral mixture1
Dry matter (DM), g kg)1
Chemical composition, g kg)1 DM
Crude protein
Crude fat
Starch
Ash
Gross energy, MJ kg)1 DM
Trypsin inhibitor activity2, mg g)1 DM
Phytic acid, mg g)1 DM
1
2
558
–
–
237
200
4.97
917
335
285
–
176
200
4.97
922
335
–
285
176
200
4.97
916
442
293
146
94
24.3
0.3
1.5
446
279
109
80
23.2
0.7
3.2
433
279
102
79
22.7
2.5
3.8
WF (presented by Romarheim et al. 2005). Fish oil (Silfas,
Karmsund, Norway) was added in the same amount to all
diets, whereas the inclusion of wheat was reduced in the SBM
and WF diets to compensate for the lower content of total
amino acids in SBM and WF compared with FM. The
chemical composition (g kg)1 DM) of the diets were: 433–
446 g kg)1 crude protein, 279–293 g kg)1 crude fat, and 146,
109 and 102 g kg)1 starch in the FM, SBM and WF diets,
respectively. The diets were extruded at the Center for Feed
Technology, Ås, Norway, during December 2003. The diets
were produced at approximately 120C with 280 g kg)1
moisture, dried, coated with fish oil and stored cold until
feeding (see Romarheim et al. 2005 for details).
Fish, rearing conditions and feeding
Juvenile cobias, R. canadum, were supplied by a local fry
dealer in Zhanjiang, Guangdong, China. The cobias were
cultured in floating sea-cages, then moved to circular tanks
where they were fed a commercial extruded feed (Evergreen
Feed Company, Zhanjiang, Guangdong, China) during the
adaptive period prior to the experiment. Two weeks before
the start of the experiment, the fish were transferred to 1-m3
circular tanks on land. They were further allocated into
groups of 24 fish (average weight: 25.9 g) per tank (mean
total weight per tank ± SD, 622.0 ± 34 g) 6 days before the
start of the experiment. The feeding trial started on 16 June
2004, and each diet was fed to triplicate groups of fish for
42 days. The tanks were supplied with flow-through seawater
(10 L min)1) at 28–30C and 32.5 g L)1 salinity. Oxygen
saturation was kept at approximately 7 mg L)1 in the outlet
water.
A 5-day pre-trial revealed that cobias (average weight:
13.7 g) fed twice per day had nearly twice the weight increase
of fish fed only once per day. Thus the fish were fed by hand
two meals per day, starting at 09:00 and 16:00, which also
was consistent with previous feeding experiments by Chou
et al. (2001, 2004). Each meal consisted of two to three
feeding rounds to satiety.
Weighing, sampling and chemical analyses
For details, see Romarheim et al. (2006).
Inhibited bovine trypsin.
..............................................................................................
2007 Blackwell Publishing Ltd Aquaculture Nutrition 14; 174–180
The fish were weighed at the start of the experiment, at day
21 and at the end of the experiment (day 42). One tank with
cobias fed the WF diet and two tanks with cobias fed
the SBM diet were affected by insufficient water supply the
night before completion of the experiment. All fish in the
affected WF diet tank died, whereas eight and 22 fish died
in the SBM diet tanks. The fish that died were weighted,
175
176
O. H. Romarheim et al.
and those that survived were kept until sampling at the
termination of the experiment the day thereafter. All fish
were anaesthetized with 60 mg MS 222 L)1 prior to
weighing. Random samples of the diets were collected and
analysed.
At the end of the experiment, fish from each tank were
taken and samples from the gastrointestinal (GI) tract were
taken for histological evaluation. The sample numbers for
histology were: FM, n = 9; SBM, n = 8 and WF, n = 6 as
the third replicate SBM tank only had two live fish left for
sampling and the third replicate WF tank had none. The fish
were opened and a 5 · 5 mm tissue sample was taken from
the following GI sections (Fig. 1): stomach (ST), central part
of the pyloric caecum (PC), proximal mid-intestine (MI1, 1=3
the distance from the pyloric caeca to the intestinal constriction), mid-intestine (MI2, 2=3 the distance between the
pyloric caeca and the intestinal constriction), DI (from the
constriction to the anus). Samples were fixed in buffered
formalin. The tissues were subsequently dehydrated in ethanol, equilibrated in xylene and embedded in paraffin
according to standard histological techniques (National
Veterinary Institute of Norway, Oslo, Norway). Sections of
approximately 5 lm were cut and stained with haematoxylin
and eosin (H&E) and examined by light microscopy. The
intestinal morphology was evaluated according to criteria
described by Baeverfjord & Krogdahl (1996) for SBMinduced enteritis in Atlantic salmon, Salmo salar. The criteria
included (1) widening and shortening of the intestinal folds;
(2) loss of the supranuclear vacuolization in the absorptive
cells (enterocytes) in the intestinal epithelium; (3) widening of
the central lamina propria within the intestinal folds, with
increased amounts of connective tissue and (4) infiltration of
a mixed leucocyte population in the lamina propria and
submucosa.
The diets were analysed for dry matter, crude protein
(Kjeldahl N · 6.25) and ash according to the methods of the
AOAC (1990), crude fat after hydrolysis with petroleum
Figure 1 Illustration of sites of tissue sampling for histological
analysis. ST, stomach; PC, pyloric ceca; MI1, proximal mid-intestine;
MI2, distal mid-intestine; DI, distal intestine.
ether on an Accelerated Solvent Extractor (ASE200) from
Dionex (Sunnyvale, CA, USA), starch (Total Starch Assay
Kit [AA/AMG]; Megazyme International Ireland Ltd,
Wicklow, Ireland) as total glucose after hydrolysis with
glucosidase, and gross energy (Parr 1281; Parr Instruments
Company, Moline, IL, USA). The trypsin inhibitor activity
was analysed according to Hamerstrand et al. (1981), and
phytic acid was determined by HPLC according to the
method of Carlsson et al. (2001).
Calculations and statistical analyses
Feed intake was estimated by subtracting feed collected at
the outlet water from the amount of feed fed into each
tank. Feed waste was calculated by counting the number of
uneaten pellets multiplied by the average pellet weight of
the diet. Specific growth rate (SGR) was calculated as
SGR ¼ 100 ðln BW1 ln BW0 Þ d 1
where BW0 and BW1 represent the initial and final body
weights, respectively, and d is the days of feeding. Feed
conversion ratio (FCR) was calculated as
FCR ¼ DMfeed ðBW1 BW0 Þ1
where DMfeed is the consumption of dry matter from the
feed.
Statistical analyses were carried out using one-way analysis
of variance by the general linear model procedure in SAS
(SAS 1988). The results for cumulative feed intake, growth
and feed conversion are presented as least-square mean
(lsmean) ± pooled standard error of the means (SEM), and
significant (P < 0.05) differences among means were ranked
by DuncanÕs multiple range method.
Results
Feed intake and growth
Fish fed the FM and SBM diets had similar cumulative feed
intake, growth and feed conversion throughout the experiment, whereas cumulative feed intake, growth and feed
conversion of fish fed the WF diet were lower in both periods
(Table 2). Cobias fed the WF diet were also observed to
frequently reject pellets after tasting. Fish fed the FM and
SBM diet increased initial weight by 365 and 346%, respectively, and fish fed the WF diet increased their initial weight
by 201% during the whole experimental period. The SGRs
in fish fed the FM and SBM diets in the second period
were roughly half those of the first period, whereas in fish fed
..............................................................................................
2007 Blackwell Publishing Ltd Aquaculture Nutrition 14; 174–180
Cobia fed two types of soybean meal
Table 2 Least-square means for cumulative feed intake, growth and feed conversion in juvenile cobia, Rachycentron
canadum
Diet
FM diet
Cumulative feed intake, g per tank
0–21 days
1156b
22–42 days
1476b
0–42 days
2632b
Mean weight increase, g per fish
0–21 days
47.1b
22–42 days
48.8b
0–42 days
95.9b
Specific growth rate
0–21 days
4.9b
22–42 days
2.4b
0–42 days
3.6b
Feed conversion ratio, g DM intake
0–21 days
0.9a
22–42 days
1.2a
SBM diet
WF diet
Pooled SEM
P-value
1226b
1463b
2690b
975a
978a
1953a
33
87
93
0.005
0.011
0.002
49.4b
43.3b
92.6b
32.0a
17.4a
49.4a
5.0b
4.0a
2.1b
1.3a
b
3.6
2.6a
(g body weight gain))1
1.0a
1.2b
1.4a
2.3b
1.6
4.7
5.7
0.001
0.007
0.002
0.17
0.17
0.14
0.009
0.009
0.004
0.04
0.10
0.005
0.001
Different superscript letters within a line indicate significant (P < 0.05) differences among
dietary treatments.
the WF diet it was reduced to 1=3. FCRs increased by 32 and
43% in the second period in fish fed the FM and SBM diets,
respectively, whereas it increased by 93% in the second
period for fish fed the WF diet. One cobia fed the WF diet
died during the first period, and two cobias fed the SBM diet
died during the second period in addition to those that died
in connection with the incident described previously.
Intestinal histology
H&E stained tissue sections from the GI tract were evaluated
blindly, and morphological changes were noted. No changes
in the GI tissues resembling those described for SBM-induced enteritis in the posterior intestine of Atlantic salmon
were observed (Fig. 2). However, incidental findings that
could not be related to diets were noted. Areas of focal
leucocyte infiltration were noted in the submucosa/propria of
the intestinal tissues, but did not appear similar to the diffuse
infiltration of the submucosa and lamina propria seen in
soybean enteritis. The width of the lamina propria of intestinal mucosal folds exhibited slight variation, but the increases in width did not appear to be a result of cellular
infiltration or hyperplasia, but rather appeared non-cellular.
The blood vessels within the lamina propria of intestinal
mucosal folds also appeared more prominent than seen in
salmonids. Vacuolization of intestinal epithelial cells,
ranging from absent to highly vacuolated, varied between
individuals.
Discussion
The lack of significant differences in growth and FCR
when substituting 400 g kg)1 of the amino acids from FM by
..............................................................................................
2007 Blackwell Publishing Ltd Aquaculture Nutrition 14; 174–180
conventional SBM is consistent with previous findings with
cobias by Chou et al. (2004) and Zhou et al. (2005). The
lower feed intake of cobias fed the WF diet compared with
cobias fed the FM and SBM diets was obviously the main
reason for the poorer growth, and the low feed intake
probably had a negative effect on the FCR as well. SGRs
vary widely among experiments with cobia depending on
factors such as size, rearing conditions and genetic variation.
For example, cobias growing from approximately 6 to 126 g
have obtained SGRs from 4.2 (Resley et al. 2006) to 6.6–6.7
(Wang et al. 2005). Cobias growing in the interval from
approximately 12 to 86 g have obtained SGRs from 3.6
(Zhou et al. 2006) to 4.2 (Lunger et al. 2006), whereas others
have obtained maximum SGRs of 2.4–2.6 (Chou et al. 2001)
and 2.7 (Chou et al. 2004) for cobias growing from approximately 32 to 140 g. The FCRs for cobias fed the FM and
SBM diets during the first period and the overall period were
in line with several previous studies (Wang et al. 2005; Resley
et al. 2006; Zhou et al. 2006), and slightly higher than
obtained by Chou et al. (2001, 2004). Comparison of growth
results with previous experiments with cobias is complicated
as there often are considerable dissimilarities regarding
genetic stock, rearing facilities, stocking density and feed
composition. Growth and FCR in the present study were
acceptable through the first 21 days, but rather poor during
the last period of 21 days, in particular in cobias fed the WF
diet. Higher age and larger size may explain some of the poor
progress during the second period, but probably not all.
The dietary crude protein level of 433–446 g kg)1 of DM
was similar to the protein level regarded as optimal for
maximum weight gain in juvenile cobias (Chou et al. 2001)
and the level commonly used in commercial feeds for cobias
in Taiwan (Liao et al. 2004). The fat level of 279–293 g kg)1
177
178
O. H. Romarheim et al.
(a)
(b)
Figure 2 Distal intestinal histology (H&E) of cobia, Rachycentron
canadum, fed (a) FM and (b) SBM diets (·40). C, circular muscular
layer; S, submucosa; LP, lamina propria; MF, mucosal folds.
of DM was close to twice the usual level in commercial cobia
feeds in Taiwan (Liao et al. 2004). Chou et al. (2001) did not
find any significant difference in growth, FCR or protein
conversion ratio of juvenile cobia fed 54, 84, 123 or
189 g kg)1 crude lipids (on DM basis). However, Wang et al.
(2005) reported significantly poorer feed intake and growth,
but better FCR and protein efficiency ratio in juvenile cobia
fed a diet with 261 g kg)1 crude lipids compared with 51 or
170 g kg)1 crude lipids (on DM basis). The high level of fat
in our study may therefore have lead to a suboptimal
digestible protein to digestible energy ratio (DP/DE), and
thereby contributed to rather low feed intake and growth.
Nevertheless, the crude protein and gross energy levels were
relatively similar among the diets, and the internal ranking of
the diets were therefore probably not affected by dietary fat
level or DP/DE.
Substitution of FM by SBM will decrease the dietary
methionine level as well as increase the level of phytic acid,
and may thereby impair growth and feed utilization (reviewed by Storebakken et al. 2000). Information about the
requirement of essential amino acids for cobias is limited,
but some studies have reported the requirement of methionine. Chou et al. (2004), using broken line analysis, estimated the dietary requirement of sulphur-containing amino
acids (methionine + cysteine) to be 2.66 g 16 g)1 N for
juvenile cobias. A more recent study by Zhou et al. (2006)
estimated the optimum methionine level for maximum
growth of juvenile cobias to be as high as 11.9 g kg)1 dry
diet in the presence of 6.7 g kg)1 cysteine, which is equal to
approximately 4.2 g 16 g)1 N sulphur-containing amino
acids. The levels of sulphur-containing amino acids in our
study where 3.31, 3.07 and 3.19 g 16 g)1 N for the FM,
SBM and WF diets, respectively, and may therefore be
limiting for maximum growth according to Zhou et al.
(2006).
A recent study by Denstadli et al. (2006) revealed that
inclusion of 4.7 g kg)1 dietary phytic acid had no direct effects on feed intake, growth and feed conversion, or on the
digestibility of the main nutrients in juvenile Atlantic salmon
during an 80-day feeding trial. Both the SBM diet and the
WF diet had phytic acid levels well below 4.7 g kg)1, and
unless cobia is more sensitive than salmonids, growth performance or feed conversion in our experiment should not be
influenced by phytic acid. Moreover, the level of phytic acid
was similar in the SBM and WF diets.
The poorer feed intake on the WF diet was most likely the
result of low palatability or a negative physiological reaction
as cobias fed the WF diet were observed to frequently reject
caught pellets. The main difference between SBM and WF
was that SBM, as opposed to WF, had been heat-treated
(toasted) prior to extrusion. Although the heat treatment
applied during the extrusion reduced the trypsin inhibitor
activity in the SBM and WF diets to 0.7 and 2.5 mg g)1 DM,
respectively, the WF diet contained 3.6 times as high trypsin
..............................................................................................
2007 Blackwell Publishing Ltd Aquaculture Nutrition 14; 174–180
Cobia fed two types of soybean meal
inhibitor activity as the SBM diet. Most cultured fish
species have a tolerance limit for trypsin inhibitor
activity below 5 mg g)1 (reviewed by Francis et al. 2001).
However, no studies have established the tolerance for
trypsin inhibitor activity in the cobia, and the WF diet might
exceed the tolerance for dietary trypsin inhibitor activity in
this species.
The results of the present study suggest that defatted
SBM can be included in the diet with up to 285 g kg)1
without inducing morphological changes in the GI tract of
juvenile cobias. This conclusion is consistent with studies of
Atlantic halibut, Hippoglossus hippoglossus, fed 360 g kg)1
full-fat SBM (Grisdale-Helland et al. 2002), mangrove red
snapper, Lutjanus argentimaculatus, fed 480 g kg)1 defatted
SBM (Catacutan & Pagador 2004), and Atlantic cod, Gadus
morhua, fed 250 g kg)1 defatted SBM (Refstie et al. 2006).
In contrast, SBM gave mild morphological changes in the
anterior intestine of Asian seabass, Lates calcarifer, fed
210–285 g kg)1 SBM (Boonyaratpalin et al. 1998) and mild
loss of supernuclear vacuolization in the DI of channel
catfish, Ictalurus punctatus, fed 450 g kg)1 defatted SBM
(Evans et al. 2005). Salmonids are more sensitive and
Atlantic salmon (S. salar) developed moderate changes in
the DI with 76 g kg)1 defatted SBM and severe changes
with 117 g kg)1 defatted SBM (Krogdahl et al. 2003),
classified after Baeverfjord & Krogdahl (1996) as noninfectious subacute enteritis. Thus, the sensitivity to dietary
SBM seems to be subject to interspecies variation. The
sensitivity of cobia with regard to soy antigens remains to
be elucidated.
In conclusion, toasted SBM can be included in extruded
diets for cobia with up to 285 g kg)1 diet without affecting
feed intake, growth and feed conversion negatively, whereas
WF promoted poorer results provided the present extrusion
temperature. In contrast to salmonids, cobia seems not to
develop SBM-induced enteritis in the DI.
Acknowledgements
The authors want to thank Guadong Evergreen Company
for providing the experimental facilities, Solae (Esteio-RS,
Brazil) for kindly donating the white flakes, and Mr Konrad
Münz from Bühler (Uzwil, Switzerland) for expertise and
help during the feed production.
References
AOAC (1990) Official Methods of Analysis, 15th edn. AOAC Inc.,
Washington, DC, USA.
..............................................................................................
2007 Blackwell Publishing Ltd Aquaculture Nutrition 14; 174–180
Baeverfjord, G. & Krogdahl, Å. (1996) Development and regression
of soybean meal induced enteritis in Atlantic salmon, Salmo salar
L., distal intestine: a comparison with the intestine of fastened fish.
J. Fish Dis., 19, 375–387.
Björck, I. & Asp, N.-G. (1983) The effects of extrusion cooking on
nutritional value – a literature review. J. Food Eng., 2, 281–308.
Boonyaratpalin, M., Suraneiranat, P. & Tunpibal, T. (1998)
Replacement of fish meal with various types of soybean products
in diets for the Asian Seabass, Lates calcarifer. Aquaculture, 161,
67–78.
Bureau, D.P., Harris, A.M. & Cho, C.Y. (1998) The effects of
purified alcohol extacts from soy products on feed intake and
growth of chinook salmon (Oncorhynchus tshawytscha) and rainbow trout (Oncorhynchus mykiss). Aquaculture, 161, 27–43.
Carlsson, N.-G., Bergman, E.-L., Skoglund, E., Hasselblad, K. &
Sandberg, A.-S. (2001) Rapid analysis of inositol phosphates.
J. Agric. Food Chem., 49, 1695–1701.
Catacutan, M.R. & Pagador, G.E. (2004) Partial replacement of
fishmeal by defatted soybean meal in formulated diets for the
mangrove red snapper, Lutjanus argentimaculatus (Forsskal 1775).
Aquacult. Res., 35, 299–306.
Chou, R.L., Su, M.S. & Chen, H.Y. (2001) Optimal dietary
protein and lipid levels for juvenile cobia (Rachycentron canadum).
Aquaculture, 193, 81–89.
Chou, R.L., Her, B.Y., Su, M.S., Hwang, G., Wu, Y.H. & Chen,
H.Y. (2004) Substituting fish meal with soybean meal in diets of
juvenile cobia Rachycentron canadum. Aquaculture, 229, 325–333.
Clarke, E. & Wiseman, J. (1999) Extrusion temperature impairs
trypsin inhibitor activity in soybean meal. Feed Tech., 3, 29–31.
Denstadli, V., Storebakken, T., Krogdahl, Å., Sahlstrøm, S. &
Skrede, A. (2006) Feed intake, growth, feed conversion, digestibility, enzyme activities and intestinal structure in Atlantic salmon
(Salmo salar L.) fed graded levels of phytic acid. Aquaculture, 256,
365–376.
Evans, J.J., Pasnik, D.J., Peres, H., Lim, C. & Klesius, P.H. (2005)
No apparent differences in intestinal histology of channel catfish
(Ictalurus punctatus) fed heat-treated and non-heat-treated raw
soybean meal. Aquacult. Nutr., 11, 123–129.
Francis, G., Makkar, H.P.S. & Becker, K. (2001) Antinutritional
factors present in plant-derived alternate fish feed ingredients and
their effects in fish. Aquaculture, 199, 197–227.
Grisdale-Helland, B., Helland, S.J., Baeverfjord, G. & Berge, G.M.
(2002) Full-fat soybean meal in diets for Atlantic halibut: growth,
metabolism and intestinal histology. Aquacult. Nutr., 8, 265–270.
Hamerstrand, G.E., Black, L.T. & Glover, J.D. (1981) Trypsin
inhibitors in soy products: modification of the standard analytical
procedure. Cer. Chem., 58, 42–45.
van den Ingh, T.S.G.A.M., Krogdahl, Å., Olli, J.J., Hendriks,
H.G.C.J. & Koninkx, J.G.J.F. (1991) Effects of soybean-containing diets on the proximal and distal intestine in Atlantic salmon
(Salmo salar): a morphological study. Aquaculture, 94, 297–305.
van den Ingh, T.S.G.A.M., Olli, J.J. & Krogdahl, Å. (1996) Alcoholsoluble components in soybeans cause morphological changes in
the distal intestine of Atlantic salmon, Salmo salar L. J. Fish Dis.,
19, 47–53.
Krogdahl, Å., Lea, T.B. & Olli, J.J. (1994) Soybean proteinase
inhibitors affect intestinal trypsin activities and amino acid
digestibility in rainbow trout (Onchynchus mykiss). Comp.
Biochem. Physiol., 107A, 215–219.
Krogdahl, Å., Bakke-McKellep, A.M. & Baeverfjord, G. (2003)
Effects of graded levels of standard soybean meal on intestinal
structure, mucosal enzyme activities, and pancreatic response in
Atlantic salmon (Salmo salar L.). Aquacult. Nutr., 9, 361–371.
179
180
O. H. Romarheim et al.
Liao, I.C., Huang, T.-S., Tsai, W.-S., Hsueh, C.-M., Chang, S.-L. &
Leaño, E.M. (2004) Cobia culture in Taiwan: current status and
problems. Aquaculture, 237, 155–165.
Lunger, A.N., Craig, S.R. & McLean, E. (2006) Replacement of fish
meal in cobia (Rachycentron canadum) diets using an organically
certified protein. Aquaculture, 257, 393–399.
Qin, G.X., Verstegen, M.W.A. & van der Poel, A.F.B. (1998) Effect
of temperature and time during steam treatment on the protein
quality of full-fat soybeans from different origins. J. Sci. Food
Agric., 77, 393–398.
Refstie, S., Landsverk, T., Bakke-McKellep, A.M., Ringø, E., Sundby, A., Shearer, K.D. & Krogdahl, Å. (2006) Digestive capacity,
intestinal morphology, and microflora of 1-yaer and 2-year old
Atlantic cod (Gadus morhua) fed standard or bioprocessed soybean
meal. Aquaculture, 261, 269–284.
Resley, M.J., Webb ., K.A. Jr & Holt, G.J. (2006) Growth and
survival of juvenile cobia, Rachycentron canadum, at different
salinities in a recirculating aquaculture system. Aquaculture, 253,
398–407.
Romarheim, O.H., Aslaksen, M.A., Storebakken, T., Krogdahl, Å.
& Skrede, A. (2005) Effect of extrusion on trypsin inhibitor activity
and nutrient digestibility of diets based on fish meal, soybean meal
and white flakes. Arch. Anim. Nutr., 59, 365–375.
Romarheim, O.H., Skrede, A., Gao, Y., Krogdahl, Å., Denstadli, V.,
Lilleeng, E. & Storebakken, T. (2006) Comparison of white flakes
and toasted soybean meal partly replacing fish meal as protein
source in extruded feed for rainbow trout (Oncorhynchus mykiss).
Aquaculture, 256, 354–364.
Rumsey, G.L., Siwicki, A.K., Anderson, D.P. & Bowser, P.R. (1994)
Effect of soybean protein on serological response, non-specific
defense mechanisms, growth, and protein utilization in rainbow
trout. Vet. Immunol. Immunopathol., 41, 323–339.
SAS (1988) SAS/STAT UserÕs Guide. SAS Institute Inc., Cary, NC,
USA.
Shepherd, C.J., Pike, I.H. & Barlow, S.M. (2005) Sustainable feed
resources of marine origin. Eur. Aquacult. Soc. Spec. Publ., 5,
59–66.
Storebakken, T., Refstie, S. & Ruyter, B. (2000) Soy products as fat
and protein sources in fish feeds for intensive aquaculture. In: Soy
in Animal Nutrition (Drackley, J.K. ed), pp. 127–170. Federation
of Animal Science Societies, Savoy, IL, USA.
Tacon, A.G.J. (2004) Use of fish meal and fish oil in aquaculture: a
global perspective. Aquat. Res. Cult. Dev., 1, 3–14.
Wang, J.-T., Liu, Y.-J., Tian, L.-X., Mai, K.-S., Du, Z.-Y., Wang, Y.
& Yang, H.-J. (2005) Effect of dietary lipid level on growth
performance, lipid deposition, hepatic lipogenesis in juvenile
cobia (Rachycentron canadum). Aquaculture, 249, 439–447.
Zhou, Q.-C., Tan, B.-P., Mai, K.-S. & Liu, Y.-J. (2004) Apparent
digestibility of selected feed ingredients for juvenile cobia Rachycentron canadum. Aquaculture, 241, 441–451.
Zhou, Q.-C., Mai, K.-S., Tan, B.-P. & Liu, Y.-J. (2005) Partial
replacement of fish meal by soybean meal in diets for juvenile
cobia (Rachycentron canadum). Aquacult. Nutr., 11, 175–182.
Zhou, Q.-C., Wu, Z.-H., Tan, B.-P., Chi, S.-Y. & Yang, Q.-H. (2006)
Optimal dietary methionine requirement for juvenile cobia
Rachycentron canadum. Aquaculture, 258, 551–557.
..............................................................................................
2007 Blackwell Publishing Ltd Aquaculture Nutrition 14; 174–180