Influence of fish meal quality and feed (11)

Aq ua C Ub %
Aquaculture 153 (1997) 251-261

Influence of fish meal quality and feed pellet on
growth, feed efficiency and muscle composition in
gilthead seabream ( Sparus aurata)
A. Aksnes a,*, M.S. Izquierdo b, L. Robaina b, J.M. Vergara b,
D. Montero ’
a Norwegian Herring Oil and Meal Research Institute, N-5033 Fyllingsdalen, Bergen, Nonvay
’ Dpto. Biologia, (ink. de Las Palmas de G.C., Campus Unit. de Tafira 35017, Las Palmas de Gran Canaria,
Canary Island, Spain
’ Institute Canario de Ciencias Marinas, Consjeria de Educacion. Cultura y Deportes des Gobierno de
Canarias, PO Box 56, Telde, Canary Island, Spain

Accepted 4 February 1997 zyxwvutsrqponmlkjihgfedcbaZYXWVUTSR

Abstract
The effect of fish meal quality on growth, feed efficiency, protein digestibility and fillet
composition was studied in a growth experiment with gilthead seabream. The experiment included
a comparison of pelleted feed with extruded feed. The fish were fed three extruded diets which
varied in the quality of the fish meal used in the respective feeds: low quality fish meal, good

quality fish meal, and a mixture (50%) of the two fish meal qualities. Fish meal quality was
judged by protein digestibility as measured with mink as the test animal and by the content of
biogenic amines. A fourth experimental group was fed a pelleted feed with the same mixed fish
meal blend. The experiment started with 70 g seabream and lasted for 3 months until the fish
reached about 160 g.
All groups showed good growth and feed efficiency during the experimental period, with daily
specific growth rates (SGR) of 0.90-1.00% and feed efficiencies (FE; fish weight gain per feed
offered) from 0.58 to 0.66. The fish fed the feed with low quality fish meal showed significantly
poorer feed efficiency than the other groups, and there was a significant correlation between feed
efficiency obtained in seabream and the protein digestibility as measured with mink. No difference
was observed among groups fed the extruded diets, for growth, fillet composition or amount of
liver or viscera, although a significant correlation was obtained between SGR and protein
digestibility in mink. Fillet lipid content was higher in fish fed the extruded feed, compared with

* Corresponding author.
0044-8486/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved.
PZZ SOO44-8486(97)00046-X

252

A. Aksnes et al./Aquaculture

153 (1997) 251-261

those fed the corresponding pelleted diet. Protein digestibilty in seabream showed no difference
among the extruded feeds, while the pelleted feed was significantly lower. 0 1997 Elsevier
Science B.V.
Keywords:

Gilthead

seabream;

Feed quality; Growth; Feed efficiency;

Gross composition

1. Introduction
Intensive fish farming of carnivorous fish is currently dependent upon the use of fish
meal and other fishery products as the sole or major source of dietary protein and lipid

(Tacon, 1994). Proper composition of feed ingredients with high digestibility is crucial
for the optimal growth and feed efficiency of fish and is of great economical interest for
the aquacultural industry. Palatability and nutrient digestibilities
will affect fish farm
effluents on the environment. In addition, any effect of fish meal quality is important for
the interpretation of the results obtained in studies of fish meal replacement, as varying
fish meal quality probably will give varying replacement effects.
The market supply of fish meal shows great variation in quality, due to differences in
freshness, kind of raw material and processing conditions. Both raw material freshness
and processing conditions have been shown to affect growth performances and feed
efficiency in different species of fish (Pike et al., 1990; Anderson et al., 1993, 1995;
Pike, 1993; Moksness et al., 1995). Thus, salmon fed fish meal produced from stale raw
materials showed a specific growth rate (SGR) that was only 72% of that of fish fed a
fish meal produced from fresh raw material, while feed intake was reduced 11% and
feed efficiency was reduced by 65% (Pike, 1993). Similar effects of fish meal quality
have been observed for turbot (Danielssen et al., 1989) and wolffish (Moksness et al.,
1995).
Those effects could be related to the reduction in amino acid availability found in
some species. Anderson et al. (1993) found that true availability of amino acids in
Atlantic salmon could vary from 84.9 to 94.3% in trials with four different commercial

fish meals, while Romero et al. (1994) reported that true protein digestibilty, measured
in raibow trout, varied from 84.5 to 97.0% in 27 samples of fish meals.
Fish meal quality is difficult to evaluate by in vitro techniques, and these methods
will often misrank the samples (Anderson et al., 1993; Romero et al., 1994). Protein
digestibility as measured by mink has been shown to be a good indicator for protein
digestibility values in fish (Mundheim and Opstvedt, 1989; Romero et al., 1994) and
shows significantly reduced values with increased processing temperatures.
Different fish species may have different digestion capacity and metabolism. No data
are available on the effect of fish meal quality or type of pellet for seabream, however.
In commercial farming of seabream, the amount of feed used per kilogram weight gain
is high compared with other marine species. The quality of the feed may be important
for feed intake, feed efficiency and waste excretion. Moreover, the quality of the feed
may be important for the health of the fish and for the sensory quality of the cultured
fish.
This paper focuses on the impacts of fish meal quality on feed acceptance, growth,

A. Aksnes et al./Aquaculture

253

153 (1997) 251-261

feed efficiency, protein digestibility, health and slaughter percentage and muscle composition of seabream. The objective of the study also includes a comparison of feeds
produced by extrusion and by dry pelleting.

2. zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
Materials and methods
2.1. Diets and experimental

design

Four experimental diets were prepared using a ‘poor quality’ fish meal (FMP) or a
‘good quality’ fish meal (FMG). Both fish meals were obtained from Norsildmel, who
characterized FMP as NorSeaMink quality and FMG as Norse-LT 94@ quality. FMP
was produced from fish raw material with an average total volatile nitrogen (TVN) of
0.8 g kg-‘, heated to 90-95°C in a cooker and dried in a steam drier at 90-95°C. FMG
was produced from fish raw material with an average total volatile nitrogen of less than
0.4 g kg-‘, heated to 90-95°C in a cooker and dried in a heated air drier at less than
70°C. The quality of the fish meals and the experimental diets were evaluated according
to chemical analyses and protein digestibility as measured by mink (Skrede, 1979) using

four animals per sample (Table 1). Diets 1, 2 and 3 were extruded to 3 mm pellets and
contained FMP, a 1: 1 mixture (based on protein) of FMP and FMG or FMG, respectively. The production of the extruded feed was performed with a twin screw extruder
(BM 52; Wenger, USA), dried in a heated air drier and coated with oil in a rotating
cement mixer. The feed blend with the fish meal mixture was also dry pelleted to 3 mm.
The pelleted feed was produced by cold compression in a Simon-Heesen (Netherlands)
monoroll laboratory pellet mill, before drying at 40°C overnight. Chromic oxide was
included at 0.5% in all the experimental feeds for determination of protein digestibility
in seabream. The composition and chemical analyses of the feeds are shown in Table 2.
2.2. Fish and experimental

conditions

Gilthead seabream (Spat-us aurata) of 68-70 g average initial body weight were
anaesthetized
(chlorobutanol,
200 mg l-l>, weighed and randomly stocked in 125 1

Table I
Analyses

of fish meals (g kg-

’ or specified)

Crude protein (N X 6.25)
Lipid
Ash
Dry matter
Water soluble protein (% of total protein)
Cadaverine
Putrescine
Histamine
True mink protein digestibility ’ (%)
a Determined

with mink as the test animal.

Fish meal 1

Fish meal 2

708
113
107
929
30.0
1.30
0.66
0.10
84.8+ 1.1

736
101
111
928
21.7
0.30
0.20
< 0.10
93.7 f 0.7

254
Table 2
Ingredients

A. Aksnes et al./Aquaculture

and chemical

composition

153 (1997) 251-261

of the experimental

diets

Extruded

Pelleted

Diet no:

1

2

3

4

Fish meal:

Poor

Mix

Good

Mix

Ingredienrs (g kg _ ‘)
Fish meal 1, FMP ’
Fish meal 2, FMG b
Fish oil
Soy lecithin ’
Extruded corn d
Vitamins e
Minerals f
Vitamin C (Rovamix stay C-25)
Chromic oxide (Cr,O,)

630
0
58
5
286
10
5
1.3
5

0
315 zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIH
315
607
304
304
70
65
65
5
5
5
297
290
290
10
10
10
5
5
5
1.3
1.3
1.3
5
5
5

Chemical composition (g kg Crude protein (N X 6.25)
Lipid
Ash
Carbohydrate g
Total starch
Gelatinized starch
Gross energy (MJ kg- ’ )
Cadaverine
Histamine
Putrescine
True mink protein digestibility

’ dv matter)

h

414
109
82
260
218
218
20.5
0.77
< 0.10
0.37
84.9 * 0.9

461
112
81
262
224
228
20.6
0.45
< 0.10
0.20
88.5 kO.8

465
115
78
259
231
226
20.5
0.44
0.05)

Feed efficiency (Table 3) of Diet 1 was low and significantly (P < 0.05) different
from Diets 2, 3 and 4. Significant correlations were found between feed efficiency and
protein digestibility in mink, cadaverine and putrescine and the regressions fitted the
following equations:
FE = -0.29

+ 0.0104 zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHG
X true protein digestibility
mink (P < 0.05)

FE = 0.74 - 0.20 X cadaverine
FE = 0.67 - 0.002 X putrescine

(P < 0.05)
(P < 0.01)

The amounts of feed fed were the same for all groups (Table 3). There were no
differences in the amount of viscera or HSI among any of the groups (P > 0.05)
(Table
3). Chemical composition of muscle was similar for fish fed the different extruded diets
(Table 3). When comparing pelleted (Diet 4) with extruded treatments (Diets 1, 2 and 3),
the most remarkable difference was muscle lipid content, being lower for those fish fed
the pelleted diet, despite its higher dietary lipid content. When comparing pelleted feed
(Diet 4) with the corresponding extruded feed (Diet 2), only muscle lipid content was
affected, being significantly lower in fish fed the pelleted diet.
Dietary levels of amino acids were about the same, except for minor reductions in
some amino acids (e.g. lysine and histidine) in diets with poor quality fish meal and as
shown by reduction in the sum of analysed amino acids (Table 4).
Apparent protein digestibility in seabream is shown in Table 3. The digestibilities
calculated were high and similar for all the extruded diets but these were significantly

258

A. Aksnes et al./Aquaculture

Table 4
Dietary levels of amino acids (g kg-’

153 (1997) 251-261

crude protein)

Extruded

Pelleted

Diet no:

1

2

3

4

Alanine
Arginine
Aspartic acid
Glutamic acid
Glycine
Histidine
Hydroxyproline
Isoleucine
Leucine
Lysine
Methionine
Phenylalanine
Proline
Serine
Threonine
Tyrosine
Valine

61
54
81
142
56
22
5
42
81
69
33
43
42
40
42
21
54

63
56
84
140
60
26
7
43
82
73
34
44
44
41
41
28
51

63
51
86
137
62
31
8
42
81
17
33
45
45
42
41
27
51

64
55
84
139
60
28
8
41
82
74
34
44
45
41
41
27
50

Sum

894

917

928

917

(P < 0.01) higher than the pelleted feed (Diet 4). No correlation was found between
protein digestibility measured in gilthead seabream and that found in mink.

4. Discussion
The growth and FE obtained in this experiment, are comparable to or better than
those previously reported for gilthead seabream at similar conditions (Robaina et al.,
1995; Vergara et al., 1996). Growth and FE will in general depend on a proper chemical
composition of the feed and any effects of protein quality will best be seen at about or
lower than the required level of dietary protein. Too high dietary level of protein may
mask any differences due to protein quality. Very few data are available for the optimal
chemical composition of feed for gilthead seabream and no or only small differences are
observed with varying levels of protein to lipid (Vergara et al., 1996). In the present
work, the protein and lipid levels were 2-5 percentage units lower than in commercial
diets for seabream, but were still thought to have met the requirements of the fish.
Protein quality in fish meal will depend both on freshness of the raw material used
and the processing conditions in the manufacturing of the fish meal. Protein digestibility
as measured in mink was ealier shown to be a good indicator for determination of fish
feed quality, due to variable quality caused by processing conditions, for salmon (Pike et
al., 1990; Romero et al., 1994), trout (Pike et al., 1990) and halibut (Aksnes, 1997). In
the present study, protein digestibility as measured by mink correlated both with FE and

A. Aksnes et al./Aquaculture

153 (1997) 251-261

259

SGR in seabream. The relative difference in FE in seabream was lower than that found
for other fish species (Danielssen et al., 1989; Mundheim and Opstvedt, 1989; Pike et
al., 1990; Anderson et al., 1993, 1995; Romero et al., 1994; Moksness et al., 19951,
while differences in growth performances due to variable protein digestibility was much
lower. Poor utilization of feed was earlier shown to be compensated by increased feed
intake in halibut (Aksnes, 1997). This was not the case for seabream fed the FMP diet as
no difference in the amount of feed eaten was observed between any groups.
Lower dietary levels of lysine, histidine and arginine (Table 4), probably reflect the
bacterial formation of cadaverine, histamine and putrescine from these amino acids in
stored raw material used for production of FMP (Aksnes and Brekken, 1988). The sum
of analysed amino acids is 3-4% lower in FMP compared to FMG. This may be due to
bacterial decomposition
and to difference in the raw material used for fish meal
production. The difference in dietary amino acids was, however probably too small to
seriously affect growth performances at the dietary protein level which was used in this
experiment.
The two fish meals varied both in protein digestibility and freshness of raw material
as judged by difference in the content of biogenic amines. These were earlier shown to
be good indicators for raw material freshness (Aksnes and Brekken, 1988; Pike, 1993;
Clancy et al., 1995). In the present experiment, the content of both cadaverine and
putrescine correlated with the observed feed efficiencies and SGR. Pike (1993) showed
that raw material freshness, will affect both feed intake, FE and SGR in salmon. This
effect was most pronounced with very stale raw material, and the levels of biogenic
amines were higher than that of fish meals used in the present study. On the contrary,
rainbow trout (Fairgrieve et al., 1994) fed casein diets supplemented with histamine got
distended stomachs, but no effect on feed intake, growth or feed efficiency was noted;
addition of cadaverine and putrescine did not have any effect.
Apparent protein digestibility values were comparable to those reported for herring
fish meal by Nengas et al. (1995) in seabream. The digestibility values did not, however,
differentiate between the extruded diets produced from fish meal of variable quality, and
thus no correlation was found between protein digestibility as measured in seabream and
in mink. This is in agreement with the results recently reported by Clancy et al. (1995),
who found that neither processing temperatures nor raw material freshness affected the
protein digestibility in experiments with salmon and trout. The results contrast however
with several digestibility studies carried out in salmon (Mundheim and Opstvedt, 1989;
Pike et al., 1990; Anderson et al., 1993, 1995; Pike, 1993; Romero et al., 1994).
The two fish meals differed both in raw material freshness and in processing
temperature, and it is therefore not possible to conclude which of these had the greatest
impact on growth and feed utilization in seabream. As no difference in apparent protein
digestibility
in seabream was observed with diets varying in fish meal quality, the
importance of raw material freshness is indicated. However, as recently pointed out by
Anderson et al. (1995), caution should be used in evaluating digestibility results in fish
due to possible artifacts obtained by different methods of collecting faeces, especially
when comparing different quality of feeds.
Apparent protein digestibility in seabream was more than 7 percentage units higher
with the extruded diets compared to the pelleted. This difference could not be supported

260

A. zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGF
Aksnes et al./Aquaculture 153 (1997) 251- 261

by difference in FE or growth performances as no differences were observed for these
parameters comparing extruded and pelleted feed. Extrusion will not affect protein
digestibility (Vens-Cappell,
1984) and artifacts due to increased digestibility of carbohydrate is unlikely as degree of gelatinization
was close to 100% for all experimental
diets (Tabel 2). Pelleted diets, however, gave lower lipid muscle content in spite of the
higher dietary lipid content (Table 2). Thus the higher lipid level in the pelleted diet
(Diet 4) compared with the corresponding extruded (Diet 2) may have compensated for
a lower digestibility for fish fed this diet in comparison with the fish fed the extruded
mixed blend diet.

Acknowledgements
This work is supported by the Norwegian Research Council. The authors thank Dr. S.
La11 from the Department of Fisheries and Oceans in Halifax, who kindly read the
manuscript and gave valuable suggestions.

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