Partial replacement of red crab (Pleuroncodes planipes) meal for fish
meal in practical diets for the white shrimp Litopenaeus vannamei.
Effects on growth and in vivo digestibility
E. Goytortúa-Bores, R. Civera-Cerecedo , S. Rocha-Meza, A. Green-Yee
Laboratorio de Nutrición Acuícola, Centro de Investigaciones Biológicas del Noroeste, S. C.
Mar Bermejo No. 195, Col. Playa Palo Santa Rita,La Paz, B.C.S. 23090, México
Abstract
The nutritional value of red crab (Pleuroncodes planipes) meal (RCM) as a protein
source and partial replacement for fish meal in diets for juvenile Litopenaeus vannamei was
Laboratorio de Nutrición Acuícola, Centro de Investigaciones Biológicas del Noroeste, S. C. Mar Bermejo No. 195, Col. Playa Palo Santa Rita,
La Paz, B.C.S. 23090, México
evaluated. Fish meal in the control diet was replaced by increasing dietary levels of red crab
meal (5%, 10% and 15%), replacing 12.7%, 25.3% and 38.0%, respectively, of the protein
derived from fish meal. A 30- day feeding trial with juvenile shrimp (0.26 g mean initial
weight) was conducted and digestibility of the diets was also determined. Survival of shrimp
in all treatments ranged from 98% to 100% and growth was significantly higher for
shrimp fed diets that contained 15% RCM (Pb 0.05). Feed conversion and protein
efficiency ratios were better when compared to the control diet. Protein digestibility
values for all RCM dietary treatments (83%, 84% and 84%, respectively) were significantly
higher than that of the control diet (80%). Digestibility of lipids ranged from 79% for the
control diet to 84% for the 15% red crab meal diet, while carbohydrate digestibility values
decreased as the level of red crab meal increased. Apparent digestible energy was significantly
higher in diets containing RCM. These results indicate that red crab meal used in this study
serves as a suitable partial replacement for tuna by-product meal, and can improve growth,
feed conversion and protein efficiency of L. vannamei juveniles.
© 2006 Elsevier B.V. All rights reserved.
Keywords: Fish meal; Red crab; Shrimp; Growth; Digestibility
1. Introduction
Feed quality, stocking density and water quality are
the main factors affecting productivity for semiintensive and intensive culture of penaeid shrimp
(Cruz-Suárez et ., 1993). Formulated feed plays an
important role as the source of nutrients, and protein is
recognized as one of the most important dietary
al
⁎ Corresponding author. Tel.: +52 612 123 84 07; fax: +52 612 125
36 25.
E-mail address: rcivera04@cibnor.mx (R. Civera-Cerecedo).
0044-8486/$ - see front matter © 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquaculture.2006.02.035
components. Levels of crude protein in commercial
shrimp feeds vary between 30% and 50%, and most
feeds contain some fish meal protein (Martinez-Cordoba
et al., 2003). Protein quality of fish meal varies widely
and its nutrient composition depends on many factors
(Davis et al., 2004). To supply the growing market of
cultured shrimp, the demand for improved feeds has
created a demand for high quality protein sources.
According to Tacon and Forster (2000), the global
supply of fish meal, around 6.5 million metric tons, will
likely remain static or decline because world capture
fisheries have reached a plateau (Lim et al., 1997). The
increase in use of fish meal, not only for penaeid shrimp
culture but also for other types of culture (livestock, fish,
etc.), has directed attention to assessing alternative
ingredients as replacements for fish meal protein
(Bharadwaj et al., 2002; El-Saidy and Gaber, 2002).
Ideally, these alternative ingredients should have good
availability and satisfactory nutritional quality for the
species to feed, and also to be economically practical
(D'Abramo and Lovell, 1991). Many plant, animal byproducts and microbial protein sources have been
evaluated as replacements for fish meal (Davis and
Arnold, 2000; Olvera-Novoa and Olivera-Castillo,
2000; Cruz-Suárez et al., 2004; Yu, 2004), and some
of them are currently used in the feed manufacture
industry. Also, it is desirable that diets be prepared with
locally available ingredients to make formulation easier
and to lower cost of production (Rajyalakshmi et al.,
1986 cited in Sudaryono et al., 1995).
The Aquatic Nutrition Laboratory of the Centro de
Investigaciones Biológicas del Noroeste (CIBNOR) has
continued to investigate suitable alternative protein
sources for feed aquaculture such as the meal prepared
from the crustacean Pleuroncodes planipes. This species
is known by the common names of red crab, pelagic
crab and langostilla (in Spanish) having lobster-like
characteristics and an overall adult length between 8 and
13 cm. It is an anomuran (Crustacea: Decapoda:
Galatheidae) that occurs in dense concentrations along
the Pacific coast of Baja California, Mexico. AuriolesGamboa et al. (1995) estimated that the potential catch
yield during the summer-autumn season is 109,000
metric tons, while the winter-spring potential catch
yield is 77,000 metric tons, for an average of 93,000
metric tons per year. The pelagic red crab is not used for
human consumption because of the small size of its
abdominal muscle. However, its nutrient composition
makes it an attractive ingredient for animal feeds. The
most abundant nutrients of red crab are protein and
minerals. Depending on the season, and age of organism
protein and ash content range from 35% to 55% and
13% to 38%, respectively (Castro-González et al.,
1995). Lipid content ranges from 5% to 14% and most
of the fatty acids are unsaturated, eicosapentaenoic and
docosahexaenoic acids being the most abundant (Pierce
et al., 1969; Van der Veen et al., 1971). Red crab is also
an excellent source of -carotene, two esters of
astaxanthin and free astaxanthin (Wilkie, 1972) with
concentrations estimated to be 8-10 mg/100 g of whole
animal. Red crab has been used previously as a feed
ingredient for aquatic organisms. Spinelli and Mahnken
(1978) used it as a source of pigments in diets for
salmonids. Coral-Hinostroza et al. (1998) used oil-
extracted pigments from red crab as a feed ingredient for
rainbow trout and obtained excellent muscle
pigmentation.
Red crab meal (RCM) has previously been evaluated
as a replacement for fish meal in crustacean diets. Van
Olst et al. (1976) cited in Villarreal et al. (2004) reported
good results when using feeds supplemented with red
crab meal for the American lobster. Villarreal et al.
(2004) found that growth of Farfantepenaeus californiensis post-larvae improved when the diet contained
RCM. Some results of investigations concerning the use
of red crab in aquaculture feeds have been reviewed in
Civera et al. (1999, 2000).
The present study was conducted to evaluate the
nutritional quality of RCM as a source of protein, by
determining the effect of partial replacement of RCM for
fish meal in practical diets for juvenile Pacific white
shrimp L. vannamei. The apparent digestibility of dry
matter, protein, lipids, carbohydrates and energy in the
diets was also determined.
2. Materials and methods
2.1. Experimental units
Twelve 60-l rectangular tanks (58×48×25 cm) were
each equipped with a 250-W submersible heater, an
airlift and filtered seawater supply. The incoming
seawater was filtered, through a sand filter and a
cartridge filter (10 m), and then flowed through an UV
irradiating unit. These experimental units were used to
conduct the growth and digestibility experiments.
2.2. Ingredients and experimental diets
Red crab and shrimp head meals were prepared at
the CIBNOR facilities. Pelagic red crabs were caught
at Puerto San Carlos, B.C.S. in May 1992, and
transported frozen to the laboratory. Whole organisms
were used to produce the red crab meal (RCM).
Shrimp-head meal was prepared from fresh heads of
commercially cultured L. vannamei. Both feed ingredients were boiled for 5 min, oven-dried for 5 h at
70 °C, ground in a hammer mill and stored in plastic
bags under refrigeration until used. The proximate
composition of each of the principal dietary protein
sources is presented in Table 1. Diets were made based
upon the results of the chemical composition of the
ingredients. The control diet contained fish meal (tuna
by-product), shrimp-heads meal and soybean meal as
the principal sources of dietary protein. All diets were
formulated to contain approximately 42% crude protein
.
Table 1
Composition (g/100 g dry wt.) of the main protein sources used in the
experimental diets fed to juvenile L. vannamei a
Ingredient
Crude
protein
Fish meal (tuna by- 57.3
product)
37.0d
Red crab
mealc
50.9d
Shrimp-head
meal
45.9
Soybean meal
a
b
c
d
Crude
fiber
Ash NFEb
7.31
1.10
26.8
9.18
4.01
31.8 18.01
10.40
5.28
23.3 10.12
0.70
3.79
17.3 32.31
Ether
extract
7.49
Values are means of three determinations.
Nitrogen-free extract.
Prepared in our laboratory from Pleuroncodes planipes.
Including non-protein nitrogen such as chitin.
and 17 kJ/g gross energy. Ingredient composition of
each of the experimental diets is presented in Table 2.
Diets were formulated to contain 0%, 5%, 10% and
15% red crab meal (replacing 0%, 12.7%, 25.3% and
38.0% of the protein contained in the fish meal ingredient, respectively). Diets for the digestibility assay
included 0.5% chromic oxide as inert marker.
Prior to preparing the experimental diets, all
ingredients were ground in a hammer mill and passed
through a 0.5-mm mesh sieve. The dry ingredients of
each diet were mixed thoroughly in a food mixer before
an oil mix (fish oil and soy lecithin) was added. After the
oil was dispersed, water was added (approximately 50%
of the total "as is" ingredient weight) and finally mixed.
The resulting mixture was pressure pelleted using a meat
grinder and a 2-mm die. The pellets were dried in a
forced-air oven at 50 °C for 12 h.
2.3. Chemical analysis
Samples of diet and feces were analyzed for dry matter,
crude protein (N×6.25), ether extract, crude fiber, ash and
nitrogen-free extract (NFE) contents according to the
methods of AOAC (1995). Gross energy values of diets
were determined with an adiabatic calorimeter (Parr
Instrument Co., Moline, IL). Total lipids were analyzed
using the technique described by Folch et al. (1957) and
carbohydrate was measured by the Antrona method
(Kabat and Mayer, 1968). Chromic oxide was determined
by the method described by Bolin et al. (1952). All
chemical determinations were made in triplicate.
(Acuacultores de la Península, S.A. de C.V., La Paz,
B.C.S.). They were fed a combination of Artemia nauplii
(Argent Laboratories, Redmon, WA) and a commercial
shrimp diet (PIASA, La Paz, B.C.S.) containing 40%
crude protein during 40 days into two 1500-l fiberglass
container (3.0×2.0×0.4 m), during this period organisms were acclimated to laboratory conditions. After this
period, shrimp were individually weighed and 180
juveniles with an average initial weight of 0.26
±0.002 g (mean±standard deviation) were stocked into
Table 2
Ingredient composition (g/100 g diet) and proximate analysis (g/100
dry wt.) of practical diets containing increasing levels of red crab meal
(RCM), to replace fish meal on an equal protein basis
Ingredients
Diets
CD
b
Fish meal (tuna by-product)
c
Red crab meal
Shrimp-head meal
d
Soybean meal
d
Wheat meal
Sorghum meald
Grenetine
b
c
Fish oil (tuna)
d
Soy lecithin
f
Vitamin premix
Vitamin C (ascorbic acid)
Mineral premixg
Chromic oxideh
i
Proximate analysis
Dry matter
Crude protein (N×6.25)
Ether extract
Crude fiber
Ash
Nitrogen-free extract
Gross energy (kJ/g)
a
RCM-5
RCM-10
RCM-15
25.5
0
10.0
29.0
15.0
10.0
4.0
1.5
1.5
0.2
0.3
3.0
22.0
5.4
10.0
29.0
15.0
8.1
4.0
1.5
1.5
0.2
0.3
3.0
19.0
10.0
10.0
29.0
15.0
6.5
4.0
1.5
1.5
0.2
0.3
3.0
16.0
14.7
10.0
29.0
15.0
4.8
4.0
1.5
1.5
0.2
0.3
3.0
95.5
44.5
7.2
3.4
14.5
30.4
17.3
96.3
43.9
7.5
3.6
14.5
30.5
17.3
95.8
43.8
7.6
3.3
15.3
30.0
17.2
96.6
42.2
7.4
3.3
16.4
30.7
16.9
a
CD=control diet without red crab meal.
Tuna by-product meal (Productos Pesqueros de la Paz, La Paz,
B.C.S., México).
c
Prepared in our laboratory.
d
Soybean meal, wheat meal, sorghum meal and fish oil (Promotora
Industrial Acuasistemas, S.A. de C.V., La Paz, B.C.S., México).
e
Grenetin (Semillera La Paz, La Paz, B.C.S., México).
b
f
Vitamin premix (mg or IU/kg of diet): A acetate, 15,000 IU; D 3,
7500 IU; E, 400; K 3, 20; choline chloride (99%), 400 mg; thiamin HCl,
150; riboflavin, 100; pyridoxine HCl, 50; pantothenic acid, 100;
niacin, 300; biotin, 1; inositol, 500; folic acid, 20; cyanocobalamin,
0.1.
g Mineral premix (g/kg of diet): KCl, 0.5; MgSO ·4H O, 0.5;
4
2
2.4. Growth trial
ZnSO 4·7H 2O, 0.09; MnCl 2·4H 2O, 0.0234; CuCl 2·2H 2O, 0.005; KI,
0.05; CoCl 2·6H 2O, 0.0025; Na 2HPO 4, 2.37.
h In the digestibility trial, 0.5% chromic oxide was included in all
diets; to compensate sorghum meal was reduced by an equivalent
Post-larvae of Litopenaeus vannamei were obtained
from a cultured broodstock at the commercial hatchery
amount.
i
Values are means of three determinations.
.
the experimental tanks. Each dietary treatment consisted
of three replicates (tanks) of 15 shrimp per tank (stocking
density related to bottom surface area: 62.5 shrimp/m 2).
Dietary treatments were randomly assigned to the tanks
and the shrimp were weighed at days 15 and 30. Shrimp
were fed to apparent satiation twice a day during the
30 days. The initial ration was 15% of the biomass and
was adjusted daily, after noting the presence or absence
of residual feed. Uneaten feed and dead shrimp were
quantified and removed daily. Temperature and salinity
were recorded once daily (28±1 °C and 37±0.5‰). A
photoperiod of 12:12 h light/dark cycle was maintained
throughout the experiment.
At the conclusion of the 30-day trial, growth (percent
weight gain), survival, feed intake, feed conversion ratio
and protein efficiency ratio were determined for each
replicate of each treatment as follows: percent weight
gain (%WG) = [(final mean weight  initial mean
weight)/initial mean weight]×100; survival (%S)=
(final number of shrimp/initial number of shrimp)×100;
feed intake (FI)=feed consumption, g/number of
shrimp/day; feed conversion ratio (FCR)=feed, g/total
weight gain, g. Total weight gain was corrected using
the formula described by Kitabayashi et al. (1971): corrected total weight gain=final total weight+[1/2(average initial weight+average final weight)×number of
dead shrimp] initial total weight. Protein efficiency
ratio (PER)=total weight gain, g/total protein intake, g
was also estimated.
2.5. Digestibility trial
Shrimp obtained from a commercial shrimp farm
(Acuacultores de la Península, S.A. de C.V., La Paz,
B.C.S., Mexico) were acclimated to laboratory conditions for 4 days in two 1500-l fiberglass tanks
(3.0×2.0×0.4 m). During this period, they were fed
a commercial feed without chromic oxide, twice daily.
After this acclimatization period, shrimp were individually weighed and 120 shrimp with an average initial
weight of 3.32±0.01 g were selected. Each of the
experimental diets was tested in three replicate tanks
(10 shrimps/tank). Salinity, temperature and dissolved
oxygen were maintained at 34.5±1.5‰, 28±0.4 °C
and 5.5±0.4 mg/l, respectively (mean±S.D.).
Shrimp were fed ad libitum three times daily and
acclimated to the experimental diets containing chromic
oxide during 7 days before starting feces collection.
Immediate pipeting was used as method for feces
collection. Early in the morning, non-consumed feed,
exuviae, overnigth feces and dead shrimp were removed
from the tanks daily. One hour after each feeding, faecal
strands were siphoned out gently using a Pasteur pipet,
then gently rinsed with distilled water and frozen at
80 °C. After termination of the collection period,
frozen faecal material pooled from each tank were
freeze-dried, ground, thoroughly mixed and kept frozen
at 20 °C until analysis. The faecal samples were
analyzed for chromic oxide (Cr 2O 3), crude protein, total
lipid and carbohydrates. Apparent digestibility coefficients (ADCs) were calculated according to the
following formula: ADC of dry matter (%)=100 [(%
Cr 2O3 in feed/% Cr 2O3 in feces)×100]; ADC of
nutrients (%)=100 100[(% Cr 2O 3 in feed/% Cr 2O 3 in
feces)×(% nutrient in feces/% nutrient in feed)]; ADC
of energy (%)=(digestible energy, kJ/g/gross energy, kJ/
g)×100. Digestible energy (kJ/g)=[(g nutrient/100 g
feed × nutrient apparent digestibility coefficient)/
100×energy value, kJ/g]. Digestible energy was
calculated based on the energy values 23, 35 and
15 kJ/g for protein, lipid and carbohydrate, respectively
(Cousin, 1995).
2.6. Statistical methods
Normality of distribution (Llilieford test) and homogeneity of variance (Bartlet test) were tested (Sokal,
1995; Conover, 1980; Ott, 1992). Normal and homoscedastic data were analyzed with a one-way analysis of
variance (ANOVA), and Tukey's test was the multiple
comparison test used. All analyses were made at 0.05
significance level using STATGRAPHICS v.5.1 software (Statistical Graphics Co., Herndon, Virginia,
USA). When the data were not normally distributed, a
non-parametric analysis of variance and a multiple range
test (Kruskal-Wallis) were used to determine differences among treatments (Sokal, 1995; Ott, 1992).
Correlation analyses were done using the Spearman
rank correlation method (STATISTICA 6.0 StatSoft,
Inc., Tulsa, OK, USA).
3. Results
The nutrient composition of the main protein sources
used in the experimental diets are presented in Table 2.
Tuna by-product meal contained 57.3% crude protein
and 26.8% ash, while red crab meal (RCM) contained
37.0% crude protein and 31.8% ash.
3.1. Growth trial
Survival at the end of the experiment was high
(98%) and unaffected by diets (Table 3). Final weight,
percent weight gain and feed intake of shrimp fed the
Table 3
Response of juvenile L. vannamei to a control diet and experimental diets containing increasing levels of red crab meal (RCM), to replace fish meal on
the basis of equivalent levels of protein1
Diet
Survival
(%)
Final weight
(g)
CD2
RCM-5
RCM-10
RCM-15
100
100
98
100
1.40
1.41
1.43
1.68
b
±0.02
±0.06
b
±0.14
a
±0.06
b
Weight gain
(%)
435.8
443.6
449.4
544.1
Feed intake
(mg/shrimp/day)
b
±11.3
±16.5
b
±54.1
a
±23.7
b
58.5
57.7
56.4
65.9
b
±2.4
±8.6
b
±7.7
a
±2.2
b
Protein intake
(mg/shrimp/day)
Feed conversion
ratio
Protein efficiency
ratio
26.0 ab±1.1
25.3 ab±3.8
24.7 b±3.4
27.8 ab±0.9
1.54 a±0.04
1.50 ab±0.16
1.40 b±0.09
1.40 b±0.09
1.46 c±0.04
1.53 bc±0.16
1.58 ab±0.10
1.70 a±0.10
1Values
are means of three tanks of shrimp per dietary treatment±standard deviation. Values within the same column with different superscripts are
significantly different (Pb0.05).
2
CD=control diet without red crab meal.
diet containing 15% RCM were significantly higher
than those of shrimp fed either the control diet, the
RCM-5 or RCM-10 diets. The lowest feed conversion
ratio (FCR) was observed in shrimp fed diets RCM-10
and RCM-15 (1.40). This FCR was significantly
(Pb 0.05) better than that of shrimp fed the control
diet (1.54), whereas no difference was detected among
shrimp fed diets containing red crab meal (5%, 10% or
15% RCM). Protein efficiency ratios (PER) of diets
RCM-10 and RCM-15 were significantly higher than
that of the control diet. PER values were correlated with
growth (0.84, P =0.005) and feed intake (0.81,
P =0.007).
3.2. Digestibility trial
The apparent digestibility coefficients (ADC) of dry
matter, protein, lipid, carbohydrates and energy in the
diets are presented in Table 4. Dry matter and crude
protein digestibility of the experimental diets increased
significantly, from 79.7% to 84.0%, as the RCM
content of the diet increased to 15%, whereas no
significant differences among diets containing RCM
were found. Diet RCM-15 had a lipid digestibility
(84.4%) that was significantly higher than that of the
control and RCM-5 diets (78.9% and 80.4%) and the
lowest carbohydrate digestibility (46.2%). The digestible energy of the control diet was significantly lower
(73.9%) than that of red crab meal diets (average
77.6%).
4. Discussion
The presence of chitin interferes with the determination of crude protein in crustacean meal because
chitin contains nitrogen that is calculated as proteinnitrogen. Cruz-Suárez et al. (1993) reported that a byproduct meal of Pacific white shrimp contained 11%
chitin and Calvo-Carrillo et al. (1995) determined that
RCM contains about 9% chitin. If these different
contents of chitin are considered to calculate real
protein content, then the crude protein content for the
red crab and shrimp-head meals are overestimated by
about 0.62% and 0.75%, respectively. Hence, crude
protein content of the experimental diets might be
slightly overestimated by about 1%. Nutrient composition of red crab varies seasonally and according to
method of preparation (Castro-González et al., 1995),
so the results presented in this study may not be
applicable to all red crab meals.
Table 4
Apparent digestibility coefficients (%±S.D.) 1 for dry matter, protein, lipid, carbohydrates and energy for the control diet and experimental diets
containing increasing levels of red crab meal (RCM) fed to juvenile L. vannamei (mean initial weight 3.32±0.01 g)
Diet
Dry matter
CD3
RCM-5
RCM-10
RCM-15
68.9
73.8
74.2
74.2
1Values
b
±1.0
±0.7
a
±1.2
a
±3.7
a
Protein
79.7
82.8
83.6
84.0
b
±0.6
±1.0
a
±0.3
a
±2.4
a
Lipid
Carbohydrates
78.9 c±1.5
80.4 bc±1.6
82.7 ab±2.1
84.4 a±1.1
53.4
58.7
53.0
46.2
a
±7.4
±4.6
a
±3.0
b
±3.2
a
are means of three tanks of shrimp per dietary treatment. Values within the same column with different superscripts are significantly different
(Pb0.05).
2
Digestible energy was calculated based on the energy values 23, 35 and 15 kJ/g for protein, lipid and carbohydrate, respectively (Cousin, 1995), and
nutrient apparent digestibility values presented in this table.
3
CD=control diet without red crab meal.
Energy2
73.9
77.5
77.6
77.6
b
±1.4
±1.8
a
±1.4
a
±2.2
a
4.1. Growth
At the termination of the growth trial, high survival
for all treatments was obtained (98% to 100%).
Growth of shrimps fed the control diet was similar
to that obtained by other authors under laboratory
conditions when evaluating the replacement of fish
meals from different origins (Davis and Arnold, 2000;
Cheng et al., 2002; Tan et al., 2005). When RCM was
included in the diet to replace 38% of the fish meal
protein, weight gain was significantly greater. Villarreal et al. (2004) and Civera et al. (1994) reported
significantly better growth of juvenile P. californiensis
when dietary fish meal was partially substituted by
RCM. Villarreal et al. (1994) reported a significantly
better growth of L. vannamei and they also reported a
increase in feed consumption of diet contained red
crab meal. In the present study, a marked increase in
feed consumption of the RCM-15 diet was observed.
Crustacean meals are known to improve the palatability of diets for shrimp. Fox et al. (1994) observed
that the inclusion of shrimp-head meal in diets for
juvenile Penaeus monodon significantly improved
palatability, when compared to a diet based on fish
meal. Like other crustacean meals, RCM contains
nitrogenous compounds such as amino acids, peptides
and nucleotides that have been identified as feeding
stimulants for several species (Cruz-Suárez et al.,
1993; Harpaz, 1997; Lee and Meyers, 1997). Montemayor et al. (1998) included red crab solubles (fluid
from crushed red crab (P. planipes) as an attractant in
feeds for several crustaceans and obtained results
comparable to those obtained with commercial
attractants for shrimp.
Feed conversion ratio (FCR) and protein efficiency
ratio (PER) were also improved by the inclusion of
RCM in the diets, possibly as an effect of increased
palatability and protein digestibility. A high palatability
minimizes the time the feed remains uneaten and
thereby minimizes nutrient losses through leaching
(Tacon et al., 2000). FCR values obtained in the present
investigation (1.5 to 1.4) are better than those reported
by Villarreal et al. (1994) and Civera et al. (1994) for
juvenile F. californiensis and L. vannamei fed practical
diets and cultured under similar conditions. Although
the growth of shrimp fed the RCM-10 diet was similar to
that obtained with the control diet (CD), the FCR was
significantly better than that of the CD diet, demonstrating that even a low inclusion level of RCM in the
diet can improve feed utilization. Protein efficiency ratio
has been described as a good criterion to evaluate protein sources for aquatic feeds. There are different
nutritional factors that influence PER. Capuzzo (1983)
found that PER values for several crustaceans studied
decreased with increasing dietary protein levels. Mazid
et al. (1997) reported that protein quality also affects
PER values. In the present study, dietary protein content
was similar among diets, but different PER values
suggest differences in dietary protein quality. Nevertheless, PER results must be interpreted carefully because
this parameter assumes that all protein is used for growth
(Tacon, 1989). The highest PER in shrimp fed the RCM15 diet suggests a better utilization of dietary protein
originating from RCM. This response is possibly the
result of a slightly higher content of some essential
amino acids, such as arginine, histidine, isoleucine,
leucine, phenylalanine and threonine in red crab than in
tuna meal, as reported in Ezquerra et al. (1997).
According to Farmanfarmaian and Laurerio (1980)
cited in Capuzzo (1983), PER values for Macrobrachium rosenbergii increased with amino acid supplementation to a commercial pelleted feed, especially with
the addition of lysine and, to a lesser extent, the addition
of arginine, leucine and isoleucine, indicating that
limiting amino acids may affect PER values. An
indication of the biological value of the dietary protein
is the lysine and arginine dietary relationship. Hew and
Cuzon (1982) improved the value of casein as a protein
source for Penaeus japonicus by supplementing crystalline lysine and arginine. Akiyama et al. (1992) recommend lysine/arginine ratios of 1:1 to 1:1.1 in diets
for shrimp. Ezquerra et al. (1997) found a ratio of 1:0.7
in tuna waste meal protein and 1:0.9 in red crab meal,
hence as RCM dietary level increases (5%, 10% and
15%) the lysine/arginine ratio is closer to those
recommended for shrimp. It is probably that this
improvement in amino acid profile due to the incorporation of RCM to the diets could be the cause of the
growth enhancement of the organisms observed in the
present experiment.
4.2. Digestibility
ADMD values obtained in the present experiment
indicate that inclusion of RCM in the experimental diets
significantly improved feed utilization. The ADMD of
the control diet (68.9%) was significantly lower than
those of diets RCM-5, RCM-10 and RCM-15 (73.8%,
74.2% and 74.2%, respectively).
Brunson et al. (1997) found that inclusion of shrimp
or crab meals (30% as dry matter) in diets for juvenile
Penaeus setiferus (7.7 g) depressed apparent protein
digestibility (APD). Results of the present study indicate
that apparent protein and energy digestibilities were
enhanced by the inclusion of dietary RCM. The APD
values are similar to those reported by other investigators who used crustacean meals in shrimp diets
(Sudaryono et al., 1996; Lee and Lawrence, 1997).
APD values obtained with the diets containing RCM
were significantly higher than those obtained with the
control diet. Probably, a better amino acid profile in red
crab meal than in tuna meal (Ezquerra et al., 1997)
allows a better use of proteins (PER from growth assay)
and enhance digestibility of dietary protein.
Apparent lipid digestibility (ALD) of the diets was
improved by the inclusion of RCM, and was significantly higher when dietary RCM was included at 10%
and 15% (82.7% and 84.4%). There is little information
on ALD, but lipids are known to be highly digestible
(85-95%) in shrimp (Cuzon et al., 1994). Many factors
affect lipid digestibility (Lee and Lawrence, 1997) and
heat treatment is one of the most important. RCM is an
excellent source of triglycerides and phospholipids
(Pierce et al., 1969) that are more efficiently digested
than free fatty acids (Merican and Shim, 1995). Highly
unsaturated fatty acids, known to be components of
marine crustaceans meals, have been shown to enhance
growth and are highly digestible (Merican and Shim,
1995; Cuzon and Guillaume, 1999). Although the
quantitative level of lipids in the experimental diets
was similar, changes in the relative proportions of the
different fatty acids and also their availability probably
varied with the inclusion of RCM, and could explain at
least partially the growth enhancement observed. The
fatty acid content of the ingredients and diets was not
determined in the present study, so more research is
needed to elucidate the nutritional value of dietary fatty
acids from red crab for shrimp.
Ahamad (1996) found that the apparent carbohydrate
digestibility (ACD) in purified diets for Penaeus indicus
increased with increasing levels of dietary carbohydrate
(7.3% to 52.3%) at a constant protein level (35%).
Condrey et al. (1972) reported ACDs of 49% to 76% in
diets for P. setiferus and Penaeus aztecus. Values of
ACD obtained with L. vannamei fed the experimental
diets in our study were similar to those reported by these
investigators. Carbohydrates constitute one of the three
dietary nutrients that are used as energy sources to
support animal growth (Shiau, 1997). However, shrimp
have a limited capacity to metabolize carbohydrates
(Rosas et al., 2000) and chitin (Lee and Lawrence,
1997). If RCM in diets reduced carbohydrate digestibility, then the sparing action of dietary carbohydrates
would be reduced. This may be a result of the substitution of RCM carbohydrates, which include chitin, for
sorghum carbohydrates in the experimental diets
(Table 2). Feed intake of diet RCM-15 was significantly
higher than that of each of the other diets, resulting in an
increase in the quantity of ingested chitin that may have
contributed to the low carbohydrate digestibility observed with this diet. Nevertheless, additional investigations are needed to support this hypothesis. The
apparent digestibility coefficients determined for protein, lipid, carbohydrate and energy suggest that energy
was mainly provided by dietary protein and lipids.
5. Conclusion
Red crab meal served as a suitable partial
replacement for tuna by-product meal under the
culture conditions used in this study, and can be
considered an alternative protein source. Further
research evaluating the complete replacement of tuna
by-product meal and other fish meals in shrimp diets
is warranted.
Acknowledgements
We thank Jaime Malagamba and Ricardo Dubost,
from the commercial hatchery Acuacultores de la
Península (APSA), for providing the experimental
organisms. We thank Jean Guillaume and Lucía
Ocampo for comments and suggestions to the manuscript, and the editing staff at CIBNOR for correcting
the English text. This work was supported by CIBNOR
projects ICM1and PAC17.
References
Ahamad, A.S., 1996. Carbohydrate nutrition under different conditions in prawn Penaeus indicus. J. Aquac. Trop. 11, 13-25.
Akiyama, D.M., Dominy, W.G., Lawrence, A., 1992. Penaeid shrimp
nutrition. In: Fast, A.W., Lester, J. (Eds.), Marine Shrimp Culture:
Principles and Practices. Elsevier Science Publishers B.V.,
Amsterdam, pp. 535-567.
AOAC, 1995. 16th ed. Official Methods of Analysis of the Association
of Official Analytical Chemist, vol. I. Washington, D.C., USA.
1234 pp.
Aurioles-Gamboa, D., Balart, E.F., Castro-Aguirre, J.L., 1995.
Recomendaciones para la explotación y aprovechamiento de la
langostilla. In: Aurioles-Gamboa, D., Balart, E.F. (Eds.), La
Langostilla: Biología, Ecología y Aprovechamiento. Centro de
Investigaciones Biológicas del Noroeste, S. C. La Paz, B.C.S.,
México, pp. 221-233.
Bharadwaj, A.S., Brignon, W.R., Gould, N.L., Brown, P.B., Wu, Y.V.,
2002. Evaluation of meat and bone meal in practical diets fed to
juvenile hybrid striped bass Morone chrysops×M. saxatilis.
J. World Aquac. Soc. 33, 448-457.
Bolin, D.W., King, R.P., Klosterman, E.W., 1952. A simplified method
for the determination of chromic oxide (Cr 2O 3) when used as an
index substance. Science 116, 634-635.
Brunson, J.F., Romaire, R.P., Reigh, R.C., 1997. Apparent digestibility
of selected ingredients in diets for white shrimp Penaeus setiferus
L. Aquac. Nutr. 3, 9-16.
Calvo-Carrillo, M.C., Castro-González, M.I., Sánchezarmas-Luna, R.,
Pérez-Gil-Romo, F., 1995. Fibra cruda y quitina en el crustáceo
langostilla (Pleuroncodes planipes, Stimpson): Similitudes y
diferencias. Cienc. Mar. 21, 179-186.
Capuzzo, J.M., 1983. Crustacean bioenergetics: the role of environmental variables and dietary levels of macronutrients on energetic
efficiencies. In: Pruder, G.D., Langdon, C.J., Conklin, D.E. (Eds.),
Proceedings of the Second International Conference on Aquaculture Nutrition: Biochemical and Physiological Approaches to
Shellfish Nutrition. World Aquaculture Society, Baton Rouge, LA,
pp. 71-86.
Castro-González, M.I., Carrillo-Domínguez, S., Pérez-Gil Romo, F.,
Calvo-Carrillo, C., 1995. Composición química de la langostilla,
procesos tecnológicos. In: Aurioles-Gamboa, D., Balart, E.F.
(Eds.), La Langostilla: Biología, Ecología y Aprovechamiento.
Centro de Investigaciones Biológicas del Noroeste, S. C. La Paz,
B.C.S., México, pp. 163-178.
Cheng, Z.J., Behnke, K.C., Dominy, W.G., 2002. Effects of poultry byproduct meal as a substitute for fish meal in diets on growth and
body composition of juvenile pacific white shrimp, Litopenaeus
vannamei. J. Appl. Aquac. 12 (1), 71-83.
Civera, R., Villarreal, H., Vega-Villasante, F., Nolasco, H., Rocha, S.,
Goytortúa, E., González, M., Camarillo, T., 1994. Digestive
enzyme activity and growth of Penaeus californiensis fed diets
containing red crab (Pleuroncodes planipes) meal as a protein
source. Book of Abstracts, Conference World Aquaculture Society,
12-18 January 1994, New Orleans, LA. 106 pp.
Civera, R., Villarreal, H., Goytortúa, E., Rocha, S., Vega, F., Nolasco,
H., Pastén, J., Camarillo, T., 1999. La langostilla (Pleuroncodes
planipes) como fuente de proteína en dietas experimentales para
camarón. In: Cruz Suárez, L.E., Ricque Marie, D., Mendoza, R.
(Eds.), Avances en Nutrición Acuícola III. Memorias del Tercer
Simposium Internacional de Nutrición Acuícola, 11-13 Noviembre 1996, Monterrey, N.L., México, pp. 325-347.
Civera, R., Goytortúa, E., Rocha, S., Nolasco, H., Vega-Villasante, F.,
Balart, E., Amador, E., Ponce, G., Colado, G., Lucero, J.,
Rodríguez, C., Solano, J., Flores-Tom, A., Monroy, J., Coral, G.,
2000. Uso de la langostilla roja Pleuroncodes planipes en la
nutrición de organismos acuáticos. In: Civera-Cerecedo, R., PérezEstrada, C.J., Ricque-Marie, D., Cruz-Suárez, L.E. (Eds.), Avances
en Nutrición Acuícola IV. Memorias del IV Simposium Internacional de Nutrición Acuícola, 15-18 Noviembre 1998, La Paz,
B.C.S., México, pp. 349-365.
Condrey, R.E., Gosselink, J.G., Bennett, H.J., 1972. Comparison of
the assimilation of different diets by Penaeus setiferus and P.
aztecus. Fish. Bull. 70, 1281-1292.
Conover, W.J., 1980. Practical Nonparametric Statistics, 2 a ed. John
Wiley & Sons, New York.
Coral-Hinostroza, G., Huberman, H., De la Lanza, G., Monroy-Ruiz,
J., 1998. Muscle pigmentation of the rainbow trout (Oncorhynchus
mykiss) fed on oil extracted pigment from the langostilla
Pleuroncodes planipes compared with two commercial sources
of astaxanthin. J. Aquat. Food Prod. Technol. 7, 31-45.
Cousin, M., 1995. Etude de l'utilization des glúcides et du rapport
proteines-energie chez deux especes de crevettes penaeides:
Penaeus vannamei et Penaeus stylirostris. PhD. Dissertation
Université de Bretagne Occidentale, Brest, France. 209 pp.
Cruz-Suárez, L.E., Ricque-Marie, D., Martínez-Vega, J.A., WescheEbeling, P., 1993. Evaluation of two shrimp by-product meals as
protein sources in diets for Penaeus vannamei. Aquaculture 115,
53-62.
Cruz-Suárez, L.E., Nieto-López, M., Ricque-Marie, D., GuajardoBarbosa, C., Scholz, U., 2004. Uso de harina de subproductos
avícolas en alimentos para L. vannamei. In: Cruz Suárez, L.E.,
Ricque Marie, D., Nieto López, M.G., Villarreal, D., Scholz, U., y
González, M. (Eds.), Avances en Nutricion Acuícola VII.
Memorias del VII Simposium Internacional de Nutrición
Acuícola, Noviembre 16-19, 2004, Hermosillo, Sonora, México,
pp. 217-236.
Cuzon, G., Guillaume, J.C., 1999. Nutrition et alimentation des
crevettes en élévages intensif et extensif. In: Guillaume, J.,
Kaushik, S., Bergot, P., Métailler, R. (Eds.), Nutrition et
Alimentation des Poisons et Crustacés. INRA Editions, Paris,
pp. 325-349.
Cuzon, G., Guillaume, J., Cahu, C., 1994. Composition, preparation
and utilization of feeds for Crustacea. Aquaculture 124, 253-267.
D'Abramo, L., Lovell, T., 1991. Aquaculture research needs for the
year 2000: fish and crustacean nutrition. World Aquac. 22, 57-62.
Davis, D.A., Arnold, C.R., 2000. Replacement of fishmeal in practical
diets for the Pacific white shrimp, Litopenaeus vannamei.
Aquaculture 185, 291-298.
Davis, A., Samocha, T.M., Bullins, R.A., Patnaik, S., Browdy, C.,
Stokes, A., Atwood, H., 2004. Practical diets for Litopenaeus
vannamei (Boone, 1931): working towards organic and/or all plant
production diets. In: Cruz Suárez, L.E., Ricque Marie, D., Nieto
López, M.G., Villarreal, D., Scholz, U., y González, M. (Eds.),
Avances en Nutricion Acuícola VII. Memorias del VII Simposium
Internacional de Nutrición Acuícola, Noviembre 16-19, 2004,
Hermosillo, Sonora, México, pp. 202-214.
El-Saidy, D.M.S.D., Gaber, M.M.A., 2002. Complete replacement of
fish meal by soybean meal with dietary L-lysine supplementation
for the nile tilapia Oreochromis niloticus (L.) fingerlings. J. World
Aquac. Soc. 33, 297-306.
Ezquerra, J.M., García-Carreño, F.L., Civera, R., Haard, N.F., 1997.
pH-stat method to predict protein digestibility in white shrimp
(Penaeus vannmei). Aquaculture 157, 249-260.
Folch, J., Lees, M., Sloane-Stanley, G.H., 1957. A simple method for
the isolation and purification of total lipid from animal tissues.
J. Biol. Chem. 226, 497-509.
Fox, C.J., Blow, P., Brown, J.H., Watson, I., 1994. The effect of
various processing methods on the physical and biochemical
properties of shrimp head meals and their utilization by juvenile
Penaeus monodon. Aquaculture 122, 209-226.
Harpaz, S., 1997. Enhancement of growth in juvenile freshwater
prawns, Macrobrachium rosenbergii, through the use of a chemo
attractant. Aquaculture 156, 221-227.
Hew, W., Cuzon, G., 1982. Effects of dietary lysine and arginine
levels, and their ratio, on the growth of Penaeus japonicus
juveniles. J. World Maric. Soc. 13, 154-156.
Kabat, E.A., Mayer, M.M., 1968. Métodos y procedimientos químicos
y físicos especiales usados en inmunoquímica. In: Inmunoquímica
Experimental. Ed. La Prensa Médica Mexicana. 2nd edn. México,
D.F., pp. 499-500.
Kitabayashi, K., Kurata, H., Shudo, K., Nakamura, K., Ishikawa, S.,
1971. Studies of formula feed for kuruma prawn: I. On the
relationship among glucosamine, phosphorus and calcium. Bull.
Tokai Reg. Fish. Res. Lab. 65, 91-107.
Lee, P.G., Lawrence, A.L., 1997. Digestibility. In: D'Abramo, L.R.,
Conklin, D.E., Akiyama, D.M. (Eds.), Crustacean Nutrition. Adv.
World Aquacult., vol. 6. World Aquaculture Society, Baton Rouge,
LA, USA, pp. 194-260.
Lee, P.G., Meyers, S., 1997. Chemoattraction and feeding stimulation.
In: D'Abramo, L.R., Conklin, D.E., Akiyama, D.M. (Eds.),
Crustacean Nutrition. Adv. World Aquacult., vol. 6. World
Aquaculture Society, Baton Rouge, LA, USA, pp. 292-352.
Lim, C., Beames, R.M., Eales, J.G., Prendergast, A.F., McLeese, J.M.,
Shearer, K.D., Higgs, D.A., 1997. Nutritive values of low and high
fiber canola meals for shrimp (Penaeus vannamei). Aquac. Nutr. 3,
269-279.
Mazid, M.A., Zaher, M., Begum, N.N., Ali, M.Z., Nahar, F., 1997.
Formulation of cost-effective feeds from locally available
ingredients for carp polyculture system for increased production.
Aquaculture 151, 71-78.
Martinez-Cordoba, L.R., Campaña-Torres, A., Porchas-Cornejo, M.A.,
2003. Dietary protein level and natural food management in the
culture of blue (Litopenaeus stylirostris) and white shrimp
(Litopenaeus vannamei) in microcosms. Aquac. Nutr. 9, 155-160.
Merican, Z.O., Shim, K.F., 1995. Apparent digestibility of lipid and
fatty acids in residual lipids of meals by adult Penaeus monodon.
Aquaculture 133, 275-286.
Montemayor, J., Mendoza, R., Aguilera, C., Rodríguez, G., Lora, C.,
Civera, R., Magallón, F., 1998. Utilización de atractantes
alimenticios en dietas formuladas para crustáceos de interés
comercial. Memorias del IV Simposium Internacional de Nutrición
Acuícola, 15-18 Noviembre 1998, La Paz, B.C.S., México.
Olvera-Novoa, M.A., Olivera-Castillo, L., 2000. Potencialidad del uso
de las leguminosas como fuente proteica en alimentos para peces.
In: Civera-Cerecedo, R., Pérez-Estrada, C.J., Ricque-Marie, D., y
Cruz-Suárez, L.E. (Eds.), Avances en Nutrición Acuícola IV.
Memorias del IV Simposium Internacional de Nutrición Acuícola,
Noviembre 15-18, 1998, La Paz, B.C.S., México, pp. 327-348.
Ott, L., 1992. Analyzing data: analysis of variance methos, An
Introduction to Statistical Methods and Data Analysis, 4th. ed.
Doxbury Press, Belmot California, pp. 767-1038.
Pierce, R.W., Van der Veen, J., Olcott, H.S., 1969. Proximate and lipid
analyses of krill (Euphasia species) and red crab (Pleuroncodes
planipes). J. Agric. Food Chem. 17, 367-369.
Rosas, C., Cuzon, G., Gaxiola, G., Pascual, C., Brito, R., Chimal, M.,
Van Wormhoudt, A., 2000. El Metabolismo de los carbohidratos
de Litopenaeus setiferus, L. vannamei y L. stylirostris. In: CruzSuárez, L.E., Ricque-Marie, D., Tapia-Salazar, M., Olvera-Novoa,
M.A., Civera-Cerecedo, R. (Eds.), Avances en Nutrición Acuícola
V. Memorias del V Simposium Internacional de Nutrición
Acuícola, 19-22 Noviembre 2000, Mérida, Yucatán, México,
pp. 340-359.
Shiau, S.Y., 1997. Carbohydrates and fiber. In: D'Abramo, L.R.,
Conklin, D.E., Akiyama, D.M. (Eds.), Crustacean Nutrition. Adv.
World Aquacult., vol. 6. World Aquaculture Society, Baton Rouge,
LA, USA, pp. 108-122.
Sokal, R.R., 1995. Assumption of analysis of variance, In: Sokal, R.R.,
Rohlf, F.J. (Eds.), Biometry. The Principles and Practice of
Statistic in Biological Research, Third edition. W.H. Freeman and
Company, New York, pp. 392-450.
Sudaryono, A., Hoxey, M., Kailis, G., Evans, L., 1995. Investigation
of alternative protein sources in practical diets for juvenile shrimp
Penaeus monodon. Aquaculture 134, 313-323.
Sudaryono, A., Tsventnenko, E., Evans, L.H., 1996. Digestibility
studies on fisheries by-product based diets for Penaeus monodon.
Aquaculture 143, 331-340.
Spinelli, J., Mahnken, C., 1978. Carotenoid deposition in pen-reared
salmonids fed diets containing oil extracts of red crab
(Pleuroncodes planipes). Aquaculture 13, 213-223.
Tacon, A., 1989. Nutrición y alimentación de peces y camarones
cultivados. Manual de Capacitación. Proyecto AQUILA II.
Documento de Campo No. 4, GCP/RLA/102/ITA. Programa
Cooperativo Gubernamental FAO-Italia. 572 pp.
Tacon, A.G.J., Forster, I.P., 2000. Trends and challenges to aquaculture
and aquafeed development in the new millennium. In: CruzSuárez, L.E., Ricque-Marie, D., Tapia-Salazar, M., Olvera-Novoa,
M., Civera-Cerecedo, R. (Eds.), Avances en Nutrición Acuícola V.
Memorias del Quinto Symposium Internacional de Nutrición
Acuícola, 19-22 Noviembre 2000, Mérida, Yucatán, México,
pp. 1-12.
Tacon, A.G.J., Dominy, W.G., Pruder, G.D., 2000. Tendencias y retos
globales de los alimentos para el camarón. In: Civera-Cerecedo, R.,
Pérez-Estrada, C.J., Ricque-Marie, D., Cruz-Suárez, L.E. (Eds.),
Avances en Nutrición Acuícola IV. Memorias del IV Simposium
Internacional de Nutrición Acuícola, 15-18 Noviembre 1998, La
Paz, B.C.S., México, pp. 1-27.
Tan, B., Mai, K., Zheng, S., Zhou, Q., Liu, L., Yu, Y., 2005.
Replacement of fish meal by meat and bone meal in practical diets
for the white shrimp Litopenaeus vannamei (Boone). Aquac. Res.
26, 439-444.
Van der Veen, J., Medwodowski, B., Olcott, H.S., 1971. The lipids of
krill (Euphasia species) and red crab (Pleuroncodes planipes).
Lipids 6, 481-485.
Van Olst, J.C., Ford, R.F., Carlberg, J.M., Dorband, W.R., 1976. Use of
thermal effluent in culturing the American lobster. Proceedings of
the Power Plant Heat Waste Utilization in Aquaculture-Workshop
I, 6-7 November, 1975, Newark, N.J., pp. 71-97.
Villarreal, H., Civera, R., Pastén, J., Vega, F., Rocha, S., Goytortúa, E.,
1994. Effect of the partial and total substitution of shrimp meal,
fish meal and soy meal for red crab (Pleuroncodes planipes) meal
in the growth of juvenile white shrimp Penaeus vannamei. Book of
Abstracts. Conference World Aquaculture Society, 12-18 January
1994, New Orleans, LA. 106 pp.
Villarreal, H., Hernandez-Llamas, A., Rivera, M.C., Millan, A.,
Rocha, S., 2004. Effect of substitution of shrimp meal, fish meal
and soy meal with red crab Pleuroncodes planipes (Stimpson)
meal in pelleted diets for postlarvae and juvenile Farfantepenaeus
californiensis (Holmes). Aquac. Res. 35, 178-183.
Wilkie, W.D., 1972. The carotenoid pigmentation of Pleuroncodes
planipes Stimpson (Crustacea: Decapoda: Galatheidae). Comp.
Biochem. Physiol. 42B, 731-734.
Yu, Y., 2004. Replacement of fishmeal with poultry byproduct meal
and meat and bone meal in shrimp, tilapia and trout diets. In: Cruz
Suárez, L.E., Ricque Marie, D., Nieto López, M.G., Villarreal, D.,
Scholz, U., y González, M. (Eds.), Avances en Nutricion Acuícola
VII. Memorias del VII Simposium Internacional de Nutrición
Acuícola, Noviembre 16-19, 2004, Hermosillo, Sonora, México,
pp. 183-201.