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Historia del artículo: Una serie de verduras de hoja, sus concentrados de proteínas y hydrolasates están bajo evaluación como
Recibido el 20 de de octubre de el alterna- tivas a los ingredientes de proteína harina de pescado (FM) en los alimentos acuícolas. Este estudio
año 2016
evaluó las características nutricionales y la idoneidad de la sustitución de FM con los amaranto (Amaranthus
Aceptado 8 de enero de 2017
Disponible en Internet el 17 de
hybridus) concentrados de proteína de hoja (ALPC) como un ingrediente de proteína en la dieta de tilapia del
enero de 2017 Nilo (Oreochromis niloticus). Las dietas experimentales se lated formu-, donde el 100%, 75%, 50%, 40%,
20% y 0% de proteína FM fue sustituido por la proteína de ALPC. Los seis tratamientos dietéticos se
palabras clave: analizaron por triplicado en los tanques de OW-a través de fl estáticas. Los efectos de sustitución se
Amaranto compararon en términos de rendimiento fi sh crecimiento, la utilización de nutrientes, la composición de todo
Las proteínas vegetales el cuerpo y apa- digestibilidad de los nutrientes ent. Después de 160 días de alimentación, el crec imiento,
niloticus Leaf concentrado utilización de los nutrientes y la conversión alimenticia (FCR) en alimentados con dietas de peces que
de proteína de contienen 100%, 75%, 50%, 40% y 20% FM fueron mejores (P <0,05) que los alimentados con la dieta con
Oreochromis
0% de FM. La digestibilidad de los nutrientes aparente fue alta para proteínas, lípidos y energía y diferían
Feeds
signi cativamente fi entre los tratamientos dietéticos (P <0,05). digestibilidad de la proteína en los peces fue
Los efectos de sustitución
más alta en la alimentación formulada con 100%, 75%, 50% y 40% de FM, que eran significativamente (P
<0,05) mayor que en 25% y 0% FM. digestibilidad de lípidos fue comparable para todas las dietas excepto
peces alimentados 0% FM. hidratos de carbohy- digerible y materia seca fueron similares para todos los
tratamientos dietéticos (P <0,05). Demostramos que es posible sustituir hasta un 80% de harina de pescado
con fi ALPC sin comprometer el rendimiento O. niloticus.
© 2017 Publicado por Elsevier Este es un artículo de acceso abierto bajo la licencia CC BY -NC-ND
licencia
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
http://dx.doi.org/10.1016/j.aqrep.2017.01.003
2352-5134 / © 2017 Publicado por Elsevier Este es un artículo de acceso abierto bajo la licencia CC BY-NC-ND licencia (http://creativecommons.org/licenses/by-nc-nd/4.0/).
C.C. Ngugi et al. / Aquaculture Reports 5 (2017) 62–69 63
Tabla 2
Formulación (g kg-1 peso en seco), la composición proximal (%) y contenido de energía (MJ kg -1) De las dietas experimentales.
Las dietas
experimentales
Ingredientes (g kg-1 como alimentado) FM100 FM75 FM50 FM40 FM20 FM0
2.7. Análisis del desempeño del crecimiento, la ALPC pero inferior fenilalanina y triptófano. Excepto K, los
supervivencia y la utilización de nutrientes elementos principales fueron más abundantes en FM en
comparación con ALPC. Mn y Cu fueron más abundantes en la FM
El crecimiento en peso de los peces se expresó como la tasa de en comparación con ALPC. Hubo una considerable presencia de
crecimiento específico (SGR,% día-1) usando la fórmula: SGR × = factores anti nutricionales tales como fitatos, oxalatos, saponinas y
(por ejemplo-1) 100, donde g = (ln (W2)) - (ln (W1)) / (t2-t1) -1 y taninos en ALPC. Todas las dietas fueron isoprotenous (proteína
W2 y W1 son pesos en día t2 y t1, respectivamente. cruda 27,8%), con contenido en lípidos que van desde 6.1 a 7.0%.
El aumento de peso = peso medio fi sh- inicial ganancia media de El análisis de aminoácidos de las dietas experimentales (Tabla 3)
peso fi sh Peso final (%) = (Final significar sh- fi media fi peso mostró casi conformidad con los requisitos de aminoácidos de Nilo
sh inicial Tilapia (ver Santiago y Lovell, 1998), a excepción de la leucina y
peso) / (media inicial fi peso sh) FCR metionina.
= consumo de alimento / ganancia
de peso 3.2. Los resultados de crecimiento y la supervivencia
La supervivencia se determinó al final del experimento por
completa- mente drenar el tanque y contando el pescado restante La utilización crecimiento, la supervivencia y de nutrientes
en los tanques (teniendo en cuenta cualquier pez que murió global de O. niloti- cus bajo tratamientos dietéticos diferenciales se
durante el ejercicio de pesada) y el porcentaje de supervivencia muestran en la Tabla 4.Parámetros de desempeño de crecimiento se
calculado basado en el número de peces que queda en los vieron afectados por niveles de sustitución de FM con ALPC. No
tanques como un porcentaje de los peces abastecido. hay diferencias significativas fueron discernidas en el crecimiento
Supervivencia (%) = (Número de fi sh queda en el depósito / nú- en términos de SGR, aumento de peso y aumento de peso (%) de O.
mero inicial de fi sh abastecido) * 100 niloticus entre el control (FM100) y tratamientos que con- tienen
Utilización de nutrientes se determinó usando dos parámetros: la 75%, 50%, 40% y 20% FM en significa la alimentación (P> 0,05).
proteína de relación de e fi ciencia (PER) y valor productivo Del mismo modo, FCR, no mostró diferencias significativas entre
proteína (PPV,%). las dietas de control y los tratamientos que contienen 75%, 50%,
PER = (FB- IB) / Wprotf-1; Dónde: FB y IB = final e inicial sh fi 40% y 20% de FM. los tratamientos con 100% niveles de
biomasa (g); sustitución de FM con ALPC resultaron en menor peso nal fi,
PPV (%) = 100 x (Wprot2 - Wprot1) / Wprotf-1; donde Wprot1, aumento de peso y FCR. se observó más alta supervivencia fi sh en
Wprot2 son el peso inicial y final fi proteína en fi sh tanques con 100% FM, mientras que las dietas donde sustitución de
respectivamente (g) y Wprotf = peso del suministro de proteínas de FM se realizó supervivencia comparable mostró (74-77%),
la dieta por fi sh. independientemente de los niveles de sustitución de FM por ALPC.
La digestibilidad se evalúa durante el último mes del experi- consumo diario de alimento eran bajos en control, FM75, FM50
mento. Para las pruebas de digestibilidad, 5 g kg-1 óxido y FM40 pero aumentó con el aumento de pescado harina de
crómico se incluyó en las dietas experimentales. Las heces se sustitución (FM 20 y FM0). deficiencias de nutrientes utilización e
recogieron usando un fi modi fae- cal sistema de recogida de 28 fi de peces se vieron afectados por los niveles de sustitución de FM
días, 7 días a la semana, se centrifugaron (4 ◦C, 4000 rpm, 15
por ALPC (Tabla 4). Había signifi- signifi- (P <0,05) diferencias en
min), se liofilizó y se usó para analizar la AIA marcador
los parámetros de nutrientes de utilización entre las dietas de control
naturales (Acid ceniza insoluble). Aparentes coeficientes de
(FM100), FM75, FM50, FM40 y FM20en comparación con FM0.
digestibilidad coef fi (ADC) se calcularon utilizando la fórmula
Los tratamientos con niveles de 100% de sustitución de FM
como sigue:
. Σ Cr2O3 dietética% Σ con ALPC resultó en un menor PER y PPV que otros feeds.
ADC nutritiv (%) = 100 × 1 -
% Cr2O3 fecal
o 3.4. composición de la canal
Σ % faecalnutrients ΣΣ
×
nutriente alimenticio% Las composiciones de todo el cuerpo próximos de la tilapia
del Nilo al principio y al final del experimento se presentan en la
ADC de la energía bruta se calculó usando los datos de energía Tabla 5. El contenido de hume- dad en la composición de la
brutas (kJ g-1) canal y de la proteína de los peces no estaba claramente afectada
Σ ΣΣ por la composición de la dieta (P> 0,05). Una tendencia
. se destacó por el contenido de lípidos del cuerpo de la canal a
Cr2O3 dietética%
ADCmateria (%) = 100 × 1 - disminuir a mayores niveles de inclusión de ALPC. Por el contrario,
seca % Cr2O3 fecal
el contenido de cenizas corporal aumentó con el aumento de niveles
de inclusión planta en la dieta de O. niloticus. Significativamente
mayor (P <0,05) el contenido de cenizas se obtuvo en
2.9. Análisis de los datos
La composición de nutrientes de los ingredientes del pienso y
Los análisis estadísticos se realizaron utilizando GenStat dietas ex- perimental, así como su composición de aminoácidos se
(GenStat lanzamiento 4.24DE). El efecto de la sustitución sobre el presenta en tablas 1-3. ingrediente FM tenía mayor per fi l de
crecimiento, la supervivencia, FCR, la utilización de nutrientes, varios aminoácidos esenciales tales como la histidina, leucina,
composición de la canal y la digestibilidad se realizaron mediante lisina y metionina de
análisis de la varianza (ANOVA de una vía). Cuando se
distinguieron significantes diferencias, medias de los tratamientos
se compararon mediante la prueba HSD de Tukey post-hoc. En todo
el análisis anterior significantes fue aceptada en P <0,05.
3. resultados
4. Discusión
Tabla 3
Amino acid composition (g 100 g−1 dry diet) and mineral concentration of the experimental diets.
Las dietas
Esencial amino
ácido Arginina 2,2 ± 0,14 2,1 ± 0,12 1,9 ± 0,14 1,8 ± 0,12 1,8 ± 0,07 1,5 ± 0,09
Histidine0.8 ± 0.110.7 ± 0.180.7 ± 0.140.6 ± 0.110.6 ± 0.080.5 ± 0.07
Isoleucine1.4 ± 0.101.4 ± 0.221.3 ± 0.191.4 ± 0.131.4 ± 0.131.3 ± 0.17
Leucine1.9 ± 0.171.8 ± 0.211.7 ± 0.201.6 ± 0.141.6 ± 0.121.6 ± 0.11
Lysine2.8 ± 0.222.8 ± 0.162.6 ± 0.172.7 ± 0.192.5 ± 0.172.3 ± 0.19
Methionine1.4 ± 0.191.3 ± 0.141.5 ± 0.131.0 ± 0.091.2 ± 0.110.9 ± 0.09
Phenylalanine1.3 ± 0.061.4 ± 0.101.6 ± 0.131.7 ± 0.141.8 ± 0.182.3 ± 0.13
Threonine1.6 ± 0.121.5 ± 0.161.4 ± 0.131.1 ± 0.081.1 ± 0.101.0 ± 0.08
Tryptophan0.4 ± 0.080.4 ± 0.040.5 ± 0.080.4 ± 0.090.4 ± 0.080.5 ± 0.09
Valine1.3 ± 0.091.3 ± 0.071.2 ± 0.111.3 ± 0.121.2 ± 0.071.1 ± 0.11
Mineral composition
Major element
Sodium60.8 ± 8.450.9 ± 7.140.7 ± 4.137.0 ± 3.431.1 ± 3.026.6 ± 2.4
Potassium241.3 ± 22.1273.0 ± 21.2311.6 ± 28.3329.9 ± 30.9353.8 ± 30.3371.2 ± 35.2
Ca188.1 ± 19.5192.1 ± 17.9198.4 ± 17.5202.1 ± 19.9204.5 ± 18.3204.3 ± 22.2
Mg133.5 ± 15.6121.9 ± 13.2112.6 ± 10.3109.4 ± 10.399.9 ± 9.387.9 ± 8.1
P96.9 ± 10.288.7 ± 8.281.7 ± 8.278.9 ± 7.672.3 ± 7.063.8 ± 5.7
Minor elements
Fe5.6 ± 1.15.9 ± 0.86.1 ± 0.56.3 ± 1.26.4 ± 0.76.2 ± 0.6
Zn3.2 ± 0.43.7 ± 0.64.4 ± 0.44.7 ± 0.65.1 ± 0.75.2 ± 0.5
Mn7.2 ± 0.47.4 ± 1.28.0 ± 1.18.5 ± 0.68.5 ± 0.68.3 ± 0.7
Cu0.9 ± 0.50.9 ± 0.10.9 ± 0.10.9 ± 0.10.8 ± 0.10.8 ± 0.1
Table 4
Fish weight gain, specific growth rate (SGR), feed intake, feed conversion ratio (FCR), nutrient utilization, and survival of Oreochromis niloticus fed the experimental diets
for 160 days.
Diets
Initial mean fish stocking weight (g) 24.4 ± 0.3 24.7 ± 0.4 23.8 ± 0.5 23.1 ± 0.5 24.2 ± 0.9 24.7 ± 0.2
Final mean fish harvest weight (g)357.4 ± 37.3b 354.0 ± 41.2b 337.0 ± 33.5b 327.0 ± 29.5b 327.2 ± 24.9b 252.1 ± 14.5a
Mean fish weight gain (g)333.0 ± 21.3b 329.3 ± 23.4b 313.2 ± 16.9b 303.9 ± 16.9b 303.0 ± 18.2b 227.4 ± 11.3a
Weight gain (%)1364.8 ± 86.5b 1333.2 ± 82.4b 1316.0 ± 74.2b 1315.6 ± 61.7b 1252.1 ± 56.2b 920.6 ± 50.2a
SGR (g day−1)1.68 ± 0.12b 1.66 ± 0.11b 1.66 ± 0.12b 1.66 ± 0.09b 1.66 ± 0.10b 1.45 ± 0.07a
b
Survival (%)86.2 ± 5.1b 74.3 ± 5.6a 76.5a ± 4.6a 76.5a ± 5.5a 77.0a ± 4.9a 76.0a ± 5.1a
Daily feed intake (g day−1)9.38 ± 0.61a 8.90 ± 0.58a 9.64 ± 0.60a 9.64 ± 0.55a 10.61 ± 0.62b 11.95 ± 0.67c
FCR1.06 ± 0.07a 1.07 ± 0.09a 1.17 ± 0.08a 1.17 ± 0.07a 1.15 ± 0.08a 2.15c ± 0.09b
PER2.73 ± 0.34b 2.81 ± 0.32b 2.84 ± 0.33b 2.84 ± 0.29b 2.74b ± 0.31b 2.17 ± 0.17a
PPV17.32 ± 2.14 b 16.80 ± 2.23b 16.71 ± 2.01b 16.79 ± 2.45b 16.22 ± 2.67b 8.44a ± 2.11a
1
Means in the same row with the different letters as superscripts are significantly different (P < 0.05).
2
PER: Protein Efficiency Ratio.
3
PPV: Productive Protein Value.
Table 5
Whole body composition (% wet weight) of Oreochromis niloticus fed the experimental diets.
Diets ANOVA
Moisture content 78.9 ± 8.2 82.1 ± 10.2 82.1 ± 8.4 79.1 ± 7.2 82.8 ± 8.9 79.2 ± 9.4 0.4322
Crude protein17.5 ± 2.117.4 ± 1.717.3 ± 1.517.1 ± 1.316.9 ± 1.916.5 ± 2.30.1439
Crude lipid7.7 ± 0.7c 7.8 ± 0.5c 6.5 ± 0.4b 6.6 ± 0.3b 5.5 ± 0.6a 5.2 ± 0.5a 0.0031
Ash content3.2 ± 0.2a 3.3 ± 0.2a 3.6 ± 0.3a,b 3.9 ± 0.4b 3.9 ± 0.4b 4.8 ± 0.5c 0.0042
1
Means in the same row with the different letters as superscripts are significantly different (P < 0.05). Values are mean ± SE (n = 30 fish/treatment).
ALPC in the diet of O. niloticus formulated to contain 28% protein, in Senegalese sole (Cabral et al., 2013). Although the
without compromising fish growth performance and nutrient uti- performance of fish in present study is in agreement with those
lization. Previously, plant proteins replaced up to 75% FM without of Fontaínhas- Fernandes et al. (1999), there are differences in
impairing feed intake, growth performance and protein utilization the substitution levels of plant proteins that optimize growth
performance in O.
70 C.C. Ngugi et al. / Aquaculture Reports 5 (2017) 62–69
Table 6
Apparent digestibility coefficients (ADCs) of experimental diet containing different replacements levels of fishmeal by amaranth protein concentrate.
Dry matter (%) 73.3 ± 8.8 75.3 ± 9.9 73.5 ± 11.4 76.1 ± 9.4 75.2 ± 8.8 74.9 ± 8.3 0.6831
Protein (%)92.4 ± 2.7c 93.1 ± 3.3c 94.3 ± 4.2c 93.7 ± 5.2c 88.1 ± 4.5b 84.2 ± 4.0a 0.0000
Lipids (%)89.4 ± 5.1b 91.3 ± 4.7b 92.1 ± 5.6b 90.1 ± 2.4b 91.7 ± 3.5b 83.2 ± 4.6a 0.0142
Energy (%)82.1 ± 4.683.2 ± 5.181.9 ± 4.481.3 ± 5.782.4 ± 4.878.5 ± 5.40.6541
Means in the same row with the different letters as superscripts are significantly different (P < 0.05).
niloticus in comparison to O. mossambicus. These findings are Results on the proximate composition of the carcass indicate that
simi- lar to those which demonstrate that growth of Nile tilapia was incorporation of A. cruentus did not affect the moisture and pro-
not depressed when 20–30% dietary soybean meal was replaced tein content of the fish. However, lipid content in the fish reduced
with Azolla africana (Fasakin et al., 2001), roquette seed meal while ash content of the final flesh increased. Earlier studies, in Nile
(Soliman, 2000), Cassia fistula meal (Adebayo et al., 2004), tilapia, have also shown a decrease in carcass lipid following feed-
pigeon pea, Cajanus cajan (Obasa et al., 2006) or Ulva meal (Azaza ing diets in which FM was replaced by other plant protein sources
et al., 2008). The observed growth performance comparable to such as Cassia fistula meal (Adebayo et al., 2004); Roquette seed,
control diet at FM substitution levels of 25% (FM75), 50% (FM50), Eruca sativa (Fagbenro, 2004) and green algae Ulva rigida (Azaza et
60% (FM40) and 80% (FM20) may be due to the high protein al., 2008), possibly reflecting a reduction in lipid deposition. The
content in ALPC, presence of essential amino acids, gamma linolic decrease in the content of lipid in fish carcass corresponds to
acid, þ-caroteine and pig- ments, in addition to variable quantities decreased lipid content in the diet (Table 2) as a result of inclusion
of vitamins (Shukla and Singh, 2003; Molina-Poveda et al., 2015). of plant protein in the diet. This therefore seems to be related to the
The amino acid composi- tion of ALPC and FM was generally physiological ability of the fish to convert the lipids in the food into
similar, except for the content of histidine, leucine, lysine and fats.
methionine, which were all lower in ALPC and thus presumed to be The ADCs for all the experimental diets except FM0 were high
more limiting amino acid for fish growth. Methionine and lysine are (Table 6) and compares well with those reported for herring meal,
generally the limiting amino acid of many plant proteins (Jackson et menhaden meal and poultry borne meal (PBM) for rainbow trout
al., 1982) and methionine deficiency has been determined to cause (Oncorhynchus mykiss) diets (Sugiura et al., 1998) and for poultry
reduced growth (Gaber, 2006). Indeed, El-Saidy and Gaber (2003) borne meal and poultry feather meal in O. niloticus (Guimarães et
established that 100% of the FM protein could be replaced by plant al., 2012). They were higher than digestibility values of faba beans
protein mixtures (25% soybean meal, 25% cottonseed meal, 25% (Vicia faba var. minuta) in the diet of O. niloticus (Azaza et al.,
sunflower meal and 25% linseed meal) without reducing the growth 2009). They were higher than values for crude protein ADC for
rates of Nile tilapia after supplementing their diets with 0.5% poultry offal meal (Hanley, 1987). The high protein digestibility
methionine and lysine. In the present study, methionine content of values found in the present study when FM level was 100%, 75%,
the test diets decreased gradually from 1.4% in the control diet to 50% and 40% reflect good quality raw materials during feed
0.9% in the diets con- taining 0% FM. This indicates that formulation with the excel- lent amino acids profiles in the
methionine deficiency may be one of the reasons responsible for the ingredient used as protein source (Dias et al., 2005). In addition, the
lower growth performance and poorer diet utilization of fish groups high ADC crude protein values registered confirm Nile tilapia’s
fed high inclusion level of ALPC. We also established presence of ability to digest plant proteins.
appreciably high content of anti nutritional factors such as phytates, From the discussion on the nutritional quality of ALPC, it may
oxalates, saponins and tannins in ALPC. When diets containing be concluded that ALPC can replace up to 80% FM in the diet of O.
these antinutritional com- pounds are being digested, a portion of niloticus without compromising growth, nutrient utilization, whole
them remains bound to certain proteins of the diet rendering them body composition and nutrient digestibility. The reduced growth
inaccessible to diges- tive enzymes thus, reducing protein performance of fish fed diets with up to 0% FM may be related
digestibility and interfere with their bioavailability (Francis et al., to the limiting level of methionine and leucine, high antinutri-
2001). It is plausible that the anti- nutritional factors impaired the tional factors which depressed the feed intake and growth in fish at
absorption of some essential amino acid of the diets containing high levels of plant protein. This finding lends credence in the
ALPC, thus depressing fish growth at high levels of dietary ALPC continued research into areas of utilization of alternative plant pro-
inclusion. It has also been observed that phytate is the major teins sources in place of fishmeal based feeds as protein sources in
phosphorus storage compound in leafy vegetables and chelates improving aquaculture, which are increasingly becoming scarce and
multivalent metal ions such as Zn, Ca and Fe, thus affecting their whose prices continue to skyrocket on daily basis. However, the
bioavailability (Schlemmer et al., 2009) and could be responsible inability to establish further growth improvements after 80%
for reduced growth in fish at higher ALPC inclusion. The inclusions of ALPC could signal the need for further research into
combination of aforementioned anti-nutritional fac- tors could have pre-treatment of these plant species (A. hybridus) and addition of
caused a significant decrease in PER and PPV in diets with high the limiting ingredients before feed formulation.
inclusion levels of ALPC. The PER values in all treatments were
higher than 2, which indicates efficient protein utilization. The best
PER was obtained at FM replacement level of up to 80% (FM20) Acknowledgements
in the diets by ALPC. High PPV recorded in fish consuming diets
containing higher levels of FM substitution by ALPC, point to This research is a component of the AquaFish Innovation Lab,
optimal intake efficiency due to combination of ingredients derived which is supported in part by the US Agency for International
from plant proteins in presence of FM pro- tein sources. Thus the Devel- opment (USAID CA/LWA No. EPP-A-00-06-0012-00), and
efficiency in nutrient utilization between the feed treatments seemed in part by participating institutions. The AquaFish accession
to occur as a result of supplementation of energy generated due to number is 1462. The opinions expressed herein are those of the
combination of animal and plant protein sources. authors and do not necessarily reflect the views of the AquaFish
Innovation Lab or USAID
C.C. Ngugi et al. / Aquaculture Reports 5 (2017) 62–69 71
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