Inclusion of Anastrepha ludens fruit y pupae in poultry rations added with digestive enzymes

and yeast

Inclusión de pupas de mosca de la fruta Anastrepha ludens en raciones para aves adicionadas con

enzimas digestivas y levadura

Inclusão de pupas de mosca-das-frutas Anastrepha ludens em rações avícolas com adição de enzimas

digestivas e levedura

José Alfonso López-García

Julieta Grajales-Conesa

Víctor Jesús Albores-Flores

Rodolfo Torres de los Santos

Luis Alejandro Ramón-Javier

Liliana Carolina Cordova-Albores

Rev. Fac. Agron. (LUZ). 2022, 39(1): e223903

ISSN 2477-9407

DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v39.n1.03

Animal Production

Associate editor: Ing. Agr. MSc. Juan Vergara

Instituto de Biociencias. Universidad Autónoma de Chiapas.

Boulevard Príncipe Akishino s/n. Col. Solidaridad 2000.

Tapachula, 30798, Chiapas, México. Tel. y fax. 52 962 622 5723

Universidad Autónoma De Tamaulipas. Unidad Académica

Multidisciplinaria Mante. Blvd Enrique Cárdenas González

# 1201 PTE. Col.. Jardín CP 89840 Ciudad Mante, Tamps.

Escuela de Agronomía. Universidad de La Salle Bajío. Av.

Universidad 602, Col. Lomas del Campestre. C. P. 37150.

León Guanajuato, México.

Received: 20-10-2020

Accepted: 20-09-2021

Published: 16-12-2021

Abstract

In Mexico, poultry meat represents 24,8 % of the protein consumed. In

the search for protein sources that meet this demand, the use of insects has

been found to be of potential interest. In order to reduce the effect of the

components that affect the absorption of nutrients, additives such as digestive

enzymes and microorganisms have been used. The objective of this study

was to determine the weight gain of birds (Gallus gallus domesticus) fed with

diets formulated with fruit y pupa (Anastrepha ludens), digestive enzymes

and yeast (Saccharomyces cerevisiae). Groups were established completely

at random with different inclusions of y pupae 0 %, 12 %, 14 % and 16 %

respectively and signicant differences were found (p<0.05). The group with

14 % protein was the one with the greatest weight gain during the experiment

and the second phase used digestive enzymes and Saccharomyces cerevisiae

and it was found that treatment 3: 14 % of Anastrepha ludens pupa + 200 IU

of Protease + 1502 IU of Amylase + 80 IU of Cellulase + 62 IU of Lipase

+ 40 IU of Pectinase + 8.88x109 CFU S. cerevisiae / 100 g of feed showed

differences (p<0.05) and the best results in the weight gain of the birds. It is

concluded that inclusion of 14 % of y pupa in rations promotes the weight

gain of Gallus gallus domesticus with the addition of digestive enzymes and

S. cerevisiae.

Keywords:

Food

Probiotics

Proteases

Protein by-products

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Resumen

En México la carne de aves representa el 24,8 % de la proteina

consumida. En la búsqueda de fuentes proteicas que cubran esa

demanda se han encontrado con interés potencial la utilización de

insectos. Con la nalidad de reducir el efecto de los componentes

que afectan la absorción de nutrientes se han utilizado aditivos como

enzimas digestivas y microorganismos. El objetivo del presente

estudio fue determinar la ganancia de peso de aves (Gallus gallus

domesticus) alimentadas con dietas formuladas con pupa de mosca

de la fruta (Anastrepha ludens), enzimas digestivas y levadura

(Saccharomyces cerevisiae). Se establecieron grupos completamente

al azar con diferentes inclusiones de pupa de mosca 0 %, 12 %, 14

% y 16 % respectivamente y se encontraron diferencias signicativas

(p<0,05). El grupo con 14 % de proteína fue el que mayor ganancia

de peso tuvo durante el experimento y la segunda fase se utilizaron

enzimas digestivas y S. cerevisiae y se encontró que el tratamiento 3:

14 % de pupa de Anastrepha ludens+ 200 UI de Proteasa+1502 UI de

Amilasa+ 80 UI de Celulasa+ 62 UI de Lipasa+ 40 UI de Pectinasa+

8,88x10

UFC S. cerevisiae / 100 g de alimento mostró diferencias

(p<0,05) y los mejores resultados en la ganancia de peso de las aves.

Se concluye que la inclusión de 14 % de pupa de mosca en raciones

promueve para ganancia de peso de Gallus gallus domesticus con la

adición de enzimas digestivas y S. cerevisiae.

Palabras clave: Alimentación, probióticos, proteasas, subproductos

proteicos.

Resumo

No México, a carne de frango representa 24,8 % da proteína

consumida. Na busca por fontes proteicas que atendam a essa demanda,

o uso de insetos tem se mostrado de potencial interesse. Para reduzir o

efeito dos componentes que afetam a absorção de nutrientes, aditivos

como enzimas digestivas e microrganismos têm sido utilizados. O

objetivo deste trabalho foi determinar o ganho de peso de aves (Gallus

gallus domesticus) alimentadas com dietas formuladas com pupa de

mosca-das-frutas (Anastrepha ludens), enzimas digestivas e levedura

(Saccharomyces cerevisiae). Os grupos foram estabelecidos de forma

completamente aleatória com diferentes inclusões de pupas de mosca

0 %, 12 %, 14 % e 16 %, respetivamente, e diferenças signicativas

foram encontradas (p<0,05). O grupo com 14 % de proteína foi

o que apresentou maior ganho de peso durante o experimento e a

segunda fase utilizou enzimas digestivas e Saccharomyces cerevisiae

e vericou-se que o tratamento 3: 14 % de Anastrepha ludens pupa +

200 UI de Protease + 1502 UI de Amilase + 80 UI de Celulase + 62 UI

de Lipase + 40 UI de Pectinase + 8,88x109 UFC de S. cerevisiae / 100

g de ração apresentaram diferenças (p<0,05) e os melhores resultados

no ganho de peso das aves. Conclui-se que a inclusão de 14 % de

pupa de mosca nas rações promove o ganho de peso de Gallus gallus

domesticus com a adição de enzimas digestivas e S. cerevisiae.

Palavras-chave: Alimentos, probáticos, protéases, subprodutos de

proteínas.

Introduction

The poultry industry is one of the most important livestock

activities in Latin American countries (FAO, 2015). In Mexico, it

participates with 24.8 % of animal protein consumed (UNA, 2015;

SAGARPA, 2015); particularly in rural areas, backyard poultry

farming is the main source of animal protein (egg and meat) for

human consumption (SAGARPA, 2007; SEDESOL, 2010).

In commercial poultry farming, soybean meal, meat and sh are

the primary sources of protein (FAO, 2013), however, in backyard

conditions, the feeding is made, primarily, based on grains (corn,

sorghum) which on many occasions, do not cover the protein needs of

the birds (Medina, 2012). Such deciency limits the productive and

reproductive levels (Sánchez, 2013). In addition, since corn is the base

of the Mexican diet, a food competition is established for the same

input (SAGARPA, 2015; USDA, 2015). On the other hand, cereal-

based poultry rations contain non-starch polysaccharides (NAP)

such as cellulose and hemicellulose, which affect the absorption of

nutrients, causing deciencies in animal nutrition and development

(Choct et al., 2010).

In the search for alternative sources of protein useful for animal

feed and available in the environment, a large number of research

works have been carried out (SEDESOL, 2010; FAO, 2015). In this

sense, due to the quantity and quality of protein that insects have

(Veldkamp et al., 2012; Sancho et al., 2015), they can be an alternative

for feeding birds, with the advantage that birds naturally ingest adult

insects, larvae, and pupae (Hwangbo et al., 2009). These contain

amounts of protein and fat comparable with commercial protein meal

(Barroso et al., 2014; Józeak and Engberg, 2015), in addition, that

the composition of chitin (exoskeleton) has been found to favor the

immune response, the growth of benecial bacteria and inhibits the

growth of pathogenic microorganisms (Van Huis et al., 2013).

Likewise, the use of biological additives (microorganisms and

enzymes) in the animal diet improves the availability of nutrients

(Kiarie, 2013), within these there are yeasts, mainly Saccharomyces

cerevisiae that has been used in different species such as bovines,

pigs and poultry as an inhibitor of pathogens such as Salmonella sp.,

digestion enhancers, promoting the action of digestive enzymes and

stimulating immunity (Ogbuewu et al., 2018). Likewise, they favor

an increase in the size and number of intestinal villi, and maintain a

better state of immunocompentence and prevent colonization of the

intestine by Salmonella sp. (Hassanein and Soliman, 2010; Adebiyi et

al., 2012, Kiros, et al., 2019).

For their part, exogenous enzymes help to hydrolyze molecules

facilitating the digestion of food and producing a better development

by birds (Bedford and Patridge, 2001; Méndez et al., 2009). Enzymes

can be classied according to polygastric or monogastric species and

in the latter case it is where the catalytic biomolecules that normally

cannot be metabolized by birds, although due to their microbiota,

have been used recently. They promote better digestion, improve

intestinal transit and modify the consistency of the stool allowing

greater digestibility of the nutrients. It has also been found that in

young birds these enzymes promote a better productive performance

of the same (Mulisa, 2017). Therefore, the objective of this work

was to determine the weight gain of birds (Gallus gallus domesticus)

fed with diets formulated with fruit y pupa (Anastrepha ludens),

digestive enzymes and yeast (S. cerevisiae).

Materials and methods

The work was carried out at the “Ayol” agroecological farm

(14º49’45 ”N, 92º17’47” W) located in Tapachula, Chiapas and in the

researchLlaboratorio de Investigación del Instituto de Biociencias de

la Universidad Autónoma de Chiapas (UNACH).

2-6

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López-García et al. Rev. Fac. Agron. (LUZ). 2022, 39(1): e223903

The experiment was carried out in two phases. Phase 1: To

determine the effect of the y pupa (A. ludens) and biological

additives (digestive enzymes and S. cerevisiae) on the development

of Gallus gallus domesticus fed with isoprotein rations designed for

this purpose, the following experiment was established: Isoprotein

rations were designed according to the nutritional requirements of the

birds (NRC, 1994) with A. ludens pupa as a non-conventional protein

source. The rations were made with corn, commercial kernel and y

pupa, whose proximal chemical content was analyzed by quantifying

crude protein, crude fat, acid detergent ber, moisture, ash and

nitrogen-free extract (NMX-f-083- 1986, NMX-f-066-s-1978, NMX-

f-089-s-1978, NOM-F-68-S-1980, NOM-F-90-S-1978.) (table 1).

Table 1. Proximal chemical analysis of ingredients (g.100g

-1

Determination Maice Fly pupa Core

Crude protein 8.9 ± 0.1 49.21 ± 0.3 19.78 ± 0.17

Crude fat 2.40 ± 0.21 1.48 ± 0.38 2.74 ± 0.1

Fiber 4.49 ± 0.37 0.0025 ± 0.005 4.94 ± 0.12

Ash 0.87 ± 0.14 8.53 ± 0.27 5.6 ± 0.16

NFE

83.27 ± 0.2 40.85 ± 0.24 66.92 ± 0.13

Values on a dry basis. 1Nitrogen-free extract

To evaluate the weight gain of the birds fed these rations, 100

male individuals were assigned to treatments in 4 groups of birds of

the Sussex line of one month of age and an average weight of 415 ±

0.1 g with 25 individuals each. In a group in a completely randomized

design with 4 repetitions (one bird as an experimental unit and 24

more birds as a repetition), the weight gain and mortality rate were

measured for a period of 30 days.

Table 2. Ingredients and nutritional composition in the nal stage

rations.

Ingredients % Control

treatment

Treatment

Fly pupa 0 12 14 16

Maice 64 68 74 79

Core 36 20 12 7

Valor nutricional calculado

Protein 14.43 14.43 14.36 14.30

Fat 2.38 2.14 2.09 2.06

Fiber 4.34 3.67 3.55 3.44

Humedity 9.18 9.44 9.48 9.53

Ash 3.55 2.48 2.27 2.07

Energy

(J) 1,106.58 1,135.37 1,141.89 1,148.09

Energy in joules.100 g

-1

of feed

Management: The birds were previously adapted to the rations

with the gradual inclusion of the diet and immunized against enzootic

diseases of the region (Pasteurellosis and Newcastle).

The rst phase of the experiment concluded with the identication

of the ration that promoted the greatest weight gain in the birds

(p<0.05) (table 3). This made it possible to know the degree of

inclusion of the alternative protein source in isoprotein rations in

order to design in a second phase rations with pupae of A. ludens

added with different proportions of a biological additive: Protease

225 IU, Amylase 1690 IU, Cellulase 90 IU, Lipase 70 IU, Pectinase

45 IU; S. cerevisiae 1.0x1010 CFU per g of additive, and the weight

gain and mortality rate were evaluated with a completely randomized

design and 4x2 factorial arrangement (treatment and sex): T0: ration

without biological additive, T1: 0.044 %; T2: 0.066 %; T3: 0.088

%, according to the nutritional requirements (table 4) of the birds

during 69 days. For this, 80 female and male birds (Gallus gallus

domesticus) one week old and an average weight of 94 ± 0.7 g were

used, randomly distributed and included in each treatment (1 bird as

an experimental unit and 19 birds as a repetition).

The statistical analysis consisted for the rst and second phases of

the experiment in an analysis of variance to determine the differences

between the means of the treatments and a contrast of means by

Tukey to identify the different treatment (s) with a condence of 95

% (p<0.05) with the statistical software Statgraphics Centurion XVI

MR.

Results and discussion

The proximal chemical composition of the unconventional

protein source (A. ludens) used for the preparation of isoprotein

rations is shown in table 3. The proximal chemical composition of

a wide variety of insects has been described in advance (Kouřimská

and Adámková , 2016; Oonincx and Finke, 2020), but not the pupa

of A. ludens, which so far lacks studies that describe its nutritional

content. Pretorius (2011) found that the nutritional content of Musca

domestica pupa is close to 60 % protein, which is higher than that

found in the present work. On the other hand, Rumpold and Schlüter

(2013), determined the nutritional composition of more than 200

insects and found that those of the order Diptera have a percentage

range of 49.48 ± 13.61 of protein, lower in the reported ber content

13.56 ± 3.81 and fat 22.75 ± 10.86; noting that A. ludens is a potential

protein source to be used in domestic animal feed.

3-6|

The weight gain of the birds between the treatments was different

(P≤0.05) with the inclusion of 12 %, 14 % and 16 % of pupa in the

diet and the control group (table 4).

The highest weight gain of the birds was obtained by including 14

% of A. ludens pupae in the diet with a mean gain of 857.30 ± 112.54

g during the evaluation period and a zero mortality rate.

Pretorius (2011) determined that with an inclusion of 10 % of

Musca domestica in a conventional diet for birds, the best results are

obtained in weight gain and efciency in feed conversion, although

the range extends to 25 % with favorable results. The inclusion of

insects in the diet improved weight gain since according to Hwangbo

et al. (2009) provides a positive effect due to their digestibility and

nutritional value. According to De Marco et al. (2015) and Schiavone

et al

. (2017) the our of Tenebrio molitor and Hemetia illucens

respectively, are valuable sources of metabolizable energy and

digestible amino acids that birds can take advantage of together with

their rapid digestive process. Bovera et al. (2016) used our from

Tenebrio molitor in the larval stage and found that chickens develop

better when insects are included as a source of protein, similar to this

study. The source of ber, the type and age of the birds inuence the

response of the birds to their diet (González et al. 2010; Oonincx and

Finke, 2020).

The treatments evaluated with the inclusion of biological

additives such as enzymes and yeasts in the diet prepared with 14 %

of A. ludens (table 3) were different (P≤0.05). The treatment 3 with

biological additive (200 IU of Proteases, 1502 IU of Amylases, 80

IU of Cellulase, 62 IU of Lipase, 40 IU of Pectinase, 8.88x109 CFU

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Rev. Fac. Agron. (LUZ). 2022, 39(1): e223903. January - March. ISSN 2477-9407.

4-6|

Table 3. Nutritional composition of the rations (g100g



) with the biological additive

Nutrient Star Development End T1 T2 T3

Protein 20.1 17 14.36

Fat 2.27 2.19 2.09

Fiber 3.80 3.67 3.55

Moisture 9.19 9.35 9.48

Ash 4.77 3.44 2.27

AME

(J) 1,001.98 1,076.96 1,141.89

Enzymes

Protease

Amylase

Cellulase

Lipase

Pectinase

100

751

150

1,127

200

1,502

S. cerevisiae (CFU)

4,44x10

6,66x10

8,88x10

AME. apparent metabolizable energy (Joules).

Units of digestive enzymes.

Colony-forming unit according to the Alka Rumen NRV commercial product information,

NORVET

laboratories.

of S. cerevisiae) had the greatest positive effect on the weight gain

of birds, with an average of 1,902.09 g with respect to the control

group that had 1,699.99 g of gain and the males had a signicantly

greater gain than that of the females (P≤0.05) (table 5). However,

the interaction between the additive and sex did not show differences

(table 6 and 7), although Hristakieva et al. (2014) mention

that the

sex of the birds is decisive in their development as the males have a

higher metabolic rate. For their part, enzymes and yeasts improved

the digestibility of nutrients through hydrolytic processes, which

birds are

not capable of digesting (Carvajal and Oviedo, 2014),

for example: non-starch polysaccharides (PNA) contained in corn.

According to Choct et al. (2010), the use of enzymes for poultry

neutralizes its effects in cereals, which are not desirable since they

increase viscosity, reduce the digestion and absorption of all the

nutrients in the diet, especially fat and protein.

On the other hand, Hajati (2010); Khan (2011); Kiarie et al.

(2013), found that enzyme complexes promote weight gain and

carcass performance, by improving the nutritional value and

digestibility of poultry rations, that transform them into low

molecular weight products that can pass directly through the

intestinal mucosa or are absorbed; furthermore, Cho et al. (2012)

observed that enzymes counteract the negative effects caused by the

decrease in the concentration of nutrients.

Table 4. ANOVA Weight gain of birds with isoprotein rations.

Groups Weight gain (g)

Witness 757.67 ± 125.93

T1 524.00 ± 71.06

T2 857.33 ± 112.54

T3 653.33 ± 140.79

a, b, c

Different literals mean signicant differences (p <0.05).

Table 5. Phase two Experiment Weight gain of birds with

biological additive (Saccharomyces serevisae +

digestive enzymes) in the diet.

Source P-Value Tukey Mean value

A: Treatment

0.0471 T3 1,902.09

T2 1,777.12

T1 1,731.61

Witness 1,699.99

B: Sex

0.0000 Male 1,932.92

Female 1,622.48

0.6078

No mortality was recorded during the biological additive

inclusion phase (Saccharomyces serevisae + digestive enzymes),

according to Guida et al. (2015) S. serevisae has a probiotic function

in birds, since they observed that it can agglutinate pathogenic

bacterial strains in vitro. This, attributed to the fact that naturally its

wall formed by important natural growth promoters (β 1-3 glucan

and mannan-proteins) are capable of inhibiting the colonization

by pathogens of the digestive tract and adsorb mycotoxins

(Zhang and Wang, 2008, Ogbuewu et al. ., 2018). Shareef and Al-

Dabbagh (2009) found that including up to 2 % of Saccharomyces

in the diet was enough to achieve a competitive response in the

production and mortality parameters, which coincides with that

reported by Elghandour et al. (2019) who reported the use of yeast

as a probiotic. The use of this yeast in the diet is directly related

to the weight gain of the birds, it improves the intestinal mucosa,

increases the intestinal villi, thereby increasing the activity of the

enzymes secreted by the villi and absorption of nutrients (Arce et

al., 2008); however, the development of birds will be affected if the

availability of nutrients is correct, Adebiyi et al. (2012) found no

differences in the weight of broilers using 1 %, 1.25 % and 1.5 %

This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.

López-García et al. Rev. Fac. Agron. (LUZ). 2022, 39(1): e223903

5-6|

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Ogbuewu I. P,

Okoro, V. M, Mbajiorgu, E. F, y Mbajiorgu, C. A (2018). Yeast

(Saccharomyces cerevisiae) and its effect on production indices of

livestock and poultry—a review. Comparative Clinical pathology. PP

1-9: https://doi.org/10.1007/s00580-018-2862-7

yeast, although they presented morphological differences such as

villus elongation, crypt depth and crypt gland area. in accordance

with that described by Reyes et al. (2014) who observed that lower

cell wall concentrations than 0.1 %, allows better development of

organs in birds, increasing the absorption response.

Mortality of up to 6 % (Elghandour et al., In 2019) has been

reported in poultry fattening, although the parameters indicate

that it should be less than 3 %. In the present work, the mortality

rate was 0 % with the use of a biological additive that contained

Saccharomyces serevisae + digestive enzymes in agreement with

the previous author who mentions said yeast as a probiotic and

improves the results.

Conclusion

The use of y pupae (Anastrepha ludens) and biological

additives (Proteases, Lipases, Cellulases, Pectinases, Amylases and

Saccharomyces cerevisiae) in rations for poultry (Gallus gallus

domesticus), promotes greater weight gain.

Mortality is not inuenced by the use of the biological additives

used in the experiment.

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