Rev. Peru. Investig. Agropecu. 2(2), e51
ISSN: 2955-8530
e-ISSN: 2955-831X
DOI: 10.56926/repia.v2i2.51
Universidad Nacional Autónoma de Alto Amazonas
Revisiones / Reviews
Received: 05/08/2023
Accepted: 20/10/2023
Published: 30/10/2023
*Miriam Adriana Alvan-Aguilar - malvan@iiap.gob.pe (corresponding author)
©The authors. This is an open access article, distributed
under the terms of the Creative Commons Attribution 4.0
International License
Replacement of fishmeal with
Tenebrio molitor
meal in
diets for crustaceans: Effects on growth and immune
response
Reemplazo de la harina de pescado por harina de
Tenebrio molitor
en dietas
para crustáceos: efectos en el crecimiento y la respuesta inmune
Miriam Adriana Alvan-Aguilar1,3* ; Prísila Tello-García2,3 ; Yeng Fred Chu-Ochoa1; Fred William
Chu-Koo2,3,4
1Laboratorio de Entomología, Programa de Investigaciones para el Uso y Conservación del Agua y sus Recursos –
AQUAREC, Centro de Investigaciones “Fernando Alcántara Bocanegra”, Instituto de Investigaciones de la Amazonía
Peruana – IIAP, Quistococha, Loreto, Perú.
2Escuela Profesional de Ciencias Biológicas y Acuicultura, Facultad de Ciencias. Universidad Nacional Autónoma de Alto
Amazonas, Yurimaguas, Alto Amazonas, Loreto, Perú.
3Grupo de Investigación en Sanidad, Sostenibilidad, Bioconversión y Economía Circular Acuícola – SSBECA, Universidad
Nacional Autónoma de Alto Amazonas, Yurimaguas, Alto Amazonas, Loreto, Perú.
4Grupo de Investigación en Nutrición y Genómica Nutricional de Peces Amazónicos - NUGENUPA. Universidad Nacional
Autónoma de Alto Amazonas, Yurimaguas, Alto Amazonas, Loreto, Perú.
ABSTRACT
The use of fishmeal (FM) as a protein source in aquaculture is one of the main criticisms of this industry. Increasing
production more sustainably is a current imperative for this sector. On the other hand, insect farming has become a
promising alternative for aquafeeds, since several species can be produced using organic waste. Insects are organisms rich
in nutrients, they contain high amounts of energy, and they have a balanced amino acid profile, unlike protein sources of
plant origin that are generally deficient in certain essential amino acids. The aim of the manuscript is to present a review of
recent research on the replacement of FM by
Tenebrio molitor
larvae meal (TMM), a beetle that has become popular as an
alternative in aquaculture diets, and its effects on crustaceans’ growth and immune response. Studies indicate that TMM
can completely substitute FM in
Litopenaeus vannamei
, while the substitution levels that worked best for
Macrobrachium
rosenbergii
and crayfish range from 12 to 50%. No studies were found in Amazonian crustaceans or even in South American
freshwater prawns, which opens a window of opportunities for the development of new lines of research.
Keywords: aquaculture; feeding; insects; crustacean; health
RESUMEN
El uso de harina de pescado (FM) como fuente proteica en la acuicultura es una de las principales críticas sobre esta
industria. Aumentar la producción de un modo más sostenible es un imperativo actual para este sector. Por otra parte, la
cría de insectos se ha tornado en una alternativa prometedora para la alimentación acuícola, ya que varias especies pueden
producirse usando residuos orgánicos. Los insectos son organismos ricos en nutrientes, alta energía, y un perfil equilibrado
de aminoácidos, a diferencia de las fuentes proteicas vegetales que son deficientes en ciertos aminoácidos esenciales. El
objetivo del manuscrito es presentar una revisión de las investigaciones recientes sobre la sustitución de la FM por la harina
de larvas de
Tenebrio molitor
(TMM), un coleóptero que se ha vuelto popular como alternativa en dietas acuícolas y sus
efectos en el crecimiento y la respuesta inmune en crustáceos. Los estudios indican que la TMM puede sustituir
completamente a la FM en
Litopenaeus vannamei
, mientras que los niveles de sustitución que funcionaron mejor para
Macrobrachium rosenbergii
y el cangrejo de río van desde 12 a 50%. No se encontraron estudios en crustáceos amazónicos
ni sudamericanos, lo que abre oportunidades para nuevas líneas de investigación.
Palabras clave: acuicultura; alimentación; insectos; crustáceos; salud
Citation / Cómo citar: Alvan-Aguilar, M. A., Tello-García, P., Chu-Ochoa, Y. F. & Chu-Koo, F. W. (2023). Replacement of fishmeal with
Tenebrio molitor
meal in diets for crustaceans: Effects on growth and immune response.
Revista Peruana de Investigación Agropecuaria.
2
(2), e51. https://doi.org/10.56926/repia.v2i2.51
2 Revista Peruana de Investigación Agropecuaria
Rev. Peru. Investig. Agropecu. 2(2): e51; (jul-dic, 2023). e-ISSN: 2955-831X
1. INTRODUCTION
According to statistics reported by FAO (2021), the global harvest of crustaceans reached 10.5 million
tons in 2019, totaling a sales value of approximately 276.6 billion dollars. In productive terms, the
growth rate of crustacean farming has been on average 10% annually in the last two decades, and in
2019 it represented 9% of the global aquaculture harvest (Tacon, 2020). Recent data taken from FAO
(2021) and Tacon (2020), reveals that nearly 92% of global crustacean production depends on just
six marine species, which are the following:
Litopenaeus vannamei
(5.24 million tons),
Procambarus
clarkii
(2.16 million tons),
Eriocheir sinensis
(0.78 million tons),
Penaeus monodon
(0.77 million tons),
Macrobrachium rosenbergii
(0.27 million tons), and
M. nipponense
(0.23 million tons). It is also
important to indicate that almost 90% of farmed crustaceans are yielded in Asia, with the People's
Republic of China being the nation responsible for producing half of the world's production (Costa-
Pierce & Chopin, 2021; FAO, 2021; Naylor et al., 2021).
The increasing dependence on fishmeal for the production of aquafeeds, especially for carnivorous
species such as crustaceans, has caused an excessive increase in the operating costs of aquaculture
worldwide (Dawood, 2021). This worrying situation may even worsen due to overfishing of the
resources from which fishmeal is processed, which is causing a constant decrease in the production
of this vital protein feedstuff (Dawood, 2021).
Meals made from insects have become feedstuffs that are gaining a lot of interest in recent years
due to their potential as possible protein substitutes for fishmeal (Röthig et al., 2023; Shafique et al.,
2021). This is because insects have a high content of nutrients that not only include proteins, but also
unsaturated fatty acids, vitamins, fibers, and minerals (Makkar et al., 2014; Smetana et al., 2019).
In this sense, the meal from the larvae of
Tenebrio molitor
, a species of beetle of the Tenebrionidae
family, is one of the feeds that has been intensively evaluated as an alternative source of protein in
aquaculture diets (Shafique et al., 2021). Currently, there are a good number of studies that have
evaluated the potential use of
T. molitor
larvae meal as an alternative source in practical diets for fish
(Gasco et al., 2016; Gu et al., 2022; Henry et al., 2018; Hoffmann et al., 2021; Iaconisi et al., 201 7;
Iaconisi et al., 2018; Ido et al., 2019; Jeong et al., 2020; Melenchón et al., 2021; Rema et al., 2019;
Roncarati et al., 2015; Sankian et al., 2018; Su et al., 2017), however; it has not been previously
considered as a protein source in crustacean diets, except in
L. vannamei
, on which there are some
recent pioneering studies.
The main goal of the manuscript is to present a review of recent research on the replacement of
fishmeal (FM) by
Tenebrio molitor
larvae meal (TMM), a beetle that has become popular as an
alternative feedstuff for aquaculture diets, and its effects on farmed crustaceans’ growth performance
and immune response.
2. MATERIAL AND METHODS
The information detailed in this article was obtained from an in-depth review of the scientific
literature (scientific articles, review articles, scientific notes, books, and book chapters), existing in the
databases available on the Internet. We used the following key words as search terms:
Alvan-Aguilar, M. A. et al. 3
Rev. Peru. Investig. Agropecu. 2(2): e51; (jul-dic, 2023). e-ISSN: 2955-831X
<aquaculture>, <acuicultura>, <aquicultura>, <feed>, <alimentación>, <alimentação>, <insect>,
<
Tenebrio molitor
>, <yellow mealworm>, <fishmeal>, <harina de pescado>, <farinha de peixe>,
<replacement>, <sustitución>, <substituição>, <crustacean>, <shrimp>, <prawn>, <crab>,
<crayfish>, <camarões>, <camarón>, <langostino>, and <cangrejo>.
The period analyzed was limited to the last decade (2014 to 2023). Results from dissertations, theses,
or abstracts presented at scientific conferences were not included.
The results list the names of the crustacean species in which studies have been carried out to replace
fish meal (FM) with
Tenebrio molitor
larvae meal (TMM), as well as the main details of the
methodology used and the most outstanding results of the works found.
3. REVIEW RESULTS
After reviewing the literature, we only found a total of 12 studies published on the topic of this
research. The period in which these papers were published ranges from 2017 to 2023. Eight papers
(66.67%) were carried out on the White shrimp,
Litopenaeus vannamei
, which is reasonable, since it
is the most important crustacean in the global aquaculture industry, with 5.45 million tons harvested
in 2019, representing 52% of the crustaceans produced globally (FAO, 2021). The Giant River Prawn,
Macrobrachium rosenbergii
, is another important species for aquaculture, with 272,738 tons
harvested in 2019 (FAO, 2021). The remaining three articles were studies done on other crustaceans
such as the Red Claw Crayfish,
Cherax quadricarinatus
, Narrow-Clawed Crayfish,
Pontastacus
leptodactylus
, and the Baltic Prawn,
Palaemon adspersus
, which do not have the same economic
importance as the previous species aforementioned. Table 1 shows the results obtained from the
review carried out.
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Table 1.
Crustacean species, fish meal replacement level, study duration, feeding frequency (FF), initial body weight (IBW), main results, recommended
fishmeal replacement level, and references of 12 studies published on the fish meal replacement with Tenebrio molitor meal in diets for
crustaceans: effects on growth performance and immune response
Crustacean
Species
FM
Replacement
Level
Study
Duration
FF
IBW
(g)
Main Results
Recommended
FM
Replacement
Level
References
Litopenaeus
vannamei
(White Shrimp)
0, 15, 30, 60,
and 100%
60 days
Four times a
day
7.41
There was a significant difference in BWG, FE,
FCR, and HPI among the treatments (P<0.05).
TMM30 treatment showed expressively (P<0.05)
higher BWG, FE, and HPI; and significantly
(P<0.05) inferior FCR concerning TMM0
treatment. The levels of CHOL, TG, and GLU,
showed a decreasing trend with increasing
replacement of FM with TMM and showed a
significant difference with the TMM0 at high
levels of replacement (P<0.05). Outcomes
exhibited that replacing FM with TMM had a
significant effect on the activities of SOD, PO,
LZM, ACP, AKP, and THC in the diets compared
to the TMM0 group (P<0.05).
Up to 30% FM
replacement.
Sharifinia et al.
(2023)
0, 15, 30, and
45%
66 days
Four times a
day
0.42
Dietary TMM30 significantly increased the BWG,
WGR, and SGR of shrimps (P<0.05) when
compared with TMM0. Enzyme activity of serum
AKP, CAT, SOD, proPO, and LZM differed
significantly in TMM45 compared with TMM0
(P<0.05), and MDA decreased. Intestinal trypsin
meaningfully increased in TMM45 compared
with TMM0 (P<0.05).
Between 30 to
45% FM
replacement.
Zheng et al.
(2023)
Alvan-Aguilar, M. A. et al. 5
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0 and 30%
dietary
inclusion of
TMM
28 days
Three times
a day
3.04
Results showed that the growth performance of
shrimp fed the TMM diet meaningfully
diminished compared to that fed the control
diet (P<0:05). There was no substantial
difference in FE and SR among individuals fed
both diets (P>0.05).
Li et al. (2022)
0, 25, 50, 75
and 100%
42 days
Four times a
day
4.42
The THC, PC, and PA in the hemolymph were
not meaningfully changed (P>0.05) when FM
was substituted by TMM. The AGA of
L.
vannamei
serum determined against dog
erythrocytes was higher in the shrimp group fed
TMM25. The absolute and specific activities of
trypsin, chymotrypsin, lipase, α-amylase, and
the patterns of proteolytic activities were not
affected by the dietary treatments. The
L.
vannamei
gut bacterial microbiota profile was
comparable to the genera originally noticed.
Up to 100%
FM replacement.
Ríos et al.
(2021)
0 and 10%
65 days
Four times a
day
0.17
Shrimp BWG, SGR, FCR, PER, and SR were
similar to those fed with the control diet.
Up to 10% FM
replacement.
Shin & Lee
(2021)
0, 25, 50, 75,
and 100%
56 days
To apparent
satiation
1.56
Higher FBW, BWG, and best FCR in the TMM50
group. Dietary inclusion of TMM improved the
SR when individuals were confronted with
Vibrio parahaemolyticus
. THC and proPO
activities were found meaningfully higher when
dietary TMM was included in the
L. vannamei
feeding regime, signifying that immunity and
disease resistance in shrimp were significantly
improved with TMM diets.
Up to 50% FM
replacement
Motte et al.
(2019)
0, 25, 50 and
100%
60 days
Twice daily
2.39
Higher BWG and SGR and better FCR in fish fed
the TMM50 diet. Partly replacement of FM
(50%) with TMM led to an up-regulated
expression of immune genes, including β-1, 3-
Up to 50% FM
replacement.
Choi et al.
(2018)
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glucan binding proteins (BGBP), proPO, and
crustin, which are the important genes in
promoting disease-resistant against white spot
syndrome virus (WSSV).
0, 25, 50, 75,
and 100%
42 days
Four times a
day
4.42
BWG, SGR, FI, FCR, SR, and PRR were not
affected when FM was replaced by TMM
(P>0.05). The BPC of the shrimp body showed
no significant differences (P>0.05) between the
treatments.
Up to 100%
FM replacement
Panini et al.
(2017)
Cherax
quadricarinatus
(Red Claw
Crayfish)
0, 9, 18, 27,
and 36%
60 days
N.A.
0.20
The highest BWG and lowest FCR were
observed in crayfish fed the TMM diet at 18%
FM replacement. The maximum SOD activity
and the lowermost MDA content were noticed
in the hepatopancreas of the individuals fed
TMM18
Up to 21.9% FM
replacement
Wang et al.
(2022)
Pontastacus
leptodactylus
(Narrow-Clawed
Crayfish)
0, 50, and
100%
80 days
Twice daily
0.011
Dietary replacement of FM with up to 50%
TMM had positive effects on BWG, SGR, PER,
and ANPU, in
P. leptodactylus
(P<0.05).
Up to 50% FM
replacement
Mazlum et al.
(2021)
Palaemon
adspersus
(Baltic Prawn)
0 and 30%
60 days
Twice daily
0.49
TMM30 diets yield higher protein and energy
content in the prawn muscles. No significant
differences were detected in the activities of
hepatopancreas’ amino acid-catabolizing
enzymes.
N.A.
Mastoraki et
al. (2020)
Macrobrachium
rosenbergii
(Giant River
Prawn)
0, 4, 8, 12, and
16%
dietary
inclusion of
TMM
70 days
Three times
a day
3.26
Dietary inclusion of 12% TMM protein had the
greatest effects on growth performance,
immunological parameters, and resistance
against
L. garvieae
and
A. hydrophila
.
Up to 12% FM
replacement
Feng et al.
(2019)
Legends
: FM (fish meal), TMM (
Tenebrio molitor
meal), FF (feeding frequency), IBW (initial body weight), BWG (body weight gain), WGR (weight gain rate), SGR (specific
growth rate), FCR (feed conversion rate), FE (feed efficiency), FI (feed intake), PER (protein efficiency ratio), ANPU (apparent net protein utilization), PRR (protein retention
rate), SR (survival rate), HPI (hepatopancreas index), CHOL (cholesterol), TG (triglycerides), GLU (glucose), AKP (alkaline phosphatase), CAT (catalase), SOD (superoxide
Alvan-Aguilar, M. A. et al. 7
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dismutase), PO (phenoloxidase), LZM (lysozyme), MDA (malondialdehyde), THC (total hemocyte count), PC (protein concentration), proPO (prophenoloxidase activity),
AGA (agglutinating activity), THC (total count of hemocytes), ACP (acid phosphatase), BPC (body protein content), N.A. (no data available).
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Effects of dietary TMM on crustacean´s growth performance
Through the work carried out, we were able to verify that the inclusion of TMM in practical diets to
replace FM produced quite encouraging results in the five species of crustaceans reported in the
literature. Thus, Panini et al. (2017), pointed out that the performance of White shrimp was not
affected by replacing FM with TMM in the diets that they used. However, they suggested that the
use of TMM should be complemented by methionine to meet the White shrimp amino acids needs.
Indeed, Sharifinia et al. (2023) concluded that there is strong evidence that TMM can effectively
replace FM in the diet of
L. vannamei
, resulting in enhanced growth of this crustacean. Furthermore,
Zheng et al. (2023) found no decrease in growth performance or feed utilization due to the dietary
treatment with TMM proteins. Consequently, these authors presumed that the entire dietary
treatment provided suitable quantities of critical nutrients.
Another preliminary conclusion from this review is that even at low supplementation rates, TMM may
be considered as a form of functional feed. For instance, a compound feed comprising ~12 to 25%
TMM improved the growth parameters of
L. vannamei
,
C. quadricarinatus
,
P. leptodactylus
, and
M.
rosenbergii
(Choi et al., 2018; Motte et al., 2019; Wang et al., 2019 al., 2022; Mazlum et al., 2021; Feng
et al., 2019).
As can be seen, most data have been generated for
L. vannamei
. In this species, FM can be fully
replaced with TMM without detrimental effects (Panini et al., 2017; Ríos et al., 2021). Also, TMM was
able to replace between 12 and 50% of the FM without negative effects in
C. quadricarinatus
,
P.
leptodactylus
, and
M. rosenbergii
(Wang et al., 2022; Mazlum et al., 2021; Feng et al., 2019).
Methionine seems to be a limiting factor in
L. vannamei
because FM could only be fully replaced with
TMM if lysine and methionine supplements were also provided (Motte et al., 2019; Panini et al., 2017;
Ríos et al., 2021). Prominently, the total replacement of FM with TMM, at least in White shrimp feeds
is probable, if these species-dependent limitations are considered.
Effects of dietary TMM on crustacean´s immune response
Another interesting aspect that has been confirmed in this review is that there is sufficient scientific
evidence to assume that the inclusion of TMM to replace FM does not reduce the immune response
of crustaceans, but, on the contrary, strengthens it. For instance, the study published by Sharifinia et
al. (2023) found that replacing FM with TMM up to 30% in the diet of
L. vannamei
increased the
counts of THCs, although this increase was not significant. These findings were those described by
Feng et al. (2019) who observed a significant increase in
Macrobrachium rosenbergii
THC-fed diets
containing TMM protein in comparison with the control group. According to these authors' findings,
the level of LZM enzyme activity exhibited a growing trend with increasing the quantity of replacing
FM with TMM up to the level of 60%, which displayed that dietary TMM might expand the response
of the inborn immune system of White shrimp. Furthermore, Zheng et al. (2023) found that replacing
30% of FM with TMM increases not only growth performance but also intestinal bacterial diversity.
Indeed, these authors pointed out that TMM replacement of <45% FM expands antioxidant capacity
and immunity in the serum, as well as intestinal trypsin. In their study, the immune performance of
L. vannamei
still increased in TMM45.
Alvan-Aguilar, M. A. et al. 9
Rev. Peru. Investig. Agropecu. 2(2): e51; (jul-dic, 2023). e-ISSN: 2955-831X
Dietary supplementation of TMM improves the immune responses in White shrimp. For instance, the
study of Motte et al. (2019) showed that the immune performance of
L. vannamei
increased as the
percentage of TMM replacing FM increased. Also, Ríos et al. (2021), suggest that TMM can act as a
feasible substitute for FM, without causing any harmful effects on gut microbiota or the immune
system of
L. vannamei
. Besides, Shin & Lee (2021) also revealed that dietary supplementation of the
TMM can improve the innate immune responses and antioxidant enzyme activities of
L. vannamei
.
Finally, Choi et al (2018) concluded that dietary inclusion of 12% TMM protein had the best effects
on growth performance, immunological parameters, and resistance against
Lactococcus garvieae
and
Aeromonas hydrophila
. These authors support the inclusion of TMM protein in functional
aquafeeds.
Overall, the findings of this paper suggest that TMM is a promising alternative protein source for this
shrimp species, as it enhances both growth performance and the immune system, which only
contrasts with the results obtained by Li et al. (2022), which indicates that TMM was less effective for
L. vannamei
compared to the control diet (0% of TMM). Sharifinia et al. (2023) recommend the use
of TMM in the diet of farmed shrimps, given its lack of adverse impacts on growth performance and
its potential to reduce environmental consequences resulting from its production.
Finally, we can conclude the article by stating that there is ample evidence that dietary TMM confers
growth and health advantages to most of the crustaceans found in the analysis. Therefore, TTM can
be considered a promising alternative protein source for aquafeeds. On the other side, no studies
were found in Amazonian crustaceans or even in South American freshwater prawns, which opens a
window of opportunities for the development of new lines of research.
CONFLICT OF INTEREST
The authors declare that they have no conflict of interest.
AUTHORSHIP CONTRIBUTION
Conceptualization: Alvan-Aguilar, M. A. & Chu-Koo, F. W.
Formal analysis: Alvan-Aguilar, M. A. & Tello-García, P.
Investigation: Alvan-Aguilar, M. A., Tello-García, P., Chu-Ochoa, Y. F. & Chu-Koo, F. W.
Methodology: Alvan-Aguilar, M. A., Tello-García, P., Chu-Ochoa, Y. F. & Chu-Koo, F. W.
Supervision: Alvan-Aguilar, M. A., y Chu-Koo, F. W.
Writing-original draft: Alvan-Aguilar, M. A., Tello-García, P., & Chu-Ochoa, Y. F.
Writing-review and editing: Alvan-Aguilar, M. A., Tello-García, P., Chu-Ochoa, Y. F. & Chu-Koo, F. W.
LITERATURE CITED
Choi, I. H.; Kim, J. M.; Kim, N. J.; Kim, J. D.; Park, C.; Park, J. H.; & Chung, T. H. (2018). Replacing fish
meal by mealworm (
Tenebrio molitor
) on the growth performance and immunologic
10 Revista Peruana de Investigación Agropecuaria
Rev. Peru. Investig. Agropecu. 2(2): e51; (jul-dic, 2023). e-ISSN: 2955-831X
responses of white shrimp (
Litopenaeus vannamei
).
Acta Scientiarum - Animal Sciences
, 40,
1–9. https://doi.org/10.4025/actascianimsci.v40i1.39077
Costa-Pierce, B.A.; & Chopin, T. (2021). The hype, fantasies, and realities of aquaculture
development globally and its new geographies.
World Aquaculture Magazine
, 52: 23-35.
Dawood, M.A. (2021). Nutritional immunity of fish intestines: important insights for sustainable
aquaculture.
Reviews in Aquaculture
, 13(1):642e63. https://doi.org/10.1111/raq.12492.
Feng, P.; He, J.; Huang, G.; Chen, X.; Yang, Q.; Wang, J.; Wang, D.; & Ma, H. (2019). Effect of dietary
Tenebrio molitor
protein on growth performance and immunological parameters in
Macrobrachium rosenbergii
.
Aquaculture
, 511, 734247.
https://doi.org/10.1016/j.aquaculture.2019.734247
Food and Agriculture Organization of the United Nations – FAO (2021). Fishery and Aquaculture
Statistics. Global aquaculture production 1950-2019 (FishstatJ). FAO, Rome, Italy. Available at:
www.fao.org/fishery/statistics/software/fishstatj/en
Gasco, L.; Henry, M.; Piccolo, G.; Marono, S.; Gai, F.; Renna, M.; Lussiana, C.; Antonopoulou, E.; Mola,
P.; & Chatzifotis, S. (2016).
Tenebrio molitor
meal in diets for European sea bass
(
Dicentrarchus labrax
L.) juveniles: Growth performance, whole body composition and in vivo
apparent digestibility.
Animal Feed Science and Technology
, 220, 34–45.
https://doi.org/10.1016/j.anifeedsci.2016.07.003
Gu, J., Liang, H., Ge, X., Xia, D., Pan, L., Mi, H., & Ren, M. (2022). A study of the potential effect of
yellow mealworm (
Tenebrio molitor
) substitution for fish meal on growth, immune and
antioxidant capacity in juvenile largemouth bass (
Micropterus salmoides
).
Fish and Shellfish
Immunology
, 120, 214–221. https://doi.org/10.1016/j.fsi.2021.11.024
Henry, M.A.; Gai, F.; Enes, P.; Pérez-Jiménez, A.; & Gasco, L. (2018). Effect of partial dietary
replacement of fishmeal by yellow mealworm (
Tenebrio molitor
) larvae meal on the innate
immune response and intestinal antioxidant enzymes of rainbow trout (
Oncorhynchus
mykiss
).
Fish and Shellfish Immunology,
8: 83:30. 8e13.
https://doi.org/10.1016/j.fsi.2018.09.040.
Hoffmann, L.; Rawski, M.; Nogales-Mérida, S.; Kołodziejski, P.; Pruszyńska-Oszmałek, E.; &
Mazurkiewicz, J. (2021). Mealworm meal use in sea trout (
Salmo trutta
m.
trutta
, L.) fingerling
diets: effects on growth performance, histomorphology of the gastrointestinal tract and
blood parameters.
Aquaculture Nutrition
, 27(5), 1512–1528.
https://doi.org/10.1111/anu.13293
Iaconisi, V.; Bonelli, A.; Pupino, R.; Gai, F.; & Parisi, G. (2018). Mealworm as dietary protein source for
rainbow trout: Body and fillet quality traits.
Aquaculture
, 484: 197–204.
https://doi.org/10.1016/j.aquaculture.2017.11.034
Iaconisi, V.; Marono, S.; Parisi, G.; Gasco, L.; Genovese, L.; Maricchiolo, G.; Bovera, F.; & Piccolo, G.
(2017). Dietary inclusion of
Tenebrio molitor
larvae meal: Effects on growth performance and
Alvan-Aguilar, M. A. et al. 11
Rev. Peru. Investig. Agropecu. 2(2): e51; (jul-dic, 2023). e-ISSN: 2955-831X
final quality treats of blackspot sea bream (
Pagellus bogaraveo
).
Aquaculture
, 476: 49–58.
https://doi.org/10.1016/j.aquaculture.2017.04.007
Ido, A.; Hashizume, A.; Ohta, T.; Takahashi, T.; Miura, C.; & Miura, T. (2019). Replacement of fish
meal by defatted yellow mealworm (
Tenebrio molitor
) larvae in the diet improves growth
performance and disease resistance in red seabream (
Pargus major
).
Animals
, 9(3):100.
https://doi.org/10.3390/ani9030100.
Jeong, S. M.; Khosravi, S.; Mauliasari, I. R.; & Lee, S. M. (2020). Dietary inclusion of mealworm
(
Tenebrio molitor
) meal as an alternative protein source in practical diets for rainbow trout
(
Oncorhynchus mykiss
) fry.
Fisheries and Aquatic Sciences
, 23(1): 214–221.
https://doi.org/10.1186/s41240-020-00158-7
Li, X.Y.; Chen, Y.K.; Zheng, C.Z.; Chi, S.Y.; Zhang, S.; Tan, B.P.; & Xie, S.W. (2022). Evaluation of six
novel protein sources on apparent digestibility in Pacific White Shrimp,
Litopenaeus
vannamei
.
Aquaculture Nutrition
. https://doi.org/10.1155/2022/8225273.
Makkar, H.P.S.; Tran, G.; Heuzé, V.; & Ankers, P. (2014). State-of-the-art on use of insects as animal
feed.
Animal Feed Science and Technology
, 197: 1-33.
https://doi.org/10.1016/j.anifeedsci.2014.07.008
Mastoraki, M.; Vlahos, N.; Patsea, E.; Chatzifotis, S.; Mente, E.; & Antonopoulou, E. (2020). The effect
of insect meal as a feed ingredient on survival, growth, and metabolic and antioxidant
response of juvenile prawn
Palaemon adspersus
(Rathke, 1837).
Aquaculture Research
, 51:
3551-3562. https://doi.org/10.1111/are.14692
Mazlum, Y.; Turan, F.; & Bircan, Y. (2021). Evaluation of mealworms (Tenebrio molitor) meal as an
alternative protein source for narrow-clawed crayfish (
Pontastacus leptodactylus
) juveniles.
Aquaculture Research
. 1–9. https://doi.org/10.1111/are.15253
Melenchón, F.; Larrán, A. M.; de Mercado, E.; Hidalgo, M. C.; Cardenete, G.; Barroso, F. G.; Fabrikov,
D.; Lourenço, H. M.; Pessoa, M. F.; & Tomás-Almenar, C. (2021). Potential use of black soldier
fly (
Hermetia illucens
) and mealworm (
Tenebrio molitor
) insectmeals in diets for rainbow
trout (
Oncorhynchus mykiss
).
Aquaculture Nutrition
, 27(2): 491–505.
https://doi.org/10.1111/ANU.13201
Naylor, R.L.; Hardy, R.W.; Buschmann, A.H.; Bush, S.R.; Cao, L.; Klinger, D.H.; Little, D.C.; Lubchenco, J.;
Shumway, S.E.; & Troell, M. (2021). A 20-year retrospective review of global aquaculture.
Nature
, 591: 551-563. https://doi.org/10.1038/s41586-021-03308-6
Panini, R. L.; Freitas, L. E. L.; Guimarães, A. M.; Rios, C.; da Silva, M. F. O.; Vieira, F. N.; Fracalossi, D.
M.; Samuels, R. I.; Prudêncio, E. S.; Silva, C. P.; & Amboni, R. D. M. C. (2017). Potential use of
mealworms as an alternative protein source for Pacific white shrimp: Digestibility and
performance.
Aquaculture
, 473: 115–120. https://doi.org/10.1016/j.aquaculture.2017.02.008
Rema, P.; Saravanan, S.; Armenjon, B.; Motte, C.; & Dias, J. (2019). Graded incorporation of defatted
yellow mealworm (
Tenebrio molitor
) in rainbow trout (
Oncorhynchus mykiss
) diet improves
12 Revista Peruana de Investigación Agropecuaria
Rev. Peru. Investig. Agropecu. 2(2): e51; (jul-dic, 2023). e-ISSN: 2955-831X
growth performance and nutrient retention.
Animals
, 9(4).
https://doi.org/10.3390/ani9040187
Ríos, C.; Panini, R.L.; Acordi Menezes, L.A.; Vieira, F.N.; Fracalossi, D.M.; Samuels, R.I.; De Dea Lindner,
J.; & Silva, C.P. (2021). Effects of the substitution of fishmeal with mealworm meal on
enzymes, haemolymph and intestinal microbiota of the Pacific white shrimp.
Journal of
Insects as Food and Feed
, 7(6): 1023–1033. https://doi.org/10.3920/JIFF2020.0148
Roncarati, A.; Gasco, L.; Parisi, G.; & Terova, A. (2015). Growth performance of common catchfish
(
Ameiurus melas
Raf.) fingerlings fed mealworm (
Tenebrio molitor
) diet.
Journal of Insects as
Food and Feed
, 1(3): 233 - 240. https://doi.org/10.3920/JIFF2014.0006
Röthig, T.; Vilcinskas, A.; Barth, A.; Tschirner, M.; Schubert, P.; Wenning, M.; Billion, A.; & Wilke, T.
(2023). Insect feed in sustainable crustacean aquaculture.
Journal of Insects as Food and Feed
,
9(9): 1115-1138. https://doi.org/10.3920/JIFF2022.0117
Sankian, Z.; Khosravi, S.; Kim, Y. O.; & Lee, S. M. (2018). Effects of dietary inclusion of yellow
mealworm (
Tenebrio molitor
) meal on growth performance, feed utilization, body
composition, plasma biochemical indices, selected immune parameters and antioxidant
enzyme activities of mandarin fish (
Siniperca scherze
).
Aquaculture
, 496: 79–87.
https://doi.org/10.1016/j.aquaculture.2018.07.012
Shafique, L.; Abdel-Latif, H.M.R.; Hassan, F.-u.; Alagawany, M.; Naiel, M.A.E.; Dawood, M.A.O.; Yilmaz,
S.; & Liu, Q. (2021). The feasibility of using Yellow Mealworms (
Tenebrio molitor
): Towards a
sustainable aquafeed industry.
Animals
, 11, 811. https://doi.org/10.3390/ani11030811
Sharifinia, M.; Hossein, K.M.; Afshari, B.Z.; Keshavarzifard, M.; Daliri, M.; Koochaknejad, E.; & Sedigh,
J.M. (2023). Fishmeal replacement by mealworm (
Tenebrio molitor
) in diet of farmed Pacific
white shrimp (
Litopenaeus vannamei
): effects on growth performance, serum biochemistry,
and immune response.
Aquatic Living Resources
, 36, 19. https://doi.org/10.1051/alr/2023013
Shin, J.; & Lee, K-J. (2021). Digestibility of insect meals for Pacific white shrimp (
Litopenaeus
vannamei
) and their performance for growth, feed utilization and immune responses.
PLoS
ONE,
16(11): e0260305. https://doi.org/10.1371/journal.pone.0260305
Smetana, S.; Schmitt, E.; & Mathys, A. (2019). Sustainable use of
Hermetia illucens
insect biomass
for feed and food: Attributional and consequential life cycle assessment.
Resources,
Conservation and Recycling
, 144: 285-296. https://doi.org/10.1016/j.resconrec.2019.01.042
Su, J.; Gong, Y.; Cao, S.; Lu, F.; Han, D.; Liu, H.; Jin, J.; Yang, Y.; Zhu, X.; & Xie, S. (2017). Effects of
dietary
Tenebrio molitor
meal on the growth performance, immune response, and disease
resistance of yellow catfish (
Pelteobagrus fulvidraco
).
Fish and Shellfish Immunology
, 69: 59–
66. https://doi.org/10.1016/j.fsi.2017.08.008
Tacon, A.G.J. (2020). Trends in global aquaculture and aquafeed production: 2000-2017.
Reviews in
Fisheries Science and Aquaculture
, 28: 43-56.
https://doi.org/10.1080/23308249.2019.1649634
Alvan-Aguilar, M. A. et al. 13
Rev. Peru. Investig. Agropecu. 2(2): e51; (jul-dic, 2023). e-ISSN: 2955-831X
Wang, T.; Wang, X.; Shehata, A.I.; Wang, R.; Yang, H.; Wang, Y.; Wang, J.; & Zhan, Z. (2022). Growth
performance, physiological and antioxidant capacity responses to dietary fish meal
replacement with insect meals for aquaculture: A case study in red claw crayfish (
Cherax
quadricarinatus
).
Aquaculture Research
, 53(10): 3853-3864. https://doi.org/10.1111/are.15892
Zheng, Y.; Hou, C.; Chen, J.; Wang, H.; Yuan, H.; Hu, J.; Shi, L.; & Zhang, S. (2023). Integrating
microbiome and transcriptome analyses to understand the effect of replacing fishmeal with
Tenebrio molitor
meal in Pacific white shrimp (
Litopenaeus vannamei
) diets.
Aquaculture
, 575,
739818. https://doi.org/10.1016/j.aquaculture.2023.739818.
