Peruvian Journal of Agronomy
http://revistas.lamolina.edu.pe/index.php/jpagronomy/index

REVIEW
https://doi.org/10.21704/pja.v6i1.1893

Received for publication: 02 March 2021
Accepted for publication: 02 March 2022

Published: 30 April 2022
ISSN: 2616-4477

Management of Chloridea virescens (Noctuidae) in blueberries
(Vaccinium corymbosum L.) to promote sustainable cultivation in

Peru: A Review

Manejo de Chloridea virescens (Noctuidae) en arándanos (Vaccinium
corymbosum L.) para promover su cultivo sostenible en Perú: Una

revisión

Mónica Narrea Cango1; Elías Huanuqueño Coca2; Josué Otoniel Dilas-Jiménez3*;
Jhon Anthony Vergara Copacondori4

*Corresponding author:

Abstract

A review of current and specific literature was carried out in order to elaborate a proposal for the management
of Chloridea virescens in the cultivation of blueberry (Vaccinium corymbosum L.), developing strategies
in each component of Integrated Pest Management (IPM), including Cultural Control, Ethological Control,
Biological Control, and Chemical Control (PBUA and PQUA). Likewise, steps in the genetic improvement
for quantitative resistance of the blueberry to this pest (Lepidoptera: Noctuidae) using wild relatives of this
crop as a source of resistance genes are proposed.

Keywords: Quantitative Resistance, Wild Blueberry, Assisted Selection, Genetic Improvement, Chloridea
virescens.

Resumen

Se realizó una revisión de la literatura actual y específica para elaborar una propuesta de manejo de
Chloridea virescens en el cultivo del arándano (Vaccinium corymbosum L.), desarrollando estrategias en cada
componente del Manejo Integrado de Plagas (MIP), incluyendo el Control Cultural, el Control Etológico, el
Control Biológico y el Control Químico (PBUA y PQUA). Asimismo, se proponen pasos en el mejoramiento
genético para la resistencia cuantitativa del arándano a esta plaga (Lepidoptera: Noctuidae) utilizando parientes
silvestres de este cultivo como fuente de genes de resistencia.

Palabras clave: Resistencia cuantitativa, arándano silvestre, selección asistida, mejora genética, Chloridea
virescens.

1 Universidad Nacional Agraria La Molina, Lima, Perú.
2Universidad Nacional Agraria La Molina, Lima, Perú.
3 Universidad Nacional Autónoma de Tayacaja “Daniel Hernández Morillo”, Pampas, Huancavelica, Perú.
4 Universidad Nacional de Cajamarca, Cajamarca, Perú.

How to cite this article:

Narrea, M., Huanuqueño, E., Dilas-Jiménez, J. & Vergara, J. (2022). Management of Chloridea
virescens (Noctuidae) in blueberries (Vaccinium corymbosum L.) to promote sustainable cultivation in
Peru: A Review. Peruvian Journal of Agronomy, 6(1), 78-92. https://doi.org/10.21704/pja.v6i1.1893

Narrea, M.; Huanuqueño, E.; Otoniel, J.; Vergara, J.
Peruvian Journal of Agronomy 6(1): 78-92 (2022)

https://doi.org/10.21704/pja.v6i1.1893

INTRODUCTION
The blueberry is a shrub of the Ericaceous
family, belonging to the genus Vaccinium, which
constitutes a group of species widely distributed
throughout the northern hemisphere, basically
in North America, Central Europe, and Eurasia,
also found in South America, and a few in Africa
and Madagascar (García et al. 2018). Of the 30
species that make up the genus, only a few are
commercially important, with V. corymbosum
L., which represents approximately 80% of the
total cultivated area in the World, standing out,
followed in importance by V. ashei Reade, with
approximately 15%. Among the remaining 5%,
V. angustifolium Aiton and some hybrids of V.
angustifolium x V. corymbosum stand out (García
et al. 2018). These varieties are differentiated by
the number of chilling hours they need to break
the dormant or resting period of the plant and
are grouped as follows: Lowbush blueberry (V.
angustifolium), Rabbit-eye blueberry (V. ashei),
and Highbush blueberry (V. corymbosum)
(Buzeta, 1997). The cultivars of “highbush”
are separated into “northern” and “southern”
depending on the requirements of chilling hours
and winter hardiness (Hancock, 2009).

In Peru, in recent years, V. corymbosum has
sustained growth in both area and yield, sown
mainly on the country’s northern coast. Until
2011, Peru had not joined the International
Union for the Protection of New Varieties of
Plants (UPOV); this conditioned that the initial
development was carried out with released
varieties: Biloxi, Legacy, Misty, O’Neal, Duke,
and Brigitta, among others. Biloxi has been the
most successful variety in the low-lying areas,
estimated to have covered between 80% and 90%
of the productive coast area. In the heights of the
mountains, on the other hand, good results have
been obtained with Legacy (Febres, 2013). For
Sierra Exportadora (2011), the Biloxi, Misty, and
Legacy varieties are the ones that best adapt to our
country, but we can find other patented varieties
with different costs and production management.
These varieties, such as Ventura, Millennial,
Emerald, Susy Blue, Windsor, Springhigh, Star,
and Jewel arrive in Peru through Fall Creek Far
& Nursery, an American company that manages,

sells, and reproduces the patents obtained by the
universities of Florida and Georgia (Gargurevich,
2017).

The international market promotes crop
expansion in our country due to the optimal
climatic conditions for its development. The
main exploitable commercial window is between
the end of September and all of October, where
there is competition with Argentina and Uruguay.
In November and December, Chile is the main
competitor with South Africa and Oceania.
Given the countries above’ unpredictable frost
and rain conditions, Peru can take advantage of
better international prices (Sierra Exportadora-
PCM, 2012; Ministerio de Desarrollo Agrario y
Riego [MIDAGRI], 2016). This crop is potential
and strategic to be financed by the various
competitive funds that Peru has implemented for
years such as Innóvate Perú (formerly Fincyt),
Fondecyt, and Pnia, among others, just as coffee
cultivation has been financed (Dilas-Jiménez &
Cernaqué 2017).

According to Agrodata Peru (2020a), in 2019,
our country surpassed Chile for the first time and
was crowned as the main exporter of blueberries
worldwide, with profits of around the US $810
million (the United States, the Netherlands, and
China are the main destinations of the prized
bluish berries). Thus, blueberries have climbed
to second place in the list of Peruvian fruits for
export, surpassed by grapes - in the first place -
and above avocados. In the 2019 campaign, the
USA was the primary destination with US $458
million (57% of the total), followed by the Ne-
therlands with US $179 million (22%), and Chi-
na rose to US $70 million (9%) (Agrodata Peru,
2020a). Of the five regions of Peru where bluebe-
rries are most cultivated, La Libertad represents
the significant growing region, concentrating
more than 60% of production. The rest is distri-
buted between Ica, Lima, Ancash, and Lambaye-
que (Agrodata Peru, 2020b).

According to Gestion (2019), in 2015 the
national average yield was 9 tons/ha. On the
other hand, in 2018 it reached 15 t/ha due to
the improvement in the sowing and harvesting
technique. La Libertad and Lambayeque regions
have the highest yields, which in 2018, reached

Management of Chloridea virescens (Noctuidae) in blueberries (Vaccinium corymbosum L.) to promote sustainable cultivation in Peru: A Review

January - April 2022

17 and 15 t/ha, respectively. On the contrary, the
region of Arequipa registers the lowest yields.
In the 2019 campaign, Camposol SA led exports
with US $173 million, followed by Hortifrut
Perú SAC with US $101 million, and Hortifrut
Tal with US $68 million (Agrodata Peru, 2020a).

It is expected that in 2020, the blueberry
growing areas in Peru will reach approximately
12,500 hectares; For its part, the Pro Arandanos
Union calculated that the figure would be around
14,000 hectares next year. “This year we are sure
that the blueberry will exceed US$1,000 million
in exports and will be the first Peruvian agro-
export product,” they assure from Pro Arándanos
(AgroNegociosPerú, 2020).

Among the critical pests of the blueberry crop,
Chloridea virescens is one of the most important
ones because it causes damage to the shoots,
leaves, inflorescences, and fruits, generating
reductions in crop yield. In addition, there are
strategies for controlling H. virescens, such as
cultural, ethological, biological, and chemical
control; however, these strategies must be used
within integrated management.

In recent years, there have been limitations in
chemical control since there is a restriction on
the use of active ingredients for the cultivation
of blueberries, whose production is destined
for the international markets of Europe, the
United States, and Asia. For this reason, new
mechanisms should be used within the chemical
control, such as biological products based on
Bacillus thuringiensis, or other strategies such
as genetic improvement of the blueberry crop to
reduce the susceptibility to this pest (Contreras-
Pérez et al., 2019). On the other hand, there is
genetic improvement in this crop, For example,
the United States Department of Agriculture
(USDA)-Agricultural Research Service (ARS)-
National Clonal Germplasm Repository (NCGR)
in Corvallis – Oregon, has performed the
genotyping of 367 blueberry samples Vaccinium
spp. detecting 54 cultivars makes up important
germplasm for future genetic improvement
studies (Bassil et al., 2020).

Based on all those mentioned above, this
study aims to identify scientific and technological

advances that allow the generation of an Integrated
Management proposal of Chloridea virescens for
the sustainable cultivation of blueberries in Peru.

For this article, an exhaustive review of
relevant information related to integrated
pest management (IPM) was carried out,
emphasizing the cultivation of blueberries,
specifically in the management of Chloridea
virescens. Research articles in journals in the last
ten years were preferably consulted. Scientific
information databases were consulted, such as
SciElo, ScienceDirect, and Springer, among
others, and in a complementary way, other
sources of information provided information
about blueberries in Peru. The keywords used,
individually or conjugated, were “blueberry,
blueberries, Chloridea virescens, integrated
management, CRISPR, cry proteins, resistance,
wild cultivars, and Peruvian.”

The focus of the organization of the information
was on the IPM for the blueberry, the same that
gave rise to two management proposals: (1)
a specific proposal of integrated management
of Chloridea virescens in the cultivation of
blackberries in Peru, based on practices of
Cultural Control, Ethological Control, Biological
Control, and Chemical Control (PQUA and
PBUA). This proposal is also supported by the
results of field tests on chemical control PBUA
of Chloridea virescens in blueberry, carried out
in 2018 by the first author of this article, given its
implication in the proposed IPM; (2) a proposal
for genetic improvement in cultivated varieties of
blueberry in Peru, to allow sustainable cultivation
of this crop.

DEVELOPMENT
Strengths and Opportunities for blueberries
in Peru
According to Guo et al., 2019 and Meiners (2007),
the strengths and opportunities are summarized
in: (1) Ability to transport high volumes by sea.
In 2019, 5 million kg per week were exported; (2)
Capacity to produce ten months a year; (3) The
US will remain attractive; it is more stable and
can absorb large volumes; (4) The Asian market
has the possibility of growth and is demanding

Narrea, M.; Huanuqueño, E.; Otoniel, J.; Vergara, J.
Peruvian Journal of Agronomy 6(1): 78-92 (2022)

https://doi.org/10.21704/pja.v6i1.1893

in terms of presentation, fiber, and sweetness, for
which it is expected that “genetics” will help; (5)
We have achieved yields of up to 16.8 t/ha even
being on a learning curve; (6) There is potential
for its reproduction via tissue culture (42 days to
75 days, 75% to 100% rooting).

Phenology and pests of blueberry

Phenology requires to be based on the location
of the fruiting stage, that is, on the harvest, to
obtain the highest economic returns thanks to the
commercial window there is between September
and October; for this, pruning is the fundamental
activity since it is the starting point in the calendar
(Maticorena, 2017). Changing the phenology
and forcing not to harvest in other months often
implies a more significant presence of pests, and
for this, a good IPM program must be designed.

The plant’s growth is divided into two phases
or stages: vegetative and reproductive. Four
stages of vegetative growth are specified, where
the first is the vegetative bud, the second is the
shoot characterized by short internodes, the
third is the lengthening of the internodes and
the expansion of the leaves, and the fourth is a
new branch made up of fully extended leaves
and long internodes (Rivadeneira & Carlazara,
2011). There are six stages of reproductive
growth: first, there is a swollen bud that will give
rise to the flowers, and later the bud will open,
initiating flowering. The third is flower buds with
the closed corolla, the fourth is the flower in full
bloom with the open corolla, the fifth is the drop
of the corolla and fruit set, and the sixth is green
fruit (Meyer & Prinsloo, 2003).

Cisternas (2013) mentions the following
pests in Chile: White worms (Hylamorpha
elegans, Sericoides spp., S. viridis, S. obesa,
Brachysternus prasinus, B. spectabilis,
Phytholaema herrmanni, P. dilutipes and
Tomarus villosus); Burritos (Aegorhinus
superciliosus, Aegorhinus nodipennis,
Aegorhinus phaleratus, Otiorhynchus sulcatus,
Otiorhynchus rugosostriatus, Naupactus
xanthographus, Graphognatus leucoloma and
Naupactus cervinus); Thrips (Frankliniella
occidentalis, Thrips tabaci, and Frankliniella
australis), Cuncunillas negra (Dalaca pallens

and D. variabilis); Cutworms (Agrotis ipsilon
and Peridroma saucia), Aphids (Aphis gossypii
and Macrosiphum spp.); Leafroller (Proeulia
spp.); White piglets (Pseudococcus viburni, P.
calceolariae, P. longispinus and P. cribata);
Brown fruit bug (Leptoglossus chilensis) and
shoot borer wasp (Ametastegia glabrata).

Integrated Pest Management (IPM) in
blueberries

Since the 1940s, entomologists began work
related to Integrated Pest Management (IPM)
as a “supervised control”. The concept of IPM
has been changing over time. However, it is
still conceived as a crop protection system
that integrates pest management techniques
(cultural, ethological, biological, chemical, and
genetic practices) (Deguine et al., 2021). IPM
combines different management strategies and
practices to grow and maintain healthy crops
while minimizing the use of pesticides. As the
cornerstone of sustainable agriculture, it aims to
improve farmers’ practices to support increased
incomes while improving the conservation and
management of natural resources and the health
of rural communities and consumers. IPM
emphasizes the growth of a healthy crop with
the least possible disturbance of agroecosystems
and encourages natural pest control mechanisms
(Food and Agriculture Organization [FAO],
2014).

Among the components of IPM, we have
mainly: cultural control, ethological control,
biological control, chemical control, and genetic
control. Below we detail information about the
uses and scientific advances of these components:

Cultural Control: Tasks such as irrigation,
fertilization, weed control, and pruning can
be cited among the most important. Proper
fertilization and irrigation management are
essential to ensure high yields and good quality
characteristics in the fruit (Baiano et al. 2011).
In blueberries, factors included are choosing an
appropriate variety for the area, checking the
plants in the nursery to avoid weeds, adequate
fertilization and irrigation, planting at the
correct time, good quality of plants to ensure a
good population, a vigorous initial growth, etc.

Management of Chloridea virescens (Noctuidae) in blueberries (Vaccinium corymbosum L.) to promote sustainable cultivation in Peru: A Review

January - April 2022

(Morales, 2017).

Ethological Control: This control method
includes physical (light and color) and chemical
(semiochemical) factors intended to modify
the insect’s behavior. The behavior of insects
is determined by their response to the presence
or occurrence of stimuli of a chemical nature,
although they also respond to physical and
mechanical stimuli (CARE, 2006). For example,
acoustic communication in insects has recently
been studied with ethological control applications
(Eskov, 2017).

Biologic control: Since the 19th century, 6227
biological control agents (BCA) have been
registered, of which 686 have not yet been
identified at the species level, that is, there is a
knowledge gap for research (Cock, 2019). A
series of habitat modifications are included to
create conditions to achieve biological control
that favors the survival, fertility, longevity, and
action of natural enemies and improve their
colonization of the crop (Landis et al., 2000). In
this context, biological corridors would act as
a refuge area for beneficial insects (pollinators
and biological controllers) when the conditions
in the crop become harsh or deadly due to the
applications programmed for pest control (Landis
et al. 2000; Gurr et al. 2004).

Chemical Control: They provide quick action
and grant a wide range of uses and forms of
application (FAO 2002). Among the pesticides
for agricultural use, we find Chemical Pesticides
for Agricultural Use (PQUA) and Biological
Pesticides for Agricultural Use (PBUA). We
consider the latter within a chemical control
because they come in formulations that include
other components in addition to the biological
components. For example,in the case of PQUAs,
the term includes substances or mixtures of
substances applied to crops before or after harvest
to protect the product against deterioration
during storage and transportation. On the
other hand, PBUAs are all the substances of a
biological nature: microorganisms or products
derived from their metabolism; bacteria, fungi,
etc. Likewise, products derived directly from
vegetables, which are not chemically synthesized
such as: strychnine, nicotine, pyrethrins,

rotenone, and garlic, among others, which alone
or in combination with adjuvants, are used to
prevent, repel, combat, and destroy insects,
mites, pathogens, nematodes, weeds, rodents,
or other biological organisms harmful to plants,
their products, and derivatives (Supreme Decree
No. 001-2015-MINAGRI). Both treatments are
highly effective in-field pest control (Llanos &
Apaza, 2018).

Within the group of bacteria, there are
formulations based on Bacillus thuringiensis
a facultative anaerobic microorganism,
chemoorganotrophic, and with catalase activity
(Zhou et al., 2020). They can ferment glucose,
fructose, trehalose, maltose, and ribose, and
hydrolyze gelatin, starch, glycogen, esculin, and
N-acetyl-glucosamine (Sauka & Benintende,
2008). However, the main characteristic of
B. thuringiensis is that during the sporulation
process, it produces a parasporal inclusion formed
by one or more crystalline bodies of protein
nature that are toxic to different invertebrates,
especially insect larvae. These proteins are
called Cry (from Crystal) and constitute the basis
of the most widespread biological insecticide
worldwide (Schnepf et al., 1998; Liu et al., 2018).

Bt toxins began to be used commercially in
France in 1938; by 1958, their use had spread to
the United States. Starting in the 80s, Bt became
a pesticide of worldwide interest (Feitelson
et al., 1992). Commercialized products of
B. thuringiensis mainly consist of spore and
crystal preparations, activated or not, which are
sprayed on crops as if they were conventional
insecticides. These preparations generally come
from the subspecies kurstaki (Btk) (Kamatham
et al., 2021). B. thuringiensis is classified into
84 serovars identified by flagellar antigen H
serology (Sauka & Benintende, 2008). Since its
discovery, some subspecies active, mainly Bt
subsp. Kurstaki (Btk), Bt subsp. Thuringiensis
(Btt) y Bt subsp. Galleriae (Btg) against pest
invertebrates have been reported (Rashki et al.,
2021) based on biochemical and morphological
characteristics and flagellar antigens (Schnepf et
al., 1998).

Crystalline toxins exist in a variety of forms:
bipyramidal, spherical, rhomboid, cuboidal,

Narrea, M.; Huanuqueño, E.; Otoniel, J.; Vergara, J.
Peruvian Journal of Agronomy 6(1): 78-92 (2022)

https://doi.org/10.21704/pja.v6i1.1893

elliptical and irregular, among others, and are
active against a large number of groups of insects
mainly, as well as nematodes and protozoa (Rashki
et al., 2021; Jurat-Fuentes & Crickmore, 2017).
The genes that encode these proteins reside in
conjugable megaplasmids (Feitelson et al. 1992)
were named Cry, and their encoded proteins
were designated Cry δ-endotoxins (Ochoa &
Arrivillaga, 2009). Cry proteins are synthesized
as inactive protoxins ingested by larvae when
feeding. The inclusions are solubilized under
the alkaline conditions of the larva’s digestive
tract and are converted by insect proteases into
active peptides (Schnepf et al., 1998; Feitelson
et al., 1992). The active toxin is recognized
by a specific receptor and is inserted into the
membrane of the brush border of microvilli of
the digestive tract of the insect (Gerber & Shai,
2000). An oligomerization occurs, resulting in
the formation of cation channels of 0.5 to 1 nm
in diameter (Gerber & Shai, 2000). These pores
cause a nonspecific influx of ions, mainly K+
ions, which dissipates ionic gradients and lowers
the pH of the medium, causing osmotic cell lysis
that leaves the larva unable to feed (Schnepf et al.
1998). On the other hand, the tissue destruction
allows the mixture of the contents of the digestive
tract with the hemolymph, which, together with
the low pH, favors the germination of bacterial
spores, leading to septicemia and the death of
the larva a few days after ingestion of crystals
(Schnepf et al. 1998). When the insect consumes
the Cry protein, it presents cessation of ingestion,
intestinal paralysis, vomiting, diarrhea, osmotic
decompensation, total paralysis, and death
(Vachon et al., 2012; Bravo et al., 2007).

In the case of lepidopterans such as H.
virescens, the proteins considered toxic are
those of the Cry1 class. Cry proteins generally
show reduced activity spectra and are often
limited to a few species of insects belonging to
the same order. However, the toxicity of Cry1
proteins is not restricted to lepidopterans (Sauka
& Benintende, 2008). For H. virescens we have
the following toxic proteins: Cry1Aa, Cry1Ab,
Cry1Ac, Cry1Ae, Cry1Be, Cry1Ca, Cry1Fa,
Cry1If, Cry1Ja, Cry1Jc, Cry2Aa, Cry2Ab,
Cry2Ac, Cry2Ae, Cry9A, Cry9Ca, and Vip3
(Sauka & Benintende, 2008). B. thuringiensis

var. kurstaki HD-1 is one of the strains of B.
thuringiensis best studied and is characterized
by carrying the following cry antilepidopteran
genes: cry1Aa, cry1Ab, cry1Ac, cry2Aa, cry2Ab
and cry1Ia (Sauka, 2007). B. thuringiensis var.
kurstaki HD-1 is par excellence the strain usedto
control of lepidopteran insects, agricultural pests,
and forest pests. This strain was initially isolated
by Dulmage in 1970, constituting a milestone
in the history of the use of B. thuringiensis
as a larvicide since it was responsible for B.
thuringiensis-based products can compete with
chemical insecticides in terms of efficiency. This
strain was up to 200 times more toxic for some
species of Lepidoptera than other strains used in
the products of that time (Sauka & Benintende,
2008). These products, formulated based on Bts,
are used mainly to control lepidoptera pests in
corn, wheat, cotton, and fruit crops. Formulations
can be made from B. thuriengensis isolated from
Peruvian agroecosystems and the evaluation of
their bioinsecticidal potential.

Flores et al. (2011), managed to isolate
54 strains of Bacillus thuringiensis from 385
samples of rhizosphere, plant material, and dead
insects from central Peru; the identification of the
isolated strains was carried out by observation
in phase-contrast microscopy according to
the culture microscopic characteristics and
differential biochemical tests. Isolated strains
were compared with B. thuringiensis HD-11,
B. thuringiensis var kurstaki HD-342, and B.
thuringiensis aizawai NRRL-HD-130 to evaluate
the entomotoxic effect. The Bt-UNMSM-42
strain was the one that presented higher toxicity
than the rest of the isolated strains, with mean
mortality of 39.73% with 50 μg/mL and 71.93%
for 250 μg/mL, with a standard deviation of
11.30 and 9.98, respectively; however, it did not
outperform the reference strains B. thuringiensis
HD-11 and B. thuringiensis var kurstaki HD-
342, which reached mean mortality of 86.5%
and 82.5% respectively at a dose of 250 μg/mL.
According to Sauka & Benintende (2008), genetic
engineering developed many species of plants
that express cry genes from B. thuringiensis and
thus turned them into “insecticidal plants’’. These
plants are commonly referred to as “Bt plants or
crops” (e.g., Bt corn, Bt cotton, etc.). Tobacco

Management of Chloridea virescens (Noctuidae) in blueberries (Vaccinium corymbosum L.) to promote sustainable cultivation in Peru: A Review

January - April 2022

plants (Nicotiana tabacum) that produced
sufficient amounts of Cry protein to control first
instar larvae of Manduca sexta were developed.
Since then, at least ten different types of cry
genes have been introduced into 26 plant species:
cry1Aa, cry1Ab, cry1Ac, cry1Ba, cry1Ca,
cry1H, cry2Aa, cry3A, cry6A, and cry9C (Sauka
& Benintende, 2008).

Genetic Control: Varietal resistance is an
integrated pest management (IPM) strategy that
has been considered an alternative that can be
ecological since it can reduce dependence on the
use of synthetic insecticides and is compatible
with other control methods (Vallejo & Estrada,
2002).

According to Jiménez (2009), genetic control
of pests has been used in two ways: (1) The
crop can be genetically manipulated to increase
its resistance to attack by pests, and (2) Pests
can be subject to genetic intervention with the
introduction of masses of individuals with a
selected genotype. Over the years, varieties of
insect-resistant crops have been developed, most
notably alfalfa, corn, cotton, beans, cassava,
vegetables, rice, sorghum, soybeans, and wheat.

Within Integrated Pest Management, the
genetic resistance of a plant to insect attack
is a component that can be managed through
conventional genetic improvement programs,
which in turn are associated with desirable
agronomic characteristics (Deguine et al., 2021).
These characteristics can be found in the wild
varieties of many species, such as the blueberry,
where Rodríguez-Saona et al. (2019) found that
D. suzukii prefers cultivated fruits for oviposition
and better hosts for their offspring than wild
fruits. The cultivated fruits were also two times
larger, 47% firmer, 14% less acidic, and had lower
amounts of Brix, phenolic, and anthocyanin per
mass than wild fruits.

The review of the scientific literature
presented above suggests that through a genetic
improvement process we can select those
resistance characteristics of wild cultivars to
cultivated ones while maintaining other desirable
agronomic characteristics directly related to
higher crop yield and resistance to plagues and
diseases.

Integrated Management Proposal

The proposal developed by the authors regarding
the management of Chloridea virescens in
blueberries is the following:

Cultural Control: The implementation of 6
cultural practices is recommended: (1) Weed
control: blueberry leaves are small and few, so
the damage of H. virescens is significant in the
production of this crop. That is why weeds that
harbor H. virescens egg-laying should be avoided
such as Trifolium repens (Fabaeae), species of
the genus Geranium (Geraniaceae), and others
(Blanco et al., 2008). In addition, geomembranes
should be placed throughout the soil of the entire
crop area before the blueberry plants are installed
to prevent and control the weeds from sprouting
and developing.

(2) Management of the environment or field
edges: this is where the pest can be harbored;
management must be done with evaluations and
applications of low impact products on beneficial
fauna; (3) Use of windbreaker curtains: for both
horizontal and vertical crop management. The
wind brings thrips and sand that causes stress to
the plantation, making it susceptible to pests and
diseases; (4) Management of planting density:
in recent years we have gone from sowing 5000
pl/ha to 10,000 pl/ha. Therefore, it is essential
to handle high pruning well to avoid ambush
of the blueberry, in addition to more control in
the evaluations, evaluating a more significant
number of plants due to the high density; (5) Use
of nets: to prevent the entry of H. virescens in the
field. The use of nets reduces the entry of 80% of
lepidopterans (6) Know the neighboring crops:
to project the influence and management in the
field.

Ethological Control: The following are
recommended: (1) Use of molasses and light
traps: for H. virescens, ten molasses traps should
be used per hectare; (2) Pheromone use: the dose
for H. virescens is 10 to 15 pheromones per ha.
They must be placed from the beginning to the
end of the campaign. The pest population must
be evaluated weekly and correlated with the
captures in pheromones.

Biological Control: At least four techniques are

Narrea, M.; Huanuqueño, E.; Otoniel, J.; Vergara, J.
Peruvian Journal of Agronomy 6(1): 78-92 (2022)

https://doi.org/10.21704/pja.v6i1.1893

recommended: (1) Biological corridors: planting
the biological corridors around the field and
changing them 3 to 4 times a year. The goal is to
have flowers throughout the year because they are
a food source of pollen and nectar for predators
such as chrysopids and ladybugs, species like
fennel, yarrow, sage, alder, buttercup, and
sunflower; (2) Bedbugs: concerning predatory
bedbugs, biological corridors will be planted
to maintain them and guarantee their action of
preying eggs and larvae of H. virescens; (3)
Chrysopids: As for chrysopids, a minimum of
30 thousand per hectare should be released every
15 days and 2 to 3 releases should be made in
a row, always with prior evaluation. The larvae
need prey which are the eggs and larvae of H.
virescens. Adults need nectar and pollen; for this
reason, it is crucial to plant biological corridors;
(4) Pollinating bees: since the crop needs
pollinators, it is essential to use low-impact
products for predators and pollinators.

Chemical Control: Application of PQUAs and
PBUAs as follows:

PQUA: Use contact products such as emamectin
benzoate or chitin synthesis inhibitors as a last
resort.

PBUA: Use nuclear polyhedrosis virus in small
larvae and on well-wet foliage, preferably in
the afternoon or at night. For this, the use of
Bts products is known; the most pathogenic
commercial strains must be chosen, with doses
ranging from 300 to 700 gr per cyl. Like viruses,
they must be applied in the afternoon or at night
and are effective in stage III larvae. The larvae
are affected after feeding on the first day and
will die on the 4th-6th day. Bt continues to be a
powerful tool for controlling H. virescens larvae
as there is no resistance.

This proposal is based on organic agriculture’s
technological and profitability challenges (Dilas-
Jiménez et al., 2020).

Proposal for genetic improvement for durable
or quantitative resistance in cultivated
varieties of blueberries

The genetics of resistance to pests by crops
is under the control of two types of genes: (1)

Vertical resistance, of a specific race, of significant
effects and not durable; it is controlled by one
or a few genes, and its inheritance is qualitative;
(2) Horizontal resistance, of non-specific race,
of minor genes and long-lasting; it is controlled
by multiple genes, each of which contributes to
resistance and its inheritance is quantitative.

Quantitative resistance is the one we choose
in this work for being durable and can be used
by traditional methods with the support of
modern selection techniques. However, before
developing the genetic improvement proposal for
quantitative resistance in blueberries, we believe
it is necessary to point out the characteristics
of the techniques that we will propose to use,
and we will explain why we will not use other
techniques even though it is believed “that they
are the most indicated.”

This proposal follows these steps:

Identification of resistance genes

It is known that all cultivated varieties of
blueberries are susceptible to damage by H.
virescens; therefore, a collection of wild plant
material related to the cultivated blueberry will
be carried out; it will then be evaluated for
resistance, and those with good response will be
selected. Native varieties of wild relatives are a
pool of genes from which economic resources
are generated by developing improved varieties.

Some of the phenotypic characteristics
that should be evaluated are (1) Hardness of
the leaf in view that in the field, it is seen that
they are slightly attacked by H. virescens, (2)
Concentration of the fruit in the upper part so that
this pest does not have many organs at disposals
such as buds and flowers, in addition to being
able to program today’s scarce personnel in the
fields, (3) The distance between the buds so that
H. virescens does not have many microclimates
below the middle third of the plant. Experience:
The United States, through the United States
Department of Agriculture (USDA), the
Agricultural Research Service (ARS), and the
National Clonal Germplasm Repository (NCGR)
maintain a gene bank in Oregon with more than
1800 accessions of Vaccinium spp. which come
from 34 countries (Bassil et al., 2020).

Management of Chloridea virescens (Noctuidae) in blueberries (Vaccinium corymbosum L.) to promote sustainable cultivation in Peru: A Review

January - April 2022

Incorporation of genes from the wild relative to
the cultivated varieties

The samples (accessions) selected in the previous
step will be hybridized with the cultivated ones.
Experience: Allotetraploid hybrids derived
from the crossing of Vaccinium uliginosum and
Vaccinium vitis-idaea are fertile, thus offering
genetic variability from which to select many
characteristics, such as yield, fruit quality, and
adaptation to variable ecological conditions in
the breeding of V. vitis-idaea (Morozov, 2007).

Selection - backcross - selection, assisted by
modern techniques

In the hybrids derived from the previous cross,
the plants (F1) that have genes with quantitative
effects will be selected through modern techniques,
which will be backcrossed (F1 X cultivated)
with the cultivated varieties to recover the fruit
quality genes of the cultivated ones and will be
re-selected in the progeny of the backcross until
identifying plants with resistant quantitative trait
QTLs genes. Conventional genetic improvement
for quantitative resistance has given good results
(Kolmer, 1996); however, it has drawbacks.
First, an extensive group of individuals needs to
be evaluated to find the quantitative resistance
genes together; in addition, hundreds of plants
have to be inoculated or infested. These are
delicate activities, and it is not always possible
to inoculate or infest homogeneously in the
field. Modern techniques appear as a powerful
tool in enhancing the selection of these types
of characters. Experience: The use of molecular
markers in the genetic improvement of plants is
proven. Garkava-Gustavsson et al. (2005) used
RAPID and ISSR markers to assess the genetic
diversity of 15 mountain cranberry Vaccinium
vitis-idaea populations, 13 from Sweden,
Finland, Norway, Estonia, and Russia, and two
populations of V. minus from Japan and Canada.
Genetic differentiation between accessions
can be exploited in hybridization programs of
this species (Garkava-Gustavsson et al. 2005).
Marker-assisted selection (MAS) -for quantitative
inheritance traits- is being applied in breeding
programs and directed pyramiding in different
crops (Liu et al. 2004; Asea et al. 2009; Moloney
et al. 2010; Singh et al. 2005). Single nucleotide

polymorphisms (SNP) generated by genotyping
by sequencing (GBS) allowed identifying QTLs
of additive effect for resistance to Fusarium in
wheat (Zhang et al., 2020). In cotton, with the
same technology, 3187 polymorphic markers
were developed, which allowed the identification
of 17 quantitative trait loci (QTL) for the height
of the plant, the height of the first fruiting branch
node and the number of vegetative shoots (Qi et
al. 2017). Similarly, four QTLs for resistance and
one QTL for susceptibility to leaf rust in alfalfa
were identified in the genetic map in an alfalfa
mapping population (Adhikari & Missaoui,
2019).

Clonal propagation (asexual) of the selected
plants

Plants selected by modern techniques will be
multiplied asexually; they will be taken to field
trials with large plots. Experience: One of the most
significant advantages of the genus Vaccinium
is that it responds well to asexual propagation
both by in vitro methods and cuttings.Blueberry
species such as V. corymbosum, V. virgatum and
V. macrocarpon, they root up to 76% in medium
without growth regulators (Tetsumura et al. 2017
and Debnath and McRae 2011 cited by Erst et
al. 2018). In turn, Erst et al. 2018 specify that
most plants require specific chemicals for the
initiation of cell differentiation and the formation
of meristems, which is why, in its study by in vitro
methods, a rooting of up to 100% in blueberry
variety “Golubaya rossyp” was achieved. Guo et
al. (2019), using a rooting bag method, obtained
97.7% rooting after using the blueberry cultivar
‘Ozarkblue’ in a culture medium for woody plant
supplemented with 0.1 mg/l of IBA; likewise,
they achieved densities of 1600 seedlings per
m² compared to the traditional rooting method
that manages to put 270 to 420 seedlings per m²
(Guo et al. 2019). In micropropagation in vitro,
transgenic plants of V. corymbosum and V. vitis-
idaea had a better response in the regeneration of
shoots using zeatin at a concentration of 20μM
due to its effect on the induction of regeneration
of adventitious shoots from cut leaves. It is also
specified that in vitro they can be easily rooted
using IBA or ex vitro in a humidity chamber
without hormonal treatment (Meiners et al.
2007).

Narrea, M.; Huanuqueño, E.; Otoniel, J.; Vergara, J.
Peruvian Journal of Agronomy 6(1): 78-92 (2022)

https://doi.org/10.21704/pja.v6i1.1893

Identification of the best clone with quantitative
resistance

After vegetative multiplication, the plants
selected by modern techniques will be taken to
the field with natural and artificial inoculation;
at the end of the trial, the best material will have
been identified, which would be the improved
variety.

Why did we not choose CRISPR-Cas?: To apply
this technique, it is required that the quantitative
resistant genes have been identified first; likewise,
hundreds of genes would have to be edited at the
same time, which makes it almost impossible use
of this technique nowadays in the case of genetic
improvement in blueberry; also, it is still in the
process of refining, so it is not safe. Experience:
The CRISPR-Cas system, discovered as an
immune system acquired by certain bacteria,
seems to have notable advantages in gene editing
over ZFN and TALEN as they are potent tools
(Ran et al. 2013; Chen et al. 2019). In the yeast
Pichia pastoris, a CRISPR/Cas9 system was
developed with episomal sgRNA plasmid and
100% genome editing efficiency was obtained,
as well as high multicopy gene editing and stable
multigene editing without a substantial decrease
caused by multi-sgRNA (Yang et al. 2020).
However, off-target DNA cleavage remains
one of the major imperfections of the system,
including sequence mutation, rearrangement,
activation, and cell death during genome editing
(Chen et al. 2020).

Why do we not recommend Bt transgenic
with Cry proteins? Effects of resistance to Bt
transgenics: The main characteristic of Bt is
the production of protein crystals containing
toxins with specific activity against many pests,
including dipteran, lepidopteran and coleopteran
insects, as well as nematodes, protozoa,
trematodes, and mites (Adalat et al. 2020). The
gene variants of Cry toxins obtained from the
bacterium B. thuringiensis (Bt), due to their
insecticidal effect, have become an alternative
to chemical insecticides in agriculture (Zhou et
al. 2020; Grove et al. 2001; Zhang et al. 2018;
Zhang et al. 2020, because they control pests of
lepidoptera (moths) and coleoptera (beetles) that
feed on plants. Two bacterial isolates –variants

of Cry toxins-, controlled the cotton leaf worm,
Spodoptera littoralis (Boisd.) (Lepidoptera:
Noctuidae), with mortality rates of 100 and
96.6% (Abo-Bakr et al., 2020). Another chimeric
protein toxin involving CryIA residues 450-612,
demonstrated 30 times more activity against
H. virescens than the native parental toxin,
indicating that this region plays an essential role
in the specificity of H. virescens (Ge et al. 2020).
However, they are ineffective for sap-sucking
insects (Hemiptera) (Liu et al. 2020). Susceptible
insects acquire resistance in a few years, and
many new strains of Bt have been isolated to
avoid resistance to pests (Zhou et al., 2020).

The widespread cultivation of transgenic
soybeans has caused significant changes in the
spectrum of lepidopteran larvae, both in the
number of species and their densities in the field.
Transgenic crops that produce insecticidal toxins
from B. thuringiensis (Bt) have successfully
reduced the incidence of the most common
caterpillars that infest soybeans, such as
Anticarsia gemmatalis (Lepidoptera: Erebidae)
and Chrysodeixis includens (Lepidoptera:
Noctuidae). However, lepidopteran species
not previously registered have been found in
cultivation due to the possibility of adaptation
to genetically modified cultivars. For example,
the appearance of Peridroma saucia Hübner
(Lepidoptera: Noctuidae) is described for the first
time in Brazil, feeding on genetically modified
soybean cultivars (Takahashi et al. 2019). After
five years of research , Downes et al. (2010),
, found a significant exponential increase in
the frequency of alleles that confer resistance
to Cry2Ab in Australian field populations of
Helicoverpa punctigera, since the adoption of a
Bt cotton; in addition, the frequency of alleles of
resistance to the cry2Ab protein in populations
from cultivation areas is eight times higher than
those found for populations from regions not
cultivated with Bt; a similar result was found
for Diatraea saccharalis Fabricius (Grimi et al.
2018).

The development of resistance among
lepidopterans is a common phenomenon, and a
repertoire of resistance mechanisms to various
Cry toxins has been identified from a laboratory,
greenhouse, and field studies in this insect

Management of Chloridea virescens (Noctuidae) in blueberries (Vaccinium corymbosum L.) to promote sustainable cultivation in Peru: A Review

January - April 2022

(Peterson et al. 2017). Cases of pest resistance to
crystal proteins Bt (Cry) produced by transgenic
crops increased from 3 in 2005 to 16 in 2016
(Tabashnik et al., 2017). Gassmann (2016) found
that in laboratory selection experiments, the
western corn rootworm could develop resistance
to all types of Bt corn after three to seven
generations of selection. The “pyramids” of
transgenic crops that produce two or more toxins
of B. thuringiensis (Bt) active against the same
pest are used to delay the evolution of resistance
in insect pest populations (Santos-Amaya et
al., 2015). However, this strategy could fail if a
single gene in a pest confers resistance to many
toxins, as happened with the CP73 strain of the
cotton pest H. virescens (F.), which is resistant
to the Cry1Ac and Cry2Aa toxins of Bt (Gahan
et al. 2005). All the blueberry varieties grown in
Peru are introduced. Unfortunately, no work has
been done to evaluate resistance to Chloridea
virecens, and it seems that they are susceptible
since this pest has been found in all of them;
however, resistance genes will be donated by
wild relatives collected in Peru, if a genetic
improvement program is developed.

In 2005, seven years after releasing a transgenic
Bt variety of maize resistant to Busseola fusca
(Lepidoptera noctuidae), significant levels of
pest survival were observed (Van den Berg et al.
2013). Under laboratory conditions, Gassman
(2016), showed that between three and seven
generations of selection, the pest Diabrotica
virgifera could generate resistance to all types
of Cry proteins. In Australia, a population of
Helicoverpa armigera developed resistance to
the Cry1Ac toxin from B. thuringiensis because
around 70% of resistant larvae H. armigera were
able to survive on Cry1Ac transgenic cotton
(Gunning, 2005).

FINAL COMMENTS
The integrated management of blueberries,
especially the PBUA chemical control with
products based on Bt proteins Cry, and
the biological control are highly explicitly
recommended for controlling Chloridea
virescens.

The proposal for genetic improvement of

varieties of good yield and acceptable quality
but susceptible constitutes a good strategy in the
medium and long term. Using native varieties
would allow the possibility of accumulating
genes of lasting resistance for local pests in
the susceptible ones. With modern selection
techniques, this activity would be more efficient
and results in a shorter time than what would be
obtained with the traditional method alone.

Conflicts of interest
The signing authors of this research work declare that they
have no potential conflict of personal or economic interest
with other people or organizations that could unduly
influence this manuscript.

Author contributions
Elaboration and execution, Development of methodology,
Conception and design; Editing of articles and supervision
of the study have involved all authors.

ORCID and e-mail
M. Narrea mnarrea@lamolina.edu.pe

https://orcid.org/0000-0002-5565-746X

E. Huanuqueño ehh.coca@lamolina.edu.pe

https://orcid.org/0000-0002-9118-0662

J. Dilas-Jiménez jdilas@unat.edu.pe

https://orcid.org/0000-0003-4256-8393

J. Vergara javergara@unc.edu.pe

https://orcid.org/0000-0002-8583-4404

References

Abo-Bakr, A., Fahmy, E. M., Badawy, F., Abd El-latif, A. O.,
& Moussa, S. (2020). Isolation and characterization
of the local entomopathogenic bacterium, Bacillus
thuringiensis isolates from different Egyptian soils.
Egyptian Journal of Biological Pest Control, 30(1),
1–9.

Adalat, R., Saleem, F., Crickmore, N., Naz, S., & Shakoori,
A. R. (2017). In vivo crystallization of three-domain
Cry toxins. Toxins, 9(3), 80.

Adhikari, L., & Missaoui, A. M. (2019). Quantitative trait
loci mapping of leaf rust resistance in tetraploid
alfalfa. Physiological and Molecular Plant
Pathology, 106, 238–245.

Agrodata Perú. (2020a). Arándanos Perú Exportación
2019-diciembre. https://www.agrodataperu.
com/2020/01/arandanos-peru-exportacion-2019-
diciembre.html

Narrea, M.; Huanuqueño, E.; Otoniel, J.; Vergara, J.
Peruvian Journal of Agronomy 6(1): 78-92 (2022)

https://doi.org/10.21704/pja.v6i1.1893

Agrodata Perú. (2020b). Arándanos: ¿por qué si el
Perú es el primer exportador en el mundo aún no
conquista nuestra mesa? https://www.agrodataperu.
com/2020/03/arandanos-peru-primer-exportador-
mundial.html

Asea, G., Vivek, B. S., Bigirwa, G., Lipps, P. E., & Pratt,
R. C. (2009). Validation of consensus quantitative
trait loci associated with resistance to multiple
foliar pathogens of maize. Phytopathology, 99(5),
540–547.

Bassil, N., Bidani, A., Nyberg, A., Hummer, K., & Rowland,
L. J. (2020). Microsatellite markers confirm identity
of blueberry (Vaccinium spp.) plants in the USDA-
ARS National Clonal Germplasm Repository
collection. Genetic Resources and Crop Evolution,
1–17.

Blanco, C. A., Terán-Vargas, A. P., Abel, C. A., Portilla,
M., Rojas, M. G., Morales-Ramos, J. A., &
Snodgrass, G. L. (2008). Plant host effect on the
development of Heliothis virescens F. (Lepidoptera:
Noctuidae). Environmental Entomology, 37(6),
1538–1547.

Bravo A., Gill S.S., Soberón M. (2007). Mode of action of
Bacillus thuringiensis Cry and Cyt toxins and their
potential for insect control. Toxicon 49: 423–435.

Buzeta, A. (1997). Chile: Bayas para el 2000. Fundación
Chile 133 p. Concepción, facultad de Agronomía.
Chile.

CARE Perú. (August, 2006). Manejo integral de plagas
- Guia para pequeños productores agrarios. Lima
Perú, s.e.

Chen, K., Wang, Y., Zhang, R., Zhang, H., & Gao, C.
(2019). CRISPR/Cas genome editing and precision
plant breeding in agriculture. Annual review of plant
biology, 70, 667–697.

Chen, S., Yao, Y., Zhang, Y., & Fan, G. (2020). CRISPR
system: Discovery, development and off-target
detection. Cellular Signalling, 70, 109577.

Cisternas A., Ernesto. (2013). Insect pest of economic
importance associated with blueberry. Cap. 8
Blueberry Manual. Chile.

Cock, M. J. (2019). Unravelling the status of partially
identified insect biological control agents
introduced to control insects: an analysis of
BIOCAT2010. BioControl, 64(1), 1–7.

Contreras-Pérez, M., Hernández-Salmerón, J., Rojas-
Solís, D., Rocha-Granados, C., del Carmen Orozco-
Mosqueda, M., Parra-Cota, F. I., ... & Santoyo, G.
(2019). Draft genome analysis of the endophyte,
Bacillus toyonensis COPE52, a blueberry

(Vaccinium spp. var. Biloxi) growth-promoting
bacterium. 3 Biotech, 9(10), 1–6.

Deguine, J. P., Aubertot, J. N., Flor, R. J., Lescourret,
F., Wyckhuys, K. A., & Ratnadass, A. (2021).
Integrated pest management: good intentions,
hard realities. A review. Agronomy for Sustainable
Development, 41(3), 1–35

Dilas-Jiménez, J. O., & Cernaqué, O. (2017). El sector
cafetalero peruano: Un enfoque a la CTI para su
competitividad. Universidad Continental.

Dilas-Jiménez, J., Zapata-Ruiz, D., Arce-Almenara,
M., Ascurra-Toro, D., & Mugruza-Vassallo, C.
(2020). Análisis comparativo de los costos de
producción y rentabilidad de los cafés especiales
con certificación orgánica y sin certificación. South
Sustainability, 1(2), e017.

Downes, S., Parker, T., & Mahon, R. (2010). Incipient
resistance of Helicoverpa punctigera to the Cry2Ab
Bt toxin in Bollgard II® cotton. PLoS One, 5(9),
e12567.

Erst, A. A., Gorbunov, A. B., & Erst, A. S. (2018). Effect
of concentration, method of auxin application and
cultivation conditions on in vitro rooting of bog
blueberry (Vaccinium uliginosum L.). Journal of
Berry Research, 8(1), 41–53.

Eskov, E. K. (2017). The diversity of ethological
and physiological mechanisms of acoustic
communication in insects. Biophysics, 62(3), 466–
478.

Food and Agriculture Organization. (2002). Manual
Práctico - Manejo Integrado de Plagas y
Enfermedades en cultivos hidropónicos en
invernadero. s.l., s.e.

Food and Agriculture Organization. (2014). The
international code of conduct on pesticide
management.

Febres, F. (2013). Resultados en Arándano deben ser vistos
con serenidad. Revista Red Agrícola no. 11, 6–9.

Feitelson J. S.; Payne J., & Kim L. (1992). Bacillus
thuringiensis: insects and beyond. Nat. Biotech. 10,
271–275.

Flores, A., Alcarraz, M., Woolcott, J. C., Benavides,
E., Godoy, J., Huerta, D., ... & Patiño, A. (2011).
Biodiversidad de Bacillus thuringiensis aislados de
agroecosistemas peruanos y evaluación del potencial
bioinsecticida. Ciencia e Investigación, 14(1), 30–
35.

Gahan, L. J., Ma, Y. T., MacgregorCoble, M. L., Gould, F.,
Moar, W. J., & Heckel, D. G. (2005). Genetic basis
of resistance to Cry1Ac and Cry2Aa in Heliothis

Management of Chloridea virescens (Noctuidae) in blueberries (Vaccinium corymbosum L.) to promote sustainable cultivation in Peru: A Review

January - April 2022

virescens (Lepidoptera: Noctuidae). Journal of
economic entomology, 98(4), 1357–1368.

García Rubio, JC; Gonzáles de Lena, G; Ciordia Ara,
M. (2018). El cultivo del arándano en el norte de
España. Asturias, España, s.e. [19 jul. 2020]. http://
www.serida.org/pdfs/7452.pdf

Gargurevich, G. (2017). Biloxi ¿la red globe de los
arándanos? Revista Red agrícola, 39(1), 24-26.

Garkava-Gustavsson, L., Persson, H. A., Nybom, H.,
Rumpunen, K., Gustavsson, B. A., & Bartish, I. V.
(2005). RAPD-based analysis of genetic diversity
and selection of lingonberry (Vaccinium vitis-
idaea L.) material for ex situ conservation. Genetic
Resources and Crop Evolution, 52(6), 723–735.

Gassmann, A. J. (2016). Resistance to Bt maize by western
corn rootworm: insights from the laboratory and the
field. Current opinion in insect science, 15, 111–115.

Gerber D., & Shai Y. (2000). Insertion and organization
within membranes of the δ-endotoxin pore-forming
domain, helix 4-loop-helix 5, and inhibition of its
activity by a mutant helix 4 peptide. J. Biol. Chem.,
275, 23602–23607.

Gestión. (July, 2019). Producción de arándanos en Perú
crece 796% más que hace cuatro años, pero su
precio en chacra cae | Economía (on line)). https://
gestion.pe/economia/arandanos-produccion-
minagri-produccion-de-arandanos-en-peru-crece-
796-mas-que-hace-cuatro-anos-pero-su-precio-en-
chacra-cae-noticia/?ref=gesr

Grove, M., Kimble, W., & McCarthy, W. J. (2001). Effects
of individual Bacillus thuringiensis insecticidal
crystal proteins on adult Heliothis virescens (F.)
and Spodoptera exigua (Hubner) (Lepidoptera:
Noctuidae). BioControl, 46(3), 321–335.

Grimi, D. A., Parody, B., Ramos, M. L., Machado, M.,
Ocampo, F., Willse, A., ... & Head, G. (2018).
Field‐evolved resistance to Bt maize in sugarcane
borer (Diatraea saccharalis) in Argentina. Pest
management science, 74(4), 905–913.

Gunning, R. V., Dang, H. T., Kemp, F. C., Nicholson, I. C.,
& Moores, G. D. (2005). New resistance mechanism
in Helicoverpa armigera threatens transgenic crops
expressing Bacillus thuringiensis Cry1Ac toxin.
Applied and environmental microbiology, 71(5),
2558–2563.

Guo, Y. X., Zhao, Y. Y., Zhang, M., & Zhang, L. Y. (2019).
Development of a novel in vitro rooting culture
system for the micropropagation of highbush
blueberry (Vaccinium corymbosum) seedlings.
Plant Cell, Tissue and Organ Culture (PCTOC),
139(3), 615–620.

Gurr, G. M., Wratten, S. D., Tylianakis, J., Kean J., &
Keller M. (2004). Providing Plant Foods for Insect
Natural Enemies in Farming Systems: Balancing
Practicalities and Theory, in F.L.

Hancock, J. (2009). Producción de arándano Alto.
Agronomijas Vēstis, (12), 35–38.

Jiménez, EM. (July, 2009). Métodos de Control de Plagas.
Managua, Nicaragua, s.e. https://cenida.una.edu.ni/
relectronicos/RENH10J61me.pdf

Jurat-Fuentes, J. L., & Crickmore, N. (2017). Specificity
determinants for Cry insecticidal proteins: Insights
from their mode of action. Journal of invertebrate
pathology, 142, 5–10.

Kamatham, S., Munagapati, S., Manikanta, K. N., Vulchi,
R., Chadipiralla, K., Indla, S., & Allam, U. S.
(2021). Recent advances in engineering crop plants
for resistance to insect pests. Egypt J Biol Pest
Control, 31, 120.

Kolmer, J. A. (1996). Genetics of resistance to wheat leaf
rust. Annual review of phytopathology, 34(1), 435–
455.

Landis, D., Wratten, S., & Gurr, G. (2000). Habitat
management to conserve natural enemies of
arthropod pests in Agriculture. Annual review of
entomology, 45, 175–201. https://doi.org/10.1146/
annurev.ento.45.1.175

Liu, B., Zhang, S., Zhu, X., Yang, Q., Wu, S., Mei, M.,
... & Leung, H. (2004). Candidate defense genes as
predictors of quantitative blast resistance in rice.
Molecular Plant-Microbe Interactions, 17(10),
1146–1152.

Liu, Y., Wang, Y., Shu, C., Lin, K., Song, F., Bravo, A.,
... & Zhang, J. (2018). Cry64Ba and Cry64Ca, Two
ETX/MTX2-type Bacillus thuringiensis insecticidal
proteins active against hemipteran pests. Appl.
Environ. Microbiol., 84(3), e01996-17.

Llanos, A., & Apaza, W. (2018). Antifungal activity of
five chemical and two biological fungicides for
the management of Botrytis cinerea, causal agent
of Gray Mold in Strawberry. Peruvian Journal of
Agronomy, 2(1), 1–8

Ministerio de Desarrollo Agrario y Riego. (August, 2020).
El arándano en el Perú y en el mundo- Producción,
Comercio y Perspectivas. Lima. Perú. Pág. 8.

Meiners, J., Schwab, M., & Szankowski, I. (2007). Efficient
in vitro regeneration systems for Vaccinium species.
Plant Cell, Tissue and Organ Culture, 89(2-3), 169–
176.

Meyer, H. J. & Prinsloo N. (2003). Assessment of the
potential of blueberry production in South Africa.

Narrea, M.; Huanuqueño, E.; Otoniel, J.; Vergara, J.
Peruvian Journal of Agronomy 6(1): 78-92 (2022)

https://doi.org/10.21704/pja.v6i1.1893

Small Fruits Review, 2, 3–21.

Moloney, C., Griffin, D., Jones, P. W., Bryan, G. J.,
McLean, K., Bradshaw, J. E., & Milbourne, D.
(2010). Development of diagnostic markers for
use in breeding potatoes resistant to Globodera
pallida pathotype Pa2/3 using germplasm derived
from Solanum tuberosum ssp. andigena CPC 2802.
Theoretical and applied genetics, 120(3), 679–689.

Morales, C. G. (2017). Manual de manejo agronómico del
arándano (on line). Chile, s.e. [2 jul. 2020]. https://
www.indap.gob.cl/docs/default-source/default-
document-library/manual-arandanos.pdf?sfvrsn=0

Morozov, O. V. (2007). The Prospects for Using Vaccinium
uliginosum L.× Vaccinium vitis-idaea L. Hybrid in
Breeding. International journal of fruit science,
6(4), 43–56.

Ochoa, G., & Arrivillaga, J. (2009). Bacillus thuringiensis:
Avances y perspectivas en el control biológico de
Aedes aegypti. Boletín de Malariología y Salud
Ambiental, 49(2), 181–191.

Qi, H., Wang, N., Qiao, W., Xu, Q., Zhou, H., Shi, J., ...
& Huang, Q. (2017). Construction of a high-density
genetic map using genotyping by sequencing
(GBS) for quantitative trait loci (QTL) analysis of
three plant morphological traits in upland cotton
(Gossypium hirsutum L.). Euphytica, 213(4), 83.

Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D.
A., & Zhang, F. (2013). Genome engineering using
the CRISPR-Cas9 system. Nature protocols, 8(11),
2281–2308.

Rashki, M., Maleki, M., Torkzadeh-Mahani, M., Shakeri,
S., & Nezhad, P. S. (2021). Isolation of Iranian
Bacillus thuringiensis strains and characterization
of lepidopteran-active cry genes. Egyptian Journal
of Biological Pest Control, 31(1), 1–10.

Rivadeneira, M., & Carlazara G. (2011). Comportamiento
fenológico de variedades tradicionales y nuevas
de arándanos. Instituto Nacional de Tecnología
agropecuaria. Argentina.

Rodríguez-Saona, C., Cloonan, K. R., Sanchez-Pedraza,
F., Zhou, Y., Giusti, M. M., & Benrey, B. (2019).
Differential susceptibility of wild and cultivated
blueberries to an invasive frugivorous pest. J Chem
Ecol.45(3).

Santos-Amaya, O. F., Rodrigues, J. V., Souza, T. C.,
Tavares, C. S., Campos, S. O., Guedes, R. N.,
& Pereira, E. J. (2015). Resistance to dual-gene
Bt maize in Spodoptera frugiperda: selection,
inheritance, and cross-resistance to other transgenic
events. Scientific reports, 5, 18243.

Sauka, D. (2007). Estudio de genes y proteínas insecticidas
de aislamientos nativos de Bacillus thuringiensis.
Aportes al conocimiento de su distribución
y toxicidad en plagas agrícolas. [Doctoral
dissertation, UBA].

Sauka, D. H., & Benintende G. B. (2008). Bacillus
thuringiensis: generalidades. Un acercamiento a
su empleo en el biocontrol de insectos lepidópteros
que son plagas agrícolas. Revista Argentina de
Microbiología, 40 (2), 124–140.

Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum
J., & Feitelson J. (1998). Bt and its pesticidal cristal
proteins. Microbiol. Mol. Biol. Rev. 62, 775–806.

Sierra Exportadora. (2011). Perfil Comercial-Arándano
Deshidratado. Asociación Regional de Exportadores
de Lambayeque. Área de Comercio Exterior.

Sierra Exportadora – Presidencia del Consejo de Ministros
de Perú (PCM). (2012). Estudio de prefactibilidad
para la producción y comercialización de arándanos
(Vaccinium corymbosum L.) en condiciones de
valles andinos. Estudio elaborado por Ing. Liliana
Benavides. 146 pp.

Singh, R. P., Huerta-Espino, J. U. L. I. O., & William, H. M.
(2005). Genetics and breeding for durable resistance
to leaf and stripe rusts in wheat. Turkish Journal of
Agriculture and Forestry, 29(2), 121–127.

Tabashnik, B. E., & Carrière, Y. (2017). Surge in insect
resistance to transgenic crops and prospects for
sustainability. Nature Biotechnology, 35(10), 926.

Takahashi, T. A., Nishimura, G., Carneiro, E., & Foerster,
L. A. (2019). First record of Peridroma saucia
Hübner (Lepidoptera: Noctuidae) in transgenic
soybeans. Revista Brasileira de entomologia, 63(3),
199–201.

Peterson, B., Bezuidenhout, C. C., & Van den Berg, J.
(2017). An overview of mechanisms of Cry toxin
resistance in lepidopteran insects. Journal of
Economic Entomology, 110(2), 362–377.

Vachon V., Laprade R., & Schwartz J. L. (2012).
Current models of the mode of action of Bacillus
thuringiensis insecticidal crystal proteins: A critical
review. J. Invertebr. Pathol. In press.

Vallejo, F., & Estrada, E. (2002). Mejoramiento genético
de plantas. [Universidad Nacional de Colombia].
DIPAL. Palmira, Colombia. 404 p.

Van den Berg, J., Hilbeck, A., & Bøhn, T. (2013). Pest
resistance to Cry1Ab Bt maize: Field resistance,
contributing factors and lessons from South Africa.
Crop Protection, 54, 154–160.

Yang, Y., Liu, G., Chen, X., Liu, M., Zhan, C., Liu, X.,

Management of Chloridea virescens (Noctuidae) in blueberries (Vaccinium corymbosum L.) to promote sustainable cultivation in Peru: A Review

January - April 2022

& Bai, Z. (2020). High efficiency CRISPR/Cas9
genome editing system with an eliminable episomal
sgRNA plasmid in Pichia pastoris. Enzyme and
Microbial Technology, 138. 109556.

Zhang, P., Guo, C., Liu, Z., Bernardo, A., Ma, H., Jiang,
P., ... & Bai, G. (2020). Quantitative trait loci for
Fusarium head blight resistance in wheat cultivars
Yangmai 158 and Zhengmai 9023. The Crop
Journal, 9(1), 143–153.

Zhang, X., Gao, T., Peng, Q., Song, L., Zhang, J., Chai, Y.,
... & Song, F. (2018). A strong promoter of a non-
cry gene directs expression of the cry1Ac gene in
Bacillus thuringiensis. Applied microbiology and
biotechnology, 102(8), 3687–3699.

Zhou, Y., Wu, Z., Zhang, J., Wan, Y., Jin, W., Li, Y., &
Fang, X. (2020). Bacillus thuringiensis novel toxin
Epp is toxic to mosquitoes and Prodenia litura
larvae. Brazilian Journal of Microbiology, 1–9.