Keywords:

Biodiversity

Natural enemies

Conservation biological control

Entomofauna present in plant shelters in a vineyard var. Crimson Seedless in Ica-Peru

Entomofauna presente en refugios vegetales en un campo de vid var. Crimson Seedless en Ica-Perú

Entomofauna em faixas de plantas silvestres em um campo de vinha var. Crimson Seedless em Ica-

Peru

Mónica Narrea-Cango

Luz Gómez Pando

Rev. Fac. Agron. (LUZ). 2024, 41(2): e244119

ISSN 2477-9407

DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v41.n2.09

Crop production

Associate editor: Dra. Lilia Urdaneta

University of Zulia, Faculty of Agronomy

Bolivarian Republic of Venezuela

Programa de Doctorado en Agricultura Sustentable.

Universidad Nacional Agraria La Molina. Av. La Molina s/n,

La Molina, Lima, Perú.

Departamento Académico de Fitotecnia. Facultad de

Agronomía. Universidad Nacional Agraria La Molina. Av.

La Molina s/n, La Molina, Lima, Perú.

Received: 01-03-2024

Accepted: 19-05-2024

Published: 11-06-2024

Abstract

The use of chemical pesticides to control pests also aects

benecial insects, so it is necessary to implement mechanisms

that allow them to be protected and promote their development.

In the present investigation, three plant shelters were installed to

identify their entomofauna and determine the plant species with

the potential to host biological controllers of grapevine pests. The

study was carried out in the 2020-21 growing season, with seven

plant species to make up three plant shelters (A, B, and C) that were

installed on the edges of a vineyard of the Crimson Seedless variety

in Ica, Peru. In total, 1,209 insects were reported, in six orders, nine

families, and fteen species; the most abundant were pollinators,

followed by phytophagous, predators, and some parasitoids. There

were no statistical dierences between the shelters in terms of

the abundance of parasitoids and pollinators, but there were in

predators and phytophagous specically between shelters A and B

with C. Shelters A and B, which included the fennel Foeniculum

vulgare Mill., stood out for having a larger population of predators,

including Chrysoperla externa (Hagen), the main controller of

the “vine mealybug” (Planococcus spp.). The importance of plant

shelters was demonstrated and their implementation in vineyards

is recommended to promote biological control and contribute to

integrated pest management in this crop.

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

Rev. Fac. Agron. (LUZ). 2024, 41(2): e244119 April-June. ISSN 2477-9407.

2-6 |

Resumen

El uso de plaguicidas químicos para controlar plagas, afecta

también a los insectos benécos, por lo que es necesario implementar

mecanismos que permitan protegerlos y favorecer su desarrollo. En

la presente investigación se instalaron tres refugios vegetales con el

propósito de identicar su entomofauna y determinar las especies

vegetales con potencial para albergar controladores biológicos de

plagas de la vid. El estudio se realizó en la campaña agrícola 2020-21,

con siete especies vegetales para conformar tres refugios (A, B y C)

que fueron instalados en los bordes de un campo de vid de la variedad

Crimson Seedless en Ica, Perú. En total se reportaron 1.209 insectos,

en seis órdenes, nueve familias y 15 especies; los más abundantes

fueron los polinizadores, seguidos de tófagos, predadores y algunos

parasitoides. No hubo diferencias estadísticas entre los refugios en

cuanto a la abundancia de parasitoides y polinizadores, pero si en

predadores y tófagos especícamente entre los refugios A y B con

el C. Los refugios A y B que incluían al hinojo Foeniculum vulgare

Mill., destacaron por albergar mayor población de predadores, entre

ellos destaca Chrysoperla externa (Hagen), principal controlador de

la “cochinilla harinosa de la vid” (Planococcus spp.). Se demostró

la importancia de los refugios vegetales y se recomienda su

implementación en los viñedos para fomentar el control biológico y

contribuir al manejo integrado de plagas en este cultivo.

Palabras clave: biodiversidad, enemigos naturales, control biológico

conservativo.

Resumo

A utilização de pesticidas químicos para controlo de pragas

também afeta os insetos benécos, pelo que é necessário

implementar mecanismos que permitam protegê-los e promover

o seu desenvolvimento. Na presente investigação foram instalados

três faixas de plantas silvestres com o objetivo de identicar a sua

entomofauna e determinar as espécies vegetais com potencial para

acolher controladores biológicos de pragas da videira. O estudo

foi realizado na campanha agrícola 2020-21, com sete espécies de

plantas para compor três faixas de plantas silvestres (A, B e C) que

foram instalados nas bordas de um campo de vinha da variedade

Crimson Seedless em Ica, Peru. No total foram relatados 1.209

insetos, distribuídos em seis ordens, nove famílias e 15 espécies; os

mais abundantes foram os polinizadores, seguidos pelos lófagos,

predadores e alguns parasitoides. Não houve diferenças estatísticas

entre os faixas de plantas silvestres em termos de abundância de

parasitoides e polinizadores, mas houve em predadores e lófagos

especicamente entre os faixas de plantas silvestres A e B com C.

Destacaram-se os faixas de plantas silvestres A e B, que incluíam

a erva-doce Foeniculum vulgare Mill., por seu hospedeiro uma

maior população de predadores, dentre eles destaca-se Chrysoperla

externa (Hagen), principal controladora da “cochonilha da videira”

(Planococcus spp.). Foi demonstrada a importância dos abrigos

vegetais e recomenda-se a sua implementação nas vinhas para

promover o controlo biológico e contribuir para a gestão integrada de

pragas nesta cultura.

Palavras-chave: biodiversidade, inimigos naturais, controle

biológico por conservação.

Introduction

The grapevine is a very important crop in Peru, which is seriously

attacked by several pests such as woodlouse, thrips, and mites,

among others (Cáceres & Julca, 2018); to control them, chemical

pesticides are generally used, which at the same time aect and

reduce the population of biological controllers, aecting the natural

and applied biological control of the crop (Vázquez et al.,2008).

Therefore, promoting actions that favor the presence and growth of

benecial fauna is necessary for the development of the crop. One

of these actions is the planting of plants that provide food, shelter,

and protection for biological controllers (Landis et al., 2000); and

especially in vineyards, the planting of owering plants is preferable,

because it allows maintaining and increasing the richness, diversity,

and abundance of predators and pollinators (López et al., 2019).

The management of agricultural habitat through the planting of

varied plants or “plant shelters” then becomes one more strategy of

integrated pest management (González-Chang et al., 2019).

Plant shelters near vineyards are benecial (Altieri et al., 2007;

López et al., 2019), as long as the most suitable plants are selected

to ensure the presence of biological controllers (Fiedler & Landis,

2007) and do not promote the development of pests. Asteraki et al.

(2004) assert that diverse vegetation generates favorable conditions

for benecial entomofauna and López et al. (2003) point out that the

management of native (wild) plants can improve natural pest control.

In Peru, there are few studies on the use of plant shelters and none

on grapevines, so the objective of this work was to study three plant

shelters, identify their entomofauna, and determine the plant species

with the potential to host biological controllers of grapevine pests.

Materials and methods

The study was carried out in the surroundings of a vineyard of the

Crimson Seedless variety, located in Ica-Peru, at 75°42’0.00” south

and 14°0’0.00” west at an altitude of 535 m.a.s.l.; between march

2020 and march 2021 (2020-2021 growing season).

Selection of plant species

A bibliographic search of angiosperms with reports of harboring

biological controllers and that they met the following criteria was

carried out to make their use as a plant shelter more feasible in case

of positive results:

1: Available in nurseries or present wild in crop elds.

2: Low water requirement to withstand the grapevine dormancy

period.

3: Use as aromatic, medicinal, forage, or ornamental plants.

4: Not considered weeds or main hosts of common grapevine

pests.

Based on the established criteria, the following species were

chosen, whose distribution in the plant shelters is detailed in the

following table.

Installation of plant shelters

The plants were sown in seedbeds from commercial seeds and

when they reached a minimum of 10 cm they were distributed in

three groups (shelters A, B, and C) based on the fact that each group

was made up of botanical species from at least two dierent families

(table 1). The transplanting was carried out at the edge of the vineyard

(at each post of the vine plant support line), at a rate of six plants per

shelter (two of each plant species arranged in double rows) with eight

repetitions for each shelter and a separation of three meters between

each repetition.

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

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3-6 |

Table 1. Plants of the three plant shelters.

Shelter Scientic name Common name Family

A Calendula ocinalis L. Calendula Asteraceae

Helianthus annuus L. Sunower Asteraceae

Foeniculum vulgare Mill Fennel Apiaceae

B Zinnia acerosa (DC) Zinnia Asteraceae

Crotalaria incana L. Crotalaria Fabaceae

Foeniculum vulgare Mill Fennel Apiaceae

C Crotalaria incana L. Crotalaria Fabaceae

Salvia splendens L. Salvia Lamiaceae

Ocimum basilicum L. Basil Lamiaceae

The evaluations were carried out on a biweekly basis, at the same

time (10:00 a.m.) and with an approximate duration of one minute/

plant; the technique of direct observation was used, reviewing the

structure of each plant to detect, identify and record the entomofauna

present; unidentied specimens were manually collected in the

eld in 70 % alcohol jars and were taken to the Klaus Raven Büller

Entomology Museum Laboratory of the National Agrarian University

La Molina, for subsequent identication.

To determine species richness (Margalef Index (DMg)),

dominance (Simpson’s Index (D)), and Pielou’s evenness (J’), the

PAST: statistical software for paleontology and biodiversity was

used. Statistical analysis by functional group between shelters was

done using the InfoStat program.

Results and discussion

Abundance of general entomofauna and main species found

A total of 1,209 insects belonging to 15 species, nine families, six

orders, and four functional groups were detected in the three plant

shelters (table 2). Hymenoptera (35.7 %) was the most abundant

order and had the highest number of families and species, mainly

Apis mellifera L., the dominant species (32.5 %), presumably due to

the available supply of owers and pollen oered by the three shelters;

Zumbado & Azofeifa (2018) highlight the role of Hymenoptera as

the most important group of angiosperm pollinators, but also for

being made up of many biological controllers of agricultural pests.

The other braconid Hymenoptera and Ichneumonidae were scarce;

according to García-Gutierrez, et al. (2013), these Hymenoptera are

common parasitoids of Lepidoptera and Coleoptera, which would

explain their low presence in the surroundings of the vineyard, a crop

whose main pests do not belong to any of these orders.

Diptera (24.07 %) was the second most abundant order, and

like the Hymenoptera, it was composed of insects of importance as

pollinators and biological controllers, highlighting the blowies of

the family Calliphoridae: Chrysomya sp. (21.09 %) as the second

dominant species, which in the present study was found in owers

as well as bees; in Colombia C. putoria (Wiedemann) is common

in avocado owers (Persea americana Mill) (Carabalí-Banguero et

al., 2018) and in Turkey, much of the mango production (Mangifera

indica L.) is due to C. megacephala Fabricius (Nurul et al., 2015).

The two hovery species, Allograpta exotica and Pseudodorus

clavatus, are reported as predators of true bug pests (Hemiptera),

mainly aphids (Soca-Flores et al., 2022; Arcaya et al., 2013) and

are also associated with the importance of the presence of owering

plants in the environment of agricultural elds (Bertolaccini et al.,

2008; Morales & Köhler, 2008).

Thysanoptera, third in abundance (16.87 %) fully represented by

Thrips tabaci is usually found in the grapevine in the phenological

stage of owering and initiation of fruit set (Viglianco et al., 2021);

their presence in plant shelters should not be considered harmful,

taking into account that phytophagous act as alternative prey for

natural controllers to continue their biological cycle when they do not

nd their prey in the elds, this usually happens during agrochemical

applications (Peredo et al., 2020). Neuroptera with the green lacewing

Chrysoperla externa, occupied the fourth place in abundance (9.93 %),

the presence of this predator was an important result considering that,

Table 2. Abundance of entomofauna in three plant shelters adjacent to a vineyard in Ica-Peru.

Order Family Species/Morphospecies FG

Shelter

A B C

Coleoptera Coccinellidae Harmonia axyridis (Pallas) P 12 9 3

Hipodamia convergens Guerin-Meneville P 21 9 0

Cicloneda sanguinea L. P 12 3 0

Diptera Syrphidae Allograpta exotica (Wiedemann) P 18 0 6

Pseudodorus clavatus (Fabricius) P 6 3 3

Calliphoridae Chrysomya sp. Po 129 114 12

Hemiptera Aphididae Aphis cracivora Koch F 6 9 0

Aphis spiraecola Match F 51 27 0

Hymenoptera Braconidae Braconidae sp. 1 Pa 3 3 3

Braconidae sp. 2 Pa 0 3 3

Ichneumonidae Ichneumonidae sp. Pa 6 6 0

Apidae Apis mellifera L. Po 138 84 171

Bombus sp. Po 0 3 9

Neuroptera Chrysopidae Chrysoperla externa P 48 51 21

Thysanoptera Thripidae Thrips tabaci Lind. F 114 72 18

FG = Functional group; P = Predator; Po=Pollinator; F=Phytophagous; Pa=Parasitoid.

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

Rev. Fac. Agron. (LUZ). 2024, 41(2): e244119 April-June. ISSN 2477-9407.

4-6 |

in the vineyards of Peru, its release is common to control a wide range

of soft-bodied insects, mainly due to its eectiveness as a controller,

its adaptation to various agricultural environments and its resistance

to several pesticides (Núñez, 1989).

Finally, Hemiptera and Coleoptera, both represented by only

families, Aphididae and Coccinellidae respectively, together

constituted less than 14 % of the insects recorded in the evaluated

shelters. According to Greco & Roca (2020), Coleoptera is one of the

most used orders in biological control programs and Coccinellidae is

one of its main families, so despite the low population reported, it is

relevant if we take into account that they feed on insects considered

by Evans (2009) as pests of the grapevine: aphids (Aphididae),

mealybugs (Pseudococcidae), whiteies (Aleyrodidae) and thrips

(Thysanoptera).

The four functional groups found were: pollinators, phytophagous,

predators, and parasitoids, coinciding with similar studies carried

out in vineyards (Miles et al., 2012; López et al., 2019), where the

presence of these four functional groups conrms that when the

structure of the agricultural environment is diversied, insects appear,

including many benecial ones available to potentiate the biological

control of many pests. In the present study, the proportion of the

functional groups of shelters A and B was similar to that of the total,

except for shelter C, where there were more pollinators and fewer

phytophagous plants (gure 1).

Figure 1. Abundance of entomofauna by functional group.

Statistical analysis and biodiversity indices

As reported in table 3, there are no signicant dierences between

shelters A, B, and C in terms of the abundance of pollinators and

parasitoids, but there are signicant dierences between shelters A

and C in terms of predators and between shelters A and B with C in

terms of phytophagous; in general, and statistical terms, shelters A and

B were more similar to each other, with respect to the composition of

the functional groups.

The highest values of richness and diversity were found in shelters

A and B, being consistent with the greater number of individuals and

species that both shelters hosted. The lowest evenness index was

found in shelter C, which is explained by the majority presence of

Apis mellifera, which with 68.67 % was the dominant species in this

shelter unlike shelters A and B, where the same species represented

24.47 % and 21.21 % respectively.

Table 3. Indices of richness (Margalef), diversity (Simpson), and

venness for entomofauna by the functional group present

in three plant shelters adjacent to a vineyard.

Functional

group

Shelter Abundance

Margalef

(DMg)

Simpson

(1-D)

Evenness

(J)

Total

A 564 2.29 0.83 0.78

B 396 2.68 0.81 0.74

C 249 2.04 0.51 0.53

Predators

A (a) 117 1.05 0.75 0.88

B (ab) 75 0.93 0.51 0.64

C (b) 33 0.86 0.55 0.75

Parasitoids

A (a) 9 0.46 0.44 0.92

B (a) 12 0.80 0.63 0.95

C (a) 6 0.56 0.50 1.00

Pollinators

A (a) 267 0.18 0.50 1.00

B (a) 201 0.38 0.50 0.68

C (a) 192 0.38 0.20 0.38

Phytophagous

A (a) 171 0.39 0.47 0.68

B (a) 108 0.43 0.49 0.75

C (b) 18 0.00 0.00 -

Lowercase letters in dierent parentheses indicate signicant dierences (p≤0.05).

In terms of functional groups, predators were more abundant,

diverse, and with greater evenness in shelter A, while parasitoids

were more diverse in shelter B, but with very similar evenness in all

three shelters; pollinators had low richness and diversity in all three

shelters, with high dominance in shelter C. As for phytophagous, they

were more abundant and diverse in shelters A and B, but very scarce

in shelter C.

Composition of plant shelters and functional groups present

The distribution of functional groups according to the species

comprising the plant shelters is shown in gure 2.

0% 20% 40% 60% 80% 100%

Total

P lant shelter

Predator Parasitoid Pollinator Phytophage

Figure 2. Abundance of entomofauna in each component of the

dierent plant shelters.

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5-6 |

It is observed that in shelter A, fennel (Apiacea), calendula

and sunowers (Asteraceae), in that order, stood out for hosting

the largest population of predators in the study, mainly C. externa,

coinciding with similar studies that highlight fennel as an excellent

reservoir of green lacewings (Chrysopidae), hoveries (Manfrino

et al., 2011) and ladybugs (Coccinellidae) (Rebolledo et al., 2007).

As for the pollinator, it was observed that this plant hosted the

largest populations of Chrysomya sp. Calendula did not harbor any

phytophagous and, like the reports by Andorno et al. (2014), was

a shelter for ladybugs and parasitoid wasps. Coinciding with the

results of Ramírez-Reyes et al. (2019), the sunower did not harbor

parasitoids, but if there was a high population of Thrips tabaci, this

attraction could be due to the size of the sunower owers, which,

being very large, show much more their yellow color, a color that,

according to Joyo &Narrea (2015), exerts an attractive eect on thrips

to the point that it is common to use yellow sticky traps in vineyards

to attract and trap individuals of this pest.

Predators of shelter B were found mainly in zinnia (Asteraceae)

and fennel (Apiaeae); zinnia hosted the largest population of predator

C. externa of the entire study; fennel, as in shelter A, hosted the

four functional groups, of which predators were the most abundant,

although in smaller numbers than zinnia. In contrast, crotalaria

harbored few predators, more phytophagous species, and no

parasitoids. According to Van Rijn & Wäckers (2016), not all of the

plant species that make up the varied plants (plant shelters) produce

adequate resources, nor is it known for sure which species will be

most eective in hosting benecial organisms.

In shelter C, characterized by being the least abundant, least

diverse, and with the lowest population of biological controllers,

basil (Lamiacea) stood out for being the only plant in the entire study

in which no green lacewings were found; according to Adam et al.

(2019) and Hassan et al. (2015), this plant has a repellent eect against

several insects, which is one reason why this shelter had the lowest

insect population in general (20.6 % of the insects present throughout

the study); however, this repellent eect would not apply to bees,

which preferred basil over other plants, probably since, unlike other

plants, basil owers are small and open, conditions that, according to

Altieri & Nicholls (2012), make its pollen and nectar more accessible

to bees and other pollinators; crotalaria and salvia had the lowest

population records in the study, with bees being the most important

population.

Conclusions

In the three shelters evaluated, entomofauna composed of

predators, parasitoids, pollinators, and phytophagous was found;

pollinators are the most abundant and parasitoids are the least

abundant. Shelters A and B were similar in terms of the composition

of these functional groups.

Shelter A was the most abundant and, together with shelter B,

stood out for hosting the largest number of biological controllers of

the grapevine; in both shelters, fennel (Foeniculum vulgare) was the

outstanding plant species in richness and abundance of predators,

followed by calendula (Calendula ocinalis) (shelter A) and zinnia

(Zinnia acerosa) (shelter B), which also contributed a signicant

share of predators and parasitoids. Of lesser abundance, shelter C was

widely inhabited by pollinators, especially Apis mellifera L., which

was found mostly in basil (Ocimum basilicum).

Among all the predators found, Chrysoperla externa (Hagen)

stands out, the main controller of the “vine mealybug” (Planococcus

spp.), which means that the installation of plant shelters in vineyard

elds could represent an additional alternative to enhance the

biological control of pests in this crop.

Recommendations

Considering that the behavior of insects can vary throughout the

day and with it the composition, dominance, and evenness of the

population in plant shelters, it is recommended to carry out similar

studies with sampling at dierent times than the one in this study.

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