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J. Morales-Bautista et al// Biological Effectiveness of Insecticides to Control Cone Beetle...78-90

Biological Effectiveness of Insecticides to Control Cone Beetle in

Pinyon Pine Plantations

DOI: https://doi.org/10.38186/difcie.610.06

Jesús Morales-Bautista*

Víctor David Cibrián-Llanderal**

Javier López-Upton***

David Cibrián-Tovar****

ABSTRACT

Pinyon pine plantations are attacked by insects that feed on conelets and seeds, a

phytosanitary problem that causes economic losses in production. The study evaluated the

biological effectiveness (BE) of chemical insecticides to control Conophthorus edulis

Hopkins in a Pinus cembroides Zucc. forest plantation. The treatments abamectin (18 g of

-1

active ingredient (a.i.) L ), emamectin benzoate (19.2 g of a.i. L ), azadirachtin (738.4 g of

a.i. L ) and an untreated check with water were applied randomly with 5 repetitions. The

application was repeated 56 days later. Each repetition consisted of applying a treatment to

a tree with a cohort of 20 strobili. The BE of the insecticides was determined by the

percentage of healthy conelets for each treatment in 8 evaluations: 0, 19, 32, 50, 65, 83,

09 and 144 days. No significant differences were found between treatments at 5% error

by the ANOVA F test. Between the months of August and September, general averages

were found between 0.25 to 2.5% of attacked conelets. An increase of 21.25% was

observed in the average number of dead conelets between the initial and final evaluations

in September.

KEYWORDS: Forest management, Entomology, insect control, pesticides.

*Estudiante de la Maestría en Ciencias Forestales del Colegio de Postgraduados. Estado de México, Mexico.

Director General de la Empresa Bioforestal Innovación Sustentable, Texcoco, México. ORCID:

https://orcid.org/0000-0002-2351-7286. E-mail: jesus.morales@bioforestal.com.mx

*Investigador por México (Conahcyt) comisionado al Colegio de Postgraduados (Campus Montecillo),

Postgrado en Ciencias Forestales. Estado de México, Mexico. ORCID: https://orcid.org/0000-0003-1999-

520. E-mail: vicillan@gmail.com (corresponding author)

***Profesor e Investigador del Colegio de Postgraduados (Campus Montecillo), Postgrado en Ciencias

Forestales, Estado de México, Mexico. ORCID: https://orcid.org/0000-0002-8408-1121.

uptonj@colpos.mx

E-mail:

****Profesor e Investigador de la Universidad Autónoma Chapingo, División de Ciencias Forestales, Texcoco,

México. ORCID: https://orcid.org/0000-0001-6788-0178. E-mail: dcibrian48@gmail.com

Recibido: 07/09/2023

Aceptado: 03/11/2023

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J. Morales-Bautista et al// Biological Effectiveness of Insecticides to Control Cone Beetle...78-90

Efectividad biológica de insecticidas para controlar el escarabajo del

cono en plantaciones de pino piñonero

RESUMEN

Las plantaciones de pino piñonero son atacadas por insectos que se alimentan de piñas y

semillas, un problema fitosanitario que provoca pérdidas económicas en la producción. El

estudio evaluó la efectividad biológica (EB) de insecticidas químicos para controlar

Conophthorus edulis Hopkins en una plantación forestal de Pinus cembroides Zucc. Los

tratamientos abamectina (18 g de ingrediente activo (i.a.) L-1), benzoato de emamectina

(19.2 g de i.a. L-1), azadiractina (738.4 g de i.a. L-1) y un testigo con agua se aplicaron

aleatoriamente con 5 repeticiones. La aplicación se repitió 56 días después. Cada

repetición consistió en aplicar un tratamiento a un árbol con una cohorte de 20 estróbilos.

El BE de los insecticidas se determinó por el porcentaje de conillos sanos para cada

tratamiento en 8 evaluaciones: 0, 19, 32, 50, 65, 83, 109 y 144 días. No se encontraron

diferencias significativas entre tratamientos al 5% de error mediante la prueba F de la

ANOVA. Entre los meses de agosto y septiembre se encontraron promedios generales

entre 0.25 a 2.5% de conillos atacados. Se observó un aumento del 21.25% en el número

promedio de conillos muertos entre la evaluación inicial y final en septiembre.

PALABRAS CLAVE: Manejo forestal, Entomología, control de insectos, plaguicidas.

Introduction

One of the great challenges of forest management of pinyon-producing pine species is

the control of insects that cause damage to harvests (Botkin and Shires, 1948; Eguiluz,

982; Farjon and Filer, 2013; Mohedano-Caballero et al., 1999; Robert, 1977). In central-

eastern Mexico, the main predator of pinyons of the species of Pinus cembroides Zucc. is

cone beetle Conophthorus edulis Hopkins (Cibrián-Tovar et al., 1986; Flores Flores and

Díaz E., 1991a; Flores Flores and Díaz Esquivel, 1989; Martínez Ramírez et al., 1985).

The incidence of this insect in practically all seasons of the year in commercial plantations

in Mexico represents important economic losses (Cibrián-Tovar et al., 1986; Flores Flores

and Díaz E., 1991a; Flores Flores and Díaz Esquivel, 1989; Martínez Ramírez et al., 1985).

For this reason, chemical control methods are still an alternative for managing this problem.

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In Mexico, during the period from 2000 to 2021, approximately 240,000 hectares of

commercial forest plantations were established with support from the federal government.

Fifteen percent of this surface was planted with species of the Pinus genus (CONAFOR,

022). Within this genus is the species P. cembroides, one of the most important of the

Mexican pinyon trees (Flores Flores and Díaz E., 1991b; Flores Flores and Díaz Esquivel,

989; Flores Flores and Díaz Ezquível., 1985; J. Flores Lara and López, 1989; Granados

Victorino et al., 2015). Its importance lies in its wide natural distribution, dominance,

abundance, use in establishing plantations and economic value, since it constitutes 90% of

the Mexican pinyon harvest (Botkin and Shires, 1948; Eguiluz, 1982; Farjon and Filer, 2013;

Mohedano-Caballero et al., 1999; Robert, 1977).

In forest management scenarios focused on seed production in forests, plantations,

seed stands, seed orchards and germplasm producing units. Insects that feed on cones,

fruits, seeds, and shoots are of great importance due to the impact they have on the

harvest (Miranda, 2021). Insect predation of conelets and seeds in Mexican pinyon trees

can cause crop losses of more than 90% and is frequently greater than 60% (Cibrián-Tovar

et al., 1986; Flores Flores and Díaz E., 1991b; Flores Flores and Díaz Esquivel, 1989;

Flores Flores and Díaz Ezquível., 1985; J. Flores Lara and López, 1989; Martínez Ramírez

et al., 1985). Conophthorus edulis Hopkins is the main insect that causes mortality in cones

and conelets of P. cembroides in Mexico. Damage between 40 to 60% has been reported

in conelets production (Cibrián-Tovar et al., 1986; Flores Flores and Díaz E., 1991a; Flores

Flores and Díaz Esquivel, 1989; Martínez Ramírez et al., 1985). Looking for alternatives to

reduce the economic impact of the pest attack, the objective of the research was to

determine the biological effectiveness (BE) of chemical insecticides to control C. edulis on

a P. cembroides forest plantation.

. Materials and Methods

.1. Study area

The study was carried out in a P. cembroides forest plantation with an altitude range

between 2,361 to 2,456 masl, located in Pizarro, Tepeyahualco, Puebla. (Figure 1). The

climate according to the Köppen classification modified by García (1986) is semi-arid

(BS1k'w). According to the World Reference Base for Soil Resources (WRB), Leptosols

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(LP) Eutric (eu) Lithic (li) and Regosols (RG) Calcaric (ca) Skeletic (sk) predominate in the

study area (INEGI, 2007).

Figure 1. Forest plantation of Pinus cembroides Zucc. under attack by Conophthorus

edulis Hopkins.

1.2. Experimental design and sampling

Sampling was carried out in the period from July to December 2020 (Figure 2), during

the conelet growth stage and the attack period of adults of the second generation of the

cone beetle life cycle. From the forest plantation (Figure 2a), 20 trees were evaluated,

severely attacked by the insect, with an approximate age of 11 years, presence of conelets,

diameter between 12.5 to 15.5 cm, total height between 3 to 5 m. The experiment was

conducted in a completely randomized design with four treatments (three insecticides and

an untreated check) with five repetitions each. Each repetition consisted of applying a

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treatment to a tree with a cohort of 20 strobili (conelets), individually identified, with an

aluminium tag for monitoring during the study period (Figure 2b).

Figure 2. General information of the experiment: a) Forest plantation of Pinus cembroides

Zucc.; b) Sampling marking (sm); c) Spraying chemical treatments; d) Female strobile; e)

Male strobile; f) Conelet (ct) and cone (co); g) dead conelet (dc) and healthy conelet (hc).

Pizarro, Tepeyahualco, Puebla (July to December 2020).

The insecticides doses that corresponded to each chemical treatment were: abamectin

-1 -1

ml L (18 g of active ingredient (a.i.) L , Agrimec® 1.8 CE), emamectin benzoate 0.12 ml

-1

L (19.2 g of a.i., Denim® 19 CE), and azadirachtin 0.4 ml L (738.4 g of a.i., Progranic®

Nimicida 80 CE). The untreated check was the application of water. Applications were

made on July 31, 2020 and September 25, 2020 (56 days later). Drip point fumigations

were carried out in the tree crowns (Figure 2c), completely covering the strobili. To apply

the treatments, a Forza 25® motorized backpack sprayer was used (model 818025,

capacity 25 L, Swissmex S.A. de C.V.), with a double outlet NN-D-6 flat fan nozzle at 20

bar. The application dose was 5500 L ha . In both applications the expenditure was

approximately 5 L tree .

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Cohorts of treated conelets were evaluated at 0, 19, 32, 50, 65, 83, 109, and 144 days.

The phytosanitary status of each strobile was considered by the following damages (Figure

): 1) perforation or mass of resin at the base of the peduncle and in the structure; 2)

galleries inside; 3) adults, preimagos, pupae, larvae. A visual inspection was carried out to

identify attacked, dead and healthy conelets (Figures 2 and 3).

Figure 3. Evidence of damage caused by cone beetle in pinyon conelets (Pinus

cembroides Zucc.): a) Attacked conelet with the presence of the Conophthorus edulis

Hopkins (Ce), adult insect and tunnels (tu) and debris (de); b) Evidences of the recent

attacked conelet (ac) with the presence of secreted resin (res), and, dead conelet (dc); c)

Recent attacked conelet (ac) with perforation at the base of the peduncle (pe) with a

secreted resin; d) Tunnel formation of the with perforation at the base of the conelet with a

secreted resin; e) Attacked conelet with initial tunnel formation (itf) in the base of the

peduncle; f) dead conelet (dc) with the presence secreted old resin (ore) at the base of the

peduncle. Pizarro, Tepeyahualco, Puebla (July to December 2020).

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1.3. Statistical analysis

The BE of insecticides was calculated using the percentage of healthy conelets

Figure 2e) with no evidence of conelet beetle damage, for each treatment, replicate and

(

date from the 19th day onwards. The data were subjected to the F test of the analysis of

variance (ANOVA) with a probability level of error of 5% to determine the differences in

averages between treatments (Table 1). All statistical procedures were performed in the R

environment (R Core Team, 2023).

2. Results

The evaluation of the BE began on the 19 day of the experiment in the P. cembroides

forest plantation (Table 1). The requirements of normality and homoscedasticity of the

healthy conelets variable were met for the ANOVA, except for the evaluation on August 19,

where the variable was transformed by a standardized function (Table 1). According to the

F test in the ANOVA at 5% significance, there were no differences between averages of

healthy conelets by treatments on each of the different days (Table 1). As of October 4, the

coefficient of variation exceeds 30% and reaches 48.58% on the last day of the evaluation

(Table 1). In the last evaluation (144 days after the application of the insecticides) a general

relative average of 37.75% healthy conelets was found (Table 1; Figure 4). The

identification of attacked conelets has a relative average of 2.5% in the month of

September (Figure 4). Also, between the 1st and 19th of September there was an increase

of 21.25% in the relative average of dead conelets (Figure 4). From mid-September to

October the relative increase in dead conelets remained between 5 to 8% (Figure 4).

Between the evaluations from November to December, the average relative increase was

.75% (Figure 4).

. Discussion

There was no BE of the insecticides evaluated compared to what was reported for C.

ponderosae in P. monticolae, testing permethrin in different doses with 1 and 2 applications

Shea and McGregor, 1987). It is possible that the BE of the insecticides in the second

(

application could have been negatively affected due to precipitation that occurred in the

area after the spraying of the treatments. Only between the months of August and

September it was possible to identify signs of C. edulis attack in the conelets evaluated

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(Figure 4). On the other hand, in this study area, conelet mortality increased in the month

of September (Figure 4). Strobili cohorts were marked months before the start of the

experiment (Figure 2b). The evaluation dates of the experiment between the months of

July and August correspond to the initial stages of conelet formation (fertilized strobili).

Conelets in the developing phase were more susceptible to attack by the cone beetle

(

Figure 4a), resulting in an increase in conelet mortality in September (Figure 4b). In

addition to this, the increase in the variability of the results found from the month of October

Table 1) may indicate the need to increase the sample size for this type of field evaluations.

(

A decrease in conelet mortality was observed between the months of November and

December (Figure 4), a phenomenon that may be associated with low temperatures of

these months.

Figure 4. Time evolution of the phytosanitary condition of Pinus cembroides Zucc. conelets

(a, b, c) under attack by Conophthorus edulis Hopkins in a forest plantation in

Tepeyahualco, Puebla, Mexico.

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Table 1. Summary of the analysis of variance and descriptive statistics of the biological effectiveness of insecticides to control

Conophthorus edulis Hopkins in a Pinus cembroides Zucc. plantation, Tepeyahualco, Puebla, Mexico

Healthy Conelets (2020)

Degree of

Freedom

Variation Source

July 31

Mean Square

Aug 19

Sep 1

Sep 19

Oct 4

Oct 22

Nov 17

Dec 22

Treatments

Residuals

63.30†

125

175

143.33

340.63

141.25

349.38

348.33

350

497.92

336.25

146.39†

339.37

307.5

Total

Statistical tests

F-test

p-value

0.73†

0.45†

0.93†

0.78

0.63

0.65

0.64

0.48

0.22

0.74

0.80

0.48

0.75

0.44

0.51

0.42

0.73

0.50

0.26

0.82

0.78

Shapiro-Wilk test

Bartlett's test

Coefficient of Variation (%)

NA 13.7†

23.47

29.47

34.18

40.86

46.19

48.58

Treatments

Absolute Frequency (Average ± Standard Deviation, %)³

Untreated Check¹

100.00 ± 0.00

91.00 ± 12.45

81.00 ± 21.33

90.00 ± 11.73

92.00 ± 6.71

88.50 ± 13.68

79.00 ± 16.36

73.00 ± 23.87

77.00 ± 19.24

85.00 ± 12.25

78.50 ± 17.48

56.00 ± 9.62

59.00 ± 24.34

55.00 ± 10.61

68.00 ± 20.80

59.50 ± 16.93

47.00 ± 16.43

54.00 ± 24.85

55.00 ± 10.61

60.00 ± 19.04

54.00 ± 17.59

38.00 ± 12.04

47.00 ± 22.25

48.00 ± 13.96

50.00 ± 23.72

45.75 ± 17.79

28.00 ± 10.95

45.00 ± 23.18

44.00 ± 15.57

45.00 ± 22.36

40.50 ± 18.70

23.00 ± 13.51

45.00 ± 23.18

42.00 ± 16.81

41.00 ± 18.51

37.75 ± 19.02

Agrimec® 1.8 CE (Abamectin)²

Denim® 19 CE (Emamectin benzoate)²

Progranic® Nimicide 80 CE (Azadirachtin)²

General average

†

Variable transformed by the standardized function (z-score). ¹Water application. ²Application rate of 5500 L ha . Five repetitions per treatment.

-1 3

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It was reported for C. coniperta in a P. strobus seed stand, using the mating

interruption control method, an average reduction in conelet damage of 64% was obtained

in areas treated with the pheromone pityol (Trudel et al., 2004). In use of conventional

control methods such as chemical insecticides, it is being restricted worldwide. Research

has been carried out with semiochemicals for several species of Conophthorus from North

America, with the objective of understanding the behaviour of the insect and exploring its

use as control methods mainly in seed orchards (Miller et al., 2000; Rappaport et al., 2000;

Trudel et al., 2004).

A control method that can be implemented in plantation conditions is prescribed

burning. The application of low intensity burning in seed stands of P. resinosa increased

the number of conelets without C. resinosae infestation by between 11% and 45% (W. E.

Miller, 1978). The use of fire as a control method is limited to stands with mature trees,

species with fire-tolerant bark, and sites with sufficient fuel load, to ensure that this method

is effective in controlling insect populations (Trudel et al. al., 2004).

Conclusions

The application of evaluated insecticides did not increase the survival of P. cembroides

conelets. However, in addition to the relative percentage of healthy conelets, to better

understand the response of these chemical controls on visual inspection variables such as

attacked and dead conelets, it is suggested to expand the number of samples and increase

the number of applications in future experimental trials in the pinyon pine plantations. In

addition to chemical control methods for C. edulis, future biological effectiveness studies

should test other methods, with the aim of increasing options in a context of integrated pest

management and reducing the use of insecticides.

The general average of conelets attacked between the months of August and

September ranges between 0.25 to 2.5%. In the last evaluation, 144 days after the

application of insecticides and untreated check, the general averages of attacked, dead

and healthy conelets were 0, 62.25 and 37.75%, respectively. In the month of September

there was an increase of 21.25% in the average number of dead conelets.

The methodology used to monitor the phytosanitary status of P. cembroides conelets

can be adapted and expanded to evaluate the biological effectiveness of several control

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methods and studies evaluating the impact of insects on the production of cones and

conelets, and seeds.

Acknowledgements

The authors thank Engr. Iván Moisés Fuentes Condado for the access authorization

granted to carry out the study within his private property.

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