Research Article

Side Effects of Lambda Cyhalothrin and Thiamethoxam on Insect Pests and Natural Enemies Associated with Cotton

Nelson D. Zambrano1, Wilber Arteaga1, José Velasquez2 and Dorys T. Chirinos1*

1Facultad de Ingeniería Agronómica, Universidad Técnica de Manabí, Provincia de Manabí, Ecuador; 2Agencia de Regulación Control Fito y Zoosanitario (Agrocalidad), Manta Ecuador.

Received | April 17, 2021; Accepted | June 21, 2021; Published | August 15, 2021

*Correspondence | Dorys T. Chirinos, Facultad de Ingeniería Agronómica, Universidad Técnica de Manabí, Provincia de Manabí, Ecuador; Email: dorys.chirinos@utm.edu.ec

Citation | Zambrano, N.D., W. Arteaga, J.Velasquez and D.T. Chirinos. 2021. Side effects of lambda cyhalothrin and thiamethoxam on insect pests and natural enemies associated with cotton. Sarhad Journal of Agriculture, 37(4): 1098-1106.

DOI | https://dx.doi.org/10.17582/journal.sja/2021/37.4.1098.1106

Keywords | Insecticides, Outbreak of pests, Parasitoids, Predators, Sustainability

Introduction

The genus Gossypium (Malvaceae) comprises of 40 species, among which four are commercially cultivated. One of the latter, the upland cotton, Gossypium hirsutum L., predominates with 95% of the total production area (FAO, 2015; Trapero et al., 2016). It is grown mainly to obtain fiber as a raw material for the textile industry (FAO, 2015). In 2019, 82,589,031 tons of cotton were produced from approximately 38,640,608 hectares (FAOSTAT, 2019) cultivated in more than 78 countries (Razaq et al., 2020). This represents 2.3% of all cultivated land in the world and indicates its economic and social importance (FAO, 2015).

Until the end of the 19th century, there were few cases of pests associated with cotton (Razaq et al., 2020). However, the large number of hectares planted in different biogeographic regions, resulted in the insertion of a variety of arthropod species within the trophic networks of the agroecosystem, which expanded the diversity of these organisms, compared to what was originally found in center of origin (Naranjo, 2011). There are currently 1,300 species of phytophagous arthropods associated with cotton, among which nearly 40 are considered primary pests (Naranjo, 2011; Razaq et al., 2020).

Given the importance of the crop, as well as the existing number of arthropods, the application of synthetic insecticides is the main method used to control these pests (Razaq et al., 2020), which negatively impacts human health and the productivity of the plant cultivation are not based on an agroecosystem analysis (FAO, 2015). In addition, laboratory and field assays report that applications of organosynthetic insecticides used for the control of important pests in cotton also have side effects for non-target organisms such as predators and parasitoids (Ruberson and Roberts, 2004; Prabhaker et al., 2007; El-Wakeil et al., 2013).

In Ecuador, cotton played an important role in the agricultural sector as part of the edible oil industry from the 1970s to the 1990s (FAO, 2017). It is currently grown for the textile industry, mainly in the provinces of Guayas and Manabí, with a sowing area of approximately 1,800 ha (Cañarte-Bermudez et al., 2020) and an estimated fiber production of 1,200 tons (FAOSTAT, 2019). As in other latitudes, a wide variety of organosynthetic pesticides are used in this country for pest control (FAO, 2017).

Pest management based on the continuous use of chemical pesticides is unsustainable and does not necessarily guarantee the objective of production. In fact, the devastating attack of pests on some crops has reported despite frequent spraying of chemical insecticides, as well as the collateral effects on health and the environment (Chirinos et al., 2020). This makes it necessary to reconsider the approaches to agricultural production, especially with regard to the functioning of the agroecosystem and the socioeconomic criteria related to benefits and losses, in order to return to ancestral forms of pest management and make them evolve within the framework of new scientific and technological knowledge (Chirinos et al., 2020).

Recent projects propose the reactivation of cotton planting for Ecuador, within the framework of the strengthening of sustainable agriculture for South America (FAO, 2017). As part of these objectives, this work aimed to evaluate the impact of applications of an insecticide based on a mixture of lambda cyhalothrin and thiamethoxam on pest populations and some natural enemies.

Materials and Methods

This research was conducted at the experimental campus “La Teodomira”, located in Santa Ana canton (coordinates 01° 09’ 51” S and 80° 23’ 24” W), Manabí province, Ecuador. Its life zone corresponds to a Tropical Dry Forest.

To start the trial, a 750 m2 plot of cotton was established, variety Alcalá DP 90. Two plants per point were planted at a distance of 0.4 m x 1.0 m (planting point x row), designed in blocks completely randomized with three replicates and two treatments. Each experimental plot consisted of 125 m2 (14 rows of 9 m long) and a total of 616 plants (44 plants per row). The evaluated treatments were: T1. Applications of a commercial insecticide consisting of a mixture of lambda cyhalothrin (106 g L-1 of active ingredient (i.a.)) + thiamethoxam (141 g.L-1 i.a.) +, at a dose of 1.5 cc.L-1. T2. Control. The insecticide was applied three weeks after germination at weekly intervals, totaling ten sprays. The samplings were carried out in each experimental plot, omitting the rows of the ends, in order to avoid the effect of the borders between the treatments. In the 12 internal rows, 30 leaves per plot were randomly selected, for a total of 90 for each treatment.

Once a week during four months, the numbers of: nymphs of the whitefly, Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae), individuals of the cotton aphid, Aphis gossypii Glover, larvae of the leaf borer, Buccullatrix thurberiella Busck (Lepidoptera: Bucculatricidae) and thrips species present were counted using a Carl-Zeiss® stereoscope (magnification: 10 - 40X). The number of nymphs and parasitized individuals of B. tabaci and A. gossypii was also counted, estimating their respective percentage of parasitism [(nymphs or parasitized individuals / total individuals counted) x 100].

In bottles with ethyl alcohol (70%) individuals of predators and the cotton strainers, Dysdercus spp. (Hemiptera: Pyrrhocoridae) were collected for 20 minutes in each experimental plot. The bolls from ten plants were sampled to detect the tobacco worm, Heliothis virescens F. (Lepidoptera: Noctuidae) and the Peruvian boll weevil, Anthonomus vestitus Germar (Coleoptera: Curculionidae). These samplings were conducted from August to October 2019.

The identification of the thrips species was achieved following the taxonomic key proposed by Moritz et al. (2004). The coccinellid species were determined by the characters indicated by González (2015). The parasitoid species associated with B. tabaci was diagnosed as indicated by Polaszek et al. (1992). The predatory bug and the parasitoid of A. gossypii were identified by comparing with specimens preserved in the entomological collection of the Crop Protection Laboratory of the Agency for the Regulation of Phyto and Zoosanitary Control (Agrocalidad), Manta, Ecuador. Voucher specimens were stored in this laboratory.

To estimate the yield, three harvests were realized on plants from the two central rows per experimental plot per treatment. The fiber with seed was weighed (grams) with a weight scale and the seed subsequently removed, to obtain the weight of the fiber. The yield was calculated in kilograms per plot [(grams of fiber plant-1/1000) x 616), per plot of 125 m2 (kg plant-1 x 616 plants) and per hectare (kg plant-1 x 50000 plants ha-1). The ginning percentage was determined with the differences between the weight of the fibers, with and without seed.

All variables related to number and percentages were analyzed with the Mann-Whitney test (P <0.05), while the performance variables were compared with the student’s “t” test (P <0.05). Simple regression models were performed between the number of B. tabaci nymphs and the number of A. gossypii individuals versus the percentage of parasitism for each species (P <0.05).

Results and Discussion

Whitefly, Bemisia tabaci

The nymphs reached the highest levels in the plants treated weekly with the mixture of lambda cyhalothrin + thiamethoxam. These levels increased from 7 to 34 nymphs leaf-1 while for untreated plots varied from 0.2 to 2.0 nymphs leaf-1. The highest number of B. tabaci nymphs in plants treated with lambda cyhalothrin + thiamethoxam was related to low parasitism, that did not exceed 12% (Figure 1), while in untreated plots there was a lower number of nymphs associated with higher percentages of parasitism (ranging from 34 to 100%).

 

The high dispersion detected in the regression analysis between B. tabaci nymphs versus the percentage of parasitism suggests a low or no response of this biological control agent when the plot was treated with lambda cyhalothrin + thiamethoxam (R2: 0.087) (Figure 2). This would indicate the adverse effects of weekly applications of the chemical pesticide on parasitism. In contrast, the model calculated for untreated plots showed a high coefficient of determination (R2: 0.83) that would attribute a parasitism response to variations in population densities of B. tabaci when there was no pesticide interference. Additionally, the statistical analysis corroborates that on treated plots the populations were higher, together with the lower percentages of parasitism (Table 1, P<0.05).

Encarsia pergandiella Howard (Hymenoptera: Aphelinidae) was the parasitoid species associated with B. tabaci, identified in this research. Schuster et al. (1998) had reported this species for Ecuador in a survey of Bemisia spp. parasitoids, carried out in Florida, Central and South America. The results suggest the adverse effects of the chemical treatment on the parasitism of B. tabaci. Dutcher (2007) pointed out that pest resurgence occurs when a pesticide treatment destroys their population and kills or negatively affects their natural enemies. Thus, the residual activity of the pesticide expires and the populations of the pests can increase more quickly and to a greater abundance when the natural enemies are in low proportion. In cotton, insecticide applications for the control of this species have historically resulted in conspicuous population increases attributed in part to the development of resistance, but the main cause is the suppression of its parasitoids (Oliveira et al., 2001).

 

The cotton aphid, Aphis gossypii

Aphis gossypii increased in plots treated with lambda cyhalothrin + thiamethoxan from the eleventh week, reaching the highest levels of 63 individuals leaf-1 (thirteenth week) while in the control the increase began in the sixth week showing the maximum number of 17 individuals leaf-1 (fourteenth week) (Figure 3). Although the population peaks of the aphids were higher in treated plants, there were no differences between treatments (Table 1).

On A. gossypii parasitism by Lysiphlebus testaceipes (Cresson) (Hymenoptera: Braconidae) was observed, but in the treated plots with lambda cyhalothrin + thiamethoxam it was significantly lower (Table 1). This endoparasitoidis referred to as an important biological control agent for A. gossypii, in several crops (Tomanović et al., 2014; Albittar et al., 2016). However, in this assay, parasitism remained low, showed maximum levels of 44% (Figure 3). The absence of a functional response of parasitism to variations in the population density of aphids would be indicated by the low coefficients of determination of the calculated regression models both in treated and untreated plots (R2: 0.0002 - 0.04) (Figure 4).

 

Same results were obtained by Romero et al. (2019), who in a field study conducted in cucumber plots without insecticides, found populations of 19 individuals leaf-1 of A. gossypii, with percentages of parasitism that ranged from 35 to 70%. Kaleem et al. (2014) reported that natural biological control in aphids is effective when there are low population densities per plant. This aphid is considered an important pest that can infest cotton from the beginning of the cycle until harvest, causing delays in the development of the plant (Pinto et al., 2013).

The thrips, Thrips palmi

The species of thrips present was identified as Thrips palmi Karny (Thysanoptera: Thripidae) whose main characteristics are summarized in Figure 5. This species had not been mentioned feeding on cotton plants in Ecuador. In fact, a previous investigation, only reported another genus of thrips (Frankliniella) but without determining the species (Cañarte-Bermudez et al., 2020). A low number of T. palmi individuals was found on leaves, which showed no significant differences between treated and untreated plants (Table 2). These abundances are in contrast to those obtained in previous field investigations in other regions. Janu et al. (2017) observed population levels of Thrips tabaci Lindenmann that reached 28 and 24 individuals leaf-1 in a fieldwork conducted during two production cycles (years 2014 and 2015) to evaluate the response of some transgenic cotton genotypes in India. Jaramillo-Barrios et al. (2018) indicated maximum peaks of approximately 85 individuals of T. palmi on cotton leaves in a fieldwork performed in Colombia to determine the preference of plant organs by species of thrips.

The leaf borer, Bucculatrix thurberiella

Bucculatrix thurberiella was another species found feeding on cotton leaves at very low levels. There were no significant differences between treatments (Table 2). The population levels detected (ranging from 0.02 to 0.2 larvae leaf-1, Table 2) were very similar to those obtained by research performed in the same area that used chemical insecticide to managing. Cañarte-Bermudez et al. (2020) pointed out general averages of 0.48 individuals leaf-1 spraying lambda cyhalothrin + thiamethoxam, azadirachtin, abacmectin and cypermethrin. However, this species represents an

 

 

Table 1: General average number of nymphs of Bemisia tabaci, and of individuals of Aphis gossypii, and percentage of parasitism on cotton leaves.

	Bemisia tabaci		Aphis gossypii
Treatment	Nymphs	Parasitism (%)	Individual	Parasitism (%)
Lambda cyhalothrin + thiamethoxam	15.9 ± 2.8 a	6.5 ± 1.0 b	9.9 ± 2.8 a	3.9 ± 1.8 b
Untreated plants	1.1 ± 0.1 b	69.4 ± 2.1 a	5.3 ± 1.5 a	17.2 ± 2.1 a

Means±standard error. Mean followed by different letters in each column is significantly different at 0.05 level of significance using Mann-Whitney test.

 

Table 2: General average of the number of individuals of the species Thrips palmi, Bucculatrix thurberiella, Dysdercus spp., Heliothis virescens and Anthonomus vestitus on cotton plants.

Treatment	Thrips palmi	Bucculatrix thurberiella	Dysdercus spp.	Heliothis virescens	Anthonomus vestitus
Lambda cyhalothrin+ thiamethoxam	0.1±0.1 a	0.02±0.02 a	1.7 ± 0.3 a	0.0 b	0.0 b
Untreated plants	0.6 ± 0.1 a	0.2 ± 0.1 a	7.7 ± 1.0 b	0.5±0.2 a	0.3 ± 0.1 b

Means±standard error. Mean followed by different letters in each column is significantly different at 0.05 level of significance using Mann-Whitney test.

 

important pest on cotton crops in other regions (Gil and Lopez, 2017). Herrera and García (1978) indicated that natural enemies play an important role

in the population regulation of B. thurberiella, but the applications of chemical insecticides for other important pests could generate ecological imbalances and increase their populations in the crop.

The cotton strainers, Dysdercus spp.

The number of individuals of Dysdercus spp. showed differences between treatments. While in plots treated with lambda cyhalothrin + thiamethoxam, 1 to 2 individuals plant-1 were observed, under untreated plot, the number of individuals increased from 5 to 11 (Figure 6), resulting significantly higher than this last treatment (Table 2). The results are similar to those reported by Cañarte-Bermudez et al. (2020) who for the same area and months of evaluation reported a high incidence of Dysdercus spp. associated with the fiber formation stage. Regarding the chemical control of this pest, tests conducted by Rafiq et al. (2014) show the effectiveness of pyrethroids, carbamates and organophosphates. These researchers conclude that, to determine the number of minimum sprays necessary to control species of this genus, it is essential to study the biological cycle and estimate the population development parameters.

The tobacco worm, Heliothis virescens and the cotton weevil, Anthonomus vestitus

During this research, 0.5 and 0.3 individual boll-1 of H. virescens and A. vestitus, respectively were observed

 

on untreated plot (Table 2). Despite the fact that in other regions of South America, both species are relevant pests in cotton crops (FAO, 2017; Gil and López, 2017), the damage was no significant in this fieldwork. In Ecuador, H. virescens has been reported attacking in the flowering stage and it has been indicated that A. vestitus does not represent a devastating pest in that country due to its low incidence (FAO, 2017).

Predators

A total of 298 individuals were observed belonging to four species of predators, three from the Coccinellidae (Coleoptera) and one from the Reduviidae (Hemiptera). Of these, Coleomegilla maculata De Geer together with Zelus sp., were the most abundant species (Table 3). The latter species of predators had previously been reported in the area (Cañarte-Bermudez et al., 2020). The results showed a significantly lower number of predators in treated plants with lambda cyhalothrin + thiamethoxam (Table 3). Field investigations conducted on cotton in Egypt have reported high mortality rates of predators, Coccinella undecimpunctata L. (Coleoptera: Coccinellidae) and Chrysoperla carnea Stephens (Neuroptera: Chrysopidae) with frequent sprays of insecticides belonging to various chemical groups (El-Heneidy et al., 2015; Eldesouky, 2019).

 

Table 3: Number of individuals per species of predator found in cotton plants.

Treatment	Coleomegilla maculata	Cycloneda sanguínea	Cheilomenes sexmaculata	Zelus sp.
Lambda cyhalothrin+thiamethoxam	14 b	7 b	8 b	12 b
Untreated plants	49 a	55 a	36 a	70 a
Total	110	62	44	82

Means±standard error. Mean followed by different letters in each column is significantly different at 0.05 level of significance using Mann-Whitney test.

 

Yield cotton

The fiber yield (with and without seed) estimated for the plot and per hectare showed no significant differences between treatments (Table 4). The ginning percentage was approximately 40%.

 

Table 4: Yield of cotton fiber per plot of 125 m2 and estimated ha-1 (kg).

Treatment	Fiber with seed (kg 125 m2)	Fiber without seed (kg ha-1)	Fibra (kg ha-1)
Lambda cyhalothrin + thiamethoxam	45.98 a	3679.16 a	1471.67 a
Untreated plants	41.15 a	3291.67 a	1298.23 a

Means±standard error. Mean followed by different letters in each column is significantly different at 0.05 level of significance using the student’s “t test.

 

The fiber yields estimated ha-1 varied from 1.4 (treated plot) to 1.2 ton ha-1 (untreated plot), and were higher. These yields were higher than those of Campuzano et al. (2015) determined in a trial carried out in Colombia and similar to those obtained in another study conducted in the area (Cañarte et al., 2020), using the DP Alcalá 90 variety in both cases. Although there were no significant differences between treatments, this would represent that the yield in treated plots was 11.6% higher than that estimated in untreated plots. However, the higher percentage in yield in plots treated with the insecticide must be analyzed in the context of the ecological and economic costs involved.

Conclusions and Recommendations

In the present research, the high population levels of B. tabaci were associated with low levels of parasitism by E. perganidiella due to interference from weekly sprays with lambda cyhalothrin + thiamethoxam that also decreased the number of predators. Thrips palmi, B. thurberiella, H. virescens and A. vestitis showed low levels, despite their importance as pests in other regions. Thrips palmi is reported for the first time feeding on cotton in Ecuador. Future research should focus on evaluating the selective applications of some insecticides to control A. gossypii and Dysdercus spp. infestations that impacts as little as possible on non-target organisms such as parasitoids and predators.

Acknowledgements

To Dr. Angel Luis Viloria (IVIC, Venezuela) for kindly reviewing the manuscript and the English text. This research was partially funded by The Grants No. PYTAUTO1639-2019-FIAG0002 (Universidad Técnica de Manabí (UTM)), Ecuador and South-South Cooperation for Strengthening the Cotton Sector, Food and Agriculture Organization of the United Nations (FAO).

Novelty Statement

General average of the number of individuals of the species Thrips palmi, Bucculatrix thurberiella, Dysdercus spp., Heliothis virescens and Anthonomus vestitus on cotton plants.

Author’s Contribution

Nelson D. Zambrano and Wilber Arteaga: field evaluations lab counts; tabulation of results, interpretation of data.

José Velasquez: mounting and preservation of insects; identification of pests and natural enemies.

Dorys T. Chirinos: trial design; data analysis; wrote the manuscript.

Conflict of interest

The authors have declared no conflict of interest.

References

Albittar, L., I. Mohannad, C. Bragard and T. Hance. 2016. Host plants and aphid hosts influence the selection behavior of three aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae). Eur. J. Entomol., 113(1): 516–522. https://doi.org/10.14411/eje.2016.068

Campuzano-Duque, L.F., S. Caicedo-Guerrero and J. Guevara-Agudelo. 2015. Determination of attributes in cotton (Gossypium hirsutum L.) genotypes in corn-soybean rotation associated with acid amended soils in the Colombian Eastern Plains. Cienc. Tecnol. Agrop., 16(2): 251-263. https://doi.org/10.21930/rcta.vol16_num2_art:371

Cañarte-Bermudez, E., R. Sotelo-Proaño and B. Navarrete-Cedeño. 2020. Generation of agricultural technologies to increase the productivity of Gossypium hirsutum L. in Manabí, Ecuador. Rev. Cienc. UNEMI. 13(33): 85-89. https://doi.org/10.29076/issn.2528-7737vol13iss33.2020pp85-95p

Chirinos, D.T., R. Castro, J. Cun, J. Castro, S. Peñarrieta Bravo, L. Solis and F. Geraud-Pouey. 2020. Insecticides and agricultural pest control: the magnitude of its use in crops in some provinces of Ecuador. Cienc. Tecnol. Agrop., 21(1): 1-16. https://doi.org/10.21930/rcta.vol21_num1_art:1276

Dutcher, J.D., 2007. A review of resurgence and replacement causing pest outbreaks in IPM. P. 27-43. In: Ciancio A., Mukerji K.G. (eds). General Concepts in Integrated Pest and Disease Management. Springer Nature, Switzerland. https://doi.org/10.1007/978-1-4020-6061-8_2

Eldesouky, S.E., 2019. Effectiveness of certain insecticides against cotton aphid, Aphis gossypii and their adverse impacts on two natural enemies. Egypt. Sci. J. Pest., 5(3): 7-13.

El-Heneidy, A.H., A.A. Khidr and A.A. Taman. 2015. Side-effects of Insecticides on Non-target Organisms: 1- In Egyptian Cotton Fields. Egypt. J. Biol. Pest Contr., 25(3): 685-690.

El-Wakeil, N., N. Gaafar, A. Sallam and C. Volkmar. 2013. Side effects of insecticides on natural enemies and possibility of their integration in plant protection strategies. In: InTech (eds.). Insecticides - Development of Safer and More Effective Technologies, Lomdon, UK. pp. 3-56. https://doi.org/10.5772/54199

FAO, 2015. Measuring sustainability in cotton farming systems. Towards a guidance framework. Food and Agriculture Organization of the United Nations International Cotton Advisory Committee Rome, Rome, Italy.

FAO, 2017. El estado de arte del sector algodonero en países del Mercosur y asociados. Organización de las Naciones Unidas para la Alimentación y la Agricultura y Agência Brasileira de Cooperação - Ministério das Relações Exteriores, Santiago, Chile.

FAOSTAT, 2019. Food and Agriculture Data. (http://www.fao.org/faostat/es/#data).

Gil, A. and M. López. 2017. Principal plagues and beneficial insects of Gossypium hirsutum L. “native cotton” of green fiber in relation to its phenological cycle. Arnaldoa, 24(1): 359-368.

Gonzalez, G., 2015. Coccinellidae species from Ecuador. Neotropical Coleoptera. (http://coleoptera-neotropical.org/paginas/2_PAISES/Ecuador/CUCUJOIDEA/coccinellidae-ecu.html).

Herrera, J. and R. García. 1978. Biología y comportamiento de Bucculatrix thurberiella Busck (Lepidoptera: Lyonetiidae). Rev. Peruana Entomol., 21(1): 97-102.

Janu, A., K.K. Dahiya and J. Pritish. 2017. Population dynamics of thrips, Thrips tabaci Lindemann in American Cotton (Gossypium hirsutum). Int. J. Curr. Microbiol. Appl. Sci., 6(7): 203-209. https://doi.org/10.20546/ijcmas.2017.607.024

Jaramillo-Barrios, C.I., A. Rodríguez, E. Varón-Devia, B.B. Monje-Andrade and E. Ebratt-Ravelo. 2018. Preferences of thrips (Thysanoptera) for the aerial structures of cotton plants (Gossypium hirsutum) in Colombia. Rev. Colomb. Entomol., 44(2): 151-157. https://doi.org/10.25100/socolen.v44i2.7310

Kaleem, M., W. Iqbal, I. Azam and A. Rasdha. 2014. Cotton aphid Aphis gossypii L. (Homoptera; Aphididae); a challenging pest; biology and control strategies. A review. Int. J. Appl. Biol. Pharm. Technol., 5(1): 289-294.

Moritz, G., L.A. Mound, D.C. Morris and A. Goldarazena. 2004. Pest thrips of the world visual and molecular identification of pest thrips. Cd-rom CBIT, Brisbane. Australia.

Naranjo, S.E., 2011. Impacts of Bt transgenic cotton on integrated pest management. J. Agric. Food Chem., 59(11): 5842-5851. https://doi.org/10.1021/jf102939c

Oliveira, M., T. Henneberry and P. Anderson. 2001. History, current status, and collaborative research projects for Bemisia tabaci. Crop Prot., 20(9): 709-723. https://doi.org/10.1016/S0261-2194(01)00108-9

Pinto, E.S., E.M. Barros, T.J. Braz and S.R.C. Neves. 2013. The control and protection of cotton plants using natural insecticides against the colonization by Aphis gossypii Glover (Hemiptera: Aphididae). Acta Sci. Agron. 35(2): 169-174. https://doi.org/10.4025/actasciagron.v35i2.15764

Polaszek, A., G.A. Evans and F.D. Bennett. 1992. Encarsia parasitoids of Bemisia tabaci (Hymenoptera: Aphelinidae, Homoptera: Aleyrodidae): A preliminary guide to identification. Bull. Entomol. Res., 82(3): 375-392. https://doi.org/10.1017/S0007485300041171

Prabhaker, N., J.G. Morse, S.J. Castle, S.E. Naranjo, T.J. Henneberry and N.C. Toscano. 2007. Toxicity of seven foliar insecticides to four insect parasitoids attacking citrus and cotton pests. J. Econ. Entomol., 100(4): 1053-1061. https://doi.org/10.1093/jee/100.4.1053

Rafiq, M., S.I.A. Shah, M.T. Jan, I.R. Khan, S.A.S. Shah and Z. Hussain. 2014. Efficacy of different groups of insecticides against cotton stainer, Dysdercus koenigii in field conditions. Pak. Entomol., 36(2): 105-110.

Razaq, M., R. Mensah and H.R.U. Athar. 2020. Insect pest management in cotton. Chapter 5. pp. 85-107. In: Jabran, K. and B. Singh Chauhan (eds.). Cotton production. John Wiley and Sons Ltd. Multan, Pakistan. https://doi.org/10.1002/9781119385523.ch5

Romero, L., A. Toledo, C. Yagual, E. Segura, R. Castro and D.T. Chirinos. 2019. Control biológico natural asociado con Aphis gossypii en pepino, Cucumis sativus L. In: Intriago R., A. Llerena, K. Intriago. Memorias de VII Congreso Latinoamericano de Agroecología, Guayaquil, Ecuador. pp. 646-651.

Ruberson, J.R., M.D. Thompson and P.M. Roberts. 2004. Pesticide effects on insect natural enemies of cotton pests. In: May, O. L., Jost, P.H. Roberts P.M, (eds) Cotton research extension report, 2003. University of Georgia Ext. Publ. 6, Univ. of Georgia, Athens, GA. pp. 124-132.

Schuster, D., G. Evans, F. Bennett, P. Stansly, R. Jansson, G. Leibee and S. Webb. 1998. A survey of parasitoids of Bemisia spp. Whiteflies in Florida, the Caribbean and Central and South America. Int. J. Pest Manage. 44(4): 255-260. https://doi.org/10.1080/096708798228194

Tomanović, Z., A. Petrović, M. Mitrović, N. Kavallieratos, P. Starý, E. Rakhshani, M. Rakhshanipour, A. Popović, A. H. Shukshuk and A. Ivanovic. 2014. Molecular and morphological variability within the Aphidius colemani group with redescription of Aphidius platensis Brethes (Hymenoptera: Braconidae: Aphidiinae). Bull. Entomol. Res., 104(5): 552-565. https://doi.org/10.1017/S0007485314000327

Trapero, C., I.W. Wilson, W.N. Stiller and L.J. Wilson. 2016. Enhancing integrated pest management in GM cotton systems using host plant resistance. Front. Plant Sci., 7(500):1-12. https://doi.org/10.3389/fpls.2016.00500