Selective application of malathion: effect on boll weevil, non-target insects and natural enemiesAbstract
Non-selective chemical insecticides are the main method to manage the major insect pest of cotton in the Americas, the boll weevil Anthonomus grandis (Boheman, 1843) (Coleoptera: Curculionidae). The objective was to evaluate the effect of selective application of malathion on the boll weevil and non-target insects and natural enemies. The experimental design was in randomized blocks with the treatments control, without spraying (T1) and with all cotton plants in the rows sprayed, sequentially, after the appearance of cotton squares or all (T3) or alternated (T4), respectively, when the number of them with cotton squares with oviposition punctures by the boll weevil reached 10%. Spraying was done with malathion (1,000 g.i.a. L-1). The insecticide malathion sprayed on alternate rows of cotton is as effective in controlling the boll weevil as when sprayed on all rows. However, this insecticide applied to alternate rows controls aphid populations because it is ecologically selective to the parasitoid B. vulgaris and the predators, Coccinellidae, Syrphidae, and Araneae.
Keywords:
Anthonomus grandis; Aphis gossypii; chemical control; natural enemies
Resumo
Inseticidas químicos não seletivos são o principal método de manejo da principal praga do algodão nas Américas, o bicudo do algodoeiro Anthonomus grandis (Boheman, 1843) (Coleoptera: Curculionidae). O objetivo foi avaliar o efeito da aplicação seletiva de malation sobre o bicudo-do-algodoeiro e sobre insetos não alvo e inimigos naturais. O delineamento experimental foi em blocos casualizados com os tratamentos controle, sem pulverização (T1) e com todas as plantas de algodão nas linhas pulverizadas, sequencialmente, após o aparecimento dos botões florais de algodão ou todas (T3) ou alternadamente (T4), respectivamente, quando o número delas com botões florais de algodão com orifícios de oviposição pelo bicudo atingiu 10%. A pulverização foi feita com malation (1.000 g i.a. L-1). O inseticida malation pulverizado em fileiras alternadas de algodão é tão eficaz no controle do bicudo do algodão quanto quando pulverizado em todas as fileiras. No entanto, esse inseticida aplicado em fileiras alternadas controla populações de pulgões porque é ecologicamente seletivo para o parasitoide B. vulgaris e os predadores, Coccinellidae, Syrphidae e Araneae.
Palavras-chave:
Anthonomus grandis; Aphis gossypii; controle químico; inimigos naturais
1. Introduction
The area cultivated with upland cotton (Gossypium hirsutum L.), traditionally grown in Brazil, has been decreasing, mainly due to productivity gains (Hoffmann et al., 2020). Cotton is produced in the Cerrado biome of Brazil, with the highest production in the states of Bahia and Mato Grosso, and in the Caatinga biome (Brasil, 2023).
Investments in technology, professionalization of producers, and innovations in research and cultivation techniques increased the cotton productivity over the last 20 years (Hoffmann et al., 2020; Santos et al., 2020). The cultivated area, with transgenic cotton expressing toxic proteins from the bacteria Bacillus thuringiensis (Bt), increased from 145 thousand ha (18%) in the 2009/2010 harvest to 940 thousand ha (84%) in the 2016/2017 harvest (Rocha-Munive et al., 2018; Morello et al., 2020). The efficiency of these cultivars is high against lepidopteran pests, but reduced against the boll weevil, Anthonomus grandis (Boheman, 1843) (Coleoptera: Curculionidae) and sucking insects and mites (Alves et al., 2021). This explains, in part, the high expenditure on chemical insecticides to manage these and other cotton pests (Barros et al., 2019; Faustino et al., 2023).
In Brazil, malathion, a chemical from the organophosphate group with a broad spectrum of action and, in most cases, low selectivity towards natural enemies, is the most recommended and widely used insecticide for managing the boll weevil (Hill et al., 2017; Rolim et al., 2019; Torres et al., 2022). Control of this insect in the different cotton-producing regions of Brazil is carried out with 17 to 23 sprays with malathion and other insecticides, increasing production costs and affecting non-target insects (Torres et al., 2022). Furthermore, these applications can increase or reduce populations of certain insects, modifying the structure and functionality of the cotton agroecosystem (Sánchez-Bayo, 2021). This increases the need to develop insecticide application methods that are more compatible with biological control in the integrated management of cotton pests, particularly for non-selective compounds such as malathion (Farrar et al., 2018).
The hypothesis of this study is that the impact of the organophosphate insecticide malathion on cotton crops, as well as on natural enemies of the boll weevil and other pests, varies with the method of its application. Electrodynamic and conventional spraying of insecticides, from different chemical groups in alternating rows, is efficient and economical against the boll weevil (Ramalho and Jesus, 1989; Ramalho and Gonzaga, 1991). However, the effect of this insecticide, in different application methods, on non-target insect populations and natural enemies in cotton crops, needs to be further studied. The objective was to evaluate the effect of selective application of malathion on the boll weevil and non-target insects and natural enemies.
2. Materials and Methods
2.1. Study location
The work was carried out in the Entomology laboratory (latitude 7° 22’ 57” S, longitude 35° 90’ 53” W) and in the experimental field of Embrapa Algodão (latitude 7° 13' 50” S, longitude 35° 52’ 52” W), with a history of occurrence of the boll weevil and the aphid Aphis gossypii Glover (Hemiptera: Aphididae) (Glover, 1877) in Campina Grande, Paraíba state, Brazil. The soil of this experimental area is a eutrophic Regolithic Neosol (Santos et al., 2018), and the climate of Campina Grande is Aw, with an average annual temperature and rainfall, respectively, of 22.9 °C and 765 mm, according to the Köppen and Geiger classification.
2.2. Plant material and associated natural enemies
The BRS 433 B2RF cultivar, a transgenic cotton plant with Bollgard II Roundup Ready Flex long fiber technology, is resistant to the herbicide glyphosate and to the main species of defoliating caterpillars (Morello et al., 2020). Plants of this cultivar, with high productive potential (above 4,500 kg/ha) and fiber yield estimated at 38%, are resistant to the primary cotton diseases (angular spot – bacteriosis; blue disease and common mosaic – virus).
Specimens of the parasitoids Bracon vulgaris (Ashmead, 1894) (Hymenoptera: Braconidae) and Jaliscoa grandis (Burks, 1954) (Hymenoptera: Pteromalidae), as well as predators from the families Araneae, Coccinellidae, and Syrphidae, were found naturally in the experimental area.
2.3. Soil preparation and fertilization
The soil was prepared by plowing and harrowing and fertilized according to analyzes and technical recommendations for cotton cultivation. The fertilizers urea (45% N), phosphorus pentoxide (18% P2O5) and potassium chloride (60% K2O) as sources of N-P-K (fertilizers Heringer SA, Paulínia, SP, Brazil) were used.
2.4. Selective application of malathion
Seeds of the cotton cultivar BRS 433 B2RF were manually sown in the “Embrapa Algodão” experimental field.
The economic efficiency of malathion, in selective application, was evaluated in an area of 768 m2 (24 m x 32 m) using a randomized block design with four treatments and four replications (blocks). The treatments were control cotton plants, without spraying (T1) or with weekly and sequential spraying, with malathion (1,000 g i.a. L-1), of all cotton rows after the appearance of cotton squares (T2) or all (T3) or alternated (T4) when the number of plants with cotton squares with oviposition punctures reached 10% (Ramalho and Jesus, 1989; Ramalho et al., 1990). Each plot was five meters long with five rows of cotton plants, with approximately 320 plants spaced 0.80 m x 0.10 m between rows and plants. The distances between plots and blocks were five and 10 meters, respectively.
The boll weevil oviposition punctures were sampled every five days, examining the upper third of the canopy of each cotton plant and randomly collecting a medium-sized floral bud (4-6 mm in diameter). Aphid colonies and natural enemies of the boll weevil were monitored on the third expanded apical leaf of each plant. Thirty cotton plants were randomly chosen and examined per plot and sampling date. Cotton squares, fallen to the ground between the planting rows and with boll weevil oviposition punctures, were collected weekly, per plot. These cotton squares were taken to the laboratory and placed in ventilated plastic containers with lids to determine the number of emerged boll weevil adults and their parasitoids.
Sprays against the boll weevil, starting from the appearance of the first flower buds until the formation of the first boll, were carried out using a manual knapsack sprayer with 20 liters of syrup and an empty D2 cone nozzle, every five days. This method was used because the survival of Eriopis conexa (German, 1844) (Coleoptera: Coccinelidae), Chrysoperla externa (Hagen, 1861) (Neuroptera: Chrysopidae), Orius insidiosus (Say, 1832) (Hemiptera: Anthocoridae) and Podisus nigrispinus (Dallas, 1851) (Hemiptera: Pentatomidae) was 50 to 90% during this period (Machado et al., 2019). The sprayer tip was positioned laterally to the line, approximately 20 cm from the cotton plants (Ramalho and Jesus, 1989), with a flow rate of 150 to 300 liters of water ha-1 according to the plant's growth stage.
Standard cultural practices for cotton cultivation (application of herbicides and manual weeding, etc.) were carried out. The average temperatures, relative humidity, and accumulated monthly precipitation in the “Embrapa Algodão” experimental field, during the experiment, were obtained from the National Institute of Meteorology (INMET, 2022).
2.5. Data analysis
Data on percentages of cotton squares, with oviposition punctures of A. grandis and aphid colonies, natural enemies, and emergence of J. grandis and B. vulgaris in laboratory and seed cotton production (g), were submitted to the Shapiro-Wilk normality test, analysis of variance (ANOVA) and the means compared by the Student Newman Keuls test at 5% probability. The data, in proportions, were transformed into the square root of x + 0.5 before repeated measures analysis and presented as untransformed means, using the Statistical and Genetic Analysis System (SAEG) of the Federal University of Viçosa (Ribeiro Júnior, 2001).
Average cotton production and net profit per hectare were based on weighing the seed cotton lint, manually collected from the bolls of all plants per plot in 10 m2, multiplied by the price of lint and seeds and subtracting the cost of malathion applied per hectare.
3. Results
The average temperatures, relative humidity, and accumulated monthly precipitation at the “Embrapa Algodão” experimental field during the experiment in 2023 were, respectively, 24.4 ± 1 °C, 78.5 ± 1%, and 58.1 mm. The cotton phenological cycle was 132 days, from plant emergence, appearance of the first cotton flower buds, and boll opening, respectively, at 12, 45, and 104 days after planting.
The percentage of cotton plants with boll weevil oviposition punctures was higher in control than in the other treatments (F3,9 = 7.15; P < 0.01) (Figure 1). The number of plants, with cotton squares with oviposition punctures by the boll weevil, was similar between treatments with malathion sprays in all rows, sequentially or, when the number of punctures of oviposition reached a level of 10% in all rows and alternated rows.
Percentage of cotton plants with cotton squares showing boll weevil oviposition punctures because of the treatments. Treatments: control (no spraying) (T1), weekly spraying with the insecticide malathion (1,000 g a.i. L−1) on all cotton rows after the appearance of cotton squares (T2), or when the number of plants with cotton squares with boll weevil oviposition punctures reached 10% in all rows (T3) or in alternate rows (T4). Means followed by the same letter between treatments do not differ according to the Student Newman Keuls test (P= 0.05). Root-transformed means of x+0.5 for statistical analysis and original data presented.
The percentage of J. grandis adults that emerged from cotton squares fallen to the ground with oviposition punctures by the boll weevil was higher in the control (F3,9 = 4.20; P < 0.05) (Figure 2A), while that of B. vulgaris was similar between treatments (F3,9 = 1.30; P = 0.33) (Figure 2B).
Emergence (%) of Jaliscoa grandis (Hymenoptera: Pteromalidae) (A) and Bracon vulgaris (B) (Hymenoptera: Braconidae) from cotton squares that fell to the ground with boll weevil oviposition punctures because of the treatments. Treatments: control (no spraying) (T1), weekly spraying with the insecticide malathion (1,000 g a.i. L−1) on all cotton rows after the appearance of cotton squares (T2), or when the number of plants with cotton squares with boll weevil oviposition punctures reached 10% in all rows (T3) or in alternate rows (T4). Means followed by the same letter in the bars do not differ according to the Student Newman Keuls test (P = 0.05). Means transformed by the root of x+0.5 for statistical analysis and original data presented.
The percentages of cotton plants with colonies of the aphid A. gossypii (F3,9 = 4.31; P < 0.05) were higher in treatments with sequential spraying of malathion in all rows than in alternate rows, when the number of cotton squares with oviposition holes reached 10% and in the control (Figure 3A).
Percentages of cotton plants with colonies of the aphid Aphis gossypii (Hemiptera: Aphididae) (A) and of its natural enemies (Araneae, Coccinelidae, Syrphidae) (B) because of the treatments. Treatments: control (no spraying) (T1), weekly spraying with the insecticide malathion (1,000 g a.i. L−1) on all cotton rows after the appearance of cotton squares (T2), or when the number of plants with cotton squares with boll weevil oviposition punctures reached 10% in all rows (T3) or in alternate rows (T4). Means followed by the same letter between treatments do not differ according to the Student Newman Keuls test (P= 0.05). Root-transformed means of x+0.5 for statistical analysis and originals presented.
The percentages of natural enemies of aphids were higher in the control and in the treatment with malathion sprayed in alternated rows when the number of cotton squares with oviposition punctures reached 10% (F3,9 = 5.29; P < 0.03) (Figure 3B) than with this insecticide sprayed in all cotton rows, sequentially, or, when the number of cotton squares with oviposition punctures reached 10% (Figure 3B). Predatory arthropods from the families Coccinelidae and Syrphidae and of the order Araneae were the most collected, and Hymenoptera parasitoids of aphids were not observed.
The number of applications with malathion, targeting the boll weevil, was greater with sequential and weekly spraying than in all or alternated rows when the number of plants with cotton squares exhibiting oviposition punctures by the boll weevil reached 10%. The volume of spray, in the treatment with malathion in alternate rows, was half that applied on all cotton rows, reducing costs and the impact on the aphids' natural enemies (Table 1).
Treatment (Treat.), dosage in (L ha-1) (Do), number of spraying (No) and price of malathion EC (US$), cotton lint and seed production in kg ha-1, price of production and gross and net income from cotton cultivation(1) in US$ ha-1.
The production of cotton lint (F3,9 = 40.93; P < 0.01) and seeds (F3,9 = 40.93; P < 0.01), production price (F3,9 = 40.93; P < 0.01) and gross (F3,9 = 15.88; P < 0.01) and net income (F3,9 = 40.93; P < 0.01) were lower in the control than in the treatments with malathion applied sequentially to all or alternated rows of the cotton plants, when the number of cotton squares with oviposition punctures reached 10% (Table 1).
4. Discussion
The greater number of cotton plants with oviposition punctures by the boll weevil in the control than in those sprayed with malathion confirms the high toxicity of this organophosphate insecticide, the most widely used and the fourth most toxic against this insect pest after chlorpyrifos, metidathion, and the mixture of profenofos + cypermethrin (Torres et al., 2022). The similar number of cotton plants with cotton squares with oviposition punctures in the treatments sprayed against this insect, based on the 10% control level, on all or alternate rows of plants (Ramalho and Jesus, 1989; Ramalho and Gonzaga, 1991), or weekly and sequentially is probably due to the colonization behavior and dispersal of boll weevil adults between cotton canopies treated or not with the insecticide, becoming contaminated in the former (Arruda et al., 2021).
The higher percentage of J. grandis adults that emerged from cotton squares that had fallen to the ground and with oviposition punctures by the boll weevil, and in the control, than in the treatments sprayed with malathion, is due to the absence of application of this product in the first one (Alves et al., 2021). Malathion is not selective to parasitoids, which may be associated with the pro-insecticide activity of its molecules, penetrating the body of these organisms and becoming, through biochemical reactions, more toxic (Bacci et al., 2009; Hill et al., 2017; Dakhel et al., 2020). The toxicity of this organophosphate is also related to the lipophilic nature of its molecules and the thickness and lipid composition of the insect cuticle (Bacci et al., 2009; Balabanidou et al., 2018). The similar emergence of B. vulgaris adults in all treatments suggests lower susceptibility of this parasitoid to malathion compared to J. grandis, possibly due to differences in their searching behavior. Jaliscoa grandis, unlike B. vulgaris, prefers to parasitize cotton boll weevil larvae in green cotton bolls (Ramalho and Wanderley, 1996), when plants are more leafy, thereby reducing their exposure to insecticide spray due to the umbrella effect of cotton leaves (Costa et al., 2015).
The highest and lowest percentages, respectively, of aphid colonies and of their natural enemies in treatments sprayed with malathion on all cotton rows sequentially or when the number of cotton squares with oviposition punctures reached the 10% level, indicates low toxicity and selectivity of malathion against aphids and natural enemies, respectively (Khan et al., 2017). Furthermore, the low physiological selectivity of malathion against natural enemies favors the population increase of these sucking insects (Ali et al., 2016; Machado et al., 2019).
The higher percentages of aphid natural enemies in the control and in the treatment with malathion sprayed on alternated rows of cotton plants, when the number of cotton squares with oviposition punctures reached 10%, can be attributed, in the first case, to the absence of insecticide application and, in the second, to lower natural enemy mortality with alternated row application (Roubos et al., 2014; Alves et al., 2021). This is important for biological control tactics, based on ecological selectivity, improving the use of compounds such as malathion, physiologically non-selective, but important to protect cotton plants against pests (Duso et al., 2020; Torres et al., 2022). The lower percentages of natural enemies of aphids in treatments with malathion sprayed on all cotton rows, sequentially or when the number of cotton squares with oviposition punctures reached the level of 10%, indicate a reduction in the ecological selectivity of malathion to these insects. The occurrence of predators, but not of Hymenoptera parasitoids of aphids, is probably due to the latter being more sensitive to malathion than their hosts and the former more tolerant to this product than their prey (Croft and Brown, 1975; Megahed and El-Bamby, 2020). Variations in the number of malathion sprays against boll weevil, between treatments, were expected due to the different method of application of this insecticide (Guedes et al., 2016). This is probably also due to the lower residual effect of this insecticide, compared to thiamethoxam and lambda-cyhalothrin + thiamethoxam, favoring selective applications to reduce impacts on natural enemies (Araújo et al., 2017; Machado et al., 2019). The greater number of applications of malathion in the sprayed treatments, sequentially and weekly, than in those with this product in all or in alternated rows when the number of plants with cotton squares with oviposition punctures by the boll weevil reached the level of 10% is due to the method of application. Furthermore, sequential applications without considering the economic limit of 10% boll weevil infestation go against the precepts of the cotton IPM (Torres et al., 2022). The lower volume of malathion sprayed in alternate rows, but with boll weevil control efficiency similar to that of other treatments, agrees with previous results of spraying in alternated rows of cotton with cyfluthrin (Baytroid 50 EC), at the doses of 25 and 40g a.i. ha-1, cypermethrin (Cymbush 30 ED), white beak (1.5ml/L) at 3.91g a.i. ha-1 and cyhalothrin 10 ED, yellow beak with 2.61g a.i. ha-1, with an ElectroDyn sprayer positioned 20 cm above the cotton canopy (Ramalho and Jesus, 1989; Ramalho and Gonzaga, 1991). This confirms the movement of boll weevil adults between plants in treated or not rows, contaminating themselves in the treated ones (Ramalho and Gonzaga 1991) with a reduction in volume and costs of insecticides applied (Roubos et al., 2014; Arruda et al., 2021).
The lower production and gross and net income in the control than in the malathion treatments is due to the lack of application of this insecticide, in the first, to control the boll weevil, confirming the importance of reducing populations of this key pest and, consequently, losses (Oliveira-Marra et al., 2019; Alves et al., 2021). The reduced use of malathion, without compromising control of the boll weevil in treatments sprayed on alternated rows of cotton plants when the number of cotton squares with oviposition punctures reached 10%, decreases the volume of product applied. Furthermore, the lower volume of malathion, applied per hectare in alternated rows of cotton, reduced aphid populations and preserved populations of natural enemies (Roubos et al., 2014). This is important to managing resistant populations of boll weevil and other cotton pests, conserving populations of natural enemies, and reducing the number of individuals and damage from secondary pests, environmental contamination, and greenhouse gas emissions.
The number of plants with cotton squares exhibiting boll weevil oviposition punctures was lower in all treatments sprayed with malathion, regardless of the method of application. Malathion applied to cotton leaves was selective to the parasitoid B. vulgaris, but not to J. grandis. This insecticide did not control aphid populations when applied systematically to all rows of cotton plants or when the number of cotton squares on these plants with oviposition punctures reached 10%. However, it was effective against this pest when applied to alternate rows, likely due to its reduced impact on natural enemies. Malathion, applied on alternate rows when the number of cotton squares with oviposition punctures by the boll weevil reached 10%, was effective with a net income similar to other treatments using this organophosphate, but with half the volume of insecticide used to control this pest.
5. Conclusion
The insecticide malathion, when sprayed on alternate rows of cotton, is as effective in controlling the boll weevil as when sprayed on all rows.
The insecticide malathion, sprayed on alternate rows, controls aphid populations because it is ecologically selective for the parasitoid B. vulgaris and the predators Coccinellidae, Syrphidae, and Araneae.
Acknowledgements
To “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)” through scholarship to Samuel Ferreira Camelo and also to the Better Cotton Initiative (BCI) for financial support through the cooperative project between “Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA)” (SEG Code: 20.24.00.007.00.00)” and “Associação Mineira dos Produtores de Algodão (AMIPA)”.
Data Availability Statement
Data is available upon request.
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Editor:
Ana Paula Peron
