elocation-id: e3448
Plant fertilization may impact directly on insect pest behavior and biology. Fertilization may be accomplished by using synthetic mineral or organic fertilizers. The effect of different doses of boiled hen chicken manure, Penergetic®, Bokashi compound and mineral fertilizer on the adult population of Bemisia tabaci and Myzus persicae on collards leaves were evaluated. The experiment was conducted in the greenhouse using the treatments: Bokashi, Penergetic® bioactivator, 2.5%, 5%, and 7.5% of solution of boiled manure, mineral fertilization and control. The number of insects was counted directly on the leaves, and the nitrogen, potassium content, and total phenolic compound in the leaves were determined. Higher populations of Bemisia tabaci and M. persicae were observed on NPK-fertilized plants compared to other treatments. Higher levels of nitrogen foliar were found for Bokashi-fertilized plants; and higher concentrations of total phenolic compounds were found in the control. A negative correlation between total phenolics and B. tabaci was established suggesting the importance of these compounds in the species development. The results indicate the importance of the source of the fertilization for sustainable pest management.
Bemisia tabaci, biological control, Blattisociidae, Laelapidae, Phytoseiidae, natural enemies.
Collard green (Brassica oleracea L. var. acephala) (Brassicaceae) is an excellent source of nutrients, phenolics, organosulfurs, carotenoids, and others bioactive substances associated with the prevention of many diseases (Ramirez et al., 2020). Due to these characteristics, the vegetable is being increasingly consumed. Among the principal limitations to collards production stands out the incidence of whitefly Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) and Myzus persicae Sulzer (Hemiptera: Aphididae) which may cause significant damages and losses in production. B. tabaci is assumed to be a complex of at least 40 morphologically similar cryptic species (Li et al., 2021).
Individuals cause direct damage as phloem feeders (de Barro et al., 2011) and indirect damage as vector of more than 100 different plant viruses (Hogenhout et al., 2008). The aphid complex: M. persicae; Lipaphis pseudobrassicae Davis and Brevicoryne brassicae L. (Hemiptera: Aphididae) feeding causes chlorosis and foliar wrinkling and by the secretion of sugar solution, both aphids and whitefly, induce the development of mold fungi, which hinder photosynthesis by covering leaf surface (Michereff Filho et al., 2021).
Synthetic chemical insecticides are generally used for control of these pests; however, despite their efficiency, negative implications on the environmental and human health are frequently reported (Alengebawy et al., 2021). Furthermore, insects eventually may develop resistant to insecticides in responses to systematic applications, making their control even more difficult. These constraints generated efforts to develop eco-friendly strategies to manage these and other pests.
Studies have suggested that fertilization of plants influences the biology of pests (Hosseini et al., 2015; Hata et al., 2019; Ramachandran et al., 2020; Sousa et al., 2021). Morales et al. (2001) observed a lower incidence of aphids on maize plants fertilized with organic fertilizer when compared to those fertilized with synthetic chemicals. A higher density of B. tabaci on tomato plants was observed using increasing doses of nitrogen (Žanić et al., 2011) and similar results were found for Aphis craccivora Koch (Hemiptera: Aphididae) (Hosseini et al., 2015).
Higher amounts of nitrogen fertilizer applied in the soil results in increasing concentrations in plant tissues. A positive correlation between nitrogen/protein concentrations in leaves vs phloem feeders’ insects and mites’ population have been evidenced (Sousa et al., 2021; Puspitarini et al., 2021; Li et al., 2022). On the other hand, secondary metabolites as phenolic compounds (Hata et al., 2019; Sousa et al., 2021), glucosinolates (Dar, 2021) and terpenoids (Zanin et al., 2021) are negatively correlated with incidence.
The organic fertilizers as Bokashi compost, boiled hen chicken manure and the bioactivator Penergetic® have been used as options to produce greens, vegetables, and fruits (Xavier et al., 2019; Maass et al., 2020; Hata et al., 2021a; Hata et al., 2021b) for organic and conventional farming systems. However, information concerning the impact of these organic fertilizers and amendments on pest incidence are still scarce. Therefore, in this research, we evaluated the B. tabaci and M. persicae populations fertilized with Penergetic® bioactivator, Bokashi compound, NPK mineral fertilizer and doses of boiled hen chicken manure on collard plants in a greenhouse.
Seedlings of collards Georgia cv. were sown in trays (December 23, 2016) and transplanted (January 24, 2017) to 5 L pots containing soil (Red Latosol, clay texture) in a greenhouse of the Universidade Estadual de Londrina-UEL, (23° 20’ 28” S, 51° 12’ 34” W, 548 m). In the second cycle, plants were sown in trays on April 15, 2017, and transplanted on May 15, 2017. Each pot corresponded to a plot. Plants were irrigated twice a day.
Phytosanitary measures were not accomplished. The treatments were: control (no fertilization), doses of boiled hen chicken manure (2.5%, 5% and 7.5%), EM Bokashi, Penergetic® bioactivator and mineral fertilizer (15-10-15; 15% nitrogen, 10% phosphorous and 15% potassium).
Manure was prepared boiling 30 kg of fresh hen chicken during four hours. The solution was then filtered and diluted to the concentrations used in the experiment. The boiled manure treatments were applied twice a week (50 ml of solution per plant) from 38 days after sowing (DAS) to the last evaluation. For Penergetic treatments, 3 g of bioactivator Penergetic® k or p were diluted in 1.5 L of water and then applied on the soil (Penergetic® k) 38 DAS and sprayed on the plant (Penergetic® p) 68 DAS. Mineral fertilization was applied 38 and 48 DAS (10 and 5 g per plant, respectively). Bokashi was applied at 38, 48 and 60 DAS (25 g per plant in each stage).
The insects infesting plants were assessed twice a week in the morning, when B. tabaci adults were motionless compared to the warmer periods of the day. Seven leaves of the same size were randomly selected for each plot, carefully observing the abaxial and adaxial surfaces of the leaves. The same procedure was performed for M. persicae assessing three leaves per plot (120 samples per plot).
On March 24, 2017, sixteen leaf samples were collected from each treatment, cleaned with running water and distilled water. Next, the samples were dried in a forced air stove at 65° C for 72 h and leaves ground in a mill.
For nitrogen analysis, 0.1 g of each sample was digested at 350 °C which was gradually increased by 50 °C every 30 min, according to Kjeldahl’s analytical method. For potassium determination, flame photometry method was used.
For total phenolic determination, the methodology from (Stratil et al., 2006) with modifications was used. Extraction of 1 g of fresh leaf with 10 ml of absolute ethanol at 80% (v/v), stirring for 30 min at 120 rpm (Orbital-New Organic) was performed. After, the extract was then separated by centrifugation at 2 500 rpm (Excelsa 2 Fanem model 205 N) for 5 minutes.
For the analysis, an aliquot of 1 ml of extract, 1 ml of distilled water, 1 ml of Folin-Ciocalteau reagent 0.9 N and 1.0 of sodium carbonate 10% (m/v) were used. The mixture remained during 30 min in the dark under indoor environment temperature. Subsequently, the absorbance was measured at 720 nm in a Micronal spectrophotometer, AJX 1600. Gallic acid was used as the standard at 0.5, 20, 40, 60, 80, 100, 150 μg ml-1. The results were shown as mg of Gallic acid equivalents in g per sample (mg EAG g-1). Analysis was performed in triplicate.
A randomized block design with seven replications was used. To verify the assumptions for the analysis of variance, tests of the variance homogeneity and normality were performed. If the assumptions were met, the means were compared by the Tukey test (5%). Otherwise, the Friedman’s test (5%) was used. A Pearson correlation matrix (1%) was used in each of the variables studied to infer the relationship between them. Statistical packages Past (Hammer et al., 2001) and Bioestat 5.0 (Ayres, 2007) were used.
In the first evaluation, by using NPK fertilization, a higher number of adults of B. tabaci per leaf (F= 3.17, p< 0.05) compared to treatments non fertilized and boiled manure 2.5% was found (Table 1). Other treatments (5%, 7.5%, Bokashi and Penergetic®) were intermediate. In the second and third evaluations, higher number of B. tabaci adults was found for the mineral fertilization treatment than the other treatments (F= 61.27 and 18.1, p< 0.05) (Table 1).
In the fourth evaluation, higher adults of B. tabaci on the NPK fertilized plants than 5% of boiled manure and control were assessed. On the fifth evaluation, higher number was observed on NPK than the control treatment (74 times more insects). The means of all assessment indicated 6.82 times more insects in the NPK treatments than the means of the remaining ones.
In the fifth, sixth, and general evaluations for M. persicae in the first cycle, differences between treatments were observed (F= 17.41, p< 0.05; F= 14.94, p< 0.05; F= 61.03, p< 0.05). In the fifth and sixth evaluations, higher number of M. persicae adults was found in the NPK than the remaining treatments (Table 2). For the second cycle, higher magnitude of differences was observed for the fourth assessment in which NPK aphid treatments were higher than all other treatments (means 5.48 times more). The general means of the assessments, in general, higher populations were also found for NPK treatment (Table 3) (two times more insects).
Higher nitrogen contents were observed in plants fertilized using Bokashi than control, boiled manure 2.5% and Penergetic (Figure 1A). Higher potassium levels were found in NPK fertilized plants than boiled manure 2.5% and control (Figure 1B). For total phenolics, higher contents were found for control treatment than NPK, Bokashi, Penergetic and boiled manure 7.5% (Figure 1C).
Positive correlations between B. tabaci population and M. persicae (r2= 0.92; p< 0.01); B. tabaci and potassium content in leaves (r2= 0.84; p< 0.01) were found (Figure 2). A negative correlation was observed between total phenolics and B. tabaci (r2= -0.87; p< 0.01), nitrogen (r2= -0.9; p< 0.01) and potassium (r2=- 0.9; p< 0.01) (Figure 2).
Treatments affected the contents of the two nutrients studied (Figure 1). The nitrogen content in the current study was generally lower than that found in collard plants fertilized with pig slurry, poultry manure, and urea which varied from 29 to 35.7 g kg-1 N in collards leaves (Steiner et al., 2019). The potassium contents for control and boiled manure treatments were similar to the previous cited study, in which, varied from 17.1 to 18.7 g kg-1 K (Steiner et al., 2019).
Nitrogen is one of the most important nutrients for plant development but also impacting on arthropods plant susceptibility mostly to phloem sucking insects (Bala and Tahur, 2018). However, in the present study, no correlation was observed between nitrogen and the insects assessed. Similarly, no relation between nitrogen and Delia radicum L. or B. brassicae on rapeseed (Brassica napus L. ssp. oleifera Metzg) was reported (Szwarc et al., 2021).
Previously, B. tabaci attraction on tomato plants under NPK fertilization, raised from 29.4 (recommended dose) to 37.2 (2× recommended fertilization) (Idriss et al., 2015). Excessive use of nitrogen fertilizers was identified as promoters of imbalances in plant metabolism due to protein degradation releasing soluble amino acids, which are easily assimilated by insects favoring pest infestation (Chaboussou, 1987). Previous studies also indicated that higher amounts of nitrogen fertilizer change the volatile profile attracting more B. tabaci adults in olfactometer assays (Islam et al., 2017).
A positive correlation between potassium and B. tabaci was observed (Figure 2), what was also previously observed when evaluating Tetranychus urticae Koch (Acari: Tetranychidae) populations on strawberry leaves (Hata et al., 2019). However, in general, the potassium content in leaves is negatively correlated with arthropods infestations due to the improvement of secondary compounds and reduction of carbohydrate accumulation (Bala et al., 2018).
Decreasing populations of Hydrellia philippina Ferino (Diptera: Ephydridae), Cnaphalocrocis medinalis Guenee (Lepidoptera: Crambidae), Scirpophaga incertulas Walker (Lepidoptera: Crambidae) on rice (Oryza sativa L.) were observed after foliar sprays of potassium dihydrogen phosphate (Chatterjee et al., 2021). In the present study, the population of B. tabaci and M. persicae were higher on NPK-fertilized plants than organically-fertilized or no-fertilized plants. Similarly, on chemical-fertilized collards plants, higher B. brassicae and M. persicae populations were observed than on organic-fertilized plants (Cividanes et al., 2020).
In cabbage, reduction of populations of M. persicae was obtained by fertilizing plants using organic amendments (Staley et al., 2010). Lower aphids’ populations were also observed in maize grown using organic fertilization than those using formulated synthetic fertilizers (Morales et al., 2001). Although the N levels were higher in Bokashi treatment and similar to NPK treatment, Bokashi did not trigger growth of B. tabaci and M. persicae insect populations per plant.
Organic amendments and fertilizers release nitrogen and other nutrients slowly and improve the microbial community (Rowen et al., 2019). By using organic fertilizers, increasing abundance of predatory insects has been reported (Peñalver-Cruz et al., 2019). Furthermore, the number of natural enemies was even higher than pests (B. brassicae, M. persicae and B. tabaci) on organically-fertilized collard plants than on chemical fertilized-plants (Cividanes et al., 2020).
Then, organic manure may activate indirect defenses by increasing defensive chemical production, modifying herbivore-induced plant volatiles (Rowen et al., 2019), which should attract or ‘call’ more natural enemies for pest control. Organic fertilization and amendments, besides increasing N levels, may also increase secondary compounds. For Brassicaceae plant species increases of up to three-fold in glycosinolates (sulfur-rich compounds) have been reported (Staley, 2010).
Organic fertilizers can provide a number of nutrients, including sulfur, which are included in the composition of glucosinolates. Under these conditions, generalist insects such as B. tabaci and M. persicae would be underprivileged. The phenolic compounds may also impair the biological parameters or reduce of pest-arthropods populations (Hata et al., 2019; Sousa et al., 2021).
This was observed through a negative correlation between total phenolics and B. tabaci (Figure 2). In previous controlled study, landing and oviposition preferences of B. tabaci on cabbage were negatively correlated to total phenolic contents (Yang et al., 2020). Phenolic compounds may also exhibit toxic and antifeedant effects on insects (Singh et al., 2021).
The results reported here may be relevant to understand the dynamic of insects mostly on organic cultivation to develop suitable management strategies. Due to lower pest development by using organic fertilizers, adoption of a sustainable approach, avoiding pesticides may be facilitated. By using amendments that disfavor insect pest occurrence, complementary measures such as botanicals extracts, biological control, repellent plants etc. may work better.
In summary, major number of B. tabaci adults and M. persicae were found in NPK-fertilized plants. Plants fertilized with Bokashi compound showed higher N contents than those fertilized with boiled manure 2.5%, control and Penergetic. Overall, NPK-fertilized plants showed higher K contents than control and boiled manure 2.5% while the remaining treatments were intermediate. Positive correlations between B. tabaci population and M. persicae, B. tabaci and potassium content in leaves were found. Otherwise, negative correlation was observed between total phenolics and B. tabaci, nitrogen and potassium.
To the National Council for Scientific and Technological Development (CNPq), for the financial support and the grant of scholarship, to the State University of Londrina (UEL), to the Postgraduate Program in Agronomy, to the soil laboratory technicians
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