Carátula del artículo
Evaluation of integrated pest management modulation for mitigation of
pesticide residues in mango
Avaliação da modulação do manejo integrado de pragas para mitigação
de resíduos de pesticidas em manga
Muhammad Asif Farooq asiff06@hotmail.com
Muhammad Nawaz Sharif University of
Agriculture, Pakistan
Asim Abbasi asimuaf95@gmail.com
Kohsar University Murree, Pakistan
Muhammad Nadir Naqqash nadir.naqqash@mnsuam.edu.pk
Muhammad Nawaz Sharif University of
Agriculture, Pakistan
Bilal Atta bilalattamuhammad@yahoo.com
Rice Research Institute, Pakistan
Muhammad Arshad arshaduaf@gmail.com
University of Agriculture, Pakistan
Mariam Fatima mariamfatima178@gmail.com
University of Agriculture, Pakistan
Pesquisa Agropecuária Tropical, vol. 54, e77681, 2024
Escola de Agronomia/UFG
Received: 01 November 2023
Accepted: 11 December 2023
Published: 05 February 2024
INTRODUCTION
Fruits from tropical and subtropical regions are valuable sources of nutrition and
energy (Akhtar et al. 2013, Zia-ud-Din et al. 2019). The nutritional
profile of many fruits, along with their antioxidant potential, helps in the
prevention of chronic human diseases (Baliga et al.
2018, Van Breda & Kok
2018).
Mango [Mangifera indica (L.) Lam.], ranked fifth after banana,
apple, grape and orange, is one of the most produced fruits in the world, with
annual yield of 55.6 million metric tons (Brahmeet
et al. 2023). Mango also dominates the local fruit market of Pakistan
(Badar et al. 2019) and is substantially
exported due to its high quality, unique taste, aroma and production (Memon 2016, Musharraf et al. 2016, Ayyaz et al.
2019). However, many biotic and abiotic factors limit the normal
functioning and growth of mango plants and affect their final yield (Ahmad et al. 2019). Among the biotic
constraints, weeds, diseases and insect pest are of prime importance (Affandi et al. 2017, Shahbaz et al. 2017, Malik et
al. 2018).
In order to keep the crop output at a demanding level, the use of pesticides have
become an integral part of modern farming intensive agricultural production systems
(Masud & Akhtar 1997). In Pakistan,
the Punjab province receives the highest percentage of pesticide applications (88.3
%) (Hayat et al. 2019), of which 11.9 % are
being applied solely on fruits and vegetables, resulting in the accumulation of
pesticide residues at concentrations above their maximum residual limits (Mehmood et al. 2021).
The problem of pesticide residues in different food items have become a global
concern for human health. The scenario is even worse in the case of fruits that
receive little or no postharvest treatment before use (Phan et al. 2018, Albaseer
2019). Agrochemicals, especially pesticides, can pose serious health
hazards to humans, including certain skin diseases, paralysis, Parkinson’s disease,
blindness and even cancer (Margni et al.
2002, Kim et al. 2019). The outcomes
of pesticide applications become even more catastrophic due to lack of education and
awareness among farming communities, regarding their judicious and precise use
(Koch et al. 2017).
The mitigation of pesticide residues from agroecosystems requires time, which may be
achieved by the implementation of integrated pest management approaches in field
crops, whose goal is to successfully manage insect pests while minimizing the use of
pesticides by using a combination of biological, cultural and non-chemical control
strategies. The integrated pest management models are sustainable because they
promote the cautious use of pesticides and encourage farmers to consider alternative
methods for pest control. By adopting integrated pest management strategies, farmers
could easily mitigate the application frequency of pesticides, thus minimizing the
potential risks to the environment and human health. Thus, the present study aimed
to evaluate the effectiveness of integrated pest management control measures
employed as a pesticide residue mitigation module against pesticide residues in
mango fruits.
MATERIAL AND METHODS
Samples of mango fruit were collected from five small commercial orchards located in
the Multan region, Pakistan, during the 2019-2020 and 2020-2021 growing seasons.
They were subjected to residual analysis for calculating the concentrations of
pesticides and comparing their values with the standard maximum residue limits of
the Codex Alimentarius Commission (FAO 2023)
or the European Union (EUC 2023).
A total of 150 samples of mango fruit were collected from five orchards, out of which
four pesticide residue mitigation modules (PRMM) were integrated pest management
based. For PRMM-I, a combination of cultural, mechanical and attraction and killing
techniques was used to manage insect pests. Plastic sheets (LDPE) were wrapped
around the trunk with plant debris, as a source to collect egg-carrying females. As
a cultural control practice, fallen fruits were collected on a daily basis to
minimize further infestation. Plastic sheets wrapped around the tree trunk were
greased at every 15 days to disrupt the upward movement of the female mealybugs, as
a mechanical control. Furthermore, repeated applications of GF-120 solution (0.5 L
ha-1 in 4.5 L of water) and methyl eugenol + Tracer® 240SC (Spinosad)
were used as attraction and killing traps with no insecticide applications.
Similarly, PRMM-II included all practices mentioned for PRMM-I along with foliar
application of Tracer® 240SC (Spinosad), at the rate of 10 mL ha-1 in 100
L of water. The PRMM-III module included applications of methyl eugenol + Tracer®
240SC (Spinosad) with 6 traps ha-1. The used concentration of chemicals
included 6-8 drops of M.E and 3-4 drops of Tracer® 240SC (Spinosad) sprayed on
cotton pluck and placed in each trap. Each attraction and killing trap was refreshed
after 12-15 days. Confidor® 20 % SL (Imidacloprid) at 200 mL ha-1 in 100
L of water, Jatar® 10 % EC (Bifenthrin) at 20 mL ha-1 in 100 L of water,
and Mospilan® 20 SP (Acetameprid) at 150 gm ha-1 in 100 L of water were
used as chemical treatments. No cultural or mechanical practices were used for pest
suppression for PRMM-III. For PRMM-IV, repeated applications of Confidor® 20 % SL
(Imidacloprid) at 200 mL ha-1 and Jatar® 10 % EC (Bifenthrin) at 20 mL
ha-1 were used in 100 L of water, followed by Diptrex® 80 % WP
(Trichlorofon) at 250 g ha-1 + 100 L of water and Mospilan® 20 SP
(acetamiprid) at 150 gm ha-1 + 100 L of water as chemical control
measures. No other control tactic was used for PRMM-IV and the orchard was given the
name of conventional pest control method. All the PRMM were devised to mitigate the
pest population on mango trees and compared with a control module where no measures
were applied for pest control. All other agronomic practices, such as irrigation and
fertilizers, were applied in the same way as in the other PRMM.
The fruits were randomly collected at the end of both seasons (2019-2020 and
2020-2021). The procedures for collecting and transporting the samples followed the
standards established by the Commission Directive 2002/63/EC (Wang et al. 2018). Each sample weighed 3 kg, and consisted of 3
sub-samples of 1 kg each, collected in polyethene zippers and placed in refrigerated
containers for transportation. All the samples were homogenized in the laboratory
and stored at -80 ºC for latter analysis.
The high-performance liquid chromatography (HPLC) technique was used to grade the
amount of anhydrous magnesium sulphate (MgSO4), acetonitrile (MeCN),
primary secondary amines and anhydrous sodium acetate (NaAc), and the insecticide
reference standards were purchased from SIGMA-ALDRICH Pvt. Ltd (Qin et al. 2015). Lambda-cyhalothrin,
cypermethrin, indoxacarb, imidacloprid, pyriproxyfen, acetamiprid, buprofezine and
chlorpyrifos were used as insecticide reference standards. Each individual stock
solution was prepared at a concentration of 2,000 mg L-1 in acetonitrile
and then frozen at -18 ºC. On the day of the analysis, acetonitrile dilutions were
made to the calibration and working standards. For dispersive solid-phase extraction
(dSPE), Agilent Technologies (USA) supplied the necessary QuEChERS kits (Part nº.
5982-5755 + 5982-5058) containing 6 g of magnesium sulphate, 1.5 g of sodium acetate
and 15 mL centrifuge tubes containing 1,200 mg of magnesium sulphate and 400 mg of
primary-secondary amine.
The collected fruit samples belonging to the PRMM modules were thoroughly checked for
quantification of pesticide residues. In each PRMM, multiple tactics were used for
suppressing the pest population. These PRMM were compared for pesticide residue
concentration. The percentage of contaminated samples, or exceeding maximum residual
limits, was noted.
The fruit samples (1 kg) were homogenized by mixing 1 g of fruit with 4 mL of
acetonitrile using Precelly’s 24® (Model P002391-P24T0-A.0, Bertin France) at 6,500
rpm for 20 sec, followed by 90 sec of downtime cooling. Following three such cycles,
6 mL of acetonitrile (ACN) were added to the samples in a 15 mL vial/tube (Evard et al. 2015, Polyiem et al. 2018).
The QuEChERS (AOAC) method developed by Agilent Technologies was chosen for
extraction and cleanup because of its selectivity, sensitivity and flexibility
(Zhao et al. 2009, Malhat 2017). The homogenized sample was added to a 15 mL vial
with 100 µL of respective internal standard, followed by 1.05 g of sodium acetate
(NaOAc) and 6 g of magnesium sulphate. The mixture was then vortexed or shaken by
hand for 1 min to ensure that all the solid and liquid components were thoroughly
mixed. About 1.05 mL of supernatant from the centrifuged sample (at 4,695 g, for 5
min) was placed in a vial for dispersive SPE with 2 mL of primary and secondary
amides and MgSO4. The mixture was shaken by hand and then centrifuged at
10,285 g for 5 min. A supernatant after shaking without any solid particles was
poured into a lid vial and placed in a centrifuge overnight. The overnight dried
sample was added with 100 µL of acetonitrile for re-suspension by the vortex. The
samples were centrifuged for 1 min to separate any possible solid particles and were
transferred to liquid chromatography vials (LC) for analysis (Anastassiades et al. 2003, Adam
et al. 2018, Faraji et al.
2018).
A gas chromatograph (model 8890) and a mass spectrometer (model 5977B) by Agilent
Technologies® were used with the following parameters: the injector temperature was
220 ºC, the injection volume was 1 µL split less, the column used was 25 methyl
silicon, I.D. 0.53 mm at a temperature of 250 ºC, 2.0 µm of film thickness, the G.C
detector was a mass spectrometry detector at 300 ºC, N2 (30-32 mL mL-1)
used as carrier gas (Wang et al. 2018), the
oven temperature was 60 ºC for 0.5 min, the flow rate was 17 mL min-1 and
the injection method was the solvent flush technique (auto-sample injection).
Recoveries and linearity of the samples were calculated from calibration curves,
while detection and quantification limits were calculated by determining the minimum
values using the signal-to-noise ratio method (Darko
& Akoto 2008, Jovanov et al.
2013).
The method was validated by testing its linearity, recovery, accuracy and specificity
of peak regions. Both the detection and quantification limits were measured
experimentally from fortified samples, with the signal equal to 3 and 10 times the
noise ratio, respectively (EUC 2019). The
matrix-matched calibration standards in the acetonitrile extracts of mango were
prepared using multi-residue working solutions and blank sample extracts. The effect
of the matrix was evaluated by comparing the slopes of calibration curves based on
an eight-point matrix match to those based on mangoes. A coefficient of
determination greater than 0.990 indicating a good linearity was attained across the
board. Relative standard deviation values were below 20 % across the board, when
testing various concentrations. Analytical performance metrics, including detection
and quantification limits, linearity, matrix effect, selectivity, precision and
recovery, were examined to guarantee that the suggested method was appropriately
optimized for practical use in routine analysis.
RESULTS AND DISCUSSION
The results showed that the quantified pesticide residue levels ranged 91-99 % at
0.01 mg kg-1 and 91-98 % at 0.05 mg kg-1 for the fortification
level in 2019-2020 (Table 1), as well as
85-95 % at 0.01 mg kg-1 and 92-98 % at 0.05 mg kg-1 in
2020-2021, showing the reproducibility of the procedure (Table 2). Similar results were reported by Arora et al. (2006), who monitored pesticide residues in mango
and observed that, out of five samples, four were found contaminated with pesticides
like cypermethrin, dichlorvos, malathion, monochrotophos and hexaconazole.
Table 1
Concentration of pesticide residues quantified in mango samples collected
from pesticide residue mitigation modules (PRMM) in the 2019-2020 season
(maximum-minimum).
LOD: limit of detection; LOQ: limit of quantification: RSD: relative
standard deviation; ND: not detected.
Table 2
Concentration of pesticide residues quantified in mango samples collected
from pesticide residue mitigation modules (PRMM) in the 2020-2021 season
(maximum-minimum).
LOD: limit of detection; LOQ: limit of quantification: RSD: relative
standard deviation; ND: not detected.
The operating conditions of gas chromatography were sensitive to the analytes
indicated by the limit of detection (0.001-0.0014 mg kg-1), while the
number of replicates was 5. The relative standard deviation was less than 20 % in
the result of the repeatability of the study for all the fruits and pesticides in
both seasons. The mass to charge ratio (m/z) for different pesticides was
lambda-cyhalothrin (181, 197, 208), cypermethrin (181, 209), indoxacarb (297),
imidacloprid (256), pyriproxyfen (136, 226), buprofezin (116), acetamiprid (223) and
chlorpyriphos (97, 314). Recoveries ranged from 91.48 to 99.02 %, with relative
standard deviation of 1.03-3.97 %, in 2019-2020 (Figures 1 and 2), while it ranged
88.37-99.18 %, with relative standard deviation of 1.17-3.58 %, in 2020-2021.
Recoveries also ranged 88.37-99.02 %, with relative standard deviation of 1.07-3.97
%, for all samples in both seasons, what is directly aligned with the results of a
previous study by Rodrigues et al. (2007).
However, these findings contradicted the results of Masud & Akhtar (1997), who tested food and water samples from Gadoon
Amazai and found no traces of pesticides. The difference can be attributed to the
fact that pesticides in that region were being applied properly and judiciously.
Figure 1
Comparison of pesticides residue mitigation modules (PRMM)
contamination in the 2019-2020 and 2020-2021 seasons. Cont.:
contaminated samples; > MRL: samples with pesticide residues above
the maximum residue limit.
Figure 2
Total ion chromatogram obtained from a GC-MS of blank sample
(standards) with maximum residue limit, in mg kg-1. a:
imidacloprid (0.2); b: acetameprid (0.01); c: pyriproxifin (0.5); d:
buprofezine (0.09); e: chlorpyrifos (0.05); f: cypermethrin (0.7); g:
indoxacarb (0.02); h: lambda-cyhalothrin (0.2).
In 2019-2020, the pesticide residues were detected in the range of 0.0021-0.1350 mg
kg-1 for PRMM-I, 0.0017-0.2514 mg kg-1 for PRMM-II,
0.0019-0.1524 mg kg-1 for PRMM-III and 0.0025-0.3651 mg kg-1
for PRMM-IV, in comparison to the control (0.0075-0.0203 mg kg-1) (Table 1). In 2019-2020, they ranged
0.0036-0.3251 mg kg-1 for PRMM-I, 0.0018-0.6512 mg kg-1 for
PRMM-II, 0.0032-0.1562 mg kg-1 for PRMM-III and 0.0019-0.2540 mg
kg-1 for PRMM-IV, while the control module expressed a relatively
shorter concentration range (0.0015-0.0132 mg kg-1) (Table 2). These results are also in line with
the findings of Kumari et al. (2002), who
monitored 60 samples of market vegetables and reported that the tested samples
showed 100 % of contamination with low, but measurable, amounts of residues.
Among the four chemical groups, the organophosphates were dominant and about 23 % of
the samples showed contamination above their respective maximum residue limit
values. The findings of Bhattacherjee (2013)
were also in harmony with our findings. The researchers sprayed imidacloprid on
mango at a dose rate of 0.3 mL L-1 of water during the pre-blooming stage
to control hoppers and reported residues of imidacloprid in the peel (1.21 mg
kg-1), pulp (0.56 mg kg-1) and fruit (1.77 mg
kg-1), even after 30 days of spraying.
A comparison of the percentages of the samples contaminated and exceeding maximum
residual limits revealed that no significant difference was recorded between the
2019-2020 and 2020-2021 seasons, while a significant difference was recorded among
different PRMM, in comparison to each other and the control. Samples collected from
all the PRMM in 2019-2020 were analyzed for pesticide residues and revealed that 25
% of the samples from PRMM-I were contaminated, among which 8.33 % were above the
maximum residue limits, while 16.66 % of the samples from PRMM-II were contaminated,
for a total of 33.33 %. Similarly, 66.66 % were contaminated for PRMM-III, among
which 33.33 % were above the maximum residue limits, and PRMM-IV showed a maximum
(75 %) contamination level with a 41.66 % violation rate, while the control module
showed 8.33 % for sample contamination, with no sample exceeding the maximum residue
limits (Figure 1).
Samples collected in the 2019-2020 season depicted almost similar results, with 27.08
% of contamination, among which 9.37 % were above the maximum residue limits for
PRMM-I, while 18.75 % of the samples violated the maximum residue limits, among 37.5
% of contaminated samples. Similarly, 63.54 and 31.25 % of the samples were found
contaminated and above the maximum residue limits, respectively, for PRMM-III, while
38.54 % of the samples exceeded the maximum residue limits, from a total of 77.08 %
contaminated for PRMM-IV. In comparison to these PRMM, only 10.41 % of the samples
were found with residues, with no samples violating the maximum limit in the control
module (Figure 1). The current results were
further verified by surveys conducted in Pakistan, which reported that fruit and
vegetable samples present at the Karachi farmers’ market were found contaminated
with traces of organochlorine, organophosphate and pyrethroid insecticides (Hussain et al. 2002, Masud & Hasan 2002). Similarly, Hussain et al. (2002) also supported our results, as they
screened residues of commonly used pesticides, viz. cypermethrin, methamidophos,
monochrotophos, cyfluthrin, dieldrin and methyl parathion, in mango fruit samples
collected from the grower fields in the Multan division. They reported that all the
samples were contaminated with a degree of variation regarding pesticides
residues.
Higher levels of organochlorine and organophosphate pesticide residues can be
attributed to the fact that several organochlorine and organophosphate insecticides
have been classified as persistent organic pollutants, owing to their bulk
(intensive) properties, including persistence and biomagnification (Fremlin et al. 2020). So, even a little use of
these pesticides can result in higher levels of residues after a prolonged time
(Giesy et al. 2014). Contrarily,
neonicotinoids and pyrethroids are mostly favored by commercial growers for sucking
insect-pest management in mango crops (Karar et al.
2021, Zahid et al. 2022).
The base for the lambda-cyhalothrin ion peaked at m/z 181, followed by m/z197 and m/z
208, for cypermethrin, indoxacarb, imidacloprid, pyriproxyfen, buprofezin,
acetamiprid and chlorpyriphos.
Lambda-cyhalothrin was detected in 43.75 % of the samples, among which 23.33 % were
above the maximum residue limits, while 45 % were detected with cypermethrin, with a
24.16 % violation rate. Indoxacarb occurred in 31.25 % of the samples, with 5.41 %
of them exceeding the maximum residue limits. Similarly, 44.16 % of the samples were
found with imidacloprid, while 25 % violated the maximum limit. Pyriproxyfen
occurred in 33.33 % of the samples, with an 8.33 % violation rate among the
contaminated ones, while 43.75 % of the samples owned acetamiprid, with 22.91 % of
them above the maximum residue limits. Similarly, 37.08 % of the samples showed
contamination of buprofezin, with a 4.16 % violation of the safe limit, while
chlorpyriphos was determined in 44.58 % of the samples, with 22.92 % of them above
the maximum residue limits.
The linearity of the samples was calculated on the basis of two fortification levels
to calculate the correlation coefficient (R2), and the regression
equation was generated (Table 3). The limit
of detection for all the pesticides was less than the minimum concentration that was
quantified in the samples, while the standard deviation was calculated as less than
20 % (Tables 1 and 2). Similar results were reported by Sinha et al. (2012), where the limit of detection ranged
0.0006-0.091, while the relative standard deviation was less than 10 %, with less
than 10 % for R2. Differences were attributed to the equipment used,
which was an LC-MSMS in the latter case, while the method accuracy was above 99 % in
both studies.
Table 3
Linearity of pesticides in mango samples collected from modules in the
2019-2020 and 2021 crop seasons.
R2: correlation coefficient.
Overall, the pest population reduction efficiency of the modules was compared,
resulting in the PRMM-II reducing the pest population up to 90.79 %, followed by
PRMM-I, with 83.61 %. Similarly, PRMM-III reduced the pest population up to 75.78 %,
while 72.18 % was reduced by PRMM-IV, as already reported by Bana et al. (2015). In their study, Bana et al. (2015) formulated five modules to mitigate the
population of mango hopper in mango orchards. The module-V in their study considered
integrated pest management based on insecticides and botanicals application.
Although the maximum mango production was recorded from the tested integrated pest
management module, they did not detect pesticide residues from mango samples. After
the mango seasons of 2019-2020 and 2020-2021 were completed, the average yield of 5
modules showed a considerable difference. The fruit production loss was measured
both qualitatively and quantitatively, because not all the pests cause a quantity
loss, such as meallybug and mango hopper, but fruit fly does it. PRMM-II gave a
maximum yield of 47,211.954 kg ha-1, from which 85.24 % were marketable,
followed by PRMM-I, with 45,321.59 kg ha-1 and 81.12 % of marketable
yield. PRMM-III produced 42,699.81 kg ha-1, with 77.96 % of marketable
fruits, followed by PRMM-IV, with 41,323.43 kg ha-1 and 71.42 % of
marketable yield, and all these modules were compared with a control module, where
the yield was calculated as much as 35,941.47 kg ha-1, while only 59.95 %
were marketable yield. PRMM-II produced 25.29 % more marketable fruits, in
comparison to the control module, while PRMM-I produced 21.17 % more marketable
fruits over the control. In the case of PRMM-III and PRMM-IV, the surplus marketable
fruits over the control was calculated as 17.21 and 11.47 %, respectively. Similar
differences were reported by Karar et al.
(2020), in a study where they evaluated three modules and checked the
efficacy of insecticides on mango production. The highest production and minimum
pest population were observed in module-III, where the maximum number of pesticides
was applied, but unlike in the current study, since the focus of their study was a
higher production and minimum pest population, and pesticide residues were not
determined in their study. However, in their experiment, Farooq et al. (2019) reported that the integrated pest
management module with minimum use of insecticides was more effective, in terms of
pest population reduction and reduced pesticide residues.
A better cropping and legislative approach to minimize the injudicious use of
pesticides is required, and more efficient eco-friendly approaches should be joined
in integrated pest management modules to manage insect pests, especially in the case
of fruit crops.
CONCLUSIONS
After exposed to pesticide residue mitigation modules (PRMM), minimum pesticide
residues of 16.67 % were observed in the mango samples for PRMM-I, followed by 53.13
% for PRMM-II, 66.67 % for PRMM-III and 67.00 % for PRMM-IV, while the maximum
production was recorded for PRMM-II, followed by PRMM-I, PRMM-III and PRMM-IV.
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