Research Article

Entomopathogenic Fungi: As an Eco-Friendly Approach for the Management of Thrips Megalurothrips distalis Karny (Thysanpotera: Thripidae) and their Impact on the Yield in Mungbean (Vigna radiata (L.) Wilczek)

Muhammad Nadeem1, Jamshaid Iqbal2, Tariq Mustafa3, Gul Rehman2, Muhammad Faisal Shahzad2, Muhammad Younas4,5*, Aftab Ahmad Khan6, Ameer Hamza2, Abdul Ghaffar1 and Muneer Abbas1

1Arid Zone Research Institute, Bhakkar, Pakistan; 2Faculty of Agriculture, Gomal University, Dera Ismail Khan, Pakistan; 3University of Agriculture Faisalabad Sub Campus Depalpur Okara; 4Agricultural Research Station Bahawalpur 63100, Punjab, Pakistan; 5College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China; 6Fodder Research Institute, Sargodha, Pakistan.

Received | May 12, 2023; Accepted | August 22, 2023; Published | September 29, 2023

*Correspondence | Muhammad Younas, Agricultural Research Station Bahawalpur 63100, Punjab, Pakistan; Email: nadeemazri@gmail.com

Citation | Nadeem, M., J. Iqbal, T. Mustafa, G. Rehman, M.F. Shahzad, M. Younas, Aftab A.K., A. Hamza, A. Ghaffar and M. Abbas. 2023. Entomopathogenic fungi: As an eco-friendly approach for the management of thrips Megalurothrips distalis Karny (Thysanpotera: Thripidae) and their impact on the yield in Mungbean (Vigna radiata (L.) Wilczek). Sarhad Journal of Agriculture, 39(3): 757-764.

DOI | https://dx.doi.org/10.17582/journal.sja/2023/39.3.757.764

Keywords | Mung bean, Megalurothrips distalis, Entomopathogenic fungi, Efficacy, Yield, B. bassiana

Copyright: 2023 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

The Mung bean, Vigna radiata (L.) Wilczek, is an important pulse crop cultivated in Pakistan (Mansoor et al., 2017; Rani et al., 2018). It is broadly distributed all over the world throughout the tropical as well as subtropical regions with the primary growing regions in South and Southeast Asia (Pratap et al., 2021; Chadha, 2010; Bairwa and Singh, 2017). Because of the mung bean short life cycle, it can be adapted easily into different cropping systems. It is usually cultivated and used by the farmers because of its maximum protein contents (Tang et al., 2014; Ratnasekera and Subhashi, 2015; Hou et al., 2019; Pratap et al., 2021).

Mung bean crop is susceptible to numerous insect pests including mung bean thrips, Megalurothrips distalis Karny (Thysanoptera: Thripidae) (Sani and Umar, 2017; Rani et al., 2018; Gehlot and Prajapat, 2021; Sequeros et al., 2021). Damage from this insect pest includes a drop in flowers, distorted pods, inferior quality grains, and low yield (Kooner et al., 1983; Rani et al., 2018; Gehlot and Prajapat, 2021; Sequeros et al., 2021). Thrips is considered a sucking feeder, extensively utilizing proteins, carbohydrates, lipids, vitamins, water and inorganic salts from the host, and it affects badly to the nutritional value and resistance trait of the host (Haile and Higley, 2003; Bayu and Prayogo, 2018; Gehlot and Prajapat, 2021).

In addition to killing off the beneficial insects that would otherwise keep the mung bean flower thrips population in check, the use of chemical insecticides for thrips management also raises concerns about phytotoxicity and goes against the “3Rs” (resistance, resurgence and residue) (Siegwart et al., 2015). In recent years, entomopathogens have increasingly gained a high importance for managing numerous insect pests (Arthus et al., 2013; Shiberu et al., 2013; Ain et al., 2021; Gulzar et al., 2021). Biological control and the use of EPFs in particular, have received a lot of interest as a promising method of management (Camara et al., 2022). Microbial pesticides, including entomopathogenic; fungi, viruses, and bacteria have been proven to play a significant role in sustainable crop production (Ekesi et al., 2000; Niassy et al., 2012; Arthus et al., 2013; Shiberu et al., 2013; Ain et al., 2021; Gulzar et al., 2021). These microbial controls could provide a long lasting pest management and generally safer for the environment and non-target organisms than the chemical control (Khetan, 2000). Using virulent isolates of entomopathogenic fungi as part of biointensive integrated pest control could be a good way to get rid of thrips (Savariya and Jethva, 2023). The world’s interest in the use of entomopathogenic fungi (EPFs), as biological control in different pest management programs, has been rising in recent years (Yang et al., 2020).

EPFs as management tools for pests of mung bean have not been studied extensively. Present investigations were carried out to determine the impact of different EPFs against mung bean flower thrips under field conditions and to evaluate the efficacy of EPFs on mungbean yield parameters (flower shedding, total number of pods, total number of flowers and damaged pods and finally on yield) with suitable concentrations.

Materials and Methods

Plant source

The mung bean variety NM-2011 was cultivated. The experimental plot size was (5 × 2.4 m2). Mung bean was cultivated, using a hand drill method, at a recommended seed rate of 8-10 kg per acre. All treatments were completely randomized and replicated thrice. All cultural practices, including hoeing and removal of weeds were performed in all treatments manually.

Entomopathogenic fungi

Four different EPFs including Isaria fumosorosea, (Paecilomite®), Verticillium lecanii (Zimm) (Mealikil-®), Beauveria bassiana (Bals) (Racer®) and Metarhizium anisopliae (Pacer®) were obtained from ALM (Agri life Meda Hyderabad), Andhra Pradesh, India. The virulence of above cited EPFs Verticillium lecanii (Zimm) (Mealikil-VL) (1.3 x 109 CFU/g), Metarhizium anisopliae (Pacer-MA) (1.2 x 109 CFU/g), Beauveria bassiana (Bals) (Racer-BB) (1.4 x 109 CFU/g), and Isaria fumosorosea (Wise) (1x 109 CFu/g), was assessed at 2.5, 5.0, and 7.5 % concentration levels, in field trials.

Field pathogenicity bioassays

The pathogenicity of the different EPFs, at different concentrations, was assessed under field conditions. The EPF’s were applied at the occurrence of thrips in the experimental plots. Different concentrations of the treatments were repeated after a resurgence of thrips populations in the experimental plot, except the control treatments. Before the application of EPF’s treatment, the population of thrips was estimated from five randomly selected plants per treatment. From each plant, three opened flowers were gently shaken over a white cardboard paper. The dislodged thrips feeding inside flowers were recorded, using a magnifying lens. After EPFs’ applications, data were recorded after 3, 7 and 15 days post-treatments. Pathogenicity of different EPF concentrations was evaluated based on the reduction of thrips numbers, flower shedding, and deformed pods per plant by using the following equations (Mumutaj, 2014).

Where; FSC = Flower shedding in the control, FST = Flower shedding in the treatment.

TFT= Total flowers in treatment; TFC= Total flowers in control).

TPT= Total pods in treatment; TPC= Total pods in control).

After harvesting, the plants were sun-dried and threshed manually. Collected seeds were weighed, and the total yield per hectare was estimated manually.

Statistical analysis

All the data were analyzed using Statistix 8.1, USA. The data regarding the differences in the mean population at different time intervals and potential yield were determined, using analysis of variance (ANOVA). The means were compared, using the LSD test at a 5 % level of significance (Gomez and Gomez, 1984).

Results and Discussion

Impact of EPFs on thrips population and percent reduction of thrips population

Pathogenicity of the different EPFs against thrips in the mung bean was assessed at three different concentration levels. The results revealed that on an accumulative basis, all concentrations of EPF’s showed a highly significant differences among the tested treatments (Table 1). Aplication of B. bassiana at 7.5 % concentration exhibited significant results and showed a minimum thrips population (1.76) per flower, and it was statistically different than the other treatments, followed by M. anisopliae along with 2.06 thrips/flower (Table 1).

The percentage reduction of thrips population on an accumulative basis at the three different concentrations levels had also showed significant differences among the treatments (Table 2). Application of B. bassian at the 7.5 % concentration exhibited maximum 59.42 % reduction in thrips population followed by M. anisopliae, V. lecanii, and I. fumosorosea, with 52.64, 43.69, and 38.38 % reductions on comparison to control (Table 2).

 

Table 1: Assessment of entomopathogenic fungi against thrips population.

Treatments

2.5% concentration

Mean

5.0% concentrations

Mean

7.5% concentration

Mean

3 DAS

7 DAS

15 DAS

3 DAS

7 DAS

15 DAS

3 DAS

7 DAS

15 DAS

V. lecanii

3.66 bc

2.48 f

3.11 de

3.09 c

3.51 b

2.22 fg

2.69 de

2.81 c

3.20 b

1.81 gh

2.34 de

2.45 c

M. anisopliae

3.12 de

2.43 f

2.87 e

2.81 d

2.68 de

1.98 gh

2.34 ef

2.33 d

2.49 cd

1.69 gh

1.99 fg

2.06 d

B. bassiana

3.34 cd

2.01 g

2.31 fg

2.56 e

2.92 cd

1.61 i

1.86 hi

2.13 d

2.30 def

1.35 i

1.63 hi

1.76 e

I. fumosoroseus

3.75 b

3.07 de

3.56 bc

3.46 b

3.64 b

2.57 def

3.12 c

3.11 b

3.20 b

2.14 ef

2.69 c

2.68 b

Control

4.46 a

4.15 a

4.38 a

4.33 a

4.46 a

4.15 a

4.38 a

4.33 a

4.46 a

4.15 a

4.38 a

4.33 a

LSD value at 5%

0.35

0.20

0.36

0.21

0.31

0.18

Mean

3.67 a

2.83 c

3.25 b

3.44 a

2.51 c

2.88 b

3.13 a

2.23 c

2.61 b

LSD value at 5%

0.16

0.16

0.14

Means sharing similar letters are not significantly different by LSD test at P = 0.05

 

Table 2: Assessment of entomopathogenic fungi against percent reduction of thrips population.

Treatments	2.5% Concentration			5.0% Concentrations			7.5% Concentration			Mean
	3 DAS	7 DAS	15 DAS	3 DAS	7 DAS	15 DAS	3 DAS	7 DAS	15 DAS
V. lecanii	17.86 g	40.29 cd	28.77 ef	21.43 g	46.51 cd	38.53 e	28.42 f	56.34 c	46.30 d	43.69 c
M. anisopliae	30.09 ef	41.42 bc	34.42 de	39.91 de	52.36 bc	46.38 cd	44.14 de	59.23 bc	54.55 c	52.64 b
B. bassiana	25.13 f	51.60 a	47.27 ab	34.46 ef	61.22 a	57.67 ab	48.15 d	67.28 a	62.82 ab	59.42 a
I. fumosoroseus	15.97 g	25.97 f	18.58 g	18.59 g	38.20 e	28.64 f	28.26 f	48.29 d	38.60 e	38.38 d
Control	0.00 h	0.00 h	0.00 h	0.00 h	0.00 h	0.00 h	0.00 g	0.00 g	0.00g	0.00 e
LSD Value at 5%	5.99			6.85			6.06			3.5

Means sharing similar letters are not significantly different by LSD Test at P = 0.05

 

Table 3: Assessment of different entompathogenic fungi at different concentrations against flowers and pods formation of mungbean.

Treatments	% increase of flowers over control	Flower shedding per plant	% Flower shedding	% Reduction of flower shedding over control	% Increase of pods number over control	Deformed Pods per plant
V. lecanii (zimm) (Mealikil-VL) 2.5%	7.59 (136.53) efg	101.47 abc	74.50 bc	6.16 cde	15.50 (38.13) fg	9.27 b
V. lecanii (zimm) (Mealikil-VL) 5.0%	15.79 (146.93) cde	100.60 bc	68.62 de	6.96 cd	22.93 (40.67) def	6.40 cd
V. lecanii (zimm) (Mealikil-VL) 7.5%	27.32 (161.53) b	95.20 c	58.88 f	11.95 c	35.69 (44.87) cd	5.93 cdef
M. anisopliae (Pacer-MA) 2.5%	16.99 (148.40) cd	82.60 d	55.66 f	23.61 b	29.58 (42.80) cde	5.27 efg
M. anisopliae (Pacer-MA) 5.0%	28.58 (163.13) b	77.47 d	47.49 gh	28.36 b	37.36 (45.33) c	5.00 fg
M. anisopliae (Pacer-MA) 7.5%	42.48 (180.80) a	77.07 d	42.63 h	28.73 b	55.23 (51.27) b	4.93 fg
B. bassiana (Bals) (Racer-BB)2.5%	22.06 (154.87) bc	76.40 d	49.38 g	29.34 b	30.82 (43.20) cde	5.33 defg
B. bassiana (Bals) (Racer-BB) 5.0%	37.97 (175.07) a	75.93 de	43.34 h	29.79 ab	50.78 (49.80) b	5.00 fg
B. bassiana (Bals) (Racer-BB)7.5%	46.14 (185.40) a	68.87 e	37.14 i	36.31 a	69.33 (56.00) a	4.27 g
I. fumosoroseus 2.5%	6.50 (135.13) fg	105.13 ab	77.85 b	2.78 de	9.05 (36.07) gh	9.87 b
I. fumosoroseus 5.0%	13.13 (143.47) def	101.33 abc	70.61 cd	6.28 cde	19.75 (39.53) efg	6.67 c
I. fumosoroseus 7.5%	22.85 (155.87) bc	100.93 abc	64.90 e	6.66 cde	32.46 (43.73) cde	6.13 cde
Control	126.87 g	108.13 a	85.24 a	-	(33.07) h	10.53 a
LSD (0.05)	10.52	7.48	4.98	6.93	4.27	1.1
CV (%)	4.07	4.93	4.95	24.63	5.83	10.07

Values in parenthesis represent mean No. of total flowers and total pods per plant in their respective columns. Means sharing similar letters are not significantly different by LSD Test at P = 0.05

 

Impact of entompathogenic fungi on flowers and pods formation of mungbean

Results revealed that application of B. bassiana at maximum concentration 7.5% expressed significant results and increased 46.14% flowers followed by M. anisopliae (42.48) and V. lecanii (27.32), respectively. Similarly, application of B. bassiana at 7.5% concentration exhibited minimum flower shedding 68.87 per plant followed by M. anisopliae (77.07) and V. lecanii (95.20) respectively. Moreover, in case of % flower shedding and % reduction of flower shedding application of B. bassiana at 7.5% concentration showed minimum 37.14% flower shedding and 36.31% reduction in flower shedding followed by the M. anisopliae and V. lecanii, respectively at the same concentration (Table 3).

Impact of entomopathogenic fungi on % increase of pods number and deformed pods per plant in Mungbean

The results in response to different EPFs concentrations application against total pods and deformed pods formation significantly affected deformed pods and the total numbers of pods formation/plant (Table 3). Application of B. bassiana at the concentrations of 7.5 % produced the maximum 56.0 pods/plant than the control (Table 3). Similarly, M. anisopliae with 7.5 % and B. bassiana at 5.0 % showed a significant increase in pods formation, which was 51.27 and 49.80 pods per plant than the control, respectively (Table 3). The lowest number of 36.07 pods per plant was observed in I. fumosorosea at 2.5 % concentration on comparison to control (Table 3).

Impact of entomopathogenic fungi on seed yield of mungbean

All EPFs at different concentrations exhibited significantly higher yields than the control (Figure 1). The plot treated with B. bassiana 7.5 % produced the highest yield potential of 1018.9 kg/ha, followed by M. anisopliae (7.5%) and B. bassiana (5.0 %), with 941.1 kg ha-1 and 841.1 kg/ha-1 yields, respectively. The minimum yield of 551.7kg ha-1 was obtained in untreated plants.

 

The EPFs had a significant role against thrips in mung bean (Shiberu et al., 2013; Ain et al., 2021; Gulzar et al., 2021). The application of EPFs, has gained a lot of attention as a viable way of thrips management (Camara et al., 2022). Results of the present study are in accordance with the outcomes of other studies (Ekesi et al., 2000; Niassy et al., 2012; Arthus et al., 2013; Shiberu et al., 2013; Ain et al., 2021; Gulzar et al., 2021) who reported that different entomopathogenic fungi are used to control thrips. The findings of the contemporary study expressed that EPF treated plots are more superior to non-treated plots for the reduction of thrips population (Ekesi et al., 2000; Arthus et al., 2013; Shiberu et al., 2013; Mfuti et al., 2016; Hemalatha et al., 2017; Singh et al., 2018; Ain et al., 2021; Gulzar et al., 2021). Comparable results were obtained by (Singh et al., 2013, 2018; Ain et al., 2021; Gulzar et al., 2021), who reported that bio-pesticides were helpful in reducing thrips populations. Savariya and Jethva (2023) also reported that entomopathogenic fungi could be used as an effective method of thrips control.

The results of the present study showed that on a cumulative basis, application of B. bassiana (7.5%) had an effective capacity of killing 48.15 and 67.28%, after a 3rd and 7th day of applications. After 15 days of application, the efficacy decreased to 62.82% on comparison to the control, which mostly differed significantly than other treatments. Present results are in line with Vestergaard et al. (1995) who described that B. bassiana efficacy was 46.18, 54.31, and 60.67%, on the third, fifth and seventh day, respectively. Weekly application of the EPFs could provide a significant control against mung bean thrips in mung bean crops. Similar results were reported by Singh et al. (2018) and Maniania et al. (2003a, b). The present findings are comparable with Gill et al. (1998) who reported that Botanigard, a commercial formulation of B. bassiana, on weekly intervals expressed the full control of western flower thrips (Frankliniella occidentalis). Similarly, Singh et al. (2018) also showed that the B. bassiana showed a significant decline in thrips population in mung bean. Findings revealed that B. bassiana was superior against thrips inhibition than other tested EPFs likewise V. lecanii, which is in agreement with (Singh et al., 2013, 2018; Hemalatha et al., 2017; Ain et al., 2021; Gulzar et al., 2021), who described that B. bassiana showed significant results in inhibiting thrips populations.

Present findings showed that the highest yield potential 1018.9 kg/ha was reported by B. bassiana (7.5%), followed by the application of M. anisopliae (7.5%) and B. bassiana (5.0%) treated plots, with 941.1 and 841.1 kg ha-1 seed yield, respectively. These findings are in line the results of Bayu and Prayogo (2018), Singh et al. (2013, 2018), who reported that the application of B. bassiana can inhibit pest population in mung bean and results in higher seed weight (659.7g/plot). These results are also in partial conformity with the findings of Maniania et al. (2003a). Application of B. bassiana at the concentration of 7.5 % significantly controlled thrips in mung bean and significantly increased flowers (46.14 %) and pods (69.334 %) over the control. Moreover, B. bassiana application at the rate of 7.5 % plays a pivotal role in controlling flower shedding and deformed pods and it significantly influences the crop yield potential.

Conclusions and Recommendations

Present study revealed that applications of B. bassiana could significantly reduce thrips population and their damage in mung bean. Application of B. bassiana influenced the potential yield than the other tested EPFs. Application of B. bassiana can result in a significant yield increase of mung bean through a reduction in thrips and is recommended as a biological control in an IPM component on mung bean. However, further research work is required to understand the efficacy of B. bassiana in combination with botanical extracts and other biological agents (EPFs) for thrips control in an environmentally safe manner.

Acknowledgement

Sincere thanks to Hhigher Education Commission, Pakistan for providing financial grant, and Arid Zone Research Institute for providing research facilities.

Novelty Statement

Entomopathogenic fungi (EPF) are currently used as biocontrol agents and are alternatives of synthetic insecticides in sustainable agriculture. Beauveria bassiana is ecofriendly approach which could significantly reduce the Megalurothrips distalis population in mungbean. Moreover, B. bassiana can provide highest number of flowers and pods which ultimately increases the yield of mungbean.

Author’s Contribution

Muhammad Nadeem: Conducted research trial collected data.

Jamshaid Iqbal: Project administration.

Tariq Mustafa and Gul Rehman: Project administration.

Muhammad Faisal: Conceived the idea.

Muhammad Younas: Corrected the paper.

Aftab Ahmad Khan: Review of literature.

Ameer Hamza: Helped in data collection.

Abdul Ghaffar: Analyzed the data.

Munir Abbas: Compiled the data.

List of abbreviations

EPF: entomopathogenic fungi; DAS: days after spray

Conflict of interest

The authors have declared no conflict of interest.

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