Research Article

Insecticidal Potential of Indigenous Flora of Soon Valley against Asian Citrus Psyllid Diaphorina citri Kuwayama and Cotton Aphid Aphis gossypii Glover

Muhammad Bilal Tayyab1, Muhammad Zeeshan Majeed1*, Muhammad Asam Riaz1, Muhammad Anjum Aqueel2, Sylvain Nafiba Ouedraogo3, Muhammad Luqman4, Kanwer Shahzad Ahmed1 and Mujahid Tanvir1

1Department of Entomology, College of Agriculture, University of Sargodha, Sargodha 40100, Pakistan; 2Department of Entomology, The Islamia University of Bahawalpur, Bahawalpur 63100, Pakistan; 3Institut des Sciences de l’ Environnement et du Développement Rural (ISEDR), Université de Dédougou, Burkina Faso; 4Department of Agricultural Extension, College of Agriculture, University of Sargodha, Sargodha 40100, Pakistan.

Received | April 29, 2021; Accepted | July 19, 2021; Published | November 01, 2021

*Correspondence | Muhammad Zeeshan Majeed, Department of Entomology, College of Agriculture, University of Sargodha, Sargodha 40100, Pakistan; Email: [email protected]

Citation | Tayyab, M.B., M.Z. Majeed, M.A. Riaz, M.A. Aqueel, S.N. Ouedraogo, M. Luqman, K.S. Ahmed and M. Tanvir. 2022. Insecticidal potential of indigenous flora of soon valley against asian citrus Psyllid Diaphorina citri kuwayama and cotton aphid Aphis gossypii glover. Sarhad Journal of Agriculture, 38(1): 26-39.

DOI | https://dx.doi.org/10.17582/journal.sja/2022/38.1.26.39

Keywords | Botanical pesticides, Phytoextracts, Phloem-feeding pests, Diaphorina citri, Aphis gossypii, Toxicity evaluation, Local flora

Introduction

Insect pests adversely affect the world food production. Among these, sap-feeding insect pests have been a serious threat to horticultural and agricultural crops all over the world including Pakistan (Gavloski, 2018). Asian citrus psyllid Diaphorina citri Kuwayama (Psyllidae: Hemiptera) and cotton aphid Aphis gossypii Glover (Aphididae: Hemiptera) are destructive sap-sucking pests of citrus and cotton, respectively.

Asian citrus psyllid (ACP) D. citri Kuwayama (Psyllidae: Hemiptera) is a destructive pest of citrus. It is native to Asia (Halbert and Nunez, 2004) and has been most notorious sap-feeding pest of citrus all over the world including Pakistan (Boykin et al., 2012; Mahmood et al., 2014; Augier et al., 2017). Both nymphs and adults of ACP desap young twigs and foliage resulting in the withering of twigs and curling of leaves and flowers and premature fruit drop (Grafton-Cardwell et al., 2013; Ahmad et al., 2014). Furthermore, ACP acts as an important vector in the transmission of bacteria Candidatus liberibacter asiaticus Jagoueix, C. l. africanus Jagoueix and C. l. americanus Texeira that cause Huánglóngbìng (citrus greening) disease (Teixeira et al., 2005; Bove, 2006; Grafton-Cardwell et al., 2013; Hall et al., 2013). Citrus greening causes substantial economic loss to citrus production all over the world and its prevention solely relies on the control of its vector i.e. ACP (Halbert and Manjunath, 2004; Bove, 2006).

Cotton aphid A. gossypii is a polyphagous sap-feeding pest found ubiquitously around the globe (Kocourek et al., 1994). It has a wide host range including plant species from the Malvaceae, Cucurbitacae, Solanaceae and Rutaceae families (Ebert and Cartwright, 1997; Satar et al., 1999). It is one of the most destructive pests of cotton in the world including Pakistan (Xia et al., 1999; Henneberry et al., 2000; Razamjou et al., 2006; Ashfaq et al., 2011; Majeed et al., 2016; Eid et al., 2018; Siddiqui et al., 2021). Both nymph and adults of A. gossypii damage directly by desaping plant foliage and sprouts and indirectly by interrupting normal photosynthetic activity due to sooty mold growth on their honeydew secretions and by transferring various viruses in plants including cotton crop (Ebert and Cartwright 1997; Henneberry et al., 2000).

For the control of both these sap-feeding pests, citrus and cotton growers around the globe rely exclusively on the extensive applications of highly persistent synthetic insecticides including organochlorines, organophosphates, carbamates and pyrethroids (Ahmad and Arif, 2008; Setamou et al., 2010; Yan et al., 2013; Boina and Bloomquist, 2015; Nazir et al., 2017). However, many environmental and health issues are being manifested by this irrational and widespread use of synthetic chemicals such as soil and water contaminations (Kumari et al., 2008; Edwards, 2013; Deng et al., 2020), eradication of non-target fauna including predators and parasitoids (Desneux et al., 2007; Halstead et al., 2015; Haddi et al., 2020), insect pests resistance (Herron et al., 2001; Tiwari et al., 2011; Yan et al., 2013; Naeem et al., 2016) and human health hazards (Kim et al., 2017; Dhananjayan et al., 2020).

This situation demands for searching novel biorational pest management strategies which would be more environment-friendly and safer than synthetic chemical insecticides. For instance, plant-based pesticides appear as promising alternative control measures (Copping and Menn, 2000; Isman, 2020). Many plant essential oils and phytoextracts are well-known regarding their effectiveness against different species of sap-feeding and chewing insect pests including ACP and aphids (Borad et al., 2001; Rossetti et al., 2008; Regnault-Roger et al., 2012; Majeed et al., 2018). Moreover, botanical pesticides usually exhibit low mammalian toxicity and get degraded in the environment rapidly as compared to conventional synthetic insecticides (Turek and Stintzing, 2013).

As local flora of any biogeographical zone may be composed of certain bioactive and toxic constituents against local insect pest species (Isman, 2020), this study was conducted to explore the toxicity potential of local flora (including herbs, shrubs and trees) of Soon valley and surrounding Salt Range (Punjab, Pakistan) against D. citri and A. gossypii. This valley is located in a Salt Range of district Khushab in between latitudes 32°25 and 32°45 N and longitudes 72°00 and 72°30 E and covers an area of about 300 km2. It is usually rich in floral diversity including many valuable medicinal plants (Ahmad et al., 2002; Ahmad et al., 2009).

Material and Methods

The study was conducted to evaluate the biocidal potential of local plants of Soon valley and surrounding Salt Range of the Punjab province of Pakistan against D. citri and A. gossypii. The study was performed in the Department of Entomology, College of Agriculture, University of Sargodha, Pakistan.

Collection sites of plant material

Samples of indigenous flora (including trees, shrubs and herbs) were collected from six selected sites (Angah, Dape Shareef, Kenhatti Garden, Khabeki, Khoora and Uchhali) of Soon valley and surrounding Salt Range of district Khushab (Punjab, Pakistan) during

 

Table 1: Geographical coordinates of selected flora collection sites in Soon Valley and surrounding Salt Range of Pakistan.

Sr. No.	Localities	Latitude N	Longitude E	Elevation (m)
1	Angah	32.35° N	72.05° E	821
2	Dape Sharif	32.30° N	72.04° E	890
3	Kenhatti Garden	32.40° N	72.14° E	783
4	Khabeki	32.35° N	72.12° E	774
5	Khoora	32.23° N	72.11° E	866
6	Uchhali	32.56° N	72.02° E	794

 

the extensive surveys carried out in spring seasons of 2018 and 2019. Geographic information of these selected sites is given in Figure 1 and Table 1. Samples were composed of plant twigs, stems, leaves, roots, fruits, flowers and seeds. These collected plant samples were identified up to species level by the experts from the Department of Botany, University of Sargodha and by the native ethnobotanical experts.

Plant samples preparation

The plant materials collected were washed with tap-water and were dried under shade for approximately two weeks at room temperature (28°C). After that plant material was grinded into fine powder using a commercial electrical mix-blender (TCB-318; 750W). This powdered material was then extracted by means of Soxhlet apparatus.

Soxhlet extraction

As common method of extraction is usually not efficient to yield good amount of phyto-constituents, Soxhlet extractor (DH.WHM-12393, Daihan Scientific, South Korea) was used to extract the powdered plant materials following the following extraction procedure.

Extraction procedure

Fifty gram of each plant sample was filled in the thimble of Soxhlet apparatus. This thimble was made up of a filter-paper sheet and 500 mL acetone

 

(99% pure) was filled in the apparatus flask as the extraction solvent. Extraction was done at 60±5°C and the apparatus was connected with the cool water supply of a condenser. The extraction process was carried out for 5 to 6 h for each sample. In order to evaporate the excessive amount of extraction solvent, the crude extract obtained from the Soxhlet extraction process was transferred to the rotary evaporator (WEV-1001L, Daihan Scientific, South Korea) provided with a chiller and vacuum pump. Pure extract obtained from each plant sample was stored in a 50 mL hermetic dark glass vial and was refrigerated until its downstream utilization in the toxicity bioassays.

Insect culture

Rearing of Insects: Active adults of D. citri and A. gossypii were collected from the citrus (C. reticulata Blanco cv. kinnow mandarin) and cotton (Gossypium hirsutum L.) plants by means of an aspirator and were reared on the potted citrus jasmine (Murraya paniculata (L.) Jack) and cotton plants, respectively. These plants were potted in 500 mL disposable plastic jars, filled with the fine sand and wooden brass (50:50) as potting mixture. Insect populations were reared in laboratory within Plexiglas rearing cages at 60±5% relative humidity, 25±2°C temperature and 16h L: 8h D photoperiod.

Insecticidal bioassays: First bioassay was conducted in order to screen out the most effective botanical extracts from the total collected plant samples for their insecticidal potential. For this screening experiment, we used laboratory reared ACP (C. citri) individuals and performed bioassays using twig-dip method. Later on, based on the results of this preliminary toxicity experiment, we conducted second series of toxicity bioassays with detailed experimental parameters using laboratory reared aphid (A. gossypii) individuals using leaf-dip bioassay method.

Twig-dip method for ACP (D. citri)

Three to four centimeter twig tips of citrus jasmine (M. paniculata) were used in this bioassay. The twigs were immersed for 30 sec in 10% botanical extract solutions. In control, twigs were immersed in pure acetone. After draining them on towel paper, the petioles of these twigs were inserted into 1.5 mL eppendorf tubes filled with 2.0% agar solution to keep them fresh. These tubes with twigs were inserted in 50 mL falcon tubes (Figure 2). Adult psyllids of laboratory reared population were collected with aspirator and were inactivated by keeping them into freezer for 5 min at 4ºC, and then 5 psyllid individuals were released on each of the treated twigs with a camel hair brush. These tubes were then covered with a muslin cloth piece, tied by a rubber band to avoid the escape of insect (Figure 2) and were incubated in an environmental chamber at 27±2°C temperature and 60±5% relative humidity. Experimental design was completely randomized with three to five replicates maintained for each treatment. The mortality of exposed psyllids was noted at 1, 2 and 3 days after treatment.

Leaf-dip method for cotton aphid (A. gossypii)

Standard leaf-dip method was used to bioassay most effective botanical extracts against A. gossypii adults. In this method, young cotton leaves were dipped for 30 sec in 5, 10, 20 and 40% concentrations of botanical extracts made with acetone. Leaves dipped into acetone were served as control. After that leaves were placed at towel paper to be drained and were placed into 9 cm Petri pates layered with 2% agar solution to keep the leaves fresh till the end of bioassay. Ten freshly molted laboratory reared adult aphids were released in each Petri plate with a camel hair brush and Petri plates were incubated in an environmental chamber at 22±2°C temperature and 60±5% relative humidity. Each treatment was replicated ten times and the experimental design was completely randomized. The mortality of bioassayed aphids was noted at 0.5, 1, 2 and 3 days after treatment.

Statistical analyses of data

Data was analyzed statistically using analytical software Statistix V. 8.1® (Ahmed et al., 2004). Apart from the graphical presentation of data regarding the percent mortality of test psyllid and aphid individuals, data were analyzed by factorial analysis of variance (ANOVA) taking time intervals, botanical solutions and their concentrations as factors. Means of treatments were further compared by Tukey’s honestly significant difference (HSD) test at standard probability level of 95%. Median lethal time (LT50) and concentration (LC50) values were calculated through probit analysis using statistics regression software IBM SPSS®. Prior to statistical analysis, data of insect mortality were corrected with the help of Abbott’s formula (Abbott, 1925).

Results and Discussions

Toxicity of indigenous flora of Soon valley against ACP (D. citri)

Insecticidal potential of acetone extracts of 40 indigenous plant species was tested against D. citri using twig-dip bioassay method. Results of this preliminary screening experiment performed with 10% extracts showed that some botanical extracts caused considerable mortality of adult psyllids (F = 44.82; P ≤ 0.01) (Table 2). Among all 40 botanical extracts, maximum mortality of psyllids was exhibited by 10% extracts of M. longifolia (93%), followed by M. officinalis (91%) and N. indicum (89%), while the extracts of D. alba and S. officinalis showed 88 and 81% mortality, respectively. Whereas about 57% mortality was caused by R. smithi and remaining all botanicals caused less than 50% psyllid mortality as shown in Table 3.

 

Table 2: Analysis of variance comparison of different botanical extracts bioassayed against freshly molted adults of Asian citrus psyllid (Diaphorina citri) under laboratory conditions.

Source	DF	MS	MS	F-value	P-value
Treatment	40	163249	4081.22	44.82	≤ 0.01
Time	2	12450	6225.20	68.37	≤ 0.001
Treatment × Time	80	6550	81.87	0.90	0.708
Error	246	22400	91.06
Total	368	204649
GM / CV	37.642 / 25.35

DF = degree of freedom; SS = sum of squares; MS = mea square; P ≤ 0.001 (highly significant) and P ≤ 0.01 (significant); one-way factorial ANOVA at α = 0.05.

 

Response of cotton aphid (A. gossypii) to botanical extracts

Detailed toxicological bioassays were carried out against A. gossypii using ten most effective plant extracts screened out from the previous bioassay with D. citri. Results of these bioassays revealed a differential response of aphid individuals against different plant extracts. According to results, all plant extracts showed considerable mortality of A. gossypii and this mortality response was concentration and exposure time dependent as it increased along with the

 

Table 3: Percent mortality of Asian citrus psyllids (D. citri) by 10% acetone extracts of different plant species collected from Soon Valley and surrounding Salt Range.

Botanicals	Common / Vernacular name	Plant part extracted	Mortality a ± S.E (%)	Homogenous groups
Chenopodium album L.	Bathu	Leaves	24.44 ± 6.89	F-L
Buxus papillosa Schneid.	Shamshad	Leaves	23.33 ± 2.58	G-L
Cynodon dactylon (L.) Pers.	Khabal	Leaves	20.00 ± 6.56	I-L
Petrophytum caespitosum Rydb.	Mat rock spraea	Leaves	27.78 ± 10.02	E-K
Astragalus spp. L.	Koohni	Leaves	13.33 ± 2.58	L
Trichodesma indicum (L.) Lehm.	Juri	Leaves	18.89 ± 4.16	J-L
Dicliptera bupleuroides Nees	Kaalu	Leaves	30.00 ± 7.67	E-K
Marrubium vulgare L.	Pahari gandana	Leaves	45.56 ± 5.92	B-D
Fagonia indica Burm.f.	Dhamasa	Leaves	37.78 ± 7.65	C-H
Maerua arenaria Hook and Thomson	Hemkand	Leaves/Stem	41.11 ± 6.69	B-F
Mentha longifolia (L.) Huds.	Desi podina	Leaves	93.33 ± 4.85	A
Solanum surattense Burm. f.	Kanda kari	Leaves	44.00 ± 2.50	B-E
Nerium indicum Mill.	Kanera	Leaves	89.00 ± 5.00	A
Nerium indicum Mill.	Kanera	Fruits	47.78 ± 8.58	BCD
Acacia melanoxylon R.Br.	Hickory	Leaves	33.33 ± 5.91	G-J
Rhamnus smithi Greene	Buckthorn	Leaves/Stem	56.67 ± 5.34	B
Datura alba L.	Datura	Leaves/Flowers	87.78 ± 4.37	A
Suaeda fruticosa (L.) Delile	Lahnra	Leaves	37.78 ± 5.20	C-H
Alternanthera pungens Kunth	Phakra	Leaves	30.00 ± 6.56	E-K
Murraya koenigii (L.) Spreng.	Jungli kari patta	Leaves	17.78 ± 6.50	JKL
Periploca aphylla Decne.	Bata	Stem	20.00 ± 4.80	E-K
Dryopteris filix-mas (L.) Schott	Male fern	Leaves	28.89 ± 5.54	D-J
Ricinus communis L.	Harnoli	Leaves	32.22 ± 5.18	D-J
Cassia occidentalis L.	Bana chakunda	Leaves	33.33 ± 5.45	G-K
Cassia occidentalis L.	Bana chakunda	Fruits	22.22 ± 6.04	I-L
Adiantum capillus-veneris L.	Khatti booti	Leaves	26.67 ± 4.62	E-K
Justicia adhatoda L.	Dhodak booti	Leaves	30.00 ± 3.83	E-K
Salvia virgata Jacq.	Meadow sage	Leaves	28.89 ± 5.67	B-F
Amaranthus viridis L.	Jungli cholai	Leaves	41.11 ± 4.29	D-I
Sonchus asper (L.) Hill	Bhattal	Leaves	20.00 ± 5.45	J-L
Melilotus officinalis (L.) Pall.	Yellow sweet clover	Leaves	91.11 ± 4.29	A
Salvia officinalis L.	Sage	Leaves	81.11 ± 6.83	A
Solanum incanum L.	Mahoori	Leaves	33.33 ± 5.45	G-K
Portulaca oleracea L.	Loonak	Leaves	41.11 ± 6.07	D-I
Dodonaea viscosa (L.) Jacq.	Santha	Leaves	24.44 ± 6.89	JKL
Olea ferruginea Wall. ex Aitch.	Kao	Leaves	17.78 ± 6.50	J-L
Rumex dentatus L.	Toothed dock	Leaves	41.11 ± 4.26	D-I
Withania coagulans (Stocks) Dunal	Khamjeera	Leaves	40.00 ± 6.37	E-J
Eruca sativa Mill.	Jamahoon	Leaves	35.56 ± 4.66	F-K
Opuntia dillenii (Ker Gawl.) Haw.	Thor	Leaves	28.89 ± 5.67	KL

a = mean of three to five independent replications.

 

increase of concentration of botanicals and exposure time (Figure 3). There was a significant effect of all botanical extracts on aphid mortality (F = 181.30; P ≤ 0.01; Table 4). Overall, the highest average mortality

 

Table 4: Analysis of variance comparison of different botanical extracts bioassayed against freshly molted adults of cotton aphid (Aphis gossypii) under laboratory conditions.

Source	DF	SS	MS	F-value	P-value
Concentration	3	111399	37132.9	942.95	≤ 0.001
Time	3	106209	35402.9	899.02	≤ 0.001
Treatment	9	64257	7139.6	181.30	≤ 0.01
Concentration × Time	9	2275	252.8	6.42	≤ 0.001
Concentration × Treatment	27	14916	552.4	14.03	≤ 0.001
Time × Treatment	27	2447	90.6	2.30	≤ 0.01
Error	881	34693	39.4
Total	959	336196
GM / CV	35.06/ 17.90

DF = degree of freedom; SS = sum of squares; MS = mea square; P ≤ 0.001 (highly significant) and P ≤ 0.01 (significant); one-way factorial ANOVA at α = 0.05.

 

(63%) of aphid individuals was observed by the extract of S. officinalis, followed by D. viscosa and O. ferruginea exhibiting 62 and 60% average aphid mortality, respectively, while M. longifolia and N. indicum both exhibited about 58% aphid mortality for 40% concentrations (Figure 3). Moreover at 20% concentration, the highest mortality (50%) was also observed in case of S. officinalis while remaining all phyto-extracts showed less than 50% aphid mortality (Figure 3).

Similar trend of toxicity was observed regarding LC50 and LT50 values of these botanical extracts. According to probit analysis, S. officinalis was the most effective at 48 h (LC50 = 18.59%), followed by the extract of N. indicum (LC50 = 20.27%) and M. longifolia (LC50 = 20.73%), while the extracts of S. officinalis, M. longifolia and N. indicum showed minimum LC50 values (i.e. 9.24, 9.51 and 10.98%, respectively) at 72 h (Table 5). Similar trend was found in case of median lethal time (LT50) values. The 40% extracts of S. officinalis and O. ferruginea showed minimum LT50 values (i.e. 17.73 and 20.05 %, respectively) (Table 6).

 

Table 5: Median lethal concentration (LC50) values of different acetone extracts of Soon valley flora bioassayed against freshly molted adults of cotton aphid (Aphis gossypii).

Treatments	Observation time (h)	LC50 (%)	Lower and Upper 95% Fiducial Limits (%)	X2 (DF = 10)*	P-value
Maerua arenaria Hook and homon	48	63.76	50.29-110.45	52.28	≤ 0.001
	72	58.80	46.71-104.04	47.09	0.001
Mentha longifolia (L.) Huds.	48	20.27	-38.57-42.65	31.59	0.06
	72	10.98	-53.43-34.84	42.51	≤ 0.001
Nerium indicum Mill.	48	20.73	-233.28-52.07	76.59	≤ 0.001
	72	9.51	-192.30-43.54	77.35	≤ 0.001
Rhamnus smithi Greene	48	25.63	-5.3-36.68	53.36	≤ 0.001
	72	15.67	-21.99-29.56	60.05	≤ 0.001
Datura alba L.	48	66.67	NC	83.58	≤ 0.001
	72	72.40	NC	67.28	≤ 0.001
Periploca aphylla Decne.	48	54.17	40.16-91.96	67.92	≤ 0.001
	72	50.03	38.06-75.57	63.27	≤ 0.001
Sonchus asper (L.) Hill	48	41.13	NC	83.23	≤ 0.001
	72	30.11	NC	69.70	≤ 0.001
Salvia officinalis L.	48	18.59	-37.88-37.87	48.74	0.001
	72	9.24	-64.61-32.39	52.07	≤ 0.001
Dodonaea viscosa (L.) Jacq.	48	22.51	-55.11-41.97	17.49	0.012
	72	27.61	19.66-32.07	27.63	0.015
Olea ferruginea Wall. ex Aitch.	48	21.50	-2.12-32.91	46.10	0.001
	72	14.62	-29.37-33.02	45.71	0.001

*Since the significance level is less than 0.150, a heterogeneity factor is used in the calculation of confidence limits. DF = degree of freedom; NC = not calculable.

 

Table 6: Median lethal time (LT50) values of different acetone extracts of Soon valley flora bioassayed against freshly molted adults of cotton aphid (Aphis gossypii).

Treatment	Botanical Concentration (%)	LT50 (h)	Lower and Upper 95% Fiducial Limits (h)	X2 (DF = 10)*	P-value
Maerua arenaria Hook $ Thomson	20	80.88	72.35-93.52	35.85	0.02
	40	70.16	58.43-93.37	96.97	≤ 0.001
Mentha longifolia (L.) Huds.	20	41.29	37.63-45.06	29.76	0.012
	40	21.63	16.03-26.18	25.33	0.028
Nerium indicum Mill.	20	42.47	35.19-50.49	58.94	≤ 0.001
	40	21.63	10.56-29.21	60.37	≤ 0.001
Rhamnus smithi Greene	20	51.90	48.71-55.49	28.81	0.15
	40	30.55	26.00-34.65	64.08	≤ 0.001
Datura alba L.	20	90.19	78.09-110.94	59.75	≤ 0.001
	40	86.16	69.68-126.09	129.43	≤ 0.001
Periploca aphylla Decne.	20	79.35	65.92-107.27	102.96	≤ 0.001
	40	59.87	49.81-77.61	101.16	≤ 0.001
Sonchus asper (L.) Hill	20	90.51	73.84-128.55	103.87	≤ 0.001
	40	53.02	46.06-62.48	52.03	≤ 0.001
Salvia officinalis L.	20	38.93	34.72-43.14	27.85	0.018
	40	17.73	8.81-24.14	57.99	≤ 0.01
Dodonaea viscosa (L.) Jacq.	20	60	51.87-72.54	25.22	0.028
	40	21.09	17.28-24.37	28.22	0.016
Olea ferruginea Wall. ex Aitch.	20	43.17	39.21-47.39	25.28	0.028
	40	20.05	11.69-26.22	44.63	≤ 0.001

*Since the significance level is less than 0.150, a heterogeneity factor is used in the calculation of confidence limits. DF = degree of freedom.

 

This study determined the bioactivity of acetonic extracts of indigenous flora (including 40 species of plants, herbs and shrubs) of Soon valley and surrounding Salt Range of Pakistan against ACP (D. citri) and cotton aphid (A. gossypii). Among all 40 botanical extracts, maximum mortality of psyllids was exhibited by 10% extracts of M. longifolia (93%), followed by M. officinalis (91%) and N. indicum (89), while the extracts of D. alba and S. officinalis showed 88 and 81% mortality, respectively. Similarly, 2nd bioassay results revealed that the highest mortality (63%) of A. gossypii was exhibited by S. officinalis, followed by D. viscosa (62%), and O. ferruginea (60%), while the extracts of M. longifolia and N. indicum both exhibited 58% aphid mortality at 40% concentration. Remaining all phyto-extracts showed less than 50% mortality against psyllids and aphids. Overall, the extracts of M. longifolia, M. officinalis and N. indicum and extracts of S. officinalis, D. viscosa and O. ferruginea proved to be most toxic against D. citri and A. gossypii, respectively, exhibiting minimum LC50 and LT50 values.

The overall mortality of psyllid individuals recorded in this study by M. officinalis, N. indicum and M. longifolia might be because of the bioactivity of different phenolic and terpenoid compounds found in these plants (Hiremath et al., 1997; Pascual-Villalobos and Robledo, 1998; Lee et al., 2001; Thomas et al., 2002; Odeyemi et al., 2008; Song et al., 2009; Hussain et al., 2010). Odeyemi et al. (2008) evaluated the toxicity of essential oils from M. longifolia against maize weevil (Sitophilus zeamais) by contact, fumigation and repellency bioassays. Their results showed that this herb contains compounds such as 1, 8-cinole, pulegone and menthone that are toxic to insects. In our study, M. longifolia exhibited about 90% mortality of D. citri and 58% mortality of A. gossypii. The observed psyllid and aphid mortality in this study would be due to such bioactive compounds documented in this plant species as flavonoids, phenol, saponins, tannin and terpenoids (Lee et al., 2001; Govindappa and Poojashri, 2011).

Tomczyk and Suszko (2011) demonstrated the biocidal activity of S. officinalis essential oil against Tetranychus urticae (two spotted spider mites). Likewise, different phyto-constituents found in the extracts of M. officinalis such as saponins, flavonoids, terpenoids, phenol, and tannins (Govindappa and Poojashri, 2011) would be the cause of psyllid mortality recorded in this study. Similarly, N. indicum extracts have many phyto-constituents such as saponins, triterpenoids, tannins, carbohydrates, lipids, glycosides, proteins, alkaloids and sterols (Bhuvaneshwari et al., 2007). The extract of N. indicum showed 100% mortality of Nilaparvata lugens (Hiremath et al., 1997). Mortality of psyllids in this experiment exhibited by the extract of N. indicum might be due to presence of these different compounds. Moreover, D. alba is well-known for its medicinal value and insecticidal potential. Our results corroborate this fact regarding the insecticidal potential of D. alba. Many previous studies have demonstrated significant mortality of aphids (Kuganathan et al., 2008) and psyllids (Khan et al., 2013) possibly because of different alkaloids found in this plant (Uddin et al., 2012).

D. viscosa has a great ethnomedicinal importance (Shah and Rahim, 2017) and its extracts contain many bioactive phytochemicals such as diterpenoids, flavonoids, stimgasterols, lupeol, fatty acids and ethers which have revealed toxicity against many insect pests including homopterous pests (Uddin et al., 2012; Díaz et al., 2015), coleopterous (Dimetry et al., 2015) and lepidopterous (Malarvannan et al., 2009; Abbes et al., 2016; Mohammed and Nawar, 2020). Likewise, O. europaea and many other species of Oleaceae family constitute different terpenes e.g. maslinic acid and phenolic contents showing considerable toxic effects against stored grain pests (Tribolium confusum and Sitophilus granaries) and aphids (Myzus persicae) (Hamouda et al., 2015; Alliche and Boughani, 2017; Kısa et al., 2018).

Conclusions and Recommendations

In brief, the extracts of M. officinalis, D. alba, M. longifolia, S. officinalis and N. indicum are found relatively toxic to ACP (D. citri) adults, while the phytoextracts of S. officinalis, O. ferruginea, D. viscosa and M. longifolia appeared effective against cotton aphid (A. gossypii). Overall study findings suggest the incorporation of the botanical extracts of above mentioned indigenous plant species in future integrated pest management for sucking insect pests. Nevertheless, the biochemical characterization of these plant extracts in order to find out their bioactive constituents responsible for the observed psyllid and aphid mortality and the laboratory and field evaluation of these plant extracts against natural enemies (insect predators and parasitoids) constitute important future perspective of this research work.

Acknowledgements

This research work was supported financially by Higher Education Commission (HEC) of Pakistan through a research project (No. 6702) funded under its National Research Programme for Universities (NRPU).

Novelty Statement

This laboratory work evaluated the anti-insect potential of local plant species from Soon valley and surrounding salt range of Pakistan against two destructive sap-feeding insect pests i.e. Asian citrus psyllid (Diaphorina citri) and cotton aphid (Aphis gossypii). Bioassays revealed that out of 40 plant species, acetone extracts of many plant species, particularly of Dodonaea viscosa, Datura alba, Mentha longifolia, Melilotus officinalis, Nerium indicum, Olea ferruginea and Salvia officinalis, exhibited considerable mortality of both insect pest individuals suggesting their biocidal potential against these sap-feeding insect pests.

Author’s Contribution

Muhammad Zeeshan Majeed: Conceived the research idea and prepared experimental protocols.

Muhammad Bilal Tayyab, Kanwer Shahzad Ahmed and Mujahid Tanvir: Conducted the bioassays.

Sylvain Nafiba Ouedraogo and Muhammad Luqman: Performed statistical analyses and prepared results.

Muhammad Asam Riaz and Muhammad Zeeshan Majeed: Wrote the first draft of the manuscript.

Muhammad Asam Riaz: Provided technical support.

Muhammad Anjum Aqueel: Technically revised the manuscript.

Sylvain Nafiba Ouedraogo: Proofread the manuscript. Final manuscript has been read and approved by all authors.

Conflict of interest

The authors declare no competing interest regarding the publication of this research work.

References

Abbes, K., A. Harbi, M. Elimem, A. Hafsi and B. Chermiti. 2016. Bioassay of three solanaceous weeds as alternative hosts for the invasive tomato leafminer Tuta absoluta (Lepidoptera: Gelechiidae) and insights on their carryover potential. Afr. Entomol., 24(2): 334-342. https://doi.org/10.4001/003.024.0334

Abbot, W.S. 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol., 18(2): 265-267. https://doi.org/10.1093/jee/18.2.265a

Ahmad, F., M.A. Khan, F. Gul, A. Suhail, M. Ullah and M. Salman. 2014. Evaluation of different plant extracts against citrus psylla (Diaphorina citri Kuwayama). Pak. J. Weed Sci. Res., 20(3): 347-358.

Ahmad, H., A. Ahmad and M.M. Jan. 2002. The medicinal plants of salt range. J. Biol. Sci., 2(3): 175-177. https://doi.org/10.3923/jbs.2002.175.177

Ahmad, I., M.S.A. Ahmad, M. Hussain, M. Hameed, M.Y. Ashraf, M. Saghir and S. Koukab. 2009. Spatio-temporal effects on species classification of medicinal plants in Soone Valley of Pakistan. Int. J. Agric. Biol. Engin., 11(1): 64-68.

Ahmad, M. and M.I. Arif. 2008. Susceptibility of Pakistani populations of cotton aphid Aphis gossypii (Homoptera: Aphididae) to endosulfan, organophosphorus and carbamate insecticides. Crop Prot., 27: 523-531. https://doi.org/10.1016/j.cropro.2007.08.006

Ahmed, S., N. Ahmad and R.R. Khan. 2004. Studies on population dynamics and chemical control of citrus psylla, Diaphorina citri. Int. J. Agric. Biol., 6(6): 970-973.

Alliche, S. and D. Boughani. 2017. Etude de la toxicité de l’huile d’olive de différentes régions de la Kabylie à l’égard de quelques ravageurs des denrées stockées. PhD dissertation, Université Mouloud Mammeri, Algeria. pp. 44.

Ashfaq, S., I.A. Khan, M. Saeed, A.U.R. Saljoqi, F. Manzoor, K. Sohail and A. Sadozai. 2011. Population dynamics of insect pests of cotton and their natural enemies., Sarhad J. Agric., 27(2): 251-253.

Augier, L., G. Gastaminza, M. Lizondo, M. Argañaraz and E. Willink. 2017. Record of Diaphorina citri (Hemiptera: Psyllidae) in North West Argentina. Rev. Soc. Entomol. Argent., 65(3-4): 67-68.

Bhuvaneshwari, L., E. Arthy, C. Anitha, K. Dhanabalan and M. Meena. 2007. Phytochemical analysis and antibacterial activity of Nerium oleander. Anc. Sci. Life., 26(4): 24-29.

Boina, D.R. and J.R. Bloomquist. 2015. Chemical control of the Asian citrus psyllid and of Huánglóngbìng disease in citrus. Pest Manage. Sci., 71(6): 808-823. https://doi.org/10.1002/ps.3957

Borad, P.K., M.J. Patel, B. Patel, M. Patel, B.H. Patel and J.R. Patel. 2001. Evaluation of some botanicals against citrus leafminer (Phyllocnistis citrella) and psylla (Diaphorina citri) on kagzilime (Citrus aurantifolia). Ind. J. Agric. Sci., 71(3): 177-179.

Bove, J.M. 2006. Huánglóngbìng: a destructive, newly-emerging, century-old disease of citrus. J. Plant Pathol., 88(1): 7-37.

Boykin, L.M., P. De Barro, D.G. Hall, W.B. Hunter, C.L. McKenzie, C.A. Powell and R.G. Shatters. 2012. Overview of worldwide diversity of Diaphorina citri Kuwayama mitochondrial cytochrome oxidase 1 haplotypes: two old world lineages and a new world invasion. Bull. Entomol. Res., 102(5): 573-582. https://doi.org/10.1017/S0007485312000181

Copping, L.G. and J.J. Menn. 2000. Biopesticides: a review of their action, applications and efficacy. Pest Manage. Sci., 56(8): 651-676. https://doi.org/10.1002/1526-4998(200008)56:8<651::AID-PS201>3.0.CO;2-U

Deng, F., J. Sun, R. Dou, X. Yu, Z. Wei, C. Yang, ... and L. Zhu. 2020. Contamination of pyrethroids in agricultural soils from the Yangtze River Delta, China. Sci. Total Environ., 731: 139-181. https://doi.org/10.1016/j.scitotenv.2020.139181

Desneux, N., A. Decourtye and J.M. Delpuech. 2007. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol., 52: 81-106. https://doi.org/10.1146/annurev.ento.52.110405.091440

Dhananjayan, V., S. Jayakumar, and B. Ravichandran. 2020. Conventional methods of pesticide application in agricultural field and fate of the pesticides in the environment and human health. Controlled Release of Pesticides for Sustainable Agriculture (eds.) Rakhimol, K.R., S. Thomas, T. Volova and K. Jayachandran, Springer, Switzerland. pp. 1-39. https://doi.org/10.1007/978-3-030-23396-9_1

Díaz, M., C.E. Díaz, R.G. Álvarez, A. González, L. Castillo, A. González-Coloma and C. Rossini. 2015. Differential anti-insect activity of natural products isolated from Dodonaea viscosa Jacq. (Sapindaceae). J. Plant Prot. Res., 55(2): 172-178. https://doi.org/10.1515/jppr-2015-0023

Dimetry, N.Z., S. El-Gengaihi, M. Hafez and M.H. Abbass. 2015. Pesticidal activity of certain plant extracts and their isolates against the cowpea beetle Callosobruchus maculatus (F.) (Coleoptera: Chrysomelidae: Bruchinae). Herb. Polon. J., 61(3): 77-92. https://doi.org/10.1515/hepo-2015-0024

Ebert, T. and B. Cartwright. 1997. Biology and ecology of Aphis gossypii Glover (Homoptera: aphididae). Southwest. Entomol., 22(1): 116-153.

Edwards, C.A. 2013. Environmental pollution by pesticides. Springer Science and Business Media, New York. pp. 1-542.

Eid, A.E., A.H. El-Heneidy, A.A. Hafez, F.F. Shalaby and D. Adly. 2018. On the control of the cotton aphid, Aphis gossypii Glov. (Hemiptera: Aphididae), on cucumber in greenhouses. Egypt. J. Biol. Pest Co., 28(1): 64-70. https://doi.org/10.1186/s41938-018-0065-9

Gavloski, J. 2018. Integrated management of sap feeding insects of pulse crops. Ann. Entomol. Soc. Am., 111(4): 184-194. https://doi.org/10.1093/aesa/say008

Govindappa, M. and M.N. Poojashri. 2011. Antimicrobial, antioxidant and in vitro anti-inflammatory activity of ethanol extract and active phytochemical screening of Wedelia trilobata (L.) Hitchc. J. Pharmaco. Phytother., 3(3): 43-51.

Grafton-Cardwell, E.E., L.L. Stelinski and P.A. Stansly. 2013. Biology and management of Asian citrus psyllid, vector of the Huánglóngbìng pathogens. Annu. Rev. Entomol., 58: 413-432. https://doi.org/10.1146/annurev-ento-120811-153542

Haddi, K., L.M. Turchen, L.O. Viteri Jumbo, R.N. Guedes, E.J. Pereira, R.W. Aguiar and E.E. Oliveira. 2020. Rethinking biorational insecticides for pest management: unintended effects and consequences. Pest Manage. Sci., 76(7): 2286-2293. https://doi.org/10.1002/ps.5837

Halbert, S.E. and K.L. Manjunath. 2004. Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Fl. Entomol., 87(3): 330-353. https://doi.org/10.1653/0015-4040(2004)087[0330:ACPSPA]2.0.CO;2

Halbert, S.E., and Nunez, C.A. 2004. Distribution of the Asian citrus psyllid, Diaphorina citri Kuwayama (Rhynchota: Psyllidae), in the Caribbean basin. Florida Entomol., 87(3): 401-402. https://doi.org/10.1653/0015-4040(2004)087[0401:DOTACP]2.0.CO;2

Hall, D.G., Richardson, M.L., Ammar, E.D., and Halbert, S.E. 2013. Asian citrus psyllid, Diaphorina citri, vector of citrus Huanglongbing disease. Entomologia Experimentalis et Applicata, 146(2): 207-223. https://doi.org/10.1111/eea.12025

Halstead, N.T., D.J. Civitello and J.R. Rohr. 2015. Comparative toxicities of organophosphate and pyrethroid insecticides to aquatic macroarthropods. Chemosphere, 135: 265-271. https://doi.org/10.1016/j.chemosphere.2015.03.091

Hamouda, A.B., O. Boussadia, B. Khaoula, A. Laarif and M. Braham. 2015. Studies on insecticidal and deterrent effects of olive leaf extracts on Myzus persicae and Phthorimaea operculella. J. Entomol. Zool. Stud., 3(6): 294-297.

Henneberry, T.J., L.F. Jech, T. Torre and D.L. Hendrix. 2000. Cotton aphid (Homoptera: Aphididae) biology, honeydew production, sugar quality and quantity, and relationships to sticky cotton. Southwest. Entomol., 25(3): 161-174.

Herron, G.A., K. Powis and J. Rophail. 2001. Insecticide resistance in Aphis gossypii Glover (Hemiptera: Aphididae), a serious threat to Australian cotton. Aust. J. Entomol., 40(1): 85-91. https://doi.org/10.1046/j.1440-6055.2001.00200.x

Hiremath, G.I., Y.J. Ahn and S.I. Kim. 1997. Insecticidal activity of Indian plant extracts against Nilaparvata lugens (Homoptera: Delphacidae). Appl. Entomol. Zool., 32(1): 159-166. https://doi.org/10.1303/aez.32.159

Hussain, J., Z. Muhammad, R. Ullah, F.U. Khan, I.U. Khan, N. Khan and S. Jan. 2010. Evaluation of the chemical composition of Sonchus eruca and Sonchus asper. J. Am. Sci., 6(9): 231-235.

Isman, M.B. 2020. Botanical insecticides in the twenty-first century–fulfilling their promise?. Annu. Rev. Entomol., 65: 233-249. https://doi.org/10.1146/annurev-ento-011019-025010

Khan, A.A., M. Afzal, A.M. Raza, A.M. Khan, J. Iqbal, H.M. Tahir and M.A. Aqeel. 2013. Toxicity of botanicals and selective insecticides to Asian citrus psylla, Diaphorina citri Kuwayama.(Homoptera: Psyllidae) in laboratory conditions. Jokul. J., 63(8), 52-72.

Kim, K.H., E. Kabir and S.A. Jahan. 2017. Exposure to pesticides and the associated human health effects. Sci. Total Environ., 575, 525-535. https://doi.org/10.1016/j.scitotenv.2016.09.009

Kısa, A., M. Akyüz, H.Y. Çoğun, Ş. Kordali, A.U. Bozhüyük, B. Tezel and A. Çakır. 2018. Effects of Olea europaea L. leaf metabolites on the tilapia (Oreochromis niloticus) and three stored pests, Sitophilus granarius, Tribolium confusum and Acanthoscelides obtectus. Rec. Nat. Prod., 12(3): 201. https://doi.org/10.25135/rnp.23.17.07.126

Kocourek, F., J. Havelka, J. Berankova and V. Jarosik. 1994. Effect of temperature on development rate and intrinsic rate of increase of Aphis gossypii reared on greenhouse cucumbers. Entomol. Exp. Appl., 71(1): 59-64. https://doi.org/10.1111/j.1570-7458.1994.tb01769.x

Kuganathan, N., S. Saminathan and S. Muttukrishna. 2008. Toxicity of Datura alba leaf extract to aphids and ants. Intern. J. Toxicol., 5(2): 1559-3916. https://doi.org/10.5580/3db

Kumari, B., V.K. Madan and T.S. Kathpal. 2008. Status of insecticide contamination of soil and water in Haryana, India. Environ. Monit. Assess., 136(1-3): 239-244. https://doi.org/10.1007/s10661-007-9679-1

Lee, S.E., B.H. Lee, W.S. Choi, B.S. Park, J.G. Kim and B.C. Campbell. 2001. Fumigant toxicity of volatile natural products from Korean spices and medicinal plants towards the rice weevil, Sitophilus oryzae (L). Pest Manage. Sci., 57(6): 548-553. https://doi.org/10.1002/ps.322

Mahmood, R., A. Rehman and M. Ahmad. 2014. Prospects of biological control of citrus insect pests in Pakistan. J. Agric. Res., 52(2): 229-244.

Majeed, M.Z., M. Javed, M.A. Riaz and M. Afzal. 2016. Population dynamics of sucking pest complex on some advanced genotypes of cotton under unsprayed conditions. Pak. J. Zool., 48(2): 475-480.

Majeed, M.Z., M.I. Nawaz, R.R. Khan, U. Farooq and C.S. Ma. 2018. Insecticidal effects of acetone, ethanol and aqueous extracts of Azadirachta indica (A. Juss), Citrus aurantium (L.), Citrus sinensis (L.) and Eucalyptus camaldulensis (Dehnh.) against mealybugs (Hemiptera: Pseudococcidae). Trop. Subtrop. Agroecosys., 21(3): 421-430.

Malarvannan, S., Giridharan, R., Sekar, S., Prabavathy, V.R., and Nair, S. 2009. Ovicidal activity of crude extracts of few traditional plants against Helicoverpa armigera (Hubner) (Noctuidae: Lepidoptera). J. Biopesticides, 2(1): 64-71.

Mohammed, A.K. and M.H. Nawar. 2020. Study of the effect of alcoholic extract of Dodonaea viscosa. leaves on the life performance of the greater wax worm Galleria mellonella L. (lepidoptera: pyralidae). Plant Arch., 20: 3449-3454.

Naeem, A., S. Freed, F.L. Jin, M. Akmal and M. Mehmood. 2016. Monitoring of insecticide resistance in Diaphorina citri Kuwayama (Hemiptera: Psyllidae) from citrus groves of Punjab, Pakistan. Crop Prot., 86: 62-68. https://doi.org/10.1016/j.cropro.2016.04.010

Nazir, T., M.D. Gogi, M.Z. Majeed, A. Hanan and M.J. Arif. 2017. Field evaluation of selective systemic formulations against sucking insect pest complex and their natural enemies on a transgenic Bt cotton. Pak. J. Zool., 49(5): 1789-1796. https://doi.org/10.17582/journal.pjz/2017.49.5.1789.1796

Odeyemi, O.O., P. Masika and A.J. Afolayan. 2008. Insecticidal activities of essential oil from the leaves of Mentha longifolia L. against Sitophilus zeamais (Motschulsky) (Coleoptera: Curculionidae). Afr. Entomol., 16(2): 220-225 https://doi.org/10.4001/1021-3589-16.2.220

Pascual-Villalobos, M.J. and A. Robledo. 1998. Screening for anti-insect activity in Mediterranean plants. Ind. Crop. Prod., 8(3): 183-194. https://doi.org/10.1016/S0926-6690(98)00002-8

Razmjou, J., S. Moharramipour, Y. Fathipour and S.Z. Mirhoseini. 2006. Effect of cotton cultivar on performance of Aphis gossypii (Homoptera: Aphididae) in Iran. J. Econ. Entomol., 99(5): 1820-1825. https://doi.org/10.1093/jee/99.5.1820

Regnault-Roger, C., C. Vincent and J.T. Arnason. 2012. Essential oils in insect control: low-risk products in a high-stakes world. Annu. Rev. Entomol., 57: 405-424. https://doi.org/10.1146/annurev-ento-120710-100554

Rossetti, M.R., M.T. Defagó, M.C. Carpinella, S.M. Palacios and G. Valladares. 2008. Actividad biológica de extractos de Melia azedarach sobre larvas de Spodoptera eridania (Lepidoptera: Noctuidae). Rev. Soc. Entomol. Argent., 67(1-2): 115-125.

Satar, S., U. Kersting and N. Uygun. 1999. Development and fecundity of Aphis gossypii Glover (Homoptera: Aphididae) on three Malvaceae hosts. Turk. J. Agric. Forest., 23(6): 637-644. https://doi.org/10.1046/j.1439-0418.1999.00309.x

Setamou, M., D. Rodriguez, R. Saldana, G. Schwarzlose, D. Palrang and S.D. Nelson. 2010. Efficacy and uptake of soil-applied imidacloprid in the control of Asian citrus psyllid and a citrus leafminer, two foliar-feeding citrus pests. J. Econ. Entomol., 103(5): 1711-1719. https://doi.org/10.1603/EC09371

Shah, A. and S. Rahim. 2017. Ethnomedicinal uses of plants for the treatment of malaria in Soon Valley, Khushab, Pakistan. J. Ethnopharmacol., 200: 84-106. https://doi.org/10.1016/j.jep.2017.02.005

Siddiqui, S., G.H. Abro, T.S. Syed, A.S. Buriro, S. Ahmad, M.Z. Majeed and M.A. Riaz. 2021. Identification of cotton physio-morphological marker for the development of cotton resistant varieties against sucking insect pests: a biorational approach for insect-pest management. Pak. J. Zool., 1-9. https://doi.org/10.17582/journal.pjz/20190703060702

Song, Y.W., J.H. Ahn, C.A. Lee, G.W. Kim, S.C. Choi and Y.S. Jung. 2009. Digitalis-like toxic symptoms occurring after accidental Nerium indicum poisoning. J. Kor. Soc. Clinic. Toxicol., 7(1): 19-22.

Teixeira, C.D., C. Saillard, S. Eveillard, J.L. Danet, A.J. Ayres and J. Bové. 2005. ‘Candidatus Liberibacter americanus’, associated with citrus Huánglóngbìng (greening disease) in São Paulo State, Brazil. Int. J. Syst. Evol. Microbiol., 55(5): 1857-1862. https://doi.org/10.1099/ijs.0.63677-0

Thomas K.J., M. Selvanayagam, N. Raja and S. Ignacimuthu. 2002. Plant products in controlling rice weevil Sitophilus oryzae. J. Sci. Ind. Res., 61: 269-274.

Tiwari, S., R.S. Mann, M.E. Rogers and L.L. Stelinski. 2011. Insecticide resistance in field populations of Asian citrus psyllid in Florida. Pest Manage. Sci., 67(10): 1258-1268. https://doi.org/10.1002/ps.2181

Tomczyk, A. and M. Suszko. 2011. The role of phenols in the influence of herbal extracts from Salvia officinalis L. and Matricaria chamomilla L. on two-spotted spider mite Tetranychus urticae Koch. Biol. Lett., 48(2): 193-205. https://doi.org/10.2478/v10120-011-0020-x

Turek, C. and F.C. Stintzing. 2013. Stability of essential oils: a review. Compr. Rev. Food Sci. F., 12(1): 40-53. https://doi.org/10.1111/1541-4337.12006

Uddin, G., A. Rauf and S. Akhtar. 2012. Studies on chemical constituents, phytochemical profile and pharmacological action of Datura alba. Mid. Est. J. Med. Plant. Res., 1(1): 14-18.

Xia, J.Y., W. van der Werf and R. Rabbinge. 1999. Influence of temperature on bionomics of cotton aphid, Aphis gossypii, on cotton. Entomol. Exp. Appl., 90(1): 25-35. https://doi.org/10.1046/j.1570-7458.1999.00420.x

Yan, L., Z. Shuai and S. Zhenrun. 2013. Insecticide resistance in and chemical control of the cotton aphid, Aphis gossypii (Glover). Plant Prot., 39(9): 70-80.