Research Article · Volume 35, Issue 2, 1 January 2021 · Open Access
Comparative Toxicity of Phyto-Extracts of Indigenous Flora of Soone Valley against some Insect Pests of Agricultural and Urban Importance
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Affiliations & Notes ⌄
1Department of Entomology, College of Agriculture, University of Sargodha, Sargodha, Pakistan. 2Department of Agricultural Extension, College of Agriculture, University of Sargodha, Sargodha, Pakistan. , Corresponding author: Muhammad Zeeshan Majeed zeeshan.majeed@uos.edu.pk
Insecticidal potential of forty indigenous plant species (including trees, herbs and shrubs) was evaluated in this laboratory study against four insect pests of economic importance.
So, for the further studies’ chemical characterization of these most effective plant extracts will be analyzed for their chemical constituents.
Selected from the article's own text.
Abstract
This laboratory study encompasses comparative evaluation of insecticidal potential of indigenous ethnomedicinal flora of Soone Valley and surrounding Salt Range of Pakistan. Acetone extracts (10%) of forty plant species were evaluated against Asian citrus psyllid (Diaphorina citri), armyworm (Spodoptera litura), house mosquito (Culex quinquefasciatus) and subterranean termite (Odontotermes obesus) using twig-dip, leaf-dip, aqueous exposure and filter paper-dip bioassay methods, respectively. Results revealed that the extracts of Mentha longifolia, Sonchus asper and Nerium indicum were the most toxic to D. citri exhibiting 90% mortality. The extracts of Dodonaea viscosa and Olea ferruginea caused highest mortality of S. litura (i.e. 70 and 58%, respectively). Maximum mortality of C. quinquefasciatus larvae was observed by Maerua arenaria (87%), N. indicum (84%) and Withania coagulans (83%) extracts. While, the most toxic plant extracts against O. obesus termites were Periploca aphylla, Rhamnus spp. and Buxus papillosa causing 89, 62 and 52% mortality, respectively. These findings corroborate the effectiveness of indigenous plant extracts as safe and environment friendly alternates to hazardous synthetic insecticides and suggest the incorporation of these natural compounds in the pest management programs against agricultural and urban insect pests.
Novelty Statement | This study encompasses a first extensive evaluation of ethnomedicinal flora of Soone Valley and surrounding Salt Range for their toxicity potential against four major insect pests of economic importance. Results of this study demonstrate the relative insecticidal potential of indigenous plant extracts as biorational alternates to toxic synthetic insecticides and recommend the incorporation of these phyto-chemicals in the future insect pest management programs.
Introduction
Apart from their great ecological impact, many species of insects pose a serious threat to humans. They are destructive pests of agricultural crops, notorious vectors of
various plant and human diseases and cause many other direct and indirect losses. Insect pest problems have been an almost inevitable part of agriculture and urban sectors all over the world including Indo-Pak regions. For instance, armyworms and psyllids are among the major insect pests of agricultural and horticultural crops including fruits and vegetables. Similarly, mosquitos and termites are the most important urban and medical pests, respectively.
Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), is a sap feeding pest of citrus and other plants of Rutaceae family ; . Firstly, reported in Pakistan in 1927, it has become a major pest for all citrus growing regions of Pakistan . Both nymphs and adults desap plant foliage resulting in defoliation and curling of leaves, flowers and withering of branches and premature fruit drop . Moreover, this pest is also responsible for the transmission of citrus greening disease (Huánglóngbìng), a severe threat to citrus industry in Pakistan ; ; ; ; ; .
Armyworm, Spodoptera litura Fabricius (Lepidoptera: Noctuidae), is polyphagous pest of cosmopolitan distribution causing severe losses to agricultural production worldwide . With a host range of more than 150 plants, S. litura infests and damage many fruit and vegetable crops of economic significance ; ; . In Indo-Pak regions, considerable quantitative and qualitative losses are incurred by armyworm infestations in cotton, gram, potato, okra, tomato, chilies and many other horticultural crops.
With more than 3,500 described species, termites constitute an important part of all ecosystems and play a vital role in plant litter decomposition, turnover organic matter and soil acclimatization/reclamation ; . However, many termite species particularly subterranean species are destructive pests of forest and orchard plantations, industrial crops and wooden infrastructures . Coptotermes heimi Wasmann (Rhinotermitidae) and Odontotermes obesus Rambur (Termitidae) are most predominant and destructive termite species . In Indo-Pak regions, these termites infest a wide range of agricultural crops including wheat, maize, gram, cotton, sugarcane and sesame ; . Moreover, they are serious threat to wooden infrastructures in urban and rural areas .
Mosquitoes are of the nature’s most serious bioterrorists because they are responsible to transmit the world’s most severe life-threatening diseases including malaria, filariasies, dengue, Zika and Chickungunya fevers (WHO, 2005). Among pest mosquito species, Culex mosquitoes, especially C. quinquefasciatus, are the principal vectors of nematode, Wuchereria bancrofti that cause a disease known as Bancroftian filariasis. C. quinquefasciatus is native to the West Africa from where it has been spread throughout the Asia .
In Pakistan, synthetic insecticides have been the sole control measure being relied upon to suppress and control these agricultural and urban insect pests ; ; . Undoubtedly use of these insecticides increase farmers’ production and improve their monetary benefits by their quick action against insect pests. However, their long-term negative effects on environment health and crop production sustainability cannot be overlooked. The frequent and indiscriminate application of these persistent synthetic insecticides have resulted into many non-target effects including environmental contamination , pest resistance to insecticides ; , resurgence of secondary pests , eradiation of beneficial fauna including insect predator and parasitoid species ; , and human health hazards ; .
Due to above mentioned deleterious effects of synthetic insecticides being used in agricultural and urban environments; researchers have diverted their focus towards the development of biorational pesticides such as botanical pesticides. Many studies have demonstrated the efficacy of different phyto-extracts against D. citri ; ; , S. litura ; ; ; ; ; , O. obesus ; ; ; ; and Culex spp. ; ; . Although lack quick knock-down effects as synthetic insecticides, plant-based pesticides can be effective alternatives to synthetic pesticides as most of these extracts are volatile in nature, target-specific and have reduced environmental risks .
As indigenous plants of a particular bio-geographical area may constitute effective and bioactive compounds against indigenous insect pest species ; , the present study was aimed to determine the insecticidal potential of indigenous flora of Soone Valley situated in the North-West of district Khushab (Punjab, Pakistan). This valley and surrounding salt range harbor a rich diversity of medicinal plants including many herbs and shrubs (Ahmed et al., 2009; .
Materials and Methods
Sampling locations
Indigenous plant species were collected from Soone Valley and surrounding Salt Range. Sampling area was about 300 Km2 located between longitudes 72º00’ to 72º30’ E and latitude 32º25’ to 32º45’ N . In the sampling area, six different sites, i.e. Khura, Khabikki, Kenhatti Garden, Daep Sharif, Angah and Uchhali, were selected for the collection of flora based on their vegetation enrichment as detailed in Figure 1 and Table 1. Sampling was done during September to October, 2018 and then March to April 2019.
Table 1: Geographical coordinates of the plant sampling sites (cf: Figure 1).
Localities
Latitude N
Longitude E
Elevation (m)
Khura
32.23° N
72.11° E
866
Dape Sharif
32.30° N
72.04° E
890
Uchhali
32.56° N
72.02° E
794
Kenhatti Garden
32.40° N
72.14° E
783
Angah
32.35° N
72.05° E
821
Khabekki
32.35° N
72.12° E
774
Sampling and processing of plant samples
Samples of forty plant species were collected from above mentioned selected sites. Samples were consisted of leaves, stems, roots, fruits and flowers as mentioned in Table 2. Among this plant collection, 38 samples were identified with the help of their vernacular name told by local inhabitants and already published literature and verified by the Department of Botany, University of Sargodha, Sargodha. The collected plant samples were washed by clean tap water and shade-dried for about two weeks. After drying, plant materials were grinded to make fine powder using commercial electrical blender and were preserved separately in plastic zip bags for further processing.
Extraction of plant samples
The extraction of plant samples was carried out in the Laboratory of the Department of Entomology, College of Agriculture, University of Sargodha, Pakistan. Soxhlet apparatus (Daihan Scientific Co., Ltd. South Korea) was used to extract the phyto-constituents according to a previously described protocol . A known amount (50 g) of grounded material of each plant sample was loaded into the filter paper thimble in Soxhlet apparatus. A piece of cotton was plugged at the top of the thimble to stop the entry of crude extract into the siphoning tube. A known volume (500 mL) of organic solvent (acetone having polarity index of 5.1 and boiling point of 56 oC) was filled into the flask (1 L) fixed over the mantle of heating device. The extractions were performed for 6-8 hr at 60 °C. The crude extract obtained from Soxhlet apparatus was further concentrated by evaporating the excess of extraction solvent using rotary evaporator (Daihan Scientific Co., Ltd. South Korea) set at 60 °C. Prepared extracts were preserved in hermetic dark glass vials at 4 °C.
Insect cultures
Adults of Asian citrus psyllid (D. citri) were collected with an aspirator from the citrus (Citrus reticulara cv. kinnow mandarin) field situated near the College of Agriculture, University of Sargodha. These field collected psyllids were reared for 2-3 weeks on potted Murraya paniculata (orange jasmine) plants maintained in the insect rearing cages at optimum temperature (25±5°C), relative humidity (60±5%) and 16L:8D photoperiod. Healthy and active adult psyllids were used in toxicity bioassays.
Larvae of armyworm (S. litura) were collected from the field of sunflower (Helianthus annuus) and were maintained in the laboratory in plastic jars under controlled conditions (25±2ºC, 60±5% RH and 16:8 (L: D) photoperiod). They were fed daily on un-contaminated fresh leaves of castor (Ricinus cummunis) plants. Adults upon emerging from pupa were transferred to separate plastic jars provided with 10% honey solution. Healthy and active larvae from F2 generation were used in bioassays.
Mosquito (C. quinquefasciatus) larvae were collected from different areas of Sargodha with the help of an aquatic net and dipper. Those collected larvae were identified on the basis of different distinguished morphological characteristics under microscope by using taxonomic keys available in literature . It was ensured that collection site was never exposed to any insecticide at least two months before collection of mosquito larvae.
For subterranean termites, intact portions of termite nest were collected from the termite infested stubbles of sugarcane (Saccharum officinarum). Before collection, it was ensured that the sugarcane field was not treated with any pesticide for last three months. These termites were identified as O. obesus on the basis of their distinguished morphological characters . In order to acclimatize the termite individuals to lab conditions, collected termite nest portions were maintained in the lab in polystyrene glass cages for few weeks. Only healthy and active worker individuals were used in toxicity bioassays.
Table 2: Details of different plant samples collected from Soone Valley and surrounding Salt Range of Pakistan.
Allyl isothiocyanate, 3-butenyl isothiocyanate, 4-methylsulfinybutyl isothiocyanate, sulforaphane), 2-phenylethyl isothiocyanate and bis (isothiocyanatobutyl) disulphide, fatty acids
*NI, not informed.
Toxicity bioassays
For screening toxicity potential of forty plant extracts, 10% solutions of these extracts were made using acetone and the same was used in control treatments. Bioassays were performed using completely randomized design (CRD) with five replications for each treatment.
For D. citri, twig-dip method was used. Freshly cut twigs (5 cm long) of orange jasmine (C. reticulata) were dipped into 10% solutions of botanical extracts for 30 sec and were placed at towel paper to soak up the excess solution from leaves. These treated twigs were then fixed in 2% agar solution in sterile Eppendorf tubes (1.5 mL) and these Eppendorf tubes were placed into sterile falcon tubes (50 mL). Laboratory maintained adult psyllids were collected with the help of aspirator and were kept into freezer for 5 min at 0 ºC to inactivate psyllids. Ten inactive psyllids were released into each falcon tubes with the help of a soft camel hair brush. Each falcon tube was covered with a piece of muslin cloth and tied with rubber band and all tubes were incubated in the rearing lab at controlled conditions (25 ± 2 ºC, 60 ± 5% RH and 16:8 (L: D) photoperiod). Data regarding mortality of psyllids was recorded at 24, 48 and 72 h post-exposure.
For S. litura, leaf-disc method was used. Uncontaminated fresh leaves of R. cummunis were washed and air-dried at room temperature (24 °C) for 5 min. Leaf discs (60 mm) were prepared and treated with treatment solutions and put to dry on towel paper for 15 min at room temperature. Treated and control leaf discs were placed in Petri plates (60 mm) over a thin layer of 2% agar to maintain the moisture within the Petri plates. Ten 2nd instar starved larvae of lab reared S. litura were released into each Petri plate and these plates were incubated in the rearing lab at controlled conditions (25 ± 2 ºC, 60 ± 5% RH and 16:8 (L: D) photoperiod). Data regarding the mortality of exposed larvae was recorded at 24, 48 and 72 h post-exposure.
Aqueous solution bioassay method was used for C. quinquefasciatus. Ten early 4th instar larvae of C. quinquefasciatus mosquito were dropped into disposable glasses (200 mL) having 100 mL of 0.5% aqueous solution of each botanical. Whole experimentation was performed in controlled conditions (25 ± 2 ºC, 60 ± 5% RH and 16:8 (L: D) photoperiod). Data regarding the mortality of exposed mosquito larvae was recorded at 24, 48 and 72 h post-exposure.
For O. obesus, filter paper disc method was used. Filter paper (Whatman No. 1) discs were dipped in 10% solution of each botanical extract for 30 sec and allowed to dry for 30 min at room temperature (24 °C). Treated and control leaf discs were placed in Petri plates (60 mm) over a thin layer of 2% agar to maintain the moisture within the Petri plates. Ten healthy worker termites were released in each Petri plate and these plates were incubated in the laboratory at 25 ± 2 ºC, 60 ± 5% RH and 16:8 (L: D) photoperiod). Data regarding the mortality of exposed termite individuals was recorded at 24, 48 and 72 h post-exposure.
Statistical analysis
Statistical analysis of data was performed using Statistix V. 8.1. analytical software (Tallahassee, FL, USA). In addition to graphical presentation of percent mortality of the exposed insect individuals, one-way factorial ANOVA was run using botanical extracts and time intervals as factors. Treatment means were compared using Tukey’s honest significant difference (HSD) at standard level of significance (α = 0.05).
Results and Discussion
Insecticidal potential of forty indigenous plant species (including trees, herbs and shrubs) was evaluated in this laboratory study against four insect pests of economic importance. Most of the plant species collected belongs to Apocynaceae, Amaranthacea, Fabaceae, Lamiaceae and Solanaceae families and are usually enriched in such phyto-constitutes as alkaloids, carbohydrates, cardiac glycosides, cyanogenic glycosides, flavonoids, phenols, resins oxalates, steroids, saponins and tannins (Table 2).
Toxicity of indigenous flora of Soone Valley against D. citri
Toxicity bioassays revealed that the 10% acetone extracts of M. longifolia, S. asper, N. indicum, D. alba and S. officinalis exhibited highest average mortality of D. citri i.e. 93, 91, 89, 88, and 81%, respectively, whereas the other plant extracts caused less than 50% mortality as observed at 72 h post-exposure (Figure 2). Least toxic plant extracts were of Astragalus spp., W. coagulans, O. dillenii, T. indicum and A. viridis.
This observed mortality of D. citri by M. longifolia, S. asper and N. indicum would be due to diverse terpenoids and phenolic compounds present in these plant extracts ; ; ; ; . Our results are in line with the findings of Kuganathan et al. (2008) demonstrating significant mortality of aphids by the extracts of D. alba, probably due to the alkaloids present in the leaves of this plant. Khan et al. (2013) demonstrated significant toxicity of D. alba extract against citrus psyllids (D. citri) causing 60±9.7% nymphal mortality. Similarly, the toxic effect of essential oil of S. officinalis was revealed by Tomczyk and Suszko (2011) against two spotted spider mites and reported 56% mite mortality in 4 days of treatment. Govindappa and Poojashri (2011) examined the presence of chemicals such as flavonoids, phenol, saponins, tannin and terpenoids in M. officinalis that might be responsible for psyllid mortality in this study.
Toxicity of indigenous flora of Soone Valley against S. litura
In case of S. litura, extracts of D. viscosa and O. ferruginea caused highest average mortality of S. litura, i.e. 70 and 58%, respectively. The extracts of M. koeingii, M. longifolia, F. indica, A. pungens and R. cummunis exhibited moderate toxicity causing 20 to 40% mortality of the exposed 2nd instar larvae of S. litura, whereas other plant extracts caused minimum or negligible mortality (Figure 3).
Ethnomedicinal plant species of Soone Valley and surrounding Salt Range such as D. viscosa and O. ferruginea have been known as excellent herbal remedies against many diseases including diarrhea and malaria . D. viscosa plant extracts constitute such phytochemicals as lupeol, stimgasterols, diterpenoids, flavonol-3-methyl ethers and certain fatty acids which have been demonstrated to show bioactivity against different insect pests including lepidopterous ; , coleopterous and homopterous pests . Similarly, many species of Oleaceae family contain toxic compounds potentially effective against different insect pests. For instance, O. europaea constitute higher phenolic contents and a triterpene compound (maslinic acid) exhibiting significant toxicity against aphids (Myzus persicae) and stored grain insect pests (Sitophilus granaries and Tribolium confusum) ; Kisa et al., 2018).
Toxicity of indigenous flora of Soone Valley against C. quinquefasciatus
Figure 4 presents the average percent mortality of C. quinquefasciatus larvae by 0.5% botanical extracts. Maximum mortality of mosquito larvae was observed by the M. arenaria extract (87%), followed by the extracts N. indicum (84%), W. coagulans (83%), S. fruticosa (81%), O. ferruginea (79%), A. capillus-veneris (78%), D. bupleuroides (77%), Astragalus spp. (73%), S. surattense (73%), E. Sativa (72%), C. dactylon (71%), M. vulgare (70%), B. papillosa (69%), T. indicum (68%), D. alba (66%), O. dillenii (61%), S. incanum (53%). Other plant extracts showed less than 50% mortality. A. melanoxylon, C. occidentalis and A. pungens were least toxic extracts showing 20-25% mortality (Figure 4).
Extracts of N. indicum constitute different alkaloids and triterpenoids which show anti-feedant, ovicidal, larvicidal and repellant activities against a wide range of insect pests including mosquitoes ; ; ; ; . Acetone and methanolic extracts of N. indicum at 0.02 to 0.03% concentrations showed significant mortality (more than 50%) of C. quinquefasciatus larvae ; ; . Similarly, W. coagulans and S. fruticosa constitute different alkaloids and phenols, and α-pinene and borneol, respectively ; and these plant extracts (10%) have shown to cause significant mortality (up to 63%) in Callosobruchus chinensis and up to 50% mortality in larvae of Culex pipiens . Our results are in line with the findings of Teressa et al. (2019) showing 60% mortality in Anopheles mosquito larvae by the extract of O. europea plant. Similarly, 0.03% hexane extract of A. capillus-veneris has been found determinant to Plutella xylostella (causing 80% mortality) and to Aphis craccivora (causing up to 70% mortality) .
Toxicity of indigenous flora of Soone Valley against O. obesus
In case of subterranean termites, the most toxic plant extracts were P. aphylla, Rhamnus spp., B. papillosa and T. indicum causing 89, 62, 52 and 50% termite mortality, respectively. Minimum average termite mortality was exhibited by the 10% extracts of M. vulgare, W. coagulans, P. oleracea and A. capillus-veneris (Figure 5).
The triterpenes isolated from the stems of P. aphylla showed antibacterial activity but insecticidal activity of this plant species has not tested against any insect pest. Acetone and ethanol extracts of Rhamnus dispermus caused significant mortality of peach trunk aphid (Pterochloroides persicae) ; . The methanolic extract of B. papillosa showed acaricidal activity against Rhipicephalus microplus . Similarly, different organic solvent derived and aqueous extracts of T. indicum have been shown significant effectiveness against armyworms (Mythimna separate), dengue vector mosquitos (Aedes aegypti) and many stored grain pests ; ; .
Conclusions and Recommendations
Toxicity bioassays conducted with methanolic extracts of forty indigenous plant species of Soone Valley revealed that M. longifolia caused highest mortality in D. citri, D. viscosa caused 70% mortality in S. litura, M. arenaria caused 87% mortality in C. quinquefasciatus and P. aphylla caused 89% mortality in O. obesus. So, for the further studies’ chemical characterization of these most effective plant extracts will be analyzed for their chemical constituents.
Acknowledgements
This study was financially supported by a research project (No. UOS/ORIC/2016/11) funded by the Office of Research, Innovation and Commercialization (ORIC), University of Sargodha. Moreover, authors acknowledge the technical assistance provided by Dr. Amin Ullah Shah of Department of Botany, University of Sargodha, regarding the identification of plant samples collected during the study.
Conflict of interest
The authors have declared no conflict of interest.
Figures
Figure 1:.
Main locations selected for the collection of indigenous flora of Soone Valley and surrounding Salt Range of Pakistan (cf: Table 1).
Figure 2:.
Percent mortality (mean ± SE) of citrus psyllid (D. citri) adults bioassayed with 10% acetone solutions of different indigenous plant species collected from Soone Valley and surrounding Salt Range.
Figure 3:.
Percent mortality (mean ± SE) of armyworm (S. litura) larvae bioassayed with 10% acetone solutions of different indigenous plant species collected from Soone Valley and surrounding Salt Range.
Figure 4:.
Percent mortality (mean ± SE) of mosquito (C. quinquefasciatus) larvae bioassayed with 10% acetone solutions of different indigenous plant species collected from Soone Valley and surrounding Salt Range.
Figure 5:.
Percent mortality (mean ± SE) of subterranean termite (O. obesus) worker termites bioassayed with 10% acetone solutions of different indigenous plant species collected from Soone Valley and surrounding Salt Range.
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