Efficacy of Citrullus colocynthis seed extract on Earias vittella, Fabricius, (Lepidoptera: Noctuidae): environment sustainable approach

Eficácia do extrato de semente de Citrullus colocynthis em Earias vittella Fabricius (Lepidoptera: Noctuidae): abordagem ambiental sustentável

U. A. Hassam A. Gulzar B. Rasool S. Zafar T. Younis M. Shakeel D. Khan S. Ullah S. Khaliq S. F. Ahmad M. Hafeez About the authors

Abstract

Earias vittellaFabricius, 1794 (Noctuidae: Lepidoptera) is deliberated to be one of the most destructive pests of cotton and okra vegetation in the world including Asia. The pest has established resistance to various synthetic insecticides. The use of bio-pesticide is one of the unconventional approaches to develop a vigorous ecosystem without harming non- target pests and beneficial natural insect fauna. In the present study, the toxicity levels of Citrullus colocynthis seed extract have been evaluated against the populations of E. vittellaunder standardized laboratory conditions. The toxic effects of C. colocynthis on development periods, protein contents and esterase activity of the life stages of E. vittella were also evaluated. The toxicity levels of methanol, ethanol, hexane, water and profenofos were evaluated on the 1st instar larvae of E. vittella. LC30 and LC80 concentrations exhibited the effectiveness of methanol-based C. colocynthis seed extract against 1st instar larvae of E. vitella. The enhanced larval and pupal periods were revealed in treated samples during the comparison with untreated samples. The intrinsic rate of increase, net reproductive rate in the LC30 and LC80 concentrations exposed larvae remained less than the control treatment. Fecundity, the esterase activity and protein contents were declined in LC30 and LC80 treated samples as compared to the control. The present findings suggest that C. colosynthis extracts based botanical insecticides are beneficial, ecosystem sustainable and can be integrated with insect management programs from environment safety perspective.

Keywords:
environment sustainable; plant extracts; ecosystem safety; esterase activity; life table parameters

Resumo

Earias vittella Fabricius, 1794 (Noctuidae: Lepidoptera) é considerada uma das pragas mais destrutivas de algodão e quiabo no mundo, incluindo a Ásia. Essa praga estabeleceu resistência a vários inseticidas sintéticos. O uso de biopesticidas é uma das abordagens não convencionais para desenvolver um ecossistema saudável sem prejudicar as pragas não alvo e a fauna natural benéfica de insetos. No presente estudo, os níveis de toxicidade do extrato de semente de Citrullus colocynthis foram avaliados nas populações de E. vittella em condições de laboratório padronizadas. Os efeitos tóxicos de C. colocynthis nos períodos de desenvolvimento, conteúdo de proteína e atividade esterase das fases de vida de E. vittella também foram avaliados. Os níveis de toxicidade de metanol, etanol, hexano, água e profenofós foram avaliados em larvas de 1º instar de E. vittella. As concentrações de LC30 e LC80 apresentaram eficácia do extrato de sementes de C. colocynthis à base de metanol contra larvas de 1º instar de E. vittella. Os períodos larval e pupal aumentados foram revelados nas amostras tratadas durante a comparação com as amostras não tratadas. A taxa intrínseca de aumento e a taxa reprodutiva líquida nas concentrações de larvas expostas LC30 e LC80 permaneceram menores do que o tratamento controle. A fecundidade, a atividade da esterase e o conteúdo de proteína diminuíram nas amostras tratadas com LC30 e LC80 em comparação com o controle. As presentes descobertas sugerem que os extratos de C. colocynthis à base de inseticidas botânicos são benéficos, sustentáveis ​​para o ecossistema e podem ser integrados com programas de manejo de insetos do ponto de vista da segurança ambiental.

Palavras-chave:
meio ambiente sustentável; extratos vegetais; segurança do ecossistema; atividade da esterase; parâmetros da tabela de vida

1. Introduction

Spotted bollworm, Earias vittella Fabricius, 1794 (Noctuidae: Lepidoptera) is a global, polyphagous and most damaging pest of many economically important crops with wide host range which includes cotton, okra, hollyhock, China rose, shoe flower, sonchal and various other malvaceous plants (Syed et al., 2011SYED, T.S., ABRO, G.H., KHANUM, A. and SATTAR, M., 2011. Effect of host plants on the biology of Earias vittella (F.) (Noctuidae: Lepidoptera) under laboratory conditions. Pakistan Journal of Zoology, vol. 1, pp. 43.). Spotted bollworm caused direct damage to fruiting bodies of cotton, Gossypium hirsutum and okra, Abelmoschus esculentus (Ahmad and Arif, 2009AHMAD, M. and ARIF, M.I., 2009. Resistance of Pakistani field populations of spotted bollworm Earias vittella (Lepidoptera: Noctuidae) to pyrethroid, organophosphorus and new chemical insecticides. Pest Management Science, vol. 65, no. 4, pp. 433-439. http://dx.doi.org/10.1002/ps.1702. PMid:19165729.
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; Rahman et al., 2013RAHMAN, M.M., UDDIN, M.M. and SHAHJAHAN, M., 2013. Management of okra shoot and fruit borer, Earias vittella (F.) using chemical and botanical insecticides for different okra varieties. International Research Journal of Applied Life Sciences, vol. 2, pp. 1-9.). The larvae not only attack bolls and fruits though also damage the shoots, buds and flowers (Aziz et al., 2012AZIZ, M.A., HASAN, M.U., ALI, A. and IQBAL, J., 2012. Comparative efficacy of different strategies for management of spotted bollworms, Earias spp. on Okra, Abelmoschus esculentus (L.). Moench. Pakistan Journal of Zoology, vol. 44, pp. 1203-1208.). This notorious pest remained active throughout the year and at least 6 to 8 generations are observed each year. This pest causes up to 40% and 41.6% losses in seed cotton and okra, respectively whereas loss in cotton yield may reach up to 50% during severe infestation and larvae alone causes a damage between 50 to 70% including deformed fruits and low quality (Hassan and Ansari, 2010HASSAN, W. and ANSARI, M., 2010. Evaluation of some insecticides against spotted bollworms Earias vitella (F.) on different Okra cultivars. Trends in Biosciences, vol. 3, pp. 41-44.; Tanni et al., 2019TANNI, A.S., MALEQUE, M.A., CHOUDHURY, M.A.R., KHAN, A.U. and KHAN, U.H.S., 2019. Screening of exotic okra genotypes to explore breeding materials for developing pest resistant and high yielding okra variety. Bangladesh J. Entomol., vol. 29, pp. 17-26.).

Synthetic pesticides are the primary tools to manage insect pests of agriculture and veterinary. This sole dependence on chemicals, particularly in vegetables is not desirable due to health hazards. Furthermore, the injudicious exercise of chemicals has twisted numerous problems that jeopardize their efficiency further causing environmental pollution and intimidation to all biological and beneficial fauna (Hashmi, 1994HASHMI, R.A. 1994. Insect Pest Management. Islamabad: Cereal and Cash Crops of Pakistan Agriculture Research Council. 317 p.). Recent years the indiscriminate use of insecticides leads to the development of resistance a big challenge for chemical control in insects (Ahmad et al., 2019AHMAD, M., RASOOL, B., AHMAD, M. and RUSSELL, D.A., 2019. Resistance and synergism of novel insecticides in field populations of cotton bollwormHelicoverpa armigera(Lepidoptera: Noctuidae) in Pakistan. Journal of Economic Entomology, vol. 112, no. 2, pp. 859-871. http://dx.doi.org/10.1093/jee/toy409. PMid:30668865.
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; Gulzar and Wright, 2015GULZAR, A. and WRIGHT, D.J., 2015. Sub-lethal effects of Vip3A toxin on survival, development and fecundity of Heliothis virescens and Plutella xylostella. Ecotoxicology, vol. 24, no. 9, pp. 1815-1822. http://dx.doi.org/10.1007/s10646-015-1517-6. PMid:26162322.
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). It has been reported that many insect species have developed resistance against various insecticides (Whalon, 2008WHALON, M. 2008. Analysis of global pesticide resistance in arthropods. In M.E. WHALON, D. MOTA-SANCHEZ, and R.M. HOLLINGWORTH, eds. Global pesticide resistance in arthropods. Wallingford: CABI. http://dx.doi.org/10.1079/9781845933531.0005.
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). The increasing concern on the development of resistance and restricted usage of pesticides has encouraged the application of bio-rational and botanical insecticides (Akhtar et al., 2012AKHTAR, Y., ISMAN, M.B., NIEHAUS, L.A., LEE, C.H. and LEE, H.S., 2012. Antifeedant and toxic effects of naturally occurring and synthetic quinones to the cabbage looper, Trichoplusiani. Crop Protection, vol. 31, no. 1, pp. 8-14. http://dx.doi.org/10.1016/j.cropro.2011.09.009.
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).

Botanicals or bio-pesticides can be an effective and advantageous replacement to commercial pesticides leading towards integrated pest approaches due to target-specific, eco-friendly, low number of applications and higher acceptable properties. Phytochemicals extracted from the plant parts by using different solutions have acted as toxicants, repellents and growth regulators (Ahmad et al., 2021AHMAD, S.F., GULZAR, A., TARIQ, M. and ASAD, M.J., 2021. Field evolved resistance inEarias vittella(Lepidoptera: Noctuidae) from Punjab, Pakistan against commercial formulations ofBacillus thuringiensis kurstaki. Journal of Economic Entomology, vol. 114, no. 5, pp. 2204-2213. http://dx.doi.org/10.1093/jee/toab137. PMid:34268576.
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; Amer and Mehlhorn, 2006AMER, A. and MEHLHORN, H., 2006. Larvicidal effects of various essential oils against Aedes, Anopheles and Culex larvae (Diptera, Culicidae). Parasitology Research, vol. 99, no. 4, pp. 466-472. http://dx.doi.org/10.1007/s00436-006-0182-3. PMid:16642386.
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; Choudhury et al., 2021CHOUDHURY, M.A.R., MONDAL, M.F., KHAN, A.U., HOSSAIN, M.S., AZAD, M.O.K., PRODHAN, M.D.H., UDDAIN, J., RAHMAN, M.S., AHMED, N., CHOI, K.Y. and NAZNIN, M.T., 2021. Evaluation of biological approaches for controlling shoot and fruit borer (Earias vitella F.) of okra grown in peri-urban area in Bangladesh. Horticulturae, vol. 7, no. 1, pp. 7. http://dx.doi.org/10.3390/horticulturae7010007.
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). Synthesized chemical compounds produced by plants have the potentials to way forward to integrate insect pest control methods (Tabashnik, 1994TABASHNIK, B.E., 1994. Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology, vol. 39, no. 1, pp. 47-79. http://dx.doi.org/10.1146/annurev.en.39.010194.000403.
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). Plants have the aptitude to produce various bioactive substances and tributary metabolites such as alkaloids, glycosides, carbohydrates, terpenoids, tannins, phenols, flavonoids and sitosterols (Georges et al., 2008GEORGES, K., JAYAPRAKASAM, B., DALAVOY, S.S. and NAIR, M.G., 2008. Pest-managing activities of plant extracts and anthraquinones from Cassia nigricans from Burkina Faso. Bioresource Technology, vol. 99, no. 6, pp. 2037-2045. http://dx.doi.org/10.1016/j.biortech.2007.02.049. PMid:17478091.
http://dx.doi.org/10.1016/j.biortech.200...
; Mann, 1978MANN, J. 1978. Secondary metabolism. London: Oxford University Press. 154 p.). These chemical components of plants are necessary for the actual value of mythological cures of entomological fauna. These components are extensively utilized in agriculture, veterinary scientific researches and numerous diversified arenas (Vasu et al., 2009VASU, K., GOUD, J.V., SURYAM, A. and SINGARA, C.M.A., 2009. Biomolecular and phytochemical analysis of three aquatic angiosperms. African Journal of Microbiological Research, vol. 3, no. 8, pp. 418-421.). This plant-based stuff derived from stems, leaves, twigs, flowers, roots and fruiting portions has developed the part pesticides since ancient times (Cragg and Newman, 2001CRAGG, G.M. and NEWMAN, D.J., 2001. Natural product drug discovery in the next millennium. Journal of Pharmaceutical Biology, vol. 39, suppl. 1, pp. 8-17. PMid:21554167.).

Citrullus colocynthis is generally recognized as the colocynth, bitter apple, desert gourd and viny plant (Cucurbitaceae) intrinsic to the Asia and Mediterranean arena and well established in the temperate areas of Pakistan. Many active chemical compounds (cucurbitacin A, B, C, D, E, I, J, K, L, glucosides I, L and flavonoids) from C. colocynthis have been described in previous studies (Delazar et al., 2006DELAZAR, A., GIBBONS, S., KOSARI, A.R., NAZEMIYEH, H., MODARRESI, M., NAHAR, L. and SARKER, S.D., 2006. Flavone C-glycosides and cucurbitacin glycosides from Citrullus colocynthis. Journal of Pharmaceutical Sciences, vol. 14, pp. 109-114.; Sturm and Schneider, 2009STURM, S. and SCHNEIDER, P., 2009. Analysis of Citrullus colocynthis cucurbitacin derivatives with HPLC-SPE-NMR. Scientia Pharmaceutica, vol. 77, no. 1, pp. 254. http://dx.doi.org/10.3797/scipharm.oephg.21.PO-55.
http://dx.doi.org/10.3797/scipharm.oephg...
). Isolated compounds exhibited diverse actions against insect pests especially the compound cucurbitacin B is responsible for reduced oviposition and anti-feeding activity (Seenivasan et al., 2004SEENIVASAN, S.P., JAYAKUMAR, M., RAJA, N. and IGNACIMUTHU, S., 2004. Effect of bitter apple, Citrullus colocynthis (L.) Schrad seed extracts against pulse beetle, Callosobruchus maculatus (F.) (Coleoptera: bruchidae). Entomology Trivan, vol. 29, pp. 81-84.;Tallamy et al., 1997TALLAMY, D.W., STULL, J., EHRESMAN, N.P., GORSKI, P.M. and MASON, C.E., 1997. E. Cucurbitacins as feeding and oviposition deterrents to insects. Environmental Entomology, vol. 26, no. 3, pp. 678-683. http://dx.doi.org/10.1093/ee/26.3.678.
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) and these are also exploited as an abortifacient (Madari and Jacobs, 2004MADARI, H. and JACOBS, R.S., 2004. An analysis of cytotoxic botanical formulations used in the traditional medicine of ancient Persia as abortifacients. Journal of Natural Products, vol. 67, no. 8, pp. 1204-1210. http://dx.doi.org/10.1021/np049953r. PMid:15332833.
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). These chemical compounds can manage and control various insect pests (Ahmad, 2007AHMAD, M., 2007. Insecticide resistance mechanisms and their management in Helicoverpa armigera (Hub.) a review. Journal of Agricultural Research, vol. 45, pp. 319-335.). It's almost two millennia that plant-mediated pesticides are being used in agriculture (Thacker, 2002THACKER, J.R., 2002. An introduction to arthropod pest control. Cambridge: Cambridge University Press.).

Many investigators explored the effects of different plant extracts on the life span, fertility, fecundity and physiology of insects (Baskar et al., 2015BASKAR, K., IGNACIMUTHU, S. and JAYAKUMAR, M., 2015. Toxic effects of Couroupita guianensis against Spodoptera litura (Fab.) (Lepidoptera: noctuidae). Neotropical Entomology, vol. 44, no. 1, pp. 84-91. http://dx.doi.org/10.1007/s13744-014-0260-7. PMid:26013016.
http://dx.doi.org/10.1007/s13744-014-026...
; Pavunraj et al., 2016PAVUNRAJ, M., BASKAR, K., PAULKUMAR, K., JANARTHANAN, S. and RAJENDRAN, P., 2016. Antifeedant activity of crude extracts and fractions isolated from Catharanthus roseus leaf against spotted bollworm. Phytoparasitica, vol. 44, no. 3, pp. 419-422. http://dx.doi.org/10.1007/s12600-016-0521-6.
http://dx.doi.org/10.1007/s12600-016-052...
). C. colocynthis leaves extract with ethyl acetate, benzene, petroleum ether and methanol was commenced very effectively in populations of mosquito, C. quinquefasiatus (Mullai and Jebanesan, 2007MULLAI, K. and JEBANESAN, A., 2007. Larvicidal, ovicidal and repellent activities of the leaf extract of two cucurbitacious plants against filarial vector Culex quinquefasciatus (S.) (Diptera: culicidae). Tropical Biomedicine, vol. 24, no. 1, pp. 1-6. PMid:17568371.).

The present study investigated the lethal and sub-lethal effects of the methanol-based extracts of C. colocynthis various biological and physiological factors of E. vittella.

2. Materials and Methods

2.1. Insect culture and sampling

Laboratory culture of spotted bollworm (E. vittella) was established from the larvae collected from okra and cotton fields in the surrounding three districts (Rawalpindi, Taxila and Attock) of Punjab province, Pakistan for the continuous three years (2018-2020). The infested pods from the fields were transferred into transparent plastic jars (20 cm length and 10 cm wide) and were retained within standardized conditions (27 ± 2 ̊C, 60 ± 5% R.H., 16 hours light, 08 hours dark). Fresh Okra (Abelmoschus esculentus) fruits were utilized for sustaining the insect culture (Al-Mehmmady, 2000AL-MEHMMADY, R.M., 2000. Biological studies on the okra moth, Earias vittella (F.) (Lepidoptera: Noctuidae) in Jeddah, Saudi Arabia. Research Bulletin, vol. 96, pp. 5-18.). Fresh okra fruits were thoroughly washed in clean water and desiccated before feeding to the neonates, and latterly these were cut into 0.5-1.0 cm pieces; 4-5 larvae were released per piece and placed in the plastic container. The food was replaced daily till pupation. The larvae were carefully removed from the okra pods and the excreta were cleaned. The pupae were shifted to another plastic jar (10 cm length and 5 cm width) until adult emergence. The emerged adults were shifted to adult cages (length x height x width: 38 x 34 x 30 cm) and nourished with 10% sugar solution. Nappy strips were provided in cages for oviposition and these strips were replaced regularly after observation of eggs.

2.2. Collection of seed and solvent extraction

C. colosynthis plant seeds were collected from various crop fields throughout the temperate regions of the Punjab province, Pakistan. Impurities from the collected seeds were removed manually and kept for drying under room temperature (Memon et al., 2003MEMON, U., BROHI, A.H., AHMED, S.W., AZHAR, I. and BANO, H., 2003. Antibacterial screening of Citrullus colocynthis. Pakistan Journal of Pharmaceutical Sciences, vol. 16, no. 1, pp. 1-6. PMid:16414561.). The desiccated seeds were crushed in the shape of elusive powder with an automatic grinder. Fifty grams of the ground seeds were drenched in 100 ml of methanol, ethyl acetate, hexane and ethanol discretely for 24 h for each solvent extract separately. The mixture was stirred for 1 h and kept below 4°C in the refrigerator for 2 days. These refrigerated mixtures were stirred again for 1 h. These mixtures were filtered twice through filter paper and finally dissolved in 10 ml of their particular solvent to be conserved as a stock solution.

2.3. Phytochemical analysis

Different solvent extracts (methanol, ethanol and hexane) were utilized to carry out the preliminary phytochemical analysis of C. colocynthis with already standardized methodologies to recognize the constituents (Harbone, 1973HARBONE, J.B. 1973. Phytochemical methods. London: Chapman and Hall. 113 p.).

2.4. Bioassays

Through the diet emersion method, bioassays were performed and toxicity was measured for 1st larval instar larvae of spotted bollworm. Different concentrations of C. colosynthis were prepared using different solvents (methanol, ethanol, hexane). Fresh okra fruits were dipped separately in each concentration for 10 seconds and then desiccated for 10 minutes at room temperature. Five okra fruits were used in one replication. Two 1st instar larvae were released on each okra pod in all replications treated with different concentrations. Four replications were performed for each treatment. The control treatment was served with purified distilled water. The entire treated larvae were kept under standardized lab conditions (25 ± 2 °C; RH 65 ± 5%, 16 hours light, 08 hours dark) and datasets were recorded regarding larval mortality at 72 hours.

2.5. Sub-lethal effects of plant seed extracts on biological on biological parameters of Earias vittella

Age-stage, two-sex life table theory was considered to estimate the stuff of sub-lethal concentrations on the biological factors of E. vittella. For life table study, 210 eggs were used, which were collected after 24 hours of deposition by females of the laboratory population. Three treatments (control, LC30 and LC80) of methanolic extract were prepared for this experiment. Seventy eggs were treated with each treatment. Each egg in an individual Petri dish was reflected as a single replicate (Zhang et al., 2015ZHANG, R., JANG, E.B., HE, S.C.J. and CHEN, J., 2015. Lethal and sub-lethal effects of cyantraniliprole on Bactrocera dorsalis (Hendel) (Diptera: tephritidae). Pest Management Science, vol. 71, no. 2, pp. 250-256. http://dx.doi.org/10.1002/ps.3791. PMid:24700426.
http://dx.doi.org/10.1002/ps.3791...
; Chi and Yang, 2003CHI, H. and YANG, T.C., 2003. Two-sex life table and predation rate of Propylaea japonica Thunberg (Coleoptera: Coccinellidae) Fed on Myzus persicae (Sulzer) (Homoptera: Aphididae). Environmental Entomology, vol. 32, no. 2, pp. 327-333. http://dx.doi.org/10.1603/0046-225X-32.2.327.
http://dx.doi.org/10.1603/0046-225X-32.2...
). All petri dishes were kept under standardised conditions. The egg hatching data were recorded daily and the neonates from control, LC30, LC50 and LC80 were shifted on the okra pods. The larval development was observed daily and fresh okra pods were provided after each instar. Pupae were removed and placed in new petri dishes until adult emergence. Then, the newly emerged adults were paired (one male and one female) and transferred to an individual plastic container for oviposition. The adults were patterned for oviposition and transported to fresh containers for egg-laying daily. The fecundity (%) and survival rate of the adults were assessed until the death of the adults.

2.6. Assays for esterase activity and protein content

The general esterase activity was determined through the method proposed by Van-Asperen (1962). In this experiment, 10 mM of α-naphthyl-acetate (αNA) and β-naphthyl-acetate (βNA) were treated as substrates. The frozen supernatant from the above treatments was transported to a fresh micro tube and phosphate buffer was added for making dilution. 1mM Fast Blue RR salt was also supplemented to this solution tube. The calculation regarding the absorbance was retained at 630 nm. Bovine Serum Albumin was utilized as a standard for the determination of the total protein contents (Bradford, 1976BRADFORD, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, vol. 72, no. 1-2, pp. 248-254. http://dx.doi.org/10.1016/0003-2697(76)90527-3. PMid:942051.
http://dx.doi.org/10.1016/0003-2697(76)9...
).

2.7. Data analysis

The LC values were calculated based on mortality data using R Statistical Software version 2.9.0 (R Development Core Team, 2018R DEVELOPMENT CORE TEAM, 2018. A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.) The datasets regarding different developmental stage periods, survival rate and fecundity were scrutinized with the help of model age-stage, two-sex life table, theory and software (Chi, 1988CHI, H., 1988. Life-table analysis incorporating both sexes and variable development rates among individuals. Environmental Entomology, vol. 17, no. 1, pp. 26-34. http://dx.doi.org/10.1093/ee/17.1.26.
http://dx.doi.org/10.1093/ee/17.1.26...
, 2021CHI, H., 2021. [viewed 20 July 2021]. Computer program for the age-stage, two-sex life table analysis [online]. Taichung, Taiwan: National Chung Hsing University. Available from: http://140.120.197.173/Ecology/Download/Twosex-MSChart.
http://140.120.197.173/Ecology/Download/...
). The means of the biological parameters were compared by using 100,000 bootstrap techniques to achieve stable standard error estimates (Huang and Chi, 2012HUANG, Y.B. and CHI, H., 2012. Age‐stage, two‐sex life tables of Bactrocera cucurbitae (C.) (Diptera: Tephritidae) with a discussion on the problem of applying female age‐specific life tables to insect populations. Insect Science, vol. 19, no. 2, pp. 263-273. http://dx.doi.org/10.1111/j.1744-7917.2011.01424.x.
http://dx.doi.org/10.1111/j.1744-7917.20...
). The curves for age-specific survival rate, life expectancy, fecundity and reproductive values were generated by using Sigma Plot 14.0. The net reproductive rate was calculated using the following Formula 1:

R 0 = x = 0 l x m x (1)

The intrinsic rate of increase (r) was calculated by using the iterative bisection method through Formula 2:

x=0erx+1lxmx=1 (2)

With age indexed from zero (Goodman, 1982GOODMAN, D., 1982. Optimal life histories, optimal notation, and the value of reproductive value. American Naturalist, vol. 119, no. 6, pp. 803-823. http://dx.doi.org/10.1086/283956.
http://dx.doi.org/10.1086/283956...
) the mean generation time (T) was calculated by the Formula 3:

T = I n R 0 r (3)

The Gross reproductive rate (GRR) was calculated by the Formula 4 as follow:

G R R = x = 0 m x (4)

The age-specific survival rate (lx) and age-specific fecundity (mx) were given as (Formula 5 and 6):

l x = j = 1 k s x j (5)
m x = j = 1 k s x j f x j j = 1 k s x j (6)

3. Results

3.1. Toxicity Bioassays

The Citrullus colosynthis plant seed extract prepared in diverse solvents (methanol, ethanol and hexane) was treated against immatures (1st instar) of E. vittella. The LC30, LC50 and LC80 values of methanol-based plant extract of C. colosynthis were calculated as (1.85, 4.60, 11.45), ethanol-based extract (3.29, 5.40, 8.85), hexane--based extract (3.57, 7.01, 13.78), profenofos (0.31, 1.74, 9.42) as positive control and water (3.06, 7.80, 19.89), respectively after 72 h of treatment (Table 1).

Table 1
Efficiency of C. colosynthis seed extracts in different solvents for 1st larval instar of E. vitella.

3.2. Lethal and sub-lethal effect of methanolic extract of C. colosynthis fruit on life tables of E. vittella

The larval development period was recorded from 1st instar to pupation stage of E. vittella treated with LC80 and LC30 as lethal and sub-lethal concentrations. The data of treated insects showed significant variation when compared with the untreated (Table 2, p˂0.001, df=2 F=83.26). The maximum hatching duration (4.26 days) was recorded in LC80 treatment, which was non-significant to LC30 treatment (4.07 days) but significant (Table 2, p˂0.001, df=2, F=107.8) to untreated ones (3.66 days). A significant variation was observed in the first to fifth larval instars. All larval instars show significant dissimilarities regarding duration of larval life (larva days) among lethal and sub-lethal treatments when compared with the untreated (Table 2, p˂0.001, df=2, F=233.4). Maximum larval duration (12.54 days) was recorded in LC80 treatment followed by LC30 (11.23 days) while minimum larval days were taken by the untreated larvae (11.03 days). Mean pupal duration was found to be significantly longer in larvae treated with LC80 and LC30 concentrations compared to the control (Table 2, p˂0.001, df=2, F=94.19). The solicitation of lethal and sub-lethal concentrations significantly enhanced the total developmental period of E. vittella from 1st instar to adult as compared to the untreated (Table 2, p˂0.001, df=2, F=118.2). Female longevity was affected more than male longevity and the maximum female longevity was recorded in the control treatment (12.7 days) which was significant to sub-lethal (LC30) and lethal (LC80) concentrations (Table 2, p˂0.001, df=2, F=174.7). While male longevity was not altered significantly between the applied treatments (Table 2, p˂0.001, df=2, F=41.23). Non-significant trends were observed between all the treatments in adult pre oviposition period (APOP) and total pre oviposition period (TPOP) of E. vittella (Table 2, p˂0.001, df=2, F=79.94).

Table 2
Life table parameters of E. vittella treated with sub-lethal concentrations of methanolic extract of C. colosynthis.

The average pupal weight of the insects exposed to lethal and sub-lethal concentrations was lower than the control treatment (Table 3, p˂0.001, df=2, F=204.1). The percent pupation after LC80 treatment (52.48) was less than LC30 (58.52) and control (91.75) treatments (Table 3, p˂0.001, df=2, F=11.93). The lethal and sub-lethal concentrations were recorded to reduce the percentage of adult emergence significantly with comparison to the control treatment (Table 3, p˂0.001, df=2, F=21.49).

Table 3
Mean biological parameters of E. vittella treated with lethal and sub-lethal concentrations of methanolic extract of C. colosynthis.

The application of a methanol-based extract of C. colosynthis at lethal, sub-lethal and control concentrations (67, 41 and 89) resulted in the reduction of the mating pair's success (Table 3, p˂0.001, df=2, F=20.05). A significant decrease in the fecundity egg/female was perceived laid by each female in the lethal and sub-lethal treated population with comparison to control (Table 2, p˂0.001, df=2, F=62.93). The hatchability percentage of eggs (viability) was also affected and reduced significantly in the lethal and sub-lethal treated populations when compared to the control treatment (Table 3, p˂0.001, df=2, F=266.81).

C. colosynthis plant extracts significantly altered the population parameters of the E. vittella (Table 4). To estimate the population parameters, the bootstrap method with 100,000 replicate was applied. The increased intrinsic rate was decreased by treating with both the concentrations of C. colosynthis plant extract (0.128 d-1 and 0.140 d-1 for LC80 and LC30 respectively) as compared with the untreated larvae (0.166 d-1). Similarly, the trend was exhibited in the finite rate of increase (λ), as the highest value for λ was observed in control larvae (1.181 d-1), which gradually decreases with an increase in concentration from LC30 to LC80 as 1.150 d-1 and 1.137 d-1 respectively. A significant decrease was also observed in the net reproductive rate (Ro) after treatment from being highest in control (94.542) to 76.714 and 61.228 offsprings/individual for LC30 and LC80 treated larvae, respectively. The highest Gross reproductive rate (GRR) was recorded for control larvae (183.42), while the lowest for LC80 treated larvae (136.77) progeny/individual which was both statistically different to each other. The mean generation time was prolonged in the treated larvae in comparison with the larvae of control treatment. Minimum mean generation time was taken by the control larvae (27.255 d-1), followed by LC30 treated larvae (30.967 d-1). The maximum days were recorded on LC80 treated larvae (31.917 d-1). The Sxj represents the age-stage survival rate, it shows the chances of afresh laid eggs to survive till (age x and stage j) as shown in (Figure 1). Significant variations were observed in the growth rate of the various entities in the population (Figure 1). The lethal and sub-lethal treatments show overlapping curves of the developmental stages as compared to control. Each developmental stage showed a different pattern of the peak curves for lethal and sub-lethal of C. colosynthis plant extract and control. The curve line for the male adults ends earlier (Figure 1) as compared to female adult lines. Survival rate (lx), age-specific fecundity (mx) and age-specific maternity (lxmx) were calculated for lethal and sub-lethal concentrations for E. vittella (Figure 2). A significant decline of lx curves was observed in the lethal and sub-lethal treated population much earlier than that in control. Higher peaks for fx curves were noted in control, while much lower fx curves were noted in LC80 and LC30 treated populations. The exj (life expectancy) curves varied significantly among the treated (LC80 and LC30) and untreated for E. vittella (Figure 3). The minimum life expectancy for eggs was observed on the lethal, followed by sub-lethal, while the maximum value of life expectancy for eggs was observed in the control. Reproductive rate (vxj) is defined as the measure of dedication to newly coming offspring in the future from age x to stage j (Figure 4). The contribution of males in the population to the next generation was not well defined; therefore the curve for males was not included. A decline was observed in the reproductive values when larvae were treated with LC80 and LC30 as compared to the untreated larvae. Maximum vxj was recorded on the untreated group, while the minimum was observed in the LC80 treated group.

Table 4
Effect of sub-lethal concentration of methanolic extract of C. colosynthis on the biological parameters of E. vittella.
Figure 1
Age-stage survival rate (Sxj) of E. vittella treated with LC30 and LC80 of C. colosynthis extract.
Figure 2
Survival rate (lx), Age-specific fecundity (mx) and age-specific maternity (lxmx) of E. vittella treated with LC30 and LC80 of C. colosynthis extract.
Figure 3
Life expectancy (exj) of E. vittella treated with LC30 and LC80 of C. colosynthis extract.
Figure 4
Age-stage specific reproductive value (Vxj) of E. vittella treated with LC30 and LC80 of C. colosynthis extract.

3.3. Total protein content and esterase activity of E. vittella treated with plant extract

Total protein content in E. vittella treated with lethal and sub-lethal deliberations of C. colosynthis plant extract were shortened to a significant level as compared to the untreated treatment (Table 5, p˂0.001, df=2, F=349.5). The average esterase enzyme activity in E. vittella treated with lethal and sub-lethal concentrations was significantly reduced when compared with the untreated control populations (Table 5, p˂0.001, df=2, F=1704.2).

Table 5
Esterase activities and total protein content in E. vitella in methanolic extract of C. colosynthis.

4. Discussion

In the present study, the presentation of lethal and sub-lethal deliberations of C. colosynthis seed mines significantly influences the developmental time, pupal weight, pupal percentage, adult emergence and adult longevity. The methanolic extract of C. colosynthis prolonged larval development, pupal developmental time as compared with the control. Ramzi et al. (2015)RAMZI, S., SAHRAGARD, A., JALALI SENDI, J. and AALAMI, A., 2015. Effect of Citrullus colocynthis (Cucurbitaceae) agglutinin on the life table parameters of Apomyelois ceratoniae (Lepidoptera: pyralidae). Journal of Crop Protection, vol. 5, no. 1, pp. 19-31. http://dx.doi.org/10.18869/modares.jcp.5.1.19.
http://dx.doi.org/10.18869/modares.jcp.5...
also described related results, when the caterpillars of Apomyelois ceratoniae were pickled with C. crenata as compared with the populace of control treatment, this difference might be the metamorphosis interruption grounds.

The auspicious results of C. colosynthis to control E. vittella might be due to the presence of compound cucurbitacin B and responsible for the reduced hatchability antifeedant activity (Tallamy et al., 1997TALLAMY, D.W., STULL, J., EHRESMAN, N.P., GORSKI, P.M. and MASON, C.E., 1997. E. Cucurbitacins as feeding and oviposition deterrents to insects. Environmental Entomology, vol. 26, no. 3, pp. 678-683. http://dx.doi.org/10.1093/ee/26.3.678.
http://dx.doi.org/10.1093/ee/26.3.678...
). The present study reported that C. colocynthis seed extract significantly affects the mating, fecundity and egg viability in E. vittella treated with lethal and sub-lethal concentrations. Such kind of results was also described by various researchers (D’Incao et al., 2012D’INCAO, M.P., GOSMANN, G., MACHADO, V., FIUZA, L.M. and MOREIRA, G.R., 2012. Effect of saponin extracted from Passiflora alata Dryander (Passifloraceae) on development of the Spodoptera frugiperda (S.) (Lepidoptera, Noctuidae). International Journal of Plant Research, vol. 2, pp. 151-159. http://dx.doi.org/10.5923/j.plant.20120205.03.
http://dx.doi.org/10.5923/j.plant.201202...
; Khani et al., 2013KHANI, M., AWANG, R.M., OMAR, D. and RAHMANI, M., 2013. Toxicity, antifeedant, egg hatchability and adult emergence effect of Piper nigrum (L.) and Jatropha curcas L. extracts against rice moth, Corcyra cephalonica (S.). Journal of Medicinal Plants Research, vol. 7, pp. 1255-1262.; Khosravi et al., 2011KHOSRAVI, R., SENDI, J.J., GHADAMYARI, M. and YEZDANI, E., 2011. Effect of sweet wormwood Artemisia annua crude leaf extracts on some biological and physiological characteristics of the lesser mulberry pyralid, Glyphodes pyloalis. Journal of Insect Science, vol. 11, pp. 156. http://dx.doi.org/10.1673/031.011.15601. PMid:22239100.
http://dx.doi.org/10.1673/031.011.15601...
). Lethal and sub lethal effects along with reduced fecundity and fertility rates were reported in Spodoptra frugiperda when treated with saponins extract, obtained fromPassiflora alata(D’Incao et al., 2012D’INCAO, M.P., GOSMANN, G., MACHADO, V., FIUZA, L.M. and MOREIRA, G.R., 2012. Effect of saponin extracted from Passiflora alata Dryander (Passifloraceae) on development of the Spodoptera frugiperda (S.) (Lepidoptera, Noctuidae). International Journal of Plant Research, vol. 2, pp. 151-159. http://dx.doi.org/10.5923/j.plant.20120205.03.
http://dx.doi.org/10.5923/j.plant.201202...
). The extract of Piper nigrum and Jatropha curcas reduced the egg viability and adult emergence of C. cephalonica with control comparison (Khani et al., 2013KHANI, M., AWANG, R.M., OMAR, D. and RAHMANI, M., 2013. Toxicity, antifeedant, egg hatchability and adult emergence effect of Piper nigrum (L.) and Jatropha curcas L. extracts against rice moth, Corcyra cephalonica (S.). Journal of Medicinal Plants Research, vol. 7, pp. 1255-1262.).

The intrinsic rate of natural increase (rm) provides an estimate of the growth probability of insect populations (Rabinovich, 1972RABINOVICH, J.E., 1972. Vital statistics of Triatominae (Hemiptera: Reduviidae) under laboratory conditions. I. Triatoma infestans Klug. Journal of Medical Entomology, vol. 9, no. 4, pp. 351-370. http://dx.doi.org/10.1093/jmedent/9.4.351. PMid:4559948.
http://dx.doi.org/10.1093/jmedent/9.4.35...
) which can offer great perception into the population growth of species besides other life-history factors. Whereas it is also conceivable to estimate the net rate of reproduction (Ro) dependency of natural increase in the intrinsic rate principally based on productiveness, % hatching, growth and adult emergence (Khan et al., 2013KHAN, F.Z.A., SAGHEER, M., HASAN, M., SAEED, S., ALI, K., GUL, H.T., BUKHARI, S.A. and MANZOOR, S.A., 2013. Toxicological and repellent potential of some plant extracts against stored product insect pest, Tribolium castaneum (H.) (Coleoptera: tenebrionidae). International Journal of Biosciences, vol. 3, no. 9, pp. 280-286. http://dx.doi.org/10.12692/ijb/3.9.280-286.
http://dx.doi.org/10.12692/ijb/3.9.280-2...
; Saeed et al., 2010SAEED, M., KHAN, H., KHAN, M.A., SIMJEE, S.U., MUHAMMAD, N. and KHAN, S.A., 2010. Phytotoxic, insecticidal and leishmanicidal activities of aerial parts of Polygonatum verticillatum. African Journal of Biotechnology, vol. 8, pp. 9.). Aiming the purpose, the above mentioned divergent life-history abilities might simulate the population increase rate of E. vittella. The intrinsic rate of natural increase (rm) was significantly declined in lethal and sub-lethal concentrations as compared with control treatment. These findings are also described by Hafeez et al. (2019)HAFEEZ, M., JAN, S., NAWAZ, M., ALI, E., ALI, B., QASIM, M., FERNÁNDEZ-GRANDON, G.M., SHAHID, M. and WANG, M., 2019. Sub-lethal effects of lufenuron exposure on spotted bollworm Earias vittella (F.): key biological traits and detoxification enzymes activity. Environental Science and Pollution Research International, vol. 26, no. 14, pp. 14300-14312. http://dx.doi.org/10.1007/s11356-019-04655-8. PMid:30864030.
http://dx.doi.org/10.1007/s11356-019-046...
in a way that the intrinsic rate of increase was significantly changed due to lethal and sub-lethal concentrations of lufenuron whereas present study tested plant extracts also showed the comparable results. Correspondingly, the average generation time was significantly protracted in the treated population equal to the mean generation time of the untreated population. The escalation was observed in the mean generation time of S. litura when treated with different doses of imidacloprid (Abbas et al., 2012ABBAS, N., SHAD, S.A. and RAZAQ, M., 2012. Fitness cost, cross resistance and realized heritability of resistance to imidacloprid in Spodoptera litura (Lepidoptera: noctuidae). Pesticide Biochemistry and Physiology, vol. 103, no. 3, pp. 181-188. http://dx.doi.org/10.1016/j.pestbp.2012.05.001.
http://dx.doi.org/10.1016/j.pestbp.2012....
). Our results exhibit that parameters of the life table of E. vittella were adversely transformed with the lethal and sub-lethal concentrations of C. colocynthis plant extracts. A significant change was found in the Sxj, which decreased in the treated population compared to the untreated population. fxj and mx were also found to be decreased in the lethal treated population as compared to the control population. A measure of the influence of new individuals in population growth (exj) declined sharply in second larval instars in the lethal and sub-lethal treated population. The methanolic extract of C. colosynthis significantly reduced the esterase activities in larvae of E. vittella. The reduction in the esterase activity which is a vital detoxifying mechanism may indications to a substantial control of various insect pests (War et al., 2014WAR, A.R., PAULRAJ, M.G., HUSSAIN, B., AHMAD, T., WAR, M.Y. and IGNACIMUTHU, S., 2014. Efficacy of a combined treatment of neem oil formulation and endosulfan against Helicoverpa armigera (Hub.) (Lepidoptera: noctuidae). International Journal of Insect Science, vol. 6, pp. IJIS.S13608. http://dx.doi.org/10.4137/IJIS.S13608.
http://dx.doi.org/10.4137/IJIS.S13608...
). Equivalent results about the retarded esterase activity due to plant extract in insects were perceived (Khosravi et al., 2011KHOSRAVI, R., SENDI, J.J., GHADAMYARI, M. and YEZDANI, E., 2011. Effect of sweet wormwood Artemisia annua crude leaf extracts on some biological and physiological characteristics of the lesser mulberry pyralid, Glyphodes pyloalis. Journal of Insect Science, vol. 11, pp. 156. http://dx.doi.org/10.1673/031.011.15601. PMid:22239100.
http://dx.doi.org/10.1673/031.011.15601...
). Furthermore, by applying the C. colocynthis extracts on 1st larval instar of E. vittella reduction in total protein contents was observed. Similar reduction in the activity of α-amylase and deterioration of protease was observed when compared with the control in Glyphodes pyloalis (Khosravi et al., 2011KHOSRAVI, R., SENDI, J.J., GHADAMYARI, M. and YEZDANI, E., 2011. Effect of sweet wormwood Artemisia annua crude leaf extracts on some biological and physiological characteristics of the lesser mulberry pyralid, Glyphodes pyloalis. Journal of Insect Science, vol. 11, pp. 156. http://dx.doi.org/10.1673/031.011.15601. PMid:22239100.
http://dx.doi.org/10.1673/031.011.15601...
). The decrease in protein content might be due to the interruption intention in ATP synthesis. These insecticidal activities might be due to individual efficacy or the synergistic action of biological compounds present in these plants.

5. Conclusion

The methanol extract of C. colosynthsis displayed toxic properties on the development and survival of E. vittella. The present results suggested that plant extract-based control measures may be integrated into the pest management programs with special emphasis on the environmental tactics for ecosystem safety.

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Publication Dates

  • Publication in this collection
    07 Jan 2022
  • Date of issue
    2024

History

  • Received
    21 July 2021
  • Accepted
    25 Oct 2021
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