Indian Journal of Entomology 83(2021) Online published Ref. No. e20158 DoI No.: 10.5958/0974-8172.2020.00220.5

POTENTIAL CONTROL AGENTS AGAINST RED COTTON BUG KOENIGII- A REVIEW

Mohd Hussain, Nassreen F Kacho1*, Snigdha Mohan2 and Altaf H Mir3

Department of Zoology, University of Ladakh, Ladakh 194101, UT Ladakh 1SKUAST-K, KVK-Kargil, Kargil 194103, UT Ladakh 2I.P. extension, Patparganj, Delhi 110092; 3Department of Zoology, University of Kashmir, Kashmir 190006, UT Jammu and Kashmir *Email: [email protected] (corresponding author)

ABSTRACT

Dysdercus Koenigii, also known as red cotton bug or cotton stainer is one of the important cotton pests. It occurs in countries like China, India, Pakistan, Afghanistan, USA, and Florida, etc. It is a major pest of cotton and other malvaceous and non-malvaceous plants. It is being controlled with insecticides, but these are not safe and ecofriendly. This review highlights various chemical, botanical and biological control agents that have some potential as control agent for this pest.

Key words: , chemical control, biological control, botanical insecticides, IPM

Dysdercus spp. is commonly known as red cotton et al., 2013; Federici, 2007). This review enlists all bug (RCB) or cotton stainer. It belongs to the family the control agents including botanical insecticides and under Hemipteraand class . It is biological control agents which can be used in IPM of a well-known pest of cotton (Sprenkel, 2000), this pest. Google and Research gate searches were made (Tomas and Gajete, 2008), legumes and red gram (Singh using key words, and the research articles and books and Singh, 1978), Portia tree (Peter and Sivasothi, 1999) published in recognized journals and publishers were and orange (Hubbard, 1885). It is widely distributed taken into account. and known from India (Kapur, 1956; Mohan et al., 2010; Verma, 2012), Pakistan (Shah, 2014), Florida Insecticides (Mead, 1966), Brazil (Schaefer, 1998), Philippines Chemical insecticides are widely used in controlling (Encarnacion, 1970) and US (Hubbard, 1885). It is this pest. These are very cheap and easily available, known as cotton stainer and its name derived from the and therefore, it is also known as layman weapon. habit of staining cotton balls with indelible brownish- However, these are not ecofriendly, cause water, air yellow lint (Mead, 1966). It is a sap sucking pest which and soil pollution, kills natural enemies and affect sucks the sap of the plant. In India, it is found in Gujarat, health of human and other (Mahmood et al., Uttar Pradesh, Bihar, Madhya Pradesh and Tamil Nadu 2016; Mohapatra et al., 1995; Özkara, et al., 2016). (Kapur, 1956). There are two species of Dysdercus (D. A good number of researches have been done on the koenigii and D. cingulatus) which cause loss in cotton. effect of chemicals on the Dysdercus spp. Sehgal and This insect pest is hemimetabolous, life cycle consists Maheshwari (1974) studied the effect of different of egg, five nymphal stages and adult. Both nymph and concentrations of tetra ethylene pentamine (TEPA) on adults damage the palnts, and in cotton, these prefer D. koenigii and observed 100% sterility with a minimum to feed on the seed within developing bolls leaving dose of 0.5µg/ nymph in the third and fourth instar. a stain on lint. Feeding by puncturing flower buds Ahmad (1979) reported that D. cingulatus developed or young bolls causes a reduction in size or the boll resistance to the chemical insecticide like HMAC may abort and drop to the ground. This results in the {1,6-Hexamethylene bis (1-aziridine carboxamide)} reduction of cotton plants’ market value. Farmers use a after 4th generation. Sinha (1990) revealed the effect wide range of insecticide to control this pest, but these of parathion-methyl on nymphs and adults. Rizwan- insecticides are not ecofriendly (Mahmood et al., 2016). Ul-Haq et al. (2006) noted that with the treatment of Use of botanical insecticides and biological control are endosulfan 35EC and deltaphose 350+ 10EC on the recommended as these are safe and ecofriendly (Kareru D. koenigii, the total haemocyte count significantly 2 Indian Journal of Entomology 83(2021) Online published Ref. No. e20158 increased (19123 and 18068 cells/ mm3, respectively) Prabhu and John (1975) were the first who had tested just after application; and it decreased (10531 and the effects of plant extract on the Dysdercus sp. (Table 11804 cells/ mm3, respectively) after 30 min and 2). They studied the effect of acetone extracts of five again (8603 cells/ mm3) after one hour of application plants on the newly moulted last and 5th instar and found compared to the normal (17000 cells/ mm3). In the case that there is a direct effect on the ovarian development. of differential haemocyte count, there was a decrease Azadirachtin is a very important plant extract, isolated in % of plasmatocytes, granulocytes, prohaemocytes, from neem plant A. indica which has been used to oenocytoids and spherulocytes, compared to the normal. control various types of pests for a long time. There It is also true in the case of penfluron (Prakash et al., is a direct effect of neem extract on the physiology 2007) and acephate and organophosphorus insecticides and development of D. koenigii. This phytochemical (Qamar and Jamal, 2009). when applied to the red cotton bug causes prolonged development, wing deformities, unplasticisation of In a recent study, Sarwar et al. (2018) evaluated the wing lobes, development of wingless adult and larval effects of insecticides viz. imidacloprid, deltamethrin, mortality (Koul, 1984; Schmutterer, 1990; Yousuf et al., lamdacyhalothrin, gammacyhalothrin and cyfluthirn 2013). Rao and Gujar (1995) evaluated the toxicity of on the total and differential populations of circulating two plant extracts (plumbagin and juglone) on the egg of haemocytes in adults of D. koenigii and found that D. koenigii and observed toxicity against different age chlorpyriphos was more effective and resulted in of eggs with LC50 ranging from 0.0044 to 0.0066% and significant alterations in total haemocyte counts and proved their use as ovicide in control. Artimicia annua differential haemocyte. Verma et al. (2012) studied oil is a very important botanical and has a direct effect effects on D. koenigii and found that all the chemicals on the development and reproduction of . Rao were significantly superior over control in reducing et al. (1999) found that it causes 100% mortality after incidence; and treatment with imidacloprid 0.007% 48 hr of its application @1.0µl/ nymph. It also caused proved to be the most effective followed by dimethoate nymphal- adult intermediate and deformities in adult 0.03% with two times application of 15 days intervals. forms. Therefore, A. annua oil has both insecticidal and Yousuf et al. (2012) studied the toxicity of chlorpyriphos insect growth regulator (IGR) properties. Chowdhury and λ-cyhalotrhin also proved that these are lethal at and Walia (2000) reported that turmeric constituents 0.0625% and 0.2%, respectively. Rafiq et al. (2014) (dibutyl curcumic-I), showed growth-inhibiting with 18 synthetic chemicals on the D. koenigii, found and insecticidal activity against D. koenigii nymph. that alphacypermethrin 5EC (pyrethroid) proved to be Nicotinyl is an important botanical, which has been most effective followed by deltamethrin 2.5EC (93.8%), used in insect pest control for a long time. Rizwan-ul- cypermetrin 10EC (78.7%) and lamdacyhalothrin Haq et al. (2005) had observed that the two nicotinyl 2.5 EC (70%) after 24 hr of treatment. Akhtar et al. insecticides acetamiprid 20% SL and imidacloprid (2016) and Saeed et al. (2016) studied the toxicity of 25WP have a direct effect on the haemocyte count of insecticides on D. koenigii and found that chlorpyriphos RCB; the total haemocyte count (THC) increased soon 40EC was highly toxic followed by profenophos and after the treatment of nicotinyl insecticides while after deltamethrin; whereas lufenuron, chlorfenapyr and half an hour THC decreased and again increased after methomyl 40SP showed less toxicity. These chemicals one hour. Kodandaram et al. (2008) tested anonin 1%, had been applied by two methods viz., flooding and imidacloprid 17.8%, karanjin 2%, achook 0.15% and foliar application methods, of which earlier method is econeem1%, and observed that anonin has high toxicity very effective. Jameel et al. (2017) studied the toxicity as seen by dry film method; in the seed dip method too of thiamethoxam (0.002, 0.004, 0.006 and 0.008%) in anonin has high toxicity. All these botanicals act as th laboratory condition on the 4 instar and proved that it insect growth regulators. is a potential control agent (Table 1). Sontakke et al. (2013) reported the effect of Botanicals Ailanthus excelsa on the related species of Dysdercus Botanicals are naturally occurring chemicals cingulatus and found 95% repellency. Colocasia extracted from plants. Azadirachta indica (neem) is esculenta is a herbaceous plant that contains tuber a common one used in controlling many household agglutinin (CEA), a mannose binding lectin, exhibiting and agricultural pests and have little or no side effects insecticidal property against many sap sucking insects on human and environment (Boadu et al., 2011; including related species of D. koenigii (Roy and Schmutterer, 1990; Raj and Toppo, 2015). Probably Das, 2015). Kayesth and Gupta (2016) studied the Potential control agents against red cotton bug Dysdercus koenigii- A review 3 Mohd Hussain et al. antifeedant and insecticidal property of three plant antioxidant properties. Gadewad and Pardeshi (2018) extract viz., Catharanthus roseus, Ocimum sanctum and reported the bioinsecticidal effect of S. acuta plant Lantana camara. They reported that after the 24 hours (methanol and ethyle acetate) extract on the D. koenigii. exposure, all these extracts affect the survival of insect; They reported that ethyl acetate extract showed high in comparison to Ocimum and Lantana, Catharanthus toxicity (LD50= 6.165 µg/gm) than methanol extract has more insecticidal property. Sida acuta is a shrub (LD50= 9.690 µg/gm). also known as wire weed, distributed throughout India. It has a high medicinal value commonly used to treat Parasites diseases in children; it has antibacterial, antimicrobial, The parasite is an organism that lives in or on the antimalarial, anti-inflammatory, wound healing and other organism and obtained food and shelter on the

Table 1. Insecticides studied for effects on red cotton bug Insecticide Type of insecticide Reference Acephate 20 SP Organophosphate Varma et al., 2012; Rafiq et al., 2014; Qamar and Jamal, 2009 Acetamiprid 20SP Neonicotinoid Rafiq et ai., 2014; Saeed et al., 2016 Alphacypermethrin 5EC Pyrethroid Rafiq et al., 2014 Andalin IGR Khan et al., 2011; 2012, Bifenthrin 10EC Pyrethroid Rafiq et al., 2014; Akhtar et al., 2016 Carbosulfan 500SC/20EC Carbamate Rafiq et al., 2014; Akhtar et al., 2016 Chlorfenapyr 360SC Neonicotinoid Rafiq et al., 2014; Akhtar et al., 2016; Shafqat et al., 2016 Chlorpyrifos Organophosphate Yousuf et al., 2012; Shafqat et al., 2016 Cypermethrin 10EC Pyrethroids Rafiq et al., 2014 Cyfluthirn 20EC Carbamate Sarwar et al., 2018 Deltamethrin 2.5EC Pyrethroids Rafiq et al., 2014; Akhtar et al., 2016; Shafqat et al., 2016; Sarwar et al., 2018 Deltaphos 350 + 10 EC Organophosphate Rizwan et al., 2006 Diafenthiuron 50SC Neonicotinoids Rafiq et al., 2014; Dichlorvos 76 EC Organophosphate Varma et al., 2012; Ayesha et al., 2009 Deltamethrin Organophosphate Saeed et al.,2016 Dimethoate 40EC Organophosphate Rafiq et al., 2014; Varma et al., 2012 Endosulfan 35EC Cyclodiene Rizwan et al., 2006 organochlorine Emamectin 75 WDG Avermectin Akhtar et al., 2016; Saeed et al., 2016; Fenvalerate 10 EC Pyrethroid Varma et al., 2012 Fipronil 5%EC Akhtar et al., 2016 Gammacyhalothrin 60CS Pyrethroid Rafiq et al., 2014, Akhtar et al., 2016; Sarwar et al., 2018 HMAC: 1,6-Hexamethylene Carbametes Ahmad, 1979 bis (1-aziridine carboxamide) Imidacloprid 17.8 SL/ 20SL Neonicotinoids Varma et al., 2012; Rafiq et al., 2014; Akhtar et al., 2016; Saeed et al., 2016; Sarwar et al.,2018 Lamdacyhalothrin 2.5EC Pyrethroids Rafiq et al., 2014; Akhtar et al., 2016; Saeed et al., 2016; Sarwar et al., 2018 Lufenuron Benzoylurease Yousuf et al., 2012 Malathion 57EC Organophosphate Rafiq et al., 2014 Methomyl 40 SP Carbamate Akhtar et al., 2016 Parathion-methyl Organophosphate Sinha et al., 1990 Penfluron IGR Bharti et al., 2007 Phosphamidon 85 SL Organophosphate Varma et al., 2012 Profenophos 50EC Organophosphate Rafiq et al., 2014; Akhtar et al., 2016 Spinosad Spinosyn Saeed et al., 2016 Tetra ethylene pentamine Organophosphate Sehgal et al., 1974 (TEPA) Thiacloprid 48SC Neo-nicotinoids Rafiq et al., 2014 Thiamethoxam 70WG Neo-nicotinoids Jameel and Jamal, 2017 Triazophos 40 EC Organophosphate Varma et al., 2012; Rafiq et al., 2014 λ-cyhalothrin Pyrethroid Yousuf et al., 2012 4 Indian Journal of Entomology 83(2021) Online published Ref. No. e20158

Table 2. Botanicals studied for their effect on red cotton bug Insecticide Plant Effect on insect Reference Achook Azadirachta indica (Neem) Development Kodandaram et al., 2008 Ailanthus extract Ailanthus Excelsa Insect repellent Sontakke et al., 2013 Anonin Annona mucosa Physiological effect Kodandaram et al., 2008 Anthocephalus extract Anthocephalus cadamba Development Prabhu et al., 1975 Azadirachtin (Neem extract) Azadirachta indica (Neem) Development Koul, 1984; Yousuf et al., 2012; Varma et al., 2012 Calophyllum extract Calophyllum sp Development Prabhu et al., 1975 Catharanthus extract Catharanthus roseus Anti feedant Kayesth and Gupta, 2016 Colocasia esculenta tuber Colocasia esculenta Physiological effect Roy and Das, 2015 agglutinin (CEA) Sida extract Sida acuta Physiology Gadewad and Pardeshi, 2018 Curcuminoid Curcuma longa (turmeric) Development Chowdhury et al., 2000 Econeem Azadirachta indica (Neem) Development Kodandaram et al., 2008 Juglone (5-hydroxy-1,4- black walnut (Juglans Development Rao and Gujar, 1995 naphthalenedione) nigra) Karanjin Millettia pinnata or Development Kodandaram et al., 2008 Pongamia glabra Lantana Extract Lantana camara Antifeedent and Kayesth and Gupta, 2016; development Prabhu et al., 1975 Nicotine derivatives Development Rizvi et al., 1990 Nicotinyl Insecticides Physiology Rizwan-Ul-Haq et al., 2005 (acetamiprid) Nicotinyl Insecticides Physiology Rizwan-Ul-Haq et al., 2005 (imidacloprid) Ocimum Extract Ocimum sanctum Antifeedant Kayesth and Gupta, 2016 Phyllanthus Extract Phyllanthus embIica Development Prabhu et al., 1975 Plumbagin, (2-methyl Plumbago spp Development, Rao and Gujar, 1995 5-hydroxy-l,4-aphthoquinone) sage brush or worm wood oil Artemisia annua Development Rao et al., 1999 Tectona Extract Tectona grandis Development Prabhu et al., 1975

Table 3. Entomopathogenic fungi associated with D. koenigii Entomopathogenic fungi Reference Aspergillus niger Kumari et al., 2015 Beauveria bassiana Morthi et al., 2012; Khan et al., 2014 Isaria fumosorosea Morthi et al., 2012; Khan et al., 2014 Metarhizium anisopliae Khan et al., 2014; Lubeck et al., 2008 expanse of the host. There are many mite species complete chaetotaxy of the dorsal and ventral idiosoma which have been found parasitizing many insects. and some details of the gnathosoma and legs of motile Mite infestation on Dysdercus spp. had been reported, immature stages of H. indicus. Menon et al. (2011) probably Krantz and Khot (1962) were the first to described a mite Hemipteroseius vikrami associated report mite associated with RCB. Later on Banerjee with D. koenigii and D. cingulatus, collected from and Datta (1980) observed the predatory behaviour Varanasi and New Delhi, respectively. These mites are of Hemipterious indicus (Krantz and Knot 1962) and found throughout the season on the infested adult under their possible use in biological control of D. koenigii. the wings but not on nymphs. With heavy infestation It had been reported that this parasite causes infestation mite population increases to >100/ adult. Sarangi on winged adults only, and males are more susceptible et al. (2012) explored the population dynamics of than females. The infested insect stops feeding and dies Hemipteroseius spp. and observed that its populations after 90-120 hr after the attack. Prasad (2018) described fluctuate in their natural habitat. A positive correlation Potential control agents against red cotton bug Dysdercus koenigii- A review 5 Mohd Hussain et al. with the temperature was observed, while it was a and are alternatives to chemical insecticides (Kumar negative one with the rainfall and relative humidity. et al., 2017). As per the literature available, very few Therefore, the mite incidence was relatively less cases of microbial infestation had been reported for during winter. Another important mite associated with RCB. Most of the literature available was related to RCB is Antilochus coquebertii reported by Sahayaraj fungal infestation only. Lubeck et al. (2008) observed and Fernandez (2017). They found that this predator that fungus Metarhizium anisopliae was virulent exhibited an active hunting strategy indicative of using against Dysdercus peruvianus, with females being both olfactory and visual orientation; it was interesting more susceptible than males. Moorthi et al. (2012) result that, when immature mite feed on cotton leaves and Khan et al. (2014) showed that in addition to M. alone it failed to develop and mature into an adult and anisoplia, Beauveria bassiana and Isaria fumosorosea only successfully developed and mature when the hosts were also highly virulent against RCB. Kumari et al. feed on cotton leaves and RCB as well. (2015) observed that Aspergillus niger infected both the sexes of RCB and males were found more susceptible A parasitoid is an organism which laid eggs on or than females. inside the body of the host, after hatching larvae start feeding on the host tissue and adult are free living. Control Kumari et al. (2016) reported parasitoid infestation Among the 41 related articles perused, 16 were (Phasia varicolor) in the D. koenogii. According to related to chemical insecticides, 13 were related to this, P. varicolor inserted egg inside the body of the botanicals, 7 related to parasites, 4 related microbial RCB, and larvae develop within their host in about two and only one related to parasitoid (Table 4). weeks and 3rd larval stage exits to pupate outside the host body. The adult fly emerges in two weeks, with male The RCB can be controlled by the following ways. emerging before female. This parasitoid initially fed on Cultural control is a widely used, safe and ecofriendly the non-vital part of the host which later started feeding technique used in IPM of many insects but unfortunately the vital organs and finally killed the host. It was found there are few research reports on this. The RCB lays that this parasitoid directly affects the fecundity of D. eggs in a cluster on the soil under the debris, dried leaves koenigii. These preferably hosted on the female bugs and decaying matter (Mead, 1966; Verma et al., 2012). and caused abnormalities in the reproductive system. Therefore removal of unwanted plants, debris, dried leaves etc from the field which is also known as field Microbes sanitization before sowing the crop could be effective. The use of microbes like viruses, bacteria, fungi, Time to time irrigation of the field is also important, protozoans and nematodes for the control of insect due to proper irrigation or flooding of the field the pests is known as microbial control. Microbial control eggs and other stages will get drown and may die due agents have proved to be very effective and ecofriendly, to suffocation. Mechanical or physical control includes

Table 4. Control agents evaluated against the red cotton bug Control Number of References methods publications Botanical 13 Chowdhury et al., 2000; Gadewad and Pardeshi, 2018; Kayesth and Gupta, 2016; Kodandaram et al. 2008; Koul, 1984; Prabhu et al.,1975; Rao and Gujar, 1995; Rao et al., 1999; Rizvi et al., 1990; Rizwan-Ul-Haq et al., 2005; Roy and Das, 2015; Varma et al., 2012; Yousuf et al., 2012 Chemical 16 Ahmad, 1979; Akhtar et al., 2016; Ayesha et al., 2009; Bharti et al., 2007; Jameel and Jamal, 2017; Khan et al., 2011; Khan et al., 2012; Qamar and Jamal, 2009; Rafiq et al., 2014; Rizwan-Ul-Haq et al., 2006; Saeed, 2016;Sarwar et al., 2018; Sehgal et al., 1974; Shafqat et al., 2016 Sinha et al., 1990; Varma et al., 2012 Parasite 7 Banerjee and Datta, 1980; Fernandez, 2017; Krantz and Khot, 1962; Memon et al., 2011; Sahayaraj and Sarangi et al., 2012 Parasitoid 1 Kumari et al., 2016 Microbial 4 Khan et al., 2014; Kumari, et al., 2015; Morthi et al., 2012; Lubeck et al., 2008 Total 41 6 Indian Journal of Entomology 83(2021) Online published Ref. No. e20158 simple collecting infested host plant and handpicking of insects: economics, engineering, and environmental safety. Novel biotechnologies for biocontrol agent enhancement and the pests. In the case of RCB only adults can fly for a management. pp. 25-51. short distance and all the nymphal stages are wingless. Gadewad M G, Pardeshi A. 2018. Bioinsecticidal effect of Sida acuta Due to its conspicuous red colour it can be easily plant extract against red cotton bug, Fab. noticeable in the field as well as it may be collected International Journal of Zoology Studies 3(1): 177-181. in a bottle or any container by simply handpicking or Hubbard H G. 1885. Orange insects. Department of Agriculture, Division collecting and burn to death. Time to time surveillance of Entomology, US. pp. 165-168. Jameel M, Jamal K. 2017. Studies on the toxic effect of thiamethoxam and monitoring of RCB population is essential for against the nymphal stage of Dysdercus koenigii Fabricius assessment of damage and control. Biological control (: Pyrrhocoridae). International Journal of Entomology could be another best method for the control of RCB, and Research 2(6): 27-32. includes the use of natural enemies. In the case of RCB Kacho N F, Hussain M, Hussain N, Hussain M, ASMAT S. 2019. Comparative effect of synthetic and botanical insecticide against there are three each of parasitic mites and fungi, and one woolly apple aphid, Eriosoma lanigerum (Hausmann) on apple in parasitoid. Of these, the fungus M. anisoparium is easy cold arid zone of Kargil, Ladakh, India. Journal of Entomology to use and is widely used in the control of many insect and Zoology Studies 8(1): 1107-1109. pest groups (Charnley and Collins, 2007). Therefore, this Kapur A P, Vazirani T G. 1956. The identity and geographical distribution of the Indian species of the Dysdercus Boisduval (Hemiptera: fungal species can be used as a biological control agent Pyrrhocoridae). Zoological Survey of India 46(54): 159-175. against RCB. There is only one parasitoid i,e., Phasia Kareru P, Rotich Z K, Maina E W. 2013. Use of botanicals and safer varicolor (Diptera) associated with RCB, its biology is insecticides designed in controlling insects: The African Case. not well known. About insecticides, of the two types Intech. pp. 297-309. available, botanicals/ chemical insecticides, the former Kayesth S, Gupta K K. 2016. An assessment of antifeedant potential and cidal activity of plant extracts on fifth instar nymphs of red cotton is safer and ecofriendly. There are 22 botanicals and bug, Dysdercus koenigii Fabricius (Heteroptera: Pyrrhocoridae). 37 chemical insecticides known to be effective against Journal of Entomology and Zoology Studies 4(4): 416-422. RCB. Azadirachtin (neem extract), that is widely being Khan B A, Freed S, Zafar J, Farooq M. 2014. Evaluation of three different used against insect pests (Kacho et al., 2019; Mondédji insect pathogenic fungi for the control of Dysdercus koenigii and Oxycarenus hyalinipennis. Pakistan Journal of Zoology 46(6): and Nyamador, 2019) has shown good results (Koul, 1759-1766. 1984; Yousuf et al., 2012; Varma et al., 2012). Kodandaram M H, Thakur N S A, Shylesha A N. 2008. Toxicity and morphogenetic effects of different botanicals on red cotton bug REFERENCES Dysdercus koenigii Fab. (Hemiptera: Pyrrhocoridae) in North Eastern Ahmad I. 1979. Studies on the development of resistance to HMAC: Hill (NEH) region of India. Journal of Biopesticides 1(2): 187-189. 1,6-Hexamethylene bis (1-aziridine carboxamide) in Dysdercus Koul O. 1984. Azadirachtin: 1-interaction with the development of red cingulatus Fabr. Journal of Pesticide Science 4: 515-516. cotton bugs. 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(Manuscript Received: June, 2020; Revised: September, 2020; Accepted: September, 2020; Online Published: October, 2020) Online published (Preview) in www.entosocindia.org Ref. No. 20158