BIOLOGICAL CONTROL OF SOLENOPSIS MEALYBUG, PHENACOCCUS SOLENOPSIS TINSLEY ON COTTON: A BOON FOR INDIAN FARMERS NEETAN AND NAVEEN

AGGARWAL
Department of Entomology, Punjab Agricultural University, Ludhiana-141004, India

e-mail: naveen_ag_in@yahoo.com ABSTRACT Observations on the predators and parasitoids associated with solenopsis mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) were recorded during 2009-10 in cotton growing districts of Punjab. Different natural enemies recorded from mealybug colonies included four coccinellid predators, one parasitoid and one chrysopid. Among these lady bird beetle, Brumus suturalis was the most abundant. Its highest abundance (65.7%) was recorded in Bathinda followed by Muktsar (61.7%), Mansa (58.3%) and Faridkot (53.8%). Chielomenes sexmaculata was the second most abundant predator with 10.2 to 29.3 per cent abundance, followed by Chrysoperla zastrowi arabica (6.1 to 11.4%), Nephus regularis (4.6 to 5.6%) and Scymnus coccivora (5.2 to 9.1%). Aenasius bambawalei was the only primary parasitoid recorded from P. solenopsis on cotton in different districts. 76.6 per cent parasitism was recorded in samples collected from Bathinda followed by Mansa (64.5%), Faridkot (60.00%) and Muktsar (56.8%) district. A hyperparasitoid, Promuscidea unfasciativentris on primary parasitoid A. bambawalei was also recorded from few samples. Key words: Cotton, parasitoids, predators Phenacoccus solenopsis, Aenasius

bambawalei INTRODUCTION In 2006, a possibly introduced species of Phenacoccus (Sternorrhyncha: Coccoidea: Pseudococcidae) was found causing serious damage to cotton in Punjab. This outbreak occurred on both Bt cotton and non-Bt cotton and the growers response has been to use large amounts of pesticides to the tune of US$ 121.4 million worth in the Punjab in two months in 2007 (Dutt, 2007). In the Indian subcontinent, the pest has caused widespread and serious damage to cotton crop (Abbas et al., 2005; Dhawan et al., 2007 and Mahmood, 2008). Severe economic damage to G. hirsutum was reported in 2007

(Dhawan, 2008 and Dharajyoti et al., 2008) in four major cotton-growing districts (Bathinda, Muktsar, Faridkot and Ferozepur) of Punjab, two districts (Hisar and Sirsa) of Haryana, and low to moderate damage in parts of Maharashtra, Tamil Nadu and Andhra Pradesh. A report published by the Centre for Agro-Informatics Research in Pakistan in 2006 (Muhammad, 2007) also stated that the exotic mealy bug, P. solenopsis had destroyed 0.2 million bales and 50 000 acres (out of the 8 million acres) of cotton area across Pakistan, especially in Punjab and Sindh provinces. It warned that the pest was still increasing, and could result in an epidemic in the cotton-growing areas if unchecked. The mealy bug became a major pest in almost all cotton growing states of India and Pakistan. Apart from yield losses, the cost of insecticide application increased by US$250- 375 per acre in both India and Pakistan (Nagrare et al., 2009). Mealy bugs (Hemiptera: Pseudococcidae) are small sap-sucking Insects, and some species cause severe economic damage to a wide range of vegetables, horticultural and field crops. Infested plants can exhibit general symptoms of distorted and bushy shoots, crinkled and/or twisted bunchy leaves, and stunted plants that may dry completely. Historically, mealy bugs were never considered major pests of cotton in India. There have been isolated reports of Maconellicoccus hirsutus on the native desi species, Gossypium arboretum in Punjab (Dhawan et al., 1980) and on the new world cotton Gossypium herbaceum in Gujarat (Muralidharan and Badaya, 2000) But there was no published evidence of mealy bugs on Gossypium hirsutum which currently occupies more than 80 percent of the cotton cultivated in the country. It was earlier thought to be a new and undescribed species in the Indian subcontinent and was named as Phenacoccus gossypiphilus Abbas, Arif and Saeed (Abbas et al., 2005). Similarly, Gautam et al. (2007) probably incorrectly identified it as Phenacoccus solani (Ferris). The confusion regarding the identity of the species was later cleared based on the specimens collected from several locations in the Indian subcontinent (Hodgson et al., 2008 and Thomas and Ramamurthy, 2008). Nagrare et al. (2009) reported P. solenopsis as an exotic species originated from the USA and was reported to damage cotton and crops of 14 families. To control this pest, insecticides belonging to different groups have been recommended (Saeed et al., 2007). But it is extremely important to avoid the usage of insecticides for the management of exotic pests, considering their propensity to survive, multiply and spread in the absence of 2

native natural enemies. Also complete reliance on insecticides may result in development of resistance, insect resurgence and environmental hazards (Sparks et al., 1996 and Mascarenhas et al., 1996 and 1998). The vast host-range of cotton mealy bug requires attention for alternate control measures and it was strongly felt that further studies are essential to detect predators and parasitoids that may be occurring naturally in India to strengthen eco-friendly sustainable mealy bug management. Otherwise it would be necessary to import their natural enemies from the US. As studies on field incidence of solenopsis mealybug in cotton belt of the state were in progress, only indigenous natural enemies were observed developing appetite. Further, it was considered worthwhile to have detailed information on the predators and parasitoids associated with it and to assess the impact of prominent parasitoids on its population during different months under Punjab conditions. Thus, keeping all this in view, the present studies were carried out to record the natural enemies of P. solenopsis from different cotton growing districts of Punjab. MATERIALS AND METHODS Mealy bug infested cotton fields in the districts of Bathinda, Mansa, Muktsar and Faridkot were visited after every two weeks. Samples of mealy bug infested twigs were collected from such fields by examining 10-15 randomly selected plants from a field selected after every 3-5 km and then brought in aerated paper bags to the Biological Control Laboratory, Department of Entomology, PAU, Ludhiana. This material was kept in transparent jars in order to isolate parasitoid and predators of P. solenopsis. Samples of mealy bug infested twigs collected from such fields were examined in the laboratory under stereo zoom binocular microscope to isolate larval and pupal stages of predators, if any. The predator larvae were reared on different nymphal instars of mealybug under laboratory conditions to obtain adults. Per cent relative abundance of a predator species was calculated as:
Total number of adults of a predator species X 100 Total number of adults of all species of predators recorded For recording parasitism, the number of mealy bugs on the twigs was counted and the twigs were confined in glass jars. The mealy bugs parasitized by parasitoid A. bambawalei transformed into reddish brown mummies. Such mummies without emergence hole of parasitoid were counted, removed from the twigs and transferred to glass vials for obtaining adult parasitoids. The rate of parasitism was determined from

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the total number of mummies and surviving mealy bugs in a sample. parasitism by the primary parasitoid per sample was calculated as: Total number of mummies Total number of mummies and surviving mealy bugs

Per cent

X 100

Each specie of predator and parasitoid was isolated, properly identified and also sent to appropriate authorities for identification. RESULTS AND DISCUSSION Field survey was conducted in the cotton belt of Punjab to record natural enemies of cotton mealy bug, P. solenopsis during 2009-10. Predators were observed active throughout the cotton crop season. Different natural enemies recorded from mealy bug colonies on cotton included four coccinellid predators, one parasitoid and one chrysopid and their details are presented in table 1. Among these, ladybird beetle, Brumus suturalis was the most abundant. Its highest abundance (65.7%) was recorded in Bathinda followed by Muktsar (61.7%), Mansa (58.3%) and Faridkot (53.8%). C. sexmaculata was the second most abundant predator with 10.2 to 29.3 per cent abundance, followed by C. zastrowi arabica (6.1 to 11.4 %), N. regularis (4.6 to 5.6 %) and S. coccivora (5.2 to 9.1%) in different districts. Gautam et al. (2007) also reported five predators, viz., B. lineatus, B. suturalis, C. sexmaculata, N. regularis and S. coccivora from the field population of P. solani Ferris (probably P. solenopsis) infesting different plant species. Directorate of Pest Warning and Quality Control of Pesticides of the Department of Agriculture, Punjab, Pakistan in a survey conducted during 2007/08 found Scymnus coccivora and Diadiplosis spp in high numbers in mealy bug infested fields. NCIPM, New Delhi also supported the findings of their Pakistani counterparts by conducting a survey in cotton belt of Indian Punjab during 2008 and found in areas where there was an abundance of coccinellid beetles (Cheilomenes sexmaculata & Hippodamia convergens), mealy bug populations were low or absent (Anonymous, 2008). Ram and Saini (2010) in a survey conducted during 2008 & 2009 in cotton belt of Haryana recovered Brumoides suturalis (Fabricius) and Nephus regularis Sicard as the most abundant predators from the mealy bug infested colonies. Chrysoperla carnea was recorded for the first time preying on M. hirustus in vine yards by Krishnamoorthy and Mani (1989) and they

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further collected eggs, pupae and larvae of lacewings from mealy bug infested citrus and guava orchards and in vineyards. Aenasius bambawalei was only primary parasitoid recorded from P. solenopsis on cotton in different districts. During survey, 76.6 per cent parasitism was recorded in samples collected from Bathinda followed by Mansa (64.5%), Faridkot (60.00%) and Muktsar (56.8%) district. Similarly, different workers have reported more than 50 per cent (Mahmood, 2008), 20-70 per cent (Tanwar et al., 2008) and 37.6 -72.3 per cent (Ram et al 2009) parasitism of P. solenopsis by Aenasius sp. on cotton and other host plants. However, Aenasius sp. has earlier been recorded in India on P. citri (Narshimam et al., 1997). The other primary parasitoiids of P. solenopsis reported from other countries in the literature are Chalcaspis arizonensis (Gordh, 1979) and Chalcaspis sp. (Fuchs et al., 1991). The collected specimens of parasitized mealy bugs were sent to National Bureau of Agriculturally Important Insects (NBAII), Bangalore for proper identification and they also reported a hyperparasitoid, Promuscidea unfasciativentris on primary parasitoid A. bambawalei from few samples collected during the months of September and October. P. unfasciativentris had earlier been reported as a hyperparasitoid from P. solenopsis (Hayat, 2009 and Ram et al., 2009). Several other studies have also reported P. unfasciativentris as a hyperparasitoid from various mealy bug species through their primary encyrtid parasitoids (Hayat et al., 2007and Sureshan and Narendran, 2005). Based on surveys in different districts for recording the natural enemies of P. solenopsis it was found that Aenasius bambawalei Hayat and the coccinellid Brumus suturalis Fabricius were the predominant natural enemies of the mealy bugs under Punjab conditions. Presently, pest is no more seen except in few pockets, which may be due to heavy parasitisation by A. bambawalei. With the result, the mealybug population was drastically reduced on cotton crop. The mealy bugs flared up during 2006-08 and declined in 2009 & 2010, which could be due to this parasitoid. This type of biological control probably also seems to be an example of fortuitous biological control, where Aenasius bambawalei may have entered along with the exotic mealybug and got established. This is also supported by the fact that A. bambawalei was found parasitizing only P. solenopsis and was never observed from Maconellicoccus hirsutus (Green) in any of the locations. Therefore, Aenasius bambawalei and Brumus suturalis needs to be 5 4

conserved not only on cotton but on other host plants of the solenopsis mealybug also so as to exploit them in the development of a successful Integrated Pest Management Programme (IPM) for this pest all over the world. Table 1. Natural enemies associated with P. solenopsis on cotton during 2009 Natural enemies Predators Coleoptera: Coccinellidae Brumus suturalis Cheilomenes sexmaculata Nephus regularis Scymnus coccivora Neuroptera: Chrysopidae Chrysoperla zastrowi arabica Parasitoids Hymenoptra: Encyrtidae 10.6 11.4 9.4 6.1 65.7 10.2 7.2 6.3
Locations

Bathinda

Mansa

Muktsar

Faridkot

Relative abundance of predator species (%)

58.3 15.6 5.6 9.1

61.7 16.3 8 4.6

53.8 29.3 5.6 5.2

Mean per cent parasitism 64.5 56.8 60.3

76.6 Aenasius bambawalei * Mean of ten observations from June to October REFERENCES

Abbas, G,; Arif, M. J. and Saeed, S. 2005. Systematic status of new species of genus Phenacoccus cockrell (Pseudococcidae) a serious pest of cotton, Gossypium hirstum in Pakistan. Pakistan Entomologist 27:83-84. Annonymous. 2008. ISIS Report: Mealy Bug: A New Threat to Cotton Production in Pakistan and India. Available on http//www:i-sis.org.uk. Dharajyoti, B,; Surulivelu, T. and Gopalakrishnan, N. 2008. Status of mealybug on cotton in various parts of India. Proceedings of National Consortium on Mealybug Management. pp 8-10.Central Institute for Cotton Research, Nagpur, India. Dhawan, A .K. 2008. Historical perspective of various species as cotton pests in India and rest of world and factor affecting occurrence and outbreak on cotton. Proc Nat Cons Mealybug Mgmt. pp11-14. Central Institute for Cotton Research, Nagpur, India. Dhawan, A. K,; Singh, J. and Sidhu, A. S. 1980. Maconellicoccus spp. attacking arboreum cotton in Punjab. Science and Culture 46:258.

Dhawan, A. K,; Singh, K,; Saini, S,; Mohindru, B,; Kaur, A,; Singh, G. and Singh, S. 2007. Incidence and damage potential of mealy bug, Phenacoccus solenopsis Tinsley, on cotton in Punjab. Indian Journal of Ecology 34:166-72. Dutt, U. (2007) Mealy Bug infestation in Punjab: Bt. Cotton falls flat. Online article at http://www.countercurrents.org/ dutt210807.htm. 7 July 2007. Fuchs, T. W.; Stewart, J. W.; Minzenmayer, R. and Rose, M. 1991. First record of Phenacoccus solenopsis Tinsley in cultivated cotton in the United States. South West Entomologist 16:21521. Gautam, R. D.; Saxena, U.; Gautam, S.; Khan, M. A.. and Gautam, C. P. N. 2007. Studies on Solanum mealybug, Phenacoccus solani Ferris (Hemiptera: Pseudococcidae), its parasitoid and predator complex, reproductive potential and utilization as laboratory prey for rearing the ladybird and green lacewing predators. Journal of Entomological Research 31: 259264. Gordh, G. 1979. Family Encyrtidae pp. 890-967 In: Krombein, K. V.; Hurd, P. D. Jr.; Smith, D. R. and Burks, B. D. (eds.) Catalog hymenoptera America North Mexico. Pp 1:1198. Hayat, M. 2009. Description of a new species of Aenasius Walker (Hymenoptera:Encyrtidae). Parasitoid of the mealybug, Phenacoccus solenopsis Tinsley (Homoptera: Pseudococidae) in India. Biosystematica 3:21-26. Hayat, M.; Badruddin, S. M. A. and Khan, F. R. 2007. On some chalcids reared from a mealybug infesting Abutilon indicum in Aligarh, U.P. Bionotes 9:65 Hodgson, C. J.; Abbas, G.; Arif, M. J.; Saeed, S. and Karar, H.2008. Phenacoccus solenopsis Tinsley (Sternorrhyncha: Coccoidea: Pseudococcidae), an invasive mealybug damaging cotton in Pakistan and India, with a discussion on seasonal morphological variation. Zootaxa 1913: 135. Krishnamoorthy, A. and Mani, M. 1989. Records of green lacewings preying on mealybugs in India. Current Science 58:155-56. Mahmood, R. 2008. Breakthrough in biological control of mealybug in Pakistan. Biocontrol News and Information 29: 3839. Mascarenhas, V. J,; Graves, J. B,; Leonard, B. R. and Burris, E. 1998. Susceptibility of field populations of beet armyworm (Lepidoptera: Noctuidae) to commercial and experimental insecticides. Journalof Economic Entomology 91:827-33. Mascarenhas, V. J.; Leonard, B. R.; Burris, E. and Graves, J. B. 1996. Beet armyworm (Lepidoptera: Noctuidae) control on cotton in Louisiana. Florida Entomologist 79:336-43. Muhammad, A. 2007. Mealybug: cotton crops worst catastrophe published by the Centre for Agro-Informatics Research (CAIR), Pakistan in October 2007. Available at http://agroict.org/adss/MealyBug_Report.aspx. 7

Muralidharan, C.M. & Badaya, S.N. 2000. Mealybug (Maconellicoccus hirsutus) (Pseudococcidae: Hemiptera) outbreak on herbaceum cotton (Gossypium herbaceum) inWaged cotton belt of Kachchh. Indian Journal of Agricultural Sciences 70: 705706. Nagrare, V. S,; Kranthi, S,; Biradar, V. K,; Zade, N N,; Sangode, V,; Kakde, Gcc,; Shukla, R M,; Shivare, D,; Khadi, B. M. and Kranthi, K. R. 2009. Widespread infestation of the exotic mealybug species, Phenacoccus solenopsis (Tinsley) (Hemiptera: Pseudococcidae), on cotton in India. Bulletin of Entomological Research 99:53741. Narshimam, V.; Bhumannavar, B. S.; Ramani, S.; Poorani, J. and Rajeshwari, R. 1997. A catalogue of natural enemies and other insects in PDBC reference collection. PDBC, Bangalore, India, pp. 89-102 Ram, P. and Saini, R. K. 2010. Biological control of solenopsis mealybug, Phenacoccus solenopsis Tinsley on cotton: a typical example of fortuitous biological control. Journal of Biological Control 2: 104109. Ram, P.; Saini, R. K. and Vijaya. 2009. Preliminary studies on field parasitism and biology of solenopsis mealybug parasitoid, Aenasius bambawalei Hayat (Encyrtidae: Hymenoptera). Journal of Cotton Research and Development 23: 313 315. Saeed, S,; Ahmed, M. and Kwon, Y. J. 2007. Insecticidal control of mealybug Phenacoccus gossypiphilous (Hemiptera: Pseudococcidae), a new pest of cotton in Pakistan. Entomological Research 37:76-80. Sparks, A. N. Jr.; Norman, J. W. Jr. and Wolfenbarger, D. A. 1996. Efficacy of selected insecticides against the beet armyworm, Spodoptera exigua field and laboratory evaluation. In: Proceedings of Beltwide Cotton Conference, National Cotton Council, pp: 844846. Memphis, TN. Sureshan, P. M. and Narendran, T. C. 2005. Description of a new species of Ophelosia Riley with synonymic and taxonomic notes on Indian Eunotinae (Hymenoptera: chalcidoidea: Pteromalidae). Zoos Print Journal 20:1854-1855. Tanwar, R. K.; Bhamare, V. K.; Ramamurthy, V. V.; Hayat, M.; Jeyakumar, P.; Singh, A. and Bambawale, O. M. 2008. Record of new Parasitoids on mealy bug, Phenococcus solenopsis. Indian Journal of Entomology 70:404-05. Thomas, A. and Ramamurthy, V. V. 2008. On the problems in diagnostics of cotton mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae). Entomon 33: 277 282.

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