Ecology and distribution of papaya mealybug, Paracoccus marginatus Williams and Granara De Willink (Hemiptera: Pseudococcidae) in South Karnataka

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1 Ecology and distribution of papaya mealybug, Paracoccus marginatus Williams and Granara De Willink (Hemiptera: Pseudococcidae) in South Karnataka G. Basana Gowda *, A. K. Chakravarthy, K. S. Jagadish and Subhash B. Kandakoor Department of Entomology, University of Agricultural Sciences, GKVK, Bangalore , Karnataka, India ABSTRACT * basanagowda4099@gmail.com A study was conducted to determine host range, distribution patterns over time and space and spread of papaya mealybug, Paracoccus marginatus Williams and Granara de Willink in Bangalore. The population of mealybug was visually estimated and rated. Papaya mealybug was found to occur on 60 plant species belonging to 29 families in five districts of South Karnataka, among which the predominant families being Euphorbiaceae, Malvaceae followed by Solanaceae and Asteraceae, Fabaceae in sustaining the mealybug population. Eight species of ants belonging to three subfamilies viz., Formicinae, Myrmicinae, Dolichoderinae were found attending P. marginatus on different crops and weed hosts viz., Solenopsis geminata (Fabricius), Tapinoma melanocephalum (Fabricius), Monomorium indicum Forel, Technomyrmex albipes (Smith), Paratrechina longicornis (Latreille), Camponotus compressus (Fab.), Oecophylla smargdina (Fabricius) and Monomorium sp. were more conspicuously attending mealybugs than the other ant species. Solenopsis geminata was one of the key attendants of mealybug whenever the pest colonized on Parthenium. KEY WORDS: Euphorbiaceae, Malvaceae, Mexico, papaya mealybug, Solenopsis geminata INTRODUCTION Papaya mealybug, Paracoccus marginatus Williams and Granara de Willink a native to central America/Mexico (Miller et al., 1999) has spread to more than 50 countries ever since the first report of the pest in Carribean islands. Papaya mealybug (PMB) was first reported in 1992 by Williams and Granara de Willink. In India its incidence was first recognized in the campus orchard of Tamil Nadu Agricultural University (TNAU), Coimbatore on July 10, 2008 (Muniappan et al., 2008). Mealybug has spread to Karnataka, Maharashtra, Kerala and Tripura presumably due to the movement of fruits. Soon it attained the status of a major pest in 2009 (Shylesha et al., 2010) and is spreading at an alarming rate infesting major agricultural and horticultural crops, causing severe economic losses to agriculture and allied industry. Since published information on PMB is not available in Karnataka, a field study on the 266

2 pest was initiated in and around Bangalore during To start with observations on ecology and distribution of papaya mealybug on major host plants were recorded in South Karnataka as heavy incidence of the pest on select economically important plants was observed MATERIALS AND METHODS Determination of host range Surveys were conducted at 20 locations spread across five districts of South Karnataka viz., Chamarajanagara, Bengaluru, Mysore, Mandya and Chikkaballapura during 2011 and At each location, eight to ten randomly selected plants were observed and the level of pest incidence on each plant sample was assessed as per the 0-5 rating scale of National Bureau of Agriculturally Important Insects (NBAII), Bangalore and for each of the sampled plants and the mean rating scale was calculated (Table 1). The plant samples were collected in perforated polythene covers (30 15cm) and submitted to the botanist for identification. The mealybug specimens collected during the surveys were identified by mealybug taxonomist at National Bureau of Agriculturally Important Insects (NBAII), Bengaluru. Table 1: Rating scale adopted for assessment of mealybug incidence Grade Visual estimation of mealybug Population 0 No incidence 1 Very low 2 Low 3 Medium 4 High 5 Very high (NBAII, 2010) Association of ants with P. marginatus Ants attending P. marginatus were collected and preserved in 70% ethyl alcohol. The taxonomic identity of the different ant species was confirmed by ant taxonomist at All India Network Project on Insect Bio-systematics; Department of Agricultural Entomology, UAS, GKVK, Bengaluru. The role of different ant species in influencing the spread and colonization of the mealybug was studied and documented. RESULTS AND DISCUSSION Host range A total of 60 plant species belonging to 29 families were recorded as host plants (Table 2), with varying levels of infestation. Nymphs and adults of the mealybug were observed on all parts of the host plant viz., leaves, petioles, branches and reproductive parts. Severely infested plants were covered with black sooty mould. A comparison of the incidence of mealybug revealed that the pest was colonising on seven plant species each, belonging to family Malvaceae and Solanaceae; six species each, belonging to Euphorbiaceae, Asteraceae and Fabaceae; two species each, belonging to Acanthaceae, Amaranthaceae, Araceae, Labiatae and 267

3 Lamiaceae, which were identified as major host plants (Table 2). Across locations in South Karnataka Datura stramonium (2.50), Datura metal (2.00), Cajanus cajan (2.00), Parthenium hysterophorus (1.96), Carica papaya (1.77), Mulberry (1.69), Ipomoea campanulata (1.61), Malvaviscus arboreus (1.40), Chromaelena odorata (1.35), Solanum kasianum (1.12), Cotton (1.10) and Hibiscus sp. (1.00) recorded the maximum population, but according to NBAII rating, scale of infestation was below 3, that corresponded to low to medium infestation as these twelve host species were found to sustain the pest population in the absence of crop hosts for most part of the year (Table 1). The present findings are in conformity with Walker et al. (2003). The workers recorded PMB on more than 55 host plants in more than 25 genera. Economically important host plants of the papaya mealybug include papaya, Hibiscus, avocado, citrus, cotton, tomato, eggplant, peppers, beans, peas, sweet potato, mango, cherry and pomegranate. Similar results were also obtained by Selvaraju and Sakthivel (2011) who recorded mealybug incidence on 84 plant species belonging to 35 families of which heavy population build-up and severe damage was recorded on 21 host plants including 10 economically important species. Similar observations were also reported by Tanwar et al. (2010) where in heavy incidence of papaya mealybug was noticed on a wide range of cultivated crops and weed hosts. Similar results were also obtained by Meyerdirk and Kauffman (2001) who recorded PMB having a wide host range of over 60 plants species including Annona squamosa, Carica papaya, Hibiscus rosa-sinensis, Ipomoea spp., Manihot esculenta and Solanum melongena. Miller et al. (1999) reported that the pest is polyphagous having wider host range and reported more than 60 host plants of about 25 genera including papaya, Hibiscus, avocado, citrus, cotton, tomato, eggplant, peppers, beans, peas, sweet potato, mango, cherry and pomegranate. Association of ants with P. marginatus Eight species of ants belonging to three subfamilies under Formicidae of Hymenoptera, viz., Formicinae, Myrmicinae, Dolichoderinae were found attending to the mealybug, P. marginatus on papaya, mulberry gardens and other crop / weed hosts, nearby. Of these, three species belonged to Formicinae, three to Myrmicinae and two belonged to Dolichoderinae (Table 3). Solenopsis geminata (Fabricius), Tapinoma melanocephalum (Fabricius), Monomorium indicum Forel, Technomyrmex albipes (Smith) Paratrechina longicornis (Latreille), Camponotus compressus (Fabricius), Oecophylla smargdina (Fabricius) and Monomorium sp. were more conspicuously attending to the mealybug than the other ant species. S. geminata was one of the key attendants of mealybug whenever the pest colonized on Parthenium. Tapinoma melanocephalum (Fabricius) association was not very intensive and was 268

4 found only occasionally on few select plants. Ants were found to spread the first and second instar nymphs, especially from infested weed hosts to crop plants. In one instance heavy colonisation of O. smargdina was observed in a papaya orchard at Kundalagurkhi, Chikkaballapura district, where as very high population of P. longicornis was observed at Sultana palya, Bengaluru on Tapioca infested with PMB. The mealybugs excrete honey dew which attracts ants and in turn helps in spreading the mealybug specially crawlers. The present results of the ants association with mealybug were in close conformity with the report of earlier workers who reported the association of S. geminata with Phenacoccus solenopsis Tinsley (Jagadish and Shadakshari, 2009) association of S. geminata with homopterans (Stahl and Scaramuzza, 1930; Ghose, 1971; Ananthakrishnan and Ananthasubramanian, 1975 and Larsen et al., In addition to S. geminata, Jagadish and Shadakshari (2009) also reported the association of M. brunnea, A. gracilipes, T. monocephalum and O. smaragdina with P. solenopsis. Moreover, Ghose (1971) and Buckley and Gullan (1991) reported that honey dew producing homopterans attend to mealybugs on other crop/ host species. During the present study different ant species were found to transfer the mealybugs from one plant to another. This finding is in agreement with Genter (1925) who found that the ant, Camponotus lineolatta (Say) transferring the grape mealybug, Pseudococcus maritimus Ehrh. Saini et al. responsible for quick colonization of P. solenopsis to new areas. Smith (1928) reported that ants collected during the surveys comprised Tapinoma sessile Say, Pheidole sp., and Technomyrmex sp. (Hymenoptera: Formicidae). T. sessile was the predominant ant species and is a common and widely distributed North American ant species. In the present study, maximum colonization of PMB was recorded on Datura stramonium and the most common ant species forager was Technomyrmex albipes. CONLCUSION From the preliminary study it can be summarized that PMB is an invasive insect spreading at an exceedingly rapid rate infesting r select plant species in Karnataka: Close monitoring and releases of parasitoid, Acerophagus papayae (Hymenoptera: Encyrtidae) may therefore be undertaken on a area wide basis in South Karnataka ACKNOWLEDGEMENTS Authors acknowledge Dr. M. D. Rajanna Professor of Botany, Department of Forestry & Environmental Sciences, GKVK, Bengaluru, Dr. Sanjay Agronomist, AICRP (Weed control), MARS, Hebbal, Bengaluru and Dr. Sunil Joshi, Scientist, NBAII, Bengaluru for the taxonomic identification of mealybug. Sincere thanks to Director of Research for providing financial assistance through DR funded project Biological control of papaya mealybug. (2009) also noticed that ants were 269

5 Papaya mealybug infestation on different hosts 270

6 Table 2: Incidence of P. marginatus on different host plants Family Local name Species Rating scale Range Mean 1.Acanthaceae Crossandra 1. Crossandra sp Spatika 2. Barleria cristata Amaranthaceae Uttarani 3. Achyranthus aspera L Amaranthus viridis Linn Asteraceae Parthenium 5. Parthenium hysterophorus L Tridax procumbens L Chromaelena odorata (L.) King & Robinson 8. Helianthus annuus L Marigold 9. Tagetus erecta Synedrella nodflora Apocyanaceae Yucca 11. Calotropis gigantea (L.) W.T.Aiton 5.Araceae Money plant 12. Epipremnum aureum (L.)Engl Yam 13. Colocasia esculenta (L.) Schott 6.Cactaceae Kalli 14. Opuntia humifusa (Raf.) Raf Caricaceae Papaya 15. Carica papaya L Convolvulaceae Amrutha balli 16. Ipomoea campanulata (L.) Merr., 9.Costaceae 17. Costus igneus Dryopteridaceae Fern 18. Athyrium filix femina Crested lady fern Cristatum 11.Euphorbiaceae Castor 19. Ricinus communis Seeme yenne gida 20. Croton sparsiflorus Morong Croton 21. Croton sp Purple leaf 22. Acalypha sp Euphorbia pulcherimma Croton 24. Codiarum variegatum (L.) A Juss Jatropha 25. Jatropha integerrima L Fabaceae Wild leg 26. Cassia occidentalis L Bellary Jaali 27. Prosopis juliflora (Sw.) DC Psubabul 28. Leucaena leucocephala (Lam.) de Wit. Rain tree 29. Albizia saman F.Muell Labiatae Tulasi 30. Ocimum tenuiflorum Ocimum canum Lamiaceae Teak 32. Tectona grandis L.f Thumbe 33. Leucus aspera (Willd) Link Leguminosae Redgram 34. Cajanus cajan (L.) Millsp

7 16.Lythraceae Pomegranate 35. Punica granatum L Henna 36. Lawsonia inermis L Mimosaceae Jaali 37. Acacia sp Meliaceae Neem 38. Azadirachta indica L Moraceae Mulberry 39. Morus alba L Malvaceae Wild malvaceae 40. Abutilon indicum (Link) Sweet Cotton 41. Gossypium hirsutum L Sida acuta Burm.f Hibiscus 43. Hibiscus sp Hibiscus 44. Hibiscus rosa sinensis L Hibiscus 45. Hibiscus hirsutus Sleeping hibiscus 46. Malvaviscus arboreus Cav Oleaceae Kakada mallige 47. Jasminum grandiflorum L Phyllanthaceae Kiru nelli, 48. Phyllanthus niruri L Polygonaceae 49. Antigonon leptopus Hook. & Arn Proteaceae Silver oak 50. Grevialla robusta A.Cunn. ex R.Br. 25.Rhamnaceae Ber 51. Ziziphus mauritiana Lam (=stramonium) 26.Rosaceae Rose 52. Rose sp Rutaceae Curry leaf 53. Murraya koenigii (L.) Sprengel 28.Solanaceae Kashigida 54. Solanum kasianum C. B Clarke Wild solanaceae 55. Solanum sp Datura metal Linn Datura stramonium Chilli 58. Capsicum annuum L Tomato 59. Lycopersicum esculentum L Verbenaceae Lantana 60. Lantana camara L Table 3: Ant species attending to P. marginatus (Hymenoptera: Formicidae) Sl. No. Ant Species Subfamily Host 1 Tapinoma melanocephalum (Fabricius) Dolichoderinae Mestha 2 Technomyrmex albipes (Smith) Dolichoderinae Papaya 3 Camponotus compressus (Fab.) Formicinae Papaya 272

8 4 Oecophylla smargdina (Fabricius) Formicinae Papaya 5 Paratrechina longicornis (Latreille) Formicinae Tapioca 6 Solenopsis geminata (Fabricius) Myrmicinae Parthenium 7 Monomorium sp. Myrmicinae Mulberry 8 Monomorium indicum Forel Myrmicinae Mulberry REFERENCES Ananthakrishnan, T. N. and Ananthasubramanian, K. S., Taxonomic, biological and ecological studies of some membracids (Insect: Homoptera) parts I and II. Rec. Zool. Surv. India, 68: Borror, D. J., Triplehorn, C. A. and Johnson, N. F., An Introduction to the Study of Insects. 6th ed. Harcourt Brace College Publishers, Orlando, FL. Buckley, R. and Gullan, P More aggressive ant species (Hymenoptera: Formicidae) provide better protection for soft scales and mealybugs (Homoptera: coccidae). Biotropica, 23 (3): Downie, D. A. and Gullan, P. J Phylogenetic analysis of mealybugs (Hemiptera: Coccoidea: Pseudococcidae) based on DNA sequences from three nuclear genes, and a review of the higher classification. Syst. Entomol., 29(2): Genter, L. G., Some important grape insects. Michigan Agric. Expt. Sta. Spec. Bull., 14: Ghose, S. K., Morphology of various instars of both sexes of the mealybug, M. hirsutus (Green) (pseudococcidae; hemiptera). Indian J. Agric. Sci., 41: Jagadish, K. S. and Shadakshari, Y. G., Sunflower mealybug, Phenacoccus solenopsis Tinsley (Homoptera:Pseudococcidae) and its parasitization by Aenasius bambawalei Hayat (Hymenoptera: Larsen, K. J., Vega, F. E., Moya Raygoza, G. and Nault, L. R., Ants associated with leafhopper, Dalbulus quinquenotus on gama grasses in Mexico. Ann. Ent. Soc. America., 84(5): Meyerdirk, D. E. and Kauffman, W. C., Status on the development of a biological control program for 273

9 Paracoccus marginatus Williams, papaya mealybug, in the Caribbean. Paper presented at IV International Scientific Seminar of Plant Health. Veradero, Cuba. Miller, D. R., William, D. J. and Hamon, A. B., Notes on a new mealybug (Hemiptera: Coccoidea: Pseudococcidae) pest in Florida and the Caribbean: The papaya mealybug, Paracoccus marginatus Williams and Granara de Willink. Insecta Mundi., 13: Muniappan, R., Shepard, B. M., Watson, G. W., Carner, G. R., Sartiami, D., Rauf, A. and Hammig, M. D., First Report of the papaya Mealybug, Paracoccus marginatus (Hemiptera: Pseudococcidae) in Indonesia and India. J. Agric. Urban Entomol. 25(1): Saini, R. K., Palaram, S. S. and Rohilla, H. R., Mealybug, Phenacoccus solenopsis Tinsley and its survival in cotton ecosystem in Haryana. In: Proc. Nat. Symp. Bt Cotton: Opportunities and Prospects, Central Institute of Cotton Research, Nagpur, November 17-19, 150 pp. Selvaraju, N. G. and Sakthivel, N., Host plants of papaya mealybug (Paracoccus marginatus Williams and Granara de Willink.) in Tamil Nadu. Karnataka J. Agric. Sci., 24 (4): Shylesha, A. N., Joshi, S., Rabindra, R. J. and Bhumannavar, B. S., Classical biological control of the papaya mealybug. Folder published from National Bureau of Agriculturally Important Insects, Bengaluru. Smith, M. R., The biology of Tapinoma sessile Say, an important house-infesting ant. Ann. Entomol. Soc. Am. XXI: Stahl, C. P. and Scaramuzza, L. C., Soil insects attacking sugarcane in Cuba. Bull. Trop. Pl. Res. Fdn., 10: Tanwar, R. K., Jeyakumar, P. and Monga. D., Mealybugs and their management. Technical Bulletin (NCIPM) 19, New Delhi, India p.12. Tanwar, R. K., Jeyakumar, P. and Vennila, S., Technical Bulletin 22. National Centre for Integrated Pest Management, New Delhi. Walker, A., Hoy, M. and Meyerdirk, D., University of Florida, IEAS Extension, EENY ybugs/papaya_mealybug.html. [MS received 30 January 2014; MS accepted 5 March 2014] Disclaimer: Statements, information, scientific names, spellings, inferences, products, style, etc. mentioned in Current Biotica are attributed to the authors and do in no way imply endorsement/concurrence by Current Biotica. Queries related to articles should be directed to authors and not to editorial board

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