SCIENTIFIC CORRESPONDENCE Protective devices of the carnivorous , epius (Westwood) (: )

The apefly, is a rare butter- and hidden. Aitken6 described the larva leaf and pupates after firmly attaching on fly and an inhabitant of wooded areas. and pupa of S. epius. The larvae were its ventral side to the leaf. Usually most observers miss it due to its found feeding voraciously on the egg The length, width and height of the retiring nature, small size and rather drab masses, nymphs and adults of . pupa are 5.0–6.1 mm (5.6 ± 0.44), 3.5– colour. The species is known to occur in As the young larvae of S. epius simulate 4.2 mm (3.90 ± 0.19) and 3.2–4.1 mm Sikkim, Kolkata, Malda, South India, mealybugs, it is difficult to recognize them (3.55 ± 0.32) respectively. The bold pat- Burma and Sri Lanka1–3. Lycaenids are amidst the host population. Similarly, the tern on the hard dorsal side of the pupa unique in their larval stage as they eat young larvae of S. lemolea (Holl.) in of S. epius resembles the face of a rhesus unrelated food, including flowering plants, Africa24 and S. substrigata (Snell) in Philip- monkey (Figure 2 b). The pupa shows fungi, lichens, cycads, ferns, conifers, ant pines25 are camouflaged with the mea- clear spots of eyes, nose, mouth, cheeks larvae and homopterans4,5. The larva of lybug population. The mature larva of and forehead on the dorsal side. S. epius S. epius has been recorded as a predator S. epius measures 14.5–19.0 mm (16.48 ± pupa is light brown on the dorso-lateral on various species of pseudococcids 1.66) in length and 5.08–6.50 mm (5.72 ± side and whitish-grey on the ventral side. (mealybugs)2,6–16 and coccids (scale in- 0.38) in width. It is known that many edible, unrelated sects)8,17,18. Recently, the larvae of this The red ant, Oecophylla smaragdina species avoid predation by mimicking butterfly were found on different species (F.) or the black ant, Crematogaster sp. the appearance of a dangerous or offen- of croton plants, Codiaeum spp. infested attends the mealybugs since they secrete sive species. Many lycaenid adults dis- with , Planococcus citri (Risso) honeydew, as reported earlier26–29 (Fig- play patterns of colour, structure and (Homoptera: Pseudococcidae) at the Jnana- ure 2 a). These ants, particularly O. sma- behaviour that are consistent with deflect- bharathi campus, Bangalore University. ragdina were found attacking the mature ing predator attacks towards a false pat- Though the butterfly is known to be a larvae of S. epius whenever they encoun- tern34. There is always a chance of pre- potential predator of different species of tered them. These larvae are much bigger dation of quiescent pupae of S. epius by mealybugs19–23, its activity is rarely noti- than the mealybugs and do not secrete predatory birds or by other natural ene- ced these days in the field wherever in- honeydew sought by the ants; thus ants mies that visit mealybugs. Though the secticides are used indiscriminately for interfere with the predatory activity of -predatory bird, dull green leaf war- the control of various insect pests, parti- the larvae. Crematogaster sp. was found bler, Phylloscopus trochiloides (Sunde- cularly homopterans. to be less hostile to S. epius caterpillars. vall) seldom visited the mealybug-infes- Except for being reported as a preda- However, both the ants did not attack ted bushes and devoured the crawling tor, not much information is available on young larvae of S. epius that look like mature S. epius larvae on the leaves, it the biology and behaviour of S. epius. mealybugs. Though most of the honey- Adult of S. epius is a small butterfly with secreting lycaenids are myrmecophilous dark brown wings above, and grey under- (associated with ants), either to protect side with dark striations. Forewing has themselves against larval and pupal ene- a small quadrate spot at the cell end in mies, especially parasitoids, or to feed on male (Figure 1 a), and larger and some- the larvae of ants4,8,24,27,29,30–33, a few lyca- what diffuse in female1,2. Dorsal side of enid homopterophagous aberrant genera the thorax is dark and glossy, encircled by such as Aslauga of subfamily Leptininae, tufts of white hair. Dorso-lateral region and Spalgis, Fenisca and Megalopalpus of abdomen is dark brown, whereas ven- of subfamily Lycaeninae are amyrmeco- tral side is covered with layers of white philous (not associated with ants). They hair. The body length and wingspan of defend themselves from the homopteran- the adult are 9.95–11.50 mm (10.63 ± associated ants by means other than honey 0.48) and 18.0–22.5 mm (20.83 ± 1.44) secretion and ants derive no benefit from respectively. The butterfly flies rapidly the presence of the lycaenin larvae8,28,32. and erratically in the vicinity of bushes Unlike other lycaenids, the larvae and infested with mealybugs and it swiftly pupae of these genera lack any sort of deposits eggs in the mass of the mea- organ that yields an ant confection, and lybugs. Occasionally, it has the habit of ants that visit honey-secreting homop- landing to rest persistently on its prefer- terans are hostile to the caterpillars8,32. red perch. Owing to the dull colour, rapid However, these are protected against ants and erratic flight, and swift egg deposi- either by their obscure position among or tion habits of adult S. epius females, it is beneath their host prey, by the thick difficult for the predators (birds, lizards, cuticle on the dorsal body wall, or by etc.) to attack them in the field. their bristly vestiture8. The mature larvae The larva of the butterfly has a pecu- of S. epius seem to protect themselves liar appearance and it is morphologically against the mealybug-attending ants by different from that of other species of maintaining an adequate distance from in general, being short, slug- them and by having hard, thick dorsal like and covered with white wax coating cuticle. S. epius larva headed for pupa- Figure 1. a, Male Spalgis epius butterfly. b, (Figure 1 b). Legs of the larva are short tion, crawls to the lower surface of the Fully grown larvae of S. epius.

CURRENT SCIENCE, VOL. 87, NO. 5, 10 SEPTEMBER 2004 571 SCIENTIFIC CORRESPONDENCE avoided attacking the monkey-faced pupae ral enemies either by ants, which are 19. Chacko, M. J., Bhat, P. K. and Ramanara- that existed in the same bushes. However, attracted to pupal ant-gland, by camou- yan, E. P., J. Coffee Res., 1978, 7, 69–71. the birds were never found to attack the flage, or by making a creaking noise8,38. 20. Gowda, D. K. S., Manjunath, D., Pradip stationary larvae, probably since they re- As these features are not found in S. epius Kumar, Datta, R. K. and Kumar, P., Insect semble bird-droppings at a distance. Simi- pupae, the aposematic sign of the pupae Environ., 1996, 2, 87–88. larly, various lycaenid caterpillars are to predators perhaps has a great adaptive 21. Mani, M. and Krishnamoorthy, A., Ento- known to escape from bird predation35. value in protecting them in the sedentary mon., 1998, 23, 105–110. Moreover, the ants O. smaragdina and stage under vulnerable habitat. 22. Prakasan, C. B., J. Coffee Res., 1987, 17, Crematogaster sp. attending the mealy- It is generally agreed that the primitive 114–117. 23. Reddy, K. B., Bhat, P. K. and Naidu, R., bugs are common predators of members of lycaenids were plant-feeders, Pest Manage. Econ. Zool., 1999, 5, 119– that do not secrete honeydew8,27–29,36,37. and that homopterophagous (carnivorous) 121. Even the pupae of lycaenid, Iolaus spp. habit is a secondary specialization aris- 24. Lamborn, W. A., Trans. Entomol. Soc. are devoured by Crematogaster ants, which ing from association with ants39,40, which 35 London, 1914, 61, 438–524. conversely protect them as larvae . How- live in the vicinity of honeydew-secret- 25. Smith, H. S., Bull. St. Comm. Hort. Calif., ever, these ants never attacked amyrme- ing homopterans. Thus many species of 1914, 3, 26–29. cophilous S. epius pupae. Even though the Lycaenidae counter attack from natural 26. Anon., In Coffee Guide, Central Coffee pupa is small, it might scare away ene- enemies by associating with protective Research Institute, 1998. mies because of its appearance (monkey- ants. When many phytophagous–myrme- 27. Holldobler, B. and Wilson, E. O., In The faced). Balduf8 considers the monkey- cophilous/homopterophagous–myrmeco- Ants, The Belknap Press of Harvard Uni- faced appearance of some lycaenid pupae philous lycaenid genera get protection by versity Press, Cambridge, 1990. as a means of protection, but does not associating themselves with ants, why a 28. Wheeler, W. M., In Ants, Columbia Uni- clearly state its significance. Generally, few homopterophagous lycaenids, includ- versity Press, New York, 1960. lycaenid pupae are protected from natu- ing S. epius evolved as amyrmecophilous 29. Wilson, E. O., In The Insect Societies, type is not clearly understood. The Belknap Press of Harvard University Press, Cambridge, 1976. 1. Bingham, C. T., In The Fauna of British 30. Clark, G. C. and Dickson, C. G. C., In India Including Ceylon and Burma, But- Life Histories of South African Lycaenid terflies, Taylor and Francis, London, 1907, Butterflies, Purnell, Capetown, 1971. vol. II. 31. DeVries, P. J., Science, 1990, 248, 1104– 2. De Niceville, L., In Butterflies of India, 1106. Burma and Ceylon, The Calcutta Central 32. Hinton, H. E., Proc. Trans. Soc. London Press Co Ltd, 1890. Entomol. Nat. Hist. Soc., 1949–50, 111–175. 3. Kunte, K., In Butterflies of Peninsular 33. Pierce, N. E. and Mead, P. S., Science, India (ed. Gadgil, M.), Universities Press, 1981, 211, 1185–1187. 2000. 34. Robbins, R. K., Am. Nat., 1981, 118, 770– 4. Atsatt, P. R., Am. Nat., 1981, 118, 638–654. 775. 5. Richards, O. W. and Davies, R. G., In Imm’s 35. Farquharson, C. O., Trans. Entomol. Soc. General Textbook of Entomology, B.I. London, 1922, 69, 319–448. Publ Pvt Ltd, New Delhi, 1993. 36. Dennis, H., In Agricultural Insect Pest of 6. Aitken, E. H., J. Bombay Nat. Hist. Soc., the Tropics and their Control, Cambridge 1894, 8, 485–489. University Press, 1993. 7. Ayyar, T. V. R., J. Bombay Nat. Hist. Soc., 37. Le Pelley, R. H., In Pests of Coffee, Long- 1929, 33, 668–675. man, Green and Co Ltd, 1968. 8. Balduf, W. V., In The Bionomics of Ento- 38. De Niceville, L., J. Asiat. Soc. Bengal, 1900, mophagous Insects. Part II, Swift, St. Louis, 69, 187–278. 1939. 39. Eliot, J. N., Bull. Br. Mus. Nat. Hist. Ento- 9. Chacko, M. J. and Bhat, P. K., J. Coffee mol., 1973, 28, 373–505. Res., 1976, 6, 56–57. 40. Vane-Wright, R. E., In Diversity of Insect 10. Green, E. E., Entomologist, 1905, 35, 202. Faunas (eds Mound, L. A. and Waloff, N.), 11. Jalil, A. F. M. A. and Kabir, A. K. M. F., Blackwell Scientific, Oxford, 1978.

Agric. Pak., 1972, 22, 237–240. Received 6 March 2004; revised accepted 30 12. Mani, M., J. Entomol. Res., 1995, 19, 61–70. June 2004 13. Mani, M. and Krishnamoorthy, A., J. Biol.

Control, 1990, 4, 61–62. 14. Mani, M., Thontadarya, T. S. and Singh, S. P., Curr. Sci., 1987, 56, 624–625. M. G. VENKATESHA* 15. Pushpaveni, G., Rao, P. R. M. and Rao, L. SHASHIKUMAR P. A., Indian J. Entomol., 1974, 35, 71. S. S. GAYATHRI DEVI 16. Rao, P. R. M., Kanakaraju, A., Apparao, R. V. and Azam, K. M., In Quarterly Department Studies in Zoology, Newsletter of FAO Asia Pacific Plant Pro- tection Commission, 1984, vol. 27, p. 12. Bangalore University, 17. Ali, M., Bangladesh J. Zool., 1980, 6, Jnanabharathi Campus, Bangalore 560 056, India Figure 2. a, The black ant, Crematogaster sp. 69–70. attending mealybugs. S. epius larva seen nearby. 18. Mani, M. and Krishnamoorthy, A., Pest *For correspondence b, Monkey-faced pupae of S. epius. Manage. Hortic. Ecosyst., 1996, 2, 49–50. e-mail: [email protected]

572 CURRENT SCIENCE, VOL. 87, NO. 5, 10 SEPTEMBER 2004