J Pest Sci DOI 10.1007/s10340-010-0303-8

ORIGINAL PAPER

Development, life history characteristics and behaviour of predator, epius (Westwood) (: ) on citri (Risso) (Homoptera: Pseudococcidae)

Anegunda S. Dinesh • Melally G. Venkatesha • Sompalyam Ramakrishna

Received: 1 November 2009 / Accepted: 1 April 2010 Ó Springer-Verlag 2010

Abstract The development of immature stages, life his- Introduction tory and behaviour of mealybug predator, (Westwood) (Lepidoptera: Lycaenidae) reared on mealy- More than 99% of Lepidoptera survive solely on living bugs, (Risso) (Homoptera: Pseudococ- plants (Pierce 1995). Among the aphytophagous Lepidop- cidae) was studied in the laboratory. Larvae of S. epius are tera, about 120 in the subfamily (Lepi- a potential predator of different species of in doptera: Lycaenidae) feed on brood or India. The predator completed its life cycle in 23.8 days (Pierce 1995). Most of the aphytophagous butterflies are with four larval instars. Mean incubation period of egg was extremely rare, and several are endangered (Pierce 1995; 3.9 days. Mean duration of development of larval stages, Wynhoff et al. 1998). The genera Spalgis Moore, Tharaka prepupa and pupa was 9.4, 0.9 and 9.5 days, respectively. Doherty and Grote of Miletinae feed on ant-ten- The first and last instar larvae measured 1.9 and 11.4 mm ded Hemiptera (including Homoptera). These hemipteran- in length, respectively. Length and width were not signif- feeders live among their prey without provoking an escape icantly correlated in larvae. Head capsule width was not response or an attack response from the ant mutualists of significantly correlated with larval length in any instar. The Hemiptera (Scudder 1899). Different species of mealybugs female-to-male sex ratio was 1.45:1. Adults were ready for (Homoptera: Pseudococcidae) are serious pests of wide mating one day after eclosion. The pairs remained in range of economically important crops such as coffee, copula on an average of 61.3 min. The gravid female citrus, guava, mango, mulberry, vegetables, ornamental contained 74.6 eggs in the ovaries. Unfed butterflies (both plants, etc., worldwide (Browning 1992). The apefly, males and females) lived 3–4 days, significantly shorter Spalgis epius (Lepidoptera: Lycaenidae: Miletinae) has than those with access to water (6–7 days). The results of been recorded as a predator of various species of mealy- this study will be useful to utilize the predator as a bio- bugs viz., sp. (Aitken 1894), Planococcus control agent. virgatus (Ckll.) (Misra 1920), P. lilacinus (Ckll.) (Ayyar 1929), P. citri (Risso) (Chacko et al. 1977), Ferrisia Keywords Development Life history Lepidoptera virgata (Ckll.) (Chacko and Bhat 1976) and Maconelli- Lycaenidae Mealybugs Predator Spalgis epius coccus hirsutus (Green) (Mani et al. 1987) in India. Fur- thermore, the larva of S. epius has been reported as a potential predator of P. citri in coffee plantations, and M. hirsutus in mulberry gardens in India (Gowda et al. 1996; Mani 1995; Rahiman and Vijayalakshmi 1998). P. citri and M. hirsutus are major pests of coffee and mulberry, respectively, in India (Le Pelley 1968; Thanga- Communicated by D.C. Weber. mani and Vivekanandan 1983). S. epius occurs in India, Burma and Sri Lanka (De Niceville 1890), Philippines and A. S. Dinesh M. G. Venkatesha (&) S. Ramakrishna Bangalore University, Bengaluru, India Java (Le Pelley 1943), Bangladesh (Ali 1978), and Thai- e-mail: [email protected] land (Lohman and Samarita 2009). S. epius inhabits 123 J Pest Sci agricultural and wooded areas and is not commonly seen in pupa, and adult were measured with a calibrated eyepiece the field due to its small size and drab colour (Venkatesha micrometer in a stereo zoom microscope. External mor- et al. 2004). De Niceville (1890) and Bingham (1907) have phologies of the egg, each larval instar, prepupa, pupa and described the morphology of S. epius adults. Venkatesha adult were also studied. et al. (2004) and Venkatesha (2005) have made preliminary observations on the behaviour of S. epius and its interaction Biology with in the field. Although S. epius is an important predator of mealybugs Observations on the eclosion timing, sex ratio, mating and in India, virtually no research has been conducted on its egg-laying behaviour of adults and the larval feeding habit development and biology. Moreover, no detailed life his- were recorded. The durations of the preoviposition and tory and biology of any hemipteran-feeding lycaenid but- oviposition periods were documented. Freshly eclosed terfly has been studied so far. The objective of this study female and male adults of uniform size and age were iso- was to determine the development of immature stages, life lated and kept in nylon cages (30 cm 9 30 cm 9 30 cm) history and behaviour of S. epius that was reared on P. citri singly, and the influence of nutrition on longevity was in the laboratory. studied by feeding the adults independently on three diets: 10% honey (diluted in water), ripe banana, and tap water. Adults without food or water were maintained as controls. Materials and methods The mortality of the adults fed on different diets including control was recorded at 24-h intervals. In order to deter- Field source and lab rearing of predator mine the potential fecundity, 2-day-old adult females were dissected, and the numbers of immature and mature eggs In order to rear S. epius in the laboratory, mealybug P. citri present in the ovaries were noted. was cultured on pumpkins (Cucurbita maxima Duchesne) following the method of Serrano and Lapointe (2002). The Data analysis mealybug-infested pumpkin was maintained in a nylon rearing cage (30 cm 9 30 cm 9 30 cm). A few S. epius The student t-test was employed to analyse the differences larvae were collected from the mealybug infested croton in body length and wingspan between the female and male plants (Codiaeum spp.) at the Bangalore University cam- butterflies. The differences in longevity of the fed females pus, Bengaluru, India (latitude 12°580N, longitude 77°350E, and males on different diets as well as control were ana- elevation 921 m). The field-collected larvae were reared on lysed utilizing one way ANOVA-Tukey HSD test (SPSS the mealybug-infested pumpkins in the laboratory. Adults Inc 2001). The growth of the larval length and width, and of S. epius emerged in the laboratory were allowed to mate the larval length and head capsule width were correlated. in an outdoor nylon mating cage (6 m width 9 6m length 9 10 m height) and provided with mealybug- infested pumpkins for egg deposition in the same cage. The Results eggs laid in the mass of mealybugs on the pumpkin were carefully separated and kept individually in Petri dishes Morphology (5 cm diameter). Newly emerged larvae from these eggs were maintained in the same Petri dishes and provided with Egg: Colour greenish-blue when laid, changing to whitish egg masses and nymphs of mealybugs as food until they before hatching. Egg disk-shaped, sculptured, and both the reached prepupal stage. The predator was reared under the top and bottom flattened with micropylar depression in the variable mean maximum temperature 29.0 ± 1.8°C, mean top (Fig. 1a). Egg 0.48 ± 0.05 mm in diameter. minimum temperature 26.5 ± 1.4°C, and mean relative Larva: It moulted three times, and there were four larval humidity 44.4 ± 6.7% RH. instars. The length and width, and the head capsule width of four larval instars are given in Table 1. Life cycle and morphology First instar larva: Body pale white with dark brown head, fringed with fine white setae (Fig. 1b). The moulting of the larvae was confirmed by examining Second instar larva: Head dark brown. Body grey with the Petri dishes daily for exuviae and head capsules. The white mid-dorsal line and slightly covered with white wax egg, larval, prepupal and pupal developmental period, and coating, broken at each segment, and slug like. Setae more number of instars in a life cycle were recorded. The egg, prominent and interwoven with eggs of mealybugs each larval instar, head capsule of each instar, prepupa, (Fig. 1c).

123 J Pest Sci

Fig. 1 Spalgis epius a Egg; b I instar larva; c II instar larva; d III instar larva; e IV instar larva; f prepupa; g pupa; h female, dorsal side; i male, dorsal side; j female, ventral side; k male, ventral side; l larvae feeding on mealybugs and m adults in copula

Table 1 Measurements (mm) of the larva, prepupa, pupa and head capsule of Spalgis epius Stages n Length Width Head capsule width Mean ± SD Range Mean ± SD Range Mean ± SD Range

Larva I instar 20 1.9 ± 0.1 1.8–2.2 0.6 ± 0.08 0.5–0.8 0.23 ± 0.04 0.2–0.3 II instar 20 3.4 ± 0.1 3.2–3.8 1.7 ± 0.1 1.5–1.9 0.43 ± 0.04 0.4–0.5 III instar 20 6.6 ± 0.5 5.8–7.2 3.8 ± 0.2 3.4–4.2 0.82 ± 0.04 0.8–0.9 IV instar 20 11.4 ± 0.5 10.5–12.1 6.6 ± 0.4 5.6–7.1 1.03 ± 0.04 1.0–1.1 Prepupa 20 7.9 ± 0.6 7.0–9.0 4.1 ± 0.2 4.0–4.5 – – Pupa 20 6.9 ± 0.3 6.5–7.5 3.9 ± 0.2 3.9–4.2 – –

Third instar larva: Similar to second instar but with Pupa: Light brown on the dorso-lateral side and whitish brown mid-dorsal line and covered with thick wax coating grey on the ventral side. The bold pattern on the hard dorsal (Fig. 1d). Setae interwoven with debris of mealybugs. side of the pupa resembled the face of a rhesus monkey Fourth instar larva: Similar to third instar larva with (Fig. 1g). The pupa showed clear spots of eyes, nose and much shorter setae (Fig. 1e). Length and width were not cheeks on the dorsal side, and gradually darkened as significantly correlated in any larval instars. Similarly, development proceeded. The length and width of prepupa head capsule width was not significantly correlated with and pupa are given in Table 1. larval length. Adult: Small butterfly with dark brown wings above in Prepupa: The prepupal larva shrunk and turned to dull male, but light grayish brown in female, and grey underside black colour (Fig. 1f). Setae almost disappeared. with dark striations in both sexes. Forewing has a 123 J Pest Sci prominent small quadrate spot at the cell end in male, and thereafter it moves out of the chamber for feeding, and whereas it is larger and somewhat diffuse in female. The its setae were entangled with mealybug eggs and wax. The male is darker in colour when compared to the female third and fourth instar larvae ate the eggs, nymphs and (Fig. 1h, i). Forewing of male is elongate and sharp at adults of mealybugs, and they were far bigger than apex, but it is short and roundish in female (Fig. 1j, k). mealybugs (Fig. 1l). The first and second instar larvae were Abdomen of the male is slender, but it is broader in the almost sedentary, whereas the third and fourth instars crawl female. Mean body length and wingspan of the female and while feeding. A single larva consumed 1975–2592 eggs, male was 10.5 ± 0.6 and 11.1 ± 1.1 mm, and 27.7 ± 1.5 115–175 nymphs and 27–35 adults of mealybugs during its and 29.4 ± 2.4 mm, respectively. The body length entire development. The fourth instar larva passed through between sexes was not significantly different (t = 1.9, two distinct phases: an active feeding stage; and a non- P [ 0.05), but wingspan of male was significantly longer feeding quiescent prepupa. The larva stopped feeding and than that of female (t = 2.6, P \ 0.05). cleared debris before entering into prepupal stage. The prepupa usually moved away from mealybug colony and Life history firmly attached itself to the substratum. The prepupa secreted a small quantity of silk before moulting for Developmental period of the egg, four larval instars, pre- cementing pupa to the substratum. pupa and pupa are presented in Table 2. S. epius completed its life cycle in 23.8 ± 1.5 days under the variable mean Eclosion maximum temperature 29.0 ± 1.8°C, mean minimum temperature 26.5 ± 1.4°C, mean relative humidity The adults eclosed invariably between 1130 and 1530 h. 44.4 ± 6.7% RH and photoperiod 12L:12D. S. epius is a Wings expanded in 1–2 min following eclosion. The fresh multivoltine species, which completed 10–12 generations adults rest for varying period of time ranging from 1 to 4 h in a year. and generally the first flight took place before dusk on the day of emergence. The female and the male butterfly Larval feeding behaviour enclosed almost at same timings from the same aged pupae. The female-to-male sex ratio of 1109 laboratory- The first instar larva ate egg mass of mealybugs and made a bred individuals was 1.45:1. feeding chamber in the mealybug colony, especially amongst egg masses, and it moulted there itself. It nibbled Mating small mealybug nymphs (0.2–0.5 mm) if the eggs were not available for feeding and damaged nymphs were killed. Adults mated a day after eclosion in the outdoor mating The fresh second instar larva fed on the eggs and small cage. Mating took place generally between 1130 and nymphs of mealybugs inside the old chamber for one day 1400 h under bright or diffused sunlight. Initially male marked the territory by perching on some fixed spots. The territory was marked by dragging its abdominal tip on the substratum. Subsequently, it occasionally made spontane- Table 2 Developmental period of different stages of Spalgis epius ous flight in a limited range around the perch points. While under the laboratory conditions resting in between territory flights, the male spreads its Stages n Duration of development (days) wings to sunlight for 1–2 min. The male defended its ter- Mean ± SD Range ritory if another male intruded. Under such circumstance, the two males undertake a circling flight, and the resident Egg 20 3.9 ± 0.5 3.0–4.5 typically chased away the intruder, then resting in its ter- Larva ritory. The female was attracted to the male in the territory, I instar 20 2.1 ± 0.4 1.5–3.0 and as soon as a female entered the territory, the pair II instar 20 2.0 ± 0.2 1.5–2.5 engaged in a courtship flight. The courtship flight distance III instar 20 2.0 ± 0.1 1.9–2.5 between the pair was &12–18 cm. The pair engaged in 3–4 IV instar 20 3.4 ± 0.5 2.5–4.0 flights at an interval of 4–5 min, and then the female Total larval period 20 9.4 ± 0.9 8.5–11.0 alighted on a perch in the territory, followed by the male Prepupa 20 0.9 ± 0.0 0.9–1.0 which approached the female, and the pair copulated in Pupa 20 9.5 ± 1.3 8.0–12 tail-to-tail position. During copulation, the abdomens of Egg to adult 20 23.8 ± 1.5 19.9–26.5 both sexes were slightly raised with their head pointed Max. temp 29.0 ± 1.8°C, min. temp 26.5 ± 1.4°C and 44.4 ± 6.7% downwards (Fig. 1m). The pair remained in copula on an RH average of 61.3 ± 6.2 min. Observations were made in 68 123 J Pest Sci copulated pairs; the males and females were found to mate differences among longevities of individuals fed on dif- only once in their lifetime. ferent diets. Males lived slightly longer on honey than on banana (Tukey HSD, F = 7.8, df = 20, P \ 0.05), Fecundity whereas females lived slightly longer on water than on honey (Tukey HSD, F = 25.0, df = 20, P \ 0.05). Spalgis epius is a synovigenic butterfly, and the mean total number of mature and immature eggs present in the dis- sected gravid female was 74.6 ± 8.6. The preoviposition Discussion period was 3–4 days after mating. The gravid female flew rapidly to the vicinity of mealybug-infested pumpkin, and The Egg of Spalgis epius was disc shaped, greenish-blue in it swiftly deposited eggs in the mass of the mealybugs. The colour and sculptured as reported in predatory lycaenid, female deposited on an average of 47.3 ± 6.8 eggs per day Feniseca tarquinius (F.) (Hall et al. 2007) as well as in generally between 1130 and 1530 h under bright/diffused many other phytophagous lycaenids, Paralucia pyrodiscus sunlight in 1–2 days. It deposited eggs singly interspersed lucida Crosby (Braby 1990), Rapala takasagonis Mat- with many short flights, and in each flight, 3–6 eggs were sumura (Hsu et al. 2005), and Lampides boeticus L. laid closely at different spots. It landed to rest persistently (Vijayachander and Arivudainambi 2007). Size of S. epius on its preferred perch during egg-laying flights and cleaned egg is similar to that of other lycaenid butterflies viz., its ovipositor by rubbing against the perch. The female Philiris ziska Grose-Smith and P. intensa Butler (Parsons survived 1–3 days after oviposition. 1984), P. pyrodiscus lucida (Braby 1990) and Calycopis caulonia (Hewitson) (Duarte et al. 2005). Longevity There were four larval instars in S. epius as reported in carnivorous lycaenid butterfly, F. tarquinius (Hall et al. Both the male and female butterflies emerging in the lab- 2007) and in phytophagous lycaenids, R. takasagonis (Hsu oratory readily accepted liquid food or juicy fruits. Lon- et al. 2005) and L. boeticus (Vijayachander and Arivu- gevity of the female and male adults fed on different diets dainambi 2007). The size of four larval instars of S. epius is including starving is presented in Fig. 2. There was no similar to those reported in other species of lycaenids significant difference in longevity between males and namely, P. pyrodiscus lucida (Braby 1990) and Lycaeides females in any treatment. Overall the starved individuals melissa samuelis Nabokov (Herms et al. 1996). Similarly, died sooner than fed individuals regardless of different head capsule widths of four larval instars of S. epius are diets, and it was significantly different (Tukey HSD, almost similar to that recorded in L. boeticus (Vijayac- F = 24.2, df = 40, P \ 0.05). There were some small hander and Arivudainambi 2007). The first instar larva of the predator was whitish with fine setae, and from the second instar onwards, larva was slug like and covered 8 with white wax coating like F. tarquinius (Hall et al. 2007). Male Fe m ale b 7 B The first instar larvae were found feeding only on egg ab B a masses of the mealybugs, but the second instar larvae fed 6 A on the egg masses and young nymphs of the mealybugs. 5 However, the third and fourth instar larvae voraciously fed A 4 on all stages of the mealybugs. White wax coated larvae of c 3 S. epius were camouflaged with the mass of the mealybugs as reported earlier (Venkatesha et al. 2004). Similarly, 2 Longevity in days larvae of (Holl.) in Africa (Lamborn 1914) 1 and Spalgis substrigata (Snell) in Philippines (Smith 1914) 0 were camouflaged with the mealybug population. Mean Banana Honey Water Starved total larval period in S. epius was 9.4 days, whereas it was Nutrition 11.9 days in phytophagous lycaenid L. boeticus under similar rearing conditions (Vijayachander and Arivudain- Fig. 2 Longevity of Spalgis epius adults fed on different nutritions. Bars with different capital letters indicate significant differences ambi 2007). It is reported that hemipteran-feeding lycaenid among different nutritions within the males at P \ 0.05. Bars with larvae spend less time in the larval stage than do their different small letters indicate significant differences among different phytophagous counterparts (Clark 1926; Banno 1990). P \ nutritions within the females at 0.05 (one way ANOVA-Tukey The peculiar monkey-faced pupa of S. epius was similar HSD test). There was no significant difference between male and female longevity irrespective of any diet treatment. (Vertical line to that of F. tarquinius (Hall et al. 2007). Balduf (1939) indicates SE mean of total longevity) considered the monkey-faced appearance of some lycaenid 123 J Pest Sci pupae as a means of protection, but did not clearly state its This study provided a detailed life history and biology of significance. a predatory lycaenid butterfly, S. epius for the first time, The external morphology of Spalgis epius adults was and this information could be utilized to develop S. epius as similar to those observed by De Niceville (1890) and an effective biocontrol agent of mealybugs. Bingham (1907). Wingspan of male was greater than that of females, and it was significantly different (P \ 0.05) Acknowledgments The authors thank University Grants Commis- because of elongated forewings at apex. sion (UGC), New Delhi, India for providing financial assistance to carry out the above work. The first author is grateful to the UGC for The male and female butterflies invariably eclosed providing the fellowship. simultaneously from the pupae of the same age in the laboratory and did not show protandry as commonly reported in lycaenid butterfly, Glaucopsyche lygdamus References palosverdesensis Perkins and Emmel (Longcore et al. 2002) and other butterfly species (Neve and Singer 2008). Aitken EH (1894) The larva and pupa of Spalgis epius Westwood. Although protandry is widespread phenomenon in , J Bombay Nat Hist Soc 8:485–489 Ceroplastas pseudoce- it is not ubiquitous in butterflies (Zonneveld 1996). The Ali M (1978) A report on the wax scales, on riferus Green, and Chloropulvinaria polygonata (Ckll.) activity of adults between 1130 and 1600 h indicated that (Homoptera: ) on mango and their natural enemies. warmer weather and bright sunlight were necessary for Bangladesh J Zool 6:69–70 mating and egg-laying activities. It was reported that Ayyar TVR (1929) Notes on some Indian Lepidoptera with abnormal Lycaena arota habits. J Bombay Nat Hist Soc 33:668–675 females of (Boisduval) (Lycaenidae) lay Balduf WV (1939) The bionomics of entomophagous . Part II. eggs during warmer hours of the day from 0900 to 1430 h Swift, St. Louis (Scott 1974). Banno H (1990) Plasticity of size and relative fecundity in the Female-to-male sex ratio in S. epius was 1.45:1. The aphidophagous lycaenid butterfly, hamada. Ecol Ento- females and males of S. epius mated next day of their mol 15:111–113 Bingham CT (1907) The fauna of British India including Ceylon and emergence as observed in L. arota (Scott 1974). The territory Burma. Butterflies. Taylor and Francis, London marking and flight pattern of males and subsequent courtship Braby MF (1990) The life history and biology of Paralucia and mating behaviours in S. epius was similar to those of pyrodiscus lucida Crosby (Lepidoptera: Lycaenidae). J Aust other lycaenids such as Pseudophilotes baton Bergstrasser Entomol Soc 29:41–50 Browning HW (1992) Overview of biological control of homopterous (Vaisanen et al. 1994), Collophrys xami (Reakirt) (Cordero pests in the Caribbean. Fla Entomol 75:440–446 et al. 2000), Chrysozephyrus smaragdinus Bremer (Takeu- Chacko MJ, Bhat PK (1976) Record of Ferrisia virgata and its natural chi and Imafuku 2005) and L. boeticus (Vijayachander and enemy, Spalgis epius, on coffee in India. J Coffee Res 6:56–57 Chacko MJ, Bhat PK, Ramanarayan EP (1977) New records of Arivudainambi 2007). The average copulation duration of coccoidea with notes on natural enemies of Planococcus spp. on 61.37 min in S. epius was similar to that of L. boeticus coffee in India. J Coffee Res 7:69–71 (Vijayachander and Arivudainambi 2007). Both sexes of Clark AH (1926) Carnivorous butterflies. In: Annu Rep. Smithsonian S. epius mated only once; however, multiple matings have Institution, US, 2856, pp 439–508 been reported in males of C. xami (Cordero et al. 2000). Cordero C, Macias R, Jimenez G (2000) The number of copulations of territorial males of the butterfly Callophrys xami (Lycaeni- The gravid females of S. epius laid eggs singly as dae). J Res Lepid 35:78–89 reported in other lycaenids: Philiris helena Snellen and De Niceville L (1890) The butterflies of India, Burma and Ceylon. Philiris intensa Butler (Parsons 1984); Megisba strongyle Calcutta Central Press Co Ltd, India nigra (Miskin) (Lambkin and Samson 1989); Petrelaea Duarte M, Robbins RK, Mielke OHH (2005) Immature stages of Calycopis caulonia (Hewitson, 1877) (Lepidoptera, Lycaenidae, tombugensis Rober (Samson and Lambkin 2003); and R. , Eumaeini), with notes on rearing detritivorous takasagonis (Hsu et al. 2005). The erratic flight and swift hairstreaks on artificial diet. Zootaxa 1063:1–31 egg-laying patterns of S. epius female butterfly were sim- Fischer K, Fiedler K (2001) Effects of adult feeding and temperature F. tarquinius regime on fecundity and longevity in the butterfly Lycaena ilar to those recorded in (Hall et al. 2007). hippothoe (Lycaenidae). J Lepid Soc 54:91–95 Adults of S. epius fed on different diets showed that Gowda DKS, Manjunath D, Datta RK, Kumar P (1996) Spalgis epius females and males fed on water and honey, respectively, Westwood (Lepidoptera: Lycaenidae) a potential predator of survived longer than that of individuals fed on other diets. mulberry mealybug, Maconellicoccus hirsutus. Insect Environ Moreover, longevity of S. epius adults fed on various diets 2:87–88 Hall DW, Minno M, Butler JF (2007) Harvester butterfly, Feniseca was significantly more than that of the starved individuals. tarquinius (Fabricius) (Insecta:Lepidoptera: Lycaenidae: Melit- It clearly indicated that food enhances the longevity of inae). In: University of Florida IFAS extension. EENY-404. adults of S. epius. Sucrose was known to enhance the Available via http://creatures.ifas.ufl.edu. Accessed 10 Sept 2009 longevity of adult lycaenids viz., Jalamenus evagoras Herms CP, McCullough DG, Miller DL, Bauer LS, Haack RA (1996) Laboratory rearing of Lycaeides melissa samuelis (Lepidoptera: (Dovan) (Hill and Pierce 1989) and Lycaena hippothoe L. Lycaenidae), an endangered butterfly in Michigan. Great Lakes (Fischer and Fiedler 2001). Entomol 29:63–75 123 J Pest Sci

Hill CJ, Pierce NE (1989) The effect of adult diet on the biology of Rahiman AP, Vijayalakshmi CK (1998) Spalgius epius Westwood butterflies 1. The common imperial blue Jalmenus evagoras. (Lepidoptera: Lycaenidae)—a potential predator of coffee mealy Oecologia 81:249–257 bugs. J Entomol Res 22:191–192 Hsu Y, Wang L, Huang H, Lu C (2005) Notes on immature biology Samson PR, Lambkin TA (2003) The immature stages and seasnolity and distribution of Rapala takasagonis Matsumura (Lepidoptera: of Petrelaea tombugensis (Rober) (Lepidoptera: Lycaenidae). Lycaenidae: Theclinae). Bioformosa 40:53–57 Aust Entomol 30:181–183 Lambkin TA, Samson PR (1989) The life history of Megisba Serrano MS, Lapointe SL (2002) Evaluation of host plants and a strongyle nigra (Miskin) (Lepidoptera: Lycaenidae). Aust Ento- meridic diet for rearing Maconellicoccus hirsutus (Hemiptera: mol Mag 16:75–77 Pseudococcidae) and its parasitoid Anagyrus kamali (Hymenop- Lamborn WA (1914) On the relationship between certain West tera: Encyrtidae). Fla Entomol 85:417–425 African insects, especially ants, Lycaenidae and homoptera. Scott JA (1974) Population biology and adult behavior of Lycaena Trans Entomol Soc Lond 61:438–524 arota (Lepidoptera). J Lepid Soc 28:64–75 Le Pelley RH (1943) An oriental mealybug ( lilacinus) Scudder SH (1899) Every-day butterflies. Mifflin and Co., Boston and its natural enemies. Trans R Entomol Soc Lond 93:73–93 Smith HS (1914) Mealy bug parasites in the Far East. Mon Bull St Le Pelley RH (1968) Pests of coffee. Longmans Green and Co Ltd, Comm Hort Calif 3:26–29 London SPSS Inc (2001) SPSS for windows, Rel. 11.0.0. SPSS Inc, Chicago Lohman DJ, Samarita VU (2009) The biology of carnivorous butterfly Takeuchi T, Imafuku M (2005) Territorial behaviour of a Green larvae (Lepidoptera: Miletinae: Miletini) and their ant-tended Hairstreak Chrysozephyrus smaragdinus (Lepidoptera: Lycaeni- hemipteran prey in Thailand and the Philippines. J Nat Hist dae): site tenacity and wars of attrition. Zool Sci 22:989–994 43:569–581 Thangamani R, Vivekanandan M (1983) Effective utilization of tukra Longcore T, Mattoni R, Lipman A, Krenova Z, Rich C (2002) Palos diseased mulberry leaves as silkworm, Bombyx mori L. feed. Verdes blue butterfly year 2002 captive rearing on defense fuel Sericologia 23:211–223 support point, San Pedro, California. In: Final report. The Urban Vaisanen R, Kuussaari M, Nieminen M, Somerma P (1994) Biology Wildlands Group (Defense Logistics Agency Agreement # and conservation of Pseudophilotes baton in Finland (Lepidop- N68711-02-LT-00010), Los Angeles, 17 pp tera: Lycaenidae). Ann Zool Fenn 31:145–156 Mani M (1995) Studies on the natural enemies of oriental mealybug, Venkatesha MG (2005) Why is homopterophagous butterfly, Spalgis Planococcus lilacinus (CKll.) (Homoptera: Pseudococcidae) in epius (Westwood) (Lepidoptera: Lycaenidae) amyrmecophilous? India. J Entomol Res 19:61–70 Curr Sci 89:245–246 Mani M, Thontadarya TS, Sing SP (1987) Record of natural enemies Venkatesha MG, Shashikumar L, Gayathri Devi SS (2004) Protective on the grape mealybug, Maconellicoccus hirsutus (Green). Curr devices of the Carnivorous butterfly, Spalgis epius (Westwood) Sci 56:624–625 (Lepidoptera: Lycaenidae). Curr Sci 87:571–572 Misra CS (1920) Tukra disease of mulberry. In: Rep Proc Third Vijayachander A, Arivudainambi S (2007) Biology of pulses blue Entomological Meeting, Pusa, vol 2, pp 610–618 butterfly, Lampides boeticus Linn. Ann Plant Prot Sci 15:53–56 Neve G, Singer MC (2008) Protandry and postandry in two Wynhoff I, van der Made J, Oostermeijer G (1998) Why a Maculinea butterflies: conflicting evidence about sex specific tradeoffs special issue? J Insect Conserv 2:1 between adult size and emergence time. Evol Ecol 22:701–709 Zonneveld C (1996) Being big or emerging early? Polyandry and the Parsons M (1984) Life histories of four species of Philiris Rober trade-off between size and emergence in male butterflies. Am (Lepidoptera: Lycaenidae) from Papua New . J Lepid Soc Nat 147:946–965 38:15–22 Pierce NE (1995) Predatory and parasitic Lepidoptera: carnivores living on plants. J Lepid Soc 49:412–453

123