J Pest Sci (2010) 83:339–345 DOI 10.1007/s10340-010-0303-8
ORIGINAL PAPER
Development, life history characteristics and behaviour of mealybug predator, Spalgis epius (Westwood) (Lepidoptera: Lycaenidae) on Planococcus citri (Risso) (Homoptera: Pseudococcidae) Anegunda S. Dinesh • Melally G. Venkatesha Sompalyam Ramakrishna
•
Received: 1 November 2009 / Accepted: 1 April 2010 / Published online: 14 April 2010 Ó Springer-Verlag 2010
Abstract The development of immature stages, life history and behaviour of mealybug predator, Spalgis epius (Westwood) (Lepidoptera: Lycaenidae) reared on mealybugs, Planococcus citri (Risso) (Homoptera: Pseudococcidae) was studied in the laboratory. Larvae of S. epius are a potential predator of different species of mealybugs in India. The predator completed its life cycle in 23.8 days with four larval instars. Mean incubation period of egg was 3.9 days. Mean duration of development of larval stages, prepupa and pupa was 9.4, 0.9 and 9.5 days, respectively. The first and last instar larvae measured 1.9 and 11.4 mm in length, respectively. Length and width were not significantly correlated in larvae. Head capsule width was not significantly correlated with larval length in any instar. The female-to-male sex ratio was 1.45:1. Adults were ready for mating one day after eclosion. The pairs remained in copula on an average of 61.3 min. The gravid female contained 74.6 eggs in the ovaries. Unfed butterflies (both males and females) lived 3–4 days, significantly shorter than those with access to water (6–7 days). The results of this study will be useful to utilize the predator as a biocontrol agent. Keywords Development Life history Lepidoptera Lycaenidae Mealybugs Predator Spalgis epius
Communicated by D.C. Weber. A. S. Dinesh M. G. Venkatesha (&) S. Ramakrishna Bangalore University, Bengaluru, India e-mail:
[email protected]
Introduction More than 99% of Lepidoptera survive solely on living plants (Pierce 1995). Among the aphytophagous Lepidoptera, about 120 species in the subfamily Miletinae (Lepidoptera: Lycaenidae) feed on ant brood or Hemiptera (Pierce 1995). Most of the aphytophagous butterflies are extremely rare, and several are endangered (Pierce 1995; Wynhoff et al. 1998). The genera Spalgis Moore, Tharaka Doherty and Feniseca Grote of Miletinae feed on ant-tended Hemiptera (including Homoptera). These hemipteranfeeders live among their prey without provoking an escape response or an attack response from the ant mutualists of Hemiptera (Scudder 1899). Different species of mealybugs (Homoptera: Pseudococcidae) are serious pests of wide range of economically important crops such as coffee, citrus, guava, mango, mulberry, vegetables, ornamental plants, etc., worldwide (Browning 1992). The apefly, Spalgis epius (Lepidoptera: Lycaenidae: Miletinae) has been recorded as a predator of various species of mealybugs viz., Dactylopius sp. (Aitken 1894), Planococcus virgatus (Ckll.) (Misra 1920), P. lilacinus (Ckll.) (Ayyar 1929), P. citri (Risso) (Chacko et al. 1977), Ferrisia virgata (Ckll.) (Chacko and Bhat 1976) and Maconellicoccus hirsutus (Green) (Mani et al. 1987) in India. Furthermore, 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; Thangamani and Vivekanandan 1983). S. epius occurs in India, Burma and Sri Lanka (De Niceville 1890), Philippines and Java (Le Pelley 1943), Bangladesh (Ali 1978), and Thailand (Lohman and Samarita 2009). S. epius inhabits
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agricultural and wooded areas and is not commonly seen in the field due to its small size and drab colour (Venkatesha et al. 2004). De Niceville (1890) and Bingham (1907) have described the morphology of S. epius adults. Venkatesha et al. (2004) and Venkatesha (2005) have made preliminary observations on the behaviour of S. epius and its interaction with ants in the field. Although S. epius is an important predator of mealybugs in India, virtually no research has been conducted on its development and biology. Moreover, no detailed life history and biology of any hemipteran-feeding lycaenid butterfly has been studied so far. The objective of this study was to determine the development of immature stages, life history and behaviour of S. epius that was reared on P. citri in the laboratory.
Materials and methods Field source and lab rearing of predator In order to rear S. epius in the laboratory, mealybug P. citri was cultured on pumpkins (Cucurbita maxima Duchesne) following the method of Serrano and Lapointe (2002). The mealybug-infested pumpkin was maintained in a nylon rearing cage (30 cm 9 30 cm 9 30 cm). A few S. epius larvae were collected from the mealybug infested croton plants (Codiaeum spp.) at the Bangalore University campus, Bengaluru, India (latitude 12°580 N, longitude 77°350 E, elevation 921 m). The field-collected larvae were reared on the mealybug-infested pumpkins in the laboratory. Adults of S. epius emerged in the laboratory were allowed to mate in an outdoor nylon mating cage (6 m width 9 6 m length 9 10 m height) and provided with mealybuginfested pumpkins for egg deposition in the same cage. The eggs laid in the mass of mealybugs on the pumpkin were carefully separated and kept individually in Petri dishes (5 cm diameter). Newly emerged larvae from these eggs were maintained in the same Petri dishes and provided with egg masses and nymphs of mealybugs as food until they reached prepupal stage. The predator was reared under the variable mean maximum temperature 29.0 ± 1.8°C, mean minimum temperature 26.5 ± 1.4°C, and mean relative humidity 44.4 ± 6.7% RH. Life cycle and morphology The moulting of the larvae was confirmed by examining the Petri dishes daily for exuviae and head capsules. The egg, larval, prepupal and pupal developmental period, and number of instars in a life cycle were recorded. The egg, each larval instar, head capsule of each instar, prepupa,
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pupa, and adult were measured with a calibrated eyepiece micrometer in a stereo zoom microscope. External morphologies of the egg, each larval instar, prepupa, pupa and adult were also studied. Biology Observations on the eclosion timing, sex ratio, mating and egg-laying behaviour of adults and the larval feeding habit were recorded. The durations of the preoviposition and oviposition periods were documented. Freshly eclosed female and male adults of uniform size and age were isolated and kept in nylon cages (30 cm 9 30 cm 9 30 cm) singly, and the influence of nutrition on longevity was 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. The mortality of the adults fed on different diets including control was recorded at 24-h intervals. In order to determine the potential fecundity, 2-day-old adult females were dissected, and the numbers of immature and mature eggs present in the ovaries were noted. Data analysis The student t-test was employed to analyse the differences in body length and wingspan between the female and male butterflies. The differences in longevity of the fed females and males on different diets as well as control were analysed utilizing one way ANOVA-Tukey HSD test (SPSS Inc 2001). The growth of the larval length and width, and the larval length and head capsule width were correlated.
Results Morphology Egg: Colour greenish-blue when laid, changing to whitish before hatching. Egg disk-shaped, sculptured, and both the top and bottom flattened with micropylar depression in the top (Fig. 1a). Egg 0.48 ± 0.05 mm in diameter. Larva: It moulted three times, and there were four larval instars. The length and width, and the head capsule width of four larval instars are given in Table 1. First instar larva: Body pale white with dark brown head, fringed with fine white setae (Fig. 1b). Second instar larva: Head dark brown. Body grey with white mid-dorsal line and slightly covered with white wax coating, broken at each segment, and slug like. Setae more prominent and interwoven with eggs of mealybugs (Fig. 1c).
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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 Mean ± SD
Width Range
Mean ± SD
Head capsule width 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
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
IV instar
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 brown mid-dorsal line and covered with thick wax coating (Fig. 1d). Setae interwoven with debris of mealybugs. Fourth instar larva: Similar to third instar larva with much shorter setae (Fig. 1e). Length and width were not significantly correlated in any larval instars. Similarly, head capsule width was not significantly correlated with larval length. Prepupa: The prepupal larva shrunk and turned to dull black colour (Fig. 1f). Setae almost disappeared.
Pupa: Light brown on the dorso-lateral side and whitish grey on the ventral side. The bold pattern on the hard dorsal side of the pupa resembled the face of a rhesus monkey (Fig. 1g). The pupa showed clear spots of eyes, nose and cheeks on the dorsal side, and gradually darkened as development proceeded. The length and width of prepupa and pupa are given in Table 1. Adult: Small butterfly with dark brown wings above in male, but light grayish brown in female, and grey underside with dark striations in both sexes. Forewing has a
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prominent small quadrate spot at the cell end in male, whereas it is larger and somewhat diffuse in female. The male is darker in colour when compared to the female (Fig. 1h, i). Forewing of male is elongate and sharp at apex, but it is short and roundish in female (Fig. 1j, k). Abdomen of the male is slender, but it is broader in the female. Mean body length and wingspan of the female and male was 10.5 ± 0.6 and 11.1 ± 1.1 mm, and 27.7 ± 1.5 and 29.4 ± 2.4 mm, respectively. The body length between sexes was not significantly different (t = 1.9, P [ 0.05), but wingspan of male was significantly longer than that of female (t = 2.6, P \ 0.05). Life history Developmental period of the egg, four larval instars, prepupa and pupa are presented in Table 2. S. epius completed its life cycle in 23.8 ± 1.5 days under the variable mean maximum temperature 29.0 ± 1.8°C, mean minimum temperature 26.5 ± 1.4°C, mean relative humidity 44.4 ± 6.7% RH and photoperiod 12L:12D. S. epius is a multivoltine species, which completed 10–12 generations in a year. Larval feeding behaviour The first instar larva ate egg mass of mealybugs and made a feeding chamber in the mealybug colony, especially amongst egg masses, and it moulted there itself. It nibbled small mealybug nymphs (0.2–0.5 mm) if the eggs were not available for feeding and damaged nymphs were killed. The fresh second instar larva fed on the eggs and small nymphs of mealybugs inside the old chamber for one day
Table 2 Developmental period of different stages of Spalgis epius under the laboratory conditions Stages
n
Duration of development (days) Mean ± SD
Egg
20
Range
3.9 ± 0.5
3.0–4.5
Larva I instar
20
2.1 ± 0.4
1.5–3.0
II instar
20
2.0 ± 0.2
1.5–2.5
III instar
20
2.0 ± 0.1
1.9–2.5
IV instar
20
3.4 ± 0.5
2.5–4.0
Total larval period
20
9.4 ± 0.9
8.5–11.0
Prepupa
20
0.9 ± 0.0
0.9–1.0
Pupa
20
9.5 ± 1.3
8.0–12
Egg to adult
20
23.8 ± 1.5
19.9–26.5
Max. temp 29.0 ± 1.8°C, min. temp 26.5 ± 1.4°C and 44.4 ± 6.7% RH
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and thereafter it moves out of the chamber for feeding, and its setae were entangled with mealybug eggs and wax. The third and fourth instar larvae ate the eggs, nymphs and adults of mealybugs, and they were far bigger than mealybugs (Fig. 1l). The first and second instar larvae were almost sedentary, whereas the third and fourth instars crawl while feeding. A single larva consumed 1975–2592 eggs, 115–175 nymphs and 27–35 adults of mealybugs during its entire development. The fourth instar larva passed through two distinct phases: an active feeding stage; and a nonfeeding quiescent prepupa. The larva stopped feeding and cleared debris before entering into prepupal stage. The prepupa usually moved away from mealybug colony and firmly attached itself to the substratum. The prepupa secreted a small quantity of silk before moulting for cementing pupa to the substratum. Eclosion The adults eclosed invariably between 1130 and 1530 h. Wings expanded in 1–2 min following eclosion. The fresh adults rest for varying period of time ranging from 1 to 4 h and generally the first flight took place before dusk on the day of emergence. The female and the male butterfly enclosed almost at same timings from the same aged pupae. The female-to-male sex ratio of 1109 laboratorybred individuals was 1.45:1. Mating Adults mated a day after eclosion in the outdoor mating cage. Mating took place generally between 1130 and 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 spontaneous flight in a limited range around the perch points. While resting in between territory flights, the male spreads its wings to sunlight for 1–2 min. The male defended its territory if another male intruded. Under such circumstance, the two males undertake a circling flight, and the resident typically chased away the intruder, then resting in its territory. The female was attracted to the male in the territory, and as soon as a female entered the territory, the pair engaged in a courtship flight. The courtship flight distance between the pair was &12–18 cm. The pair engaged in 3–4 flights at an interval of 4–5 min, and then the female alighted on a perch in the territory, followed by the male which approached the female, and the pair copulated in tail-to-tail position. During copulation, the abdomens of both sexes were slightly raised with their head pointed downwards (Fig. 1m). The pair remained in copula on an average of 61.3 ± 6.2 min. Observations were made in 68
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copulated pairs; the males and females were found to mate only once in their lifetime. Fecundity Spalgis epius is a synovigenic butterfly, and the mean total number of mature and immature eggs present in the dissected gravid female was 74.6 ± 8.6. The preoviposition period was 3–4 days after mating. The gravid female flew rapidly to the vicinity of mealybug-infested pumpkin, and it swiftly deposited eggs in the mass of the mealybugs. The female deposited on an average of 47.3 ± 6.8 eggs per day generally between 1130 and 1530 h under bright/diffused sunlight in 1–2 days. It deposited eggs singly interspersed with many short flights, and in each flight, 3–6 eggs were laid closely at different spots. It landed to rest persistently on its preferred perch during egg-laying flights and cleaned its ovipositor by rubbing against the perch. The female survived 1–3 days after oviposition. Longevity Both the male and female butterflies emerging in the laboratory readily accepted liquid food or juicy fruits. Longevity of the female and male adults fed on different diets including starving is presented in Fig. 2. There was no significant difference in longevity between males and females in any treatment. Overall the starved individuals died sooner than fed individuals regardless of different diets, and it was significantly different (Tukey HSD, F = 24.2, df = 40, P \ 0.05). There were some small
8 b B
Longevity in days
7 6
Male
Fem ale
B
ab a A
5 A
4 c
3 2 1 0 Banana
Honey
Water
Starved
Nutrition
Fig. 2 Longevity of Spalgis epius adults fed on different nutritions. Bars with different capital letters indicate significant differences among different nutritions within the males at P \ 0.05. Bars with different small letters indicate significant differences among different nutritions within the females at P \ 0.05 (one way ANOVA-Tukey HSD test). There was no significant difference between male and female longevity irrespective of any diet treatment. (Vertical line indicates SE mean of total longevity)
differences among longevities of individuals fed on different diets. Males lived slightly longer on honey than on banana (Tukey HSD, F = 7.8, df = 20, P \ 0.05), whereas females lived slightly longer on water than on honey (Tukey HSD, F = 25.0, df = 20, P \ 0.05).
Discussion The Egg of Spalgis epius was disc shaped, greenish-blue in colour and sculptured as reported in predatory lycaenid, Feniseca tarquinius (F.) (Hall et al. 2007) as well as in many other phytophagous lycaenids, Paralucia pyrodiscus lucida Crosby (Braby 1990), Rapala takasagonis Matsumura (Hsu et al. 2005), and Lampides boeticus L. (Vijayachander and Arivudainambi 2007). Size of S. epius egg is similar to that of other lycaenid butterflies viz., Philiris ziska Grose-Smith and P. intensa Butler (Parsons 1984), P. pyrodiscus lucida (Braby 1990) and Calycopis caulonia (Hewitson) (Duarte et al. 2005). There were four larval instars in S. epius as reported in carnivorous lycaenid butterfly, F. tarquinius (Hall et al. 2007) and in phytophagous lycaenids, R. takasagonis (Hsu et al. 2005) and L. boeticus (Vijayachander and Arivudainambi 2007). The size of four larval instars of S. epius is similar to those reported in other species of lycaenids namely, P. pyrodiscus lucida (Braby 1990) and Lycaeides melissa samuelis Nabokov (Herms et al. 1996). Similarly, head capsule widths of four larval instars of S. epius are almost similar to that recorded in L. boeticus (Vijayachander 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 with white wax coating like F. tarquinius (Hall et al. 2007). The first instar larvae were found feeding only on egg masses of the mealybugs, but the second instar larvae fed on the egg masses and young nymphs of the mealybugs. However, the third and fourth instar larvae voraciously fed on all stages of the mealybugs. White wax coated larvae of S. epius were camouflaged with the mass of the mealybugs as reported earlier (Venkatesha et al. 2004). Similarly, larvae of Spalgis lemolea (Holl.) in Africa (Lamborn 1914) and Spalgis substrigata (Snell) in Philippines (Smith 1914) were camouflaged with the mealybug population. Mean total larval period in S. epius was 9.4 days, whereas it was 11.9 days in phytophagous lycaenid L. boeticus under similar rearing conditions (Vijayachander and Arivudainambi 2007). It is reported that hemipteran-feeding lycaenid larvae spend less time in the larval stage than do their phytophagous counterparts (Clark 1926; Banno 1990). The peculiar monkey-faced pupa of S. epius was similar to that of F. tarquinius (Hall et al. 2007). Balduf (1939) considered the monkey-faced appearance of some lycaenid
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pupae as a means of protection, but did not clearly state its significance. The external morphology of Spalgis epius adults was similar to those observed by De Niceville (1890) and Bingham (1907). Wingspan of male was greater than that of females, and it was significantly different (P \ 0.05) because of elongated forewings at apex. The male and female butterflies invariably eclosed simultaneously from the pupae of the same age in the laboratory and did not show protandry as commonly reported in lycaenid butterfly, Glaucopsyche lygdamus palosverdesensis Perkins and Emmel (Longcore et al. 2002) and other butterfly species (Neve and Singer 2008). Although protandry is widespread phenomenon in insects, it is not ubiquitous in butterflies (Zonneveld 1996). The activity of adults between 1130 and 1600 h indicated that warmer weather and bright sunlight were necessary for mating and egg-laying activities. It was reported that females of Lycaena arota (Boisduval) (Lycaenidae) lay eggs during warmer hours of the day from 0900 to 1430 h (Scott 1974). Female-to-male sex ratio in S. epius was 1.45:1. The females and males of S. epius mated next day of their emergence as observed in L. arota (Scott 1974). The territory marking and flight pattern of males and subsequent courtship and mating behaviours in S. epius was similar to those of other lycaenids such as Pseudophilotes baton Bergstrasser (Vaisanen et al. 1994), Collophrys xami (Reakirt) (Cordero et al. 2000), Chrysozephyrus smaragdinus Bremer (Takeuchi and Imafuku 2005) and L. boeticus (Vijayachander and Arivudainambi 2007). The average copulation duration of 61.37 min in S. epius was similar to that of L. boeticus (Vijayachander and Arivudainambi 2007). Both sexes of S. epius mated only once; however, multiple matings have been reported in males of C. xami (Cordero et al. 2000). The gravid females of S. epius laid eggs singly as reported in other lycaenids: Philiris helena Snellen and Philiris intensa Butler (Parsons 1984); Megisba strongyle nigra (Miskin) (Lambkin and Samson 1989); Petrelaea tombugensis Rober (Samson and Lambkin 2003); and R. takasagonis (Hsu et al. 2005). The erratic flight and swift egg-laying patterns of S. epius female butterfly were similar to those recorded in F. tarquinius (Hall et al. 2007). Adults of S. epius fed on different diets showed that females and males fed on water and honey, respectively, survived longer than that of individuals fed on other diets. Moreover, longevity of S. epius adults fed on various diets was significantly more than that of the starved individuals. It clearly indicated that food enhances the longevity of adults of S. epius. Sucrose was known to enhance the longevity of adult lycaenids viz., Jalamenus evagoras (Dovan) (Hill and Pierce 1989) and Lycaena hippothoe L. (Fischer and Fiedler 2001).
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This study provided a detailed life history and biology of a predatory lycaenid butterfly, S. epius for the first time, and this information could be utilized to develop S. epius as an effective biocontrol agent of mealybugs. Acknowledgments The authors thank University Grants Commission (UGC), New Delhi, India for providing financial assistance to carry out the above work. The first author is grateful to the UGC for providing the fellowship.
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