J. Appl. Entomol.

ORIGINAL CONTRIBUTION Cryptolaemus montrouzieri as a predator of the striped , Ferrisia virgata, reared on two hosts H. Wu1,2, Y. Zhang1, P. Liu1, J. Xie1,Y.He1, C. Deng1, P. De Clercq2 & H. Pang1

1 State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, China 2 Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium

Keywords Abstract biological control, cotton, Cryptolaemus montrouzieri, Ferrisia virgata, The striped mealybug, Ferrisia virgata (Cockerell) (: Pseudococ- citri, prey suitability cidae), is a cosmopolitan of a variety of agricultural crops including cotton. To investigate the biological control potential of the predatory Correspondence ladybird Cryptolaemus montrouzieri Mulsant (Coleoptera: ) Hong Pang (corresponding author), State Key against this pest, we evaluated its developmental and reproductive fitness Laboratory of Biological Control, School of when feeding on F. virgata reared on pumpkin fruits or on cotton leaves Life Sciences, Sun Yat-sen University, No.135 Xingang Road West, Guangzhou 510275, and compared this to a diet of Planococcus citri Risso (Hemiptera: Pseudo- China. E-mail: [email protected] and coccidae) reared on pumpkin fruits. F. virgata and P. citri reared on pump- Patrick De Clercq (corresponding author), kins were equally suitable prey for the pre-imaginal stages of Department of Crop Protection, Faculty of C. montrouzieri. Duration of total immature development was 1 day longer Bioscience Engineering, Ghent University, in C. montrouzieri offered F. virgata reared on cotton as compared with Coupure Links 653, Ghent 9000, Belgium. F. virgata or P. citri reared on pumpkin, whereas no significant difference E-mail: [email protected] was observed in survival rates. Diet significantly influenced the reproduc-

Received: January 4, 2014; accepted: February tive fitness of C. montrouzieri. Females offered P. citri reared on pumpkin 20, 2014 had significantly shorter pre-oviposition periods and higher fecundity and fertility than those given F. virgata reared on pumpkin or cotton leaves. doi: 10.1111/jen.12127 F. virgata grown on cotton leaves supported the reproduction of C. mont- rouzieri better than F. virgata reared on pumpkin. Our study established that C. montrouzieri can successfully complete its development and repro- duction when fed exclusively on F. virgata and indicates its potential as a biological control agent of this emerging cotton pest.

may fail to open, and plant senescence can be Introduction induced. Feeding also excrete a sugary The striped mealybug, Ferrisia virgata (Cockerell) solution called , which contributes to the (Hemiptera: Pseudococcidae), is a polyphagous pest development of black sooty mould (Nagrare et al. on a variety of crops, such as cotton, , 2011). In addition, mealybugs can also be vectors of cassava, coffee, cocoa, , tomato, papaya and egg- plant pathogens and cause chlorosis, stunting, defor- plant (Schreiner 2000; Ben-Dov et al. 2005). mation and death of plants (Bhat et al. 2003; Recently, it was reported to infest coloured fibre cot- Ben-Dov et al. 2005). Chemical control of the mealy- ton, and it is emerging as a serious pest in north-east bugs in cotton with conventional has often Brazil (Silva-Torres et al. 2013). In cotton, F. virgata been unsuccessful because the pest is covered with a infestation occurs in patches, feeding on all plant wax-type material that prevents toxic chemicals from parts, particularly the growing tips of leaves, petioles, being absorbed into the system (Joshi et al. 2010). leaf veins, squares and bolls (Hanchinal et al. 2011; Therefore, biological control using natural enemies is Nagrare et al. 2011; Silva-Torres et al. 2013). Mealy- an effective alternative method to manage this pest. bug infestations can be detrimental to host plants in a The ladybird Cryptolaemus montrouzieri Mulsant number of ways: they can reduce plant vigour, bolls (Coleoptera: Coccinellidae) is a highly efficient

© 2014 Blackwell Verlag GmbH 1 C. montrouzieri as a predator of F. virgata H. Wu et al. natural enemy of mealybugs and plays an important Materials and Methods role in the integrated management of mealybug pests in various cropping systems. This ladybird has been and plants reported to feed on about 21 mealybug (Jiang et al. 2009) and has been widely used as a biological All insects (C. montrouzieri, P. citri and F. virgata) were control agent in areas where mealybugs such as Pla- originally obtained from the State Key Laboratory of nococcus citri (Risso), Maconellicoccus hirsutus Green, Biocontrol, Sun Yat-sen University, Guangzhou in Phenacoccus solenopsis Tinsley and F. virgata outbreaks China. The stock colony of C. montrouzieri was reared occur (Mani and Krishnamoorthy 2008; Afifi et al. on P. citri produced on pumpkins [Cucurbita moschata 2010; Hanchinal et al. 2010; Kaur and Virk 2012; (Duch.ex Lam.) Duch. ex Poiretand] in metal frame Khan et al. 2012). Although C. montrouzieri appears cages (45 9 36 9 33 cm) covered with fine-mesh to be an opportunistic generalist predator of mealy- nylon gauze. Both the P. citri and F. virgata colonies bugs, it is plausible that only a subset of mealybug were maintained on plastic trays (40 9 30 cm) con- species serve as essential foods capable of supporting taining pumpkins as food. All colonies were main- immature growth and adult reproduction of C. mont- tained under controlled conditions [26 Æ 2°C, rouzieri. Indeed, nutrients or antinutrients present in 50 Æ 10% RH, and a 14:10 h (L:D) photoperiod]. different prey species may affect life attributes of Non-transgenic cotton plants ( hirsutum ladybirds differently (Evans et al. 1999). These influ- L., cv. Zhongmiansuo 23) were planted individually ences may vary from more serious deleterious effects in plastic pots (16 9 13 cm) with soil. Cotton plants such as mortality caused by the toxicity of prey, to were cultivated from seed in an -free minor effects such as changes in developmental and greenhouse under ambient environmental condi- survival rates or in reproductive capacity (Hauge tions. Plants used in the experiments were in the et al. 1998; Srivastava 2003; Cabral et al. 2006; 6–8 true leaf stage, which developed 7 weeks after Mignault et al. 2006). Therefore, investigating prey sowing. suitability is one of the most important steps in eval- uating the potential use of a predator in biological Egg incubation control programmes (Dixon 2000; Zhang et al. 2007, 2012). Three plastic boxes (12.0 9 5.0 9 4.0 cm, covered Cryptolaemus montrouzieri is mass reared mostly with fine-mesh nylon gauze for ventilation) contain- according to a tritrophic system using live mealybugs, ing C. montrouzieri eggs (100, 100 and 60/box) laid by such as P. citri on potato sprouts or pumpkin fruits. 40 pairs of adults within a 12 h period were collected Pumpkin has also shown to be a feasible host for mass from the stock colony and maintained in a climate rearing the striped mealybug, F. virgata (Oliveira chamber [25 Æ 1°C, 75 Æ 5% RH, and a 14:10 h et al. 2014). F. virgata is a widely spread mealybug (L:D) photoperiod]. The eggs were observed carefully and is reported in more than 100 countries around every 12 h, and numbers of larvae that hatched were the world, including the USA, Argentina, Canada, recorded. India, China, Brazil and Pakistan (Ben-Dov et al. 2005), where cotton is widely cultivated. However, Development, survival and weight studies on the development and reproduction of C. montrouzieri when feeding on F. virgata are lacking. Eggs of C. montrouzieri were randomly assigned to Further, the predator has been widely released to three groups, which were fed on three different control various mealybugs in different cropping sys- diets. In all treatments, newly hatched first instars of tems, but it has not been used in cotton against the predator were placed in individual plastic Petri F. virgata. dishes (9.0 9 1.5 cm). The first group was fed on To improve our understanding of the feeding ecol- P. citri reared on pumpkin fruits: newly hatched first ogy of C. montrouzieri and its potential role as a biolog- instars from 100 eggs (93 larvae) were supplied ad ical control agent of F. virgata, we evaluated the libitum with mixed aged P. citri collected from a col- developmental and reproductive fitness of the preda- ony reared on pumpkins. Mealybug prey were tor when feeding on this mealybug reared on pump- replaced every 24 h. In a second group, newly kin fruits or cotton leaves. The predator’s hatched first instars from 100 eggs (91 larvae) were performance on F. virgata was compared with that on offered mixed aged F. virgata reared on pumpkins. its commonly used prey in laboratory cultures, the cit- Fresh mealybugs were again provided to the preda- rus mealybug P. citri. tor larvae every 24 h. A third group was fed on

2 © 2014 Blackwell Verlag GmbH H. Wu et al. C. montrouzieri as a predator of F. virgata

F. virgata reared on cotton leaves. The mealybug Statistical analysis prey in this group had been maintained on cotton for at least a single generation. Here, the newly All data were subjected to statistical analysis (Ver. 20; hatched first instars from 60 eggs (54 larvae) of the IBM SPSS Statistics, SPSS Inc., Chicago, IL, USA) to predator were individually transferred to 9-cm Petri determine the significance of the treatment effects. dishes, which had a small hole drilled into the side The Kolmogorov–Smirnov and Levene test were used for allowing a cotton leaf to be inserted. A single leaf to test the normality and homogeneity of variances of (still attached to the plant) infested with F. virgata the data sets, respectively. Normally distributed data (~60–100 mixed age mealybugs per leaf) was intro- were analysed using a one-way analysis of variance duced into each Petri dish, which was held together (ANOVA) followed by a Tukey test (homoscedasticity) by clips. A piece of cotton wool was wrapped around or a Tamhane test (heteroscedasticity). If means were the petiole to prevent F. virgata or C. montrouzieri not normally distributed, Kruskal–Wallis ANOVA fol- from escaping. Each cotton plant received two lowed by Mann–Whitney U-tests was conducted. C. montrouzieri larvae but on two different cotton Immature survival and sex ratio of the progeny were leaves. The predators were transferred to a new compared by logistic regression, which is a generalized freshly infested leaf on the same plant every 3 days. linear model using a probit (log odds) link and a bino- Predators in all treatments were monitored for sur- mial error function. For all tests, the significance level vival and development every 12 h. was set at P < 0.05. To assess fresh body weight of C. montrouzieri in the different treatment groups, larvae of the 2nd, 3rd and Results 4th instar, pupae and adults were weighed individu- ally 24 h after moulting using an electronic balance Effects of diet on the development and survival of with a precision of 0.1 mg (Sartorius BSA124S; immature C. montrouzieri Sartorius, Goettingen, Germany). As 1st instar larvae are too small to be weighed individually, five groups The developmental time of 1st and 2nd instar larvae, of 10 newly emerged 1st instar larvae were weighed. pupae and total survival rates were similar in C. mont- The experiments were carried out in climate cham- rouzieri fed on P. citri or F. virgata irrespective of host bers set at 25 Æ 1°C, 75 Æ 5% RH, and a14:10 h plant (table 1). However, development of 3rd and 4th (L:D) photoperiod. instars, and total development from first instar to adult were significantly affected by diet. Duration of 3rd and 4th instar was longer in C. montrouzieri offered Reproduction and adult longevity F. virgata reared on cotton as compared with F. virgata When C. montrouzieri adults emerged from groups 1 or P. citri reared on pumpkin, and a similar trend was and 2, the females and males were single paired, observed for total immature development. transferred to 9-cm Petri dishes and offered P. citri (group 1) or F. virgata (group 2), respectively. A Effects of diet on body weight of C. montrouzieri piece of cotton was placed in each Petri dish for ovi- position. Mixed aged mealybugs were offered ad libi- Weights of newly emerged 1st instar larvae and female tum and replaced every 24 h. In the third group, the adults were similar among the tested diets (table 2). emerged C. montrouzieri adults were also single paired From the 2nd to the 4th instar, larval weights were and transferred to Petri dishes with a small hole in consistently lower in the group offered F. virgata the side. Again, a single leaf (still attached to the reared on cotton. Between the groups fed on F. virgata plant) infested with F. virgata (~60–100 mixed age or P. citri reared on pumpkin, individuals given F. virg- mealybugs per leaf) was introduced into each Petri ata were significantly heavier in the 2nd and 4th instar dish, as described above. The cotton wool plugging than those given P. citri. Significant differences were the hole served also as an oviposition site. Every observed between all three treatment groups only in 3 days, the predators were transferred to a new leaf the 4th instar (table 2). In contrast, the mean pupal infested with F. virgata until they died. The pre- weight of C. montrouzieri fed on F. virgata reared either oviposition period, number of eggs laid and survival on pumpkin or cotton leaves differed only marginally, of C. montrouzieri were monitored every day until the but both values were higher than those of predators death of all adults. The experiments were carried out offered P. citri reared on pumpkin. Adult males fed on in climate chambers set at above-mentioned climatic P. citri were heavier than those presented with F. virg- conditions. ata reared on pumpkin or cotton leaves.

© 2014 Blackwell Verlag GmbH 3 C. montrouzieri as a predator of F. virgata H. Wu et al.

Table 1 Developmental time (days) and total survival rate (%) of larval and pupal stages of Cryptolaemus montrouzieri when offered Ferrisia virgata reared on pumpkin fruits (F. virgata + pumpkin) or cotton leaves (F. virgata + cotton), or Planococcus citri reared on pumpkin fruits (P. citri + pumpkin)

Developmental time (days)1

Prey and plant host n 1st instar 2nd instar 3rd instar 4th instar Total Survival rate (%)2

P. citri + pumpkin 90 3.06 Æ 0.04a 2.59 Æ 0.04a 2.94 Æ 0.04a 4.77 Æ 0.06a 8.96 Æ 0.06a 22.32 Æ 0.08a 96.77 Æ 1.86a F. virgata + pumpkin 85 3.15 Æ 0.03a 2.63 Æ 0.03a 2.87 Æ 0.03a 4.93 Æ 0.05b 8.89 Æ 0.08a 22.48 Æ 0.09a 93.41 Æ 2.69a F. virgata + cotton 47 3.10 Æ 0.04a 2.75 Æ 0.05a 3.22 Æ 0.05b 5.48 Æ 0.06c 8.69 Æ 0.07a 23.32 Æ 0.08b 87.04 Æ 4.90a v2 3.67 5.92 31.27 55.14 5.73 48.33 4.68 d.f. 2 2 2 2 2 2 2 P 0.160 0.052 <0.001 <0.001 0.057 <0.001 0.097

Data represent means Æ SE. n indicates the final number of individuals reaching adulthood. Means within a column followed by the same letter are not significantly different (P > 0.05) as determined by 1Mann–Whitney U-test or 2Wald v2 test.

Table 2 Body weights upon moulting (means Æ SE) of different life stages of Cryptolaemus montrouzieri when offered Ferrisia virgata reared on pumpkin fruits (F. virgata + pumpkin) or cotton leaves (F. virgata + cotton), or Planococcus citri reared on pumpkin fruits (P. citri + pumpkin)

Body weights (mg)

Prey and plant host 1st instar 1 2nd instar 1 3rd instar 2 4th instar 1 Pupa 1 Adult (♀) 1 Adult (♂) 2

P. citri + pumpkin 0.15 Æ 0.00a 0.84 Æ 0.02b 3.18 Æ 0.08b 10.13 Æ 0.16b 13.28 Æ 0.12a 9.94 Æ 0.09a 8.90 Æ 0.09b n = 5 n = 50 n = 50 n = 50 n = 48 n = 20 n = 28 F. virgata + pumpkin 0.16 Æ 0.00a 0.97 Æ 0.04c 3.15 Æ 0.07b 10.81 Æ 0.19c 13.72 Æ 0.11b 10.04 Æ 0.09a 8.69 Æ 0.09ab n = 5 n = 47 n = 47 n = 47 n = 46 n = 21 n = 23 F. virgata + cotton 0.16 Æ 0.01a 0.75 Æ 0.03a 2.22 Æ 0.09a 7.83 Æ 0.24a 14.24 Æ 0.24b 10.17 Æ 0.19a 8.41 Æ 0.19a n = 5 n = 48 n = 48 n = 48 n = 47 n = 20 n = 27 F 2.19 15.89 48.87 61.20 8.63 0.82 6.41 d.f. 2,12 2,142 2,142 2,142 2,138 2,58 2,75 P 0.155 <0.001 <0.001 <0.001 <0.001 0.447 0.003

Data represent means Æ SE. The initial number of individuals in each weight test was 50, and n indicates the number of groups (first instars) or individuals (other stages) observed. Means within a column followed by the same letter are not significantly different (P > 0.05) as determined by 1Tamhane test or 2Tukey test.

or cotton leaves. However, prey type had no influence Effects of diet on reproduction and longevity of v2 = = = C. montrouzieri on egg hatch ( 1.24; d.f. 2; P 0.539), female longevity (v2 = 2.51; d.f. = 2; P = 0.286), male lon- All C. montrouzieri females successfully reproduced gevity (F = 2.84; d.f. = 2, 78; P = 0.064) and sex ratio when maintained on P. citri or on F. virgata reared on of offspring, with the proportion of females ranging either host plant (table 3). Pre-oviposition period was from 0.44 to 0.46 (v2 = 1.95; d.f. = 2; P = 0.378). significantly influenced by prey type, with F. virgata on pumpkin or cotton leaves yielding a significantly Age-dependent fecundity of C. montrouzieri as a longer pre-oviposition period as compared with P. citri function of diet on pumpkin (v2 = 40.51; d.f. = 2; P < 0.001). On the other hand, oviposition period was highest in the During the first 150 days after adult emergence, the group offered F. virgata on cotton and lowest in the fecundity of C. montrouzieri females offered P. citri group given F. virgata on pumpkin (v2 = 8.98; reared on pumpkin was significantly higher than that d.f. = 2; P = 0.011). Fecundity (v2 = 37.21; d.f. = 2; of those offered F. virgata reared on pumpkin or cot- P < 0.001), oviposition rate (F = 42.79; d.f. = 2, 78; ton leaves (F = 38.33; d.f. =2, 78; P < 0.001) (fig. 1). P < 0.001) and fertility (v2 = 42.85; d.f. = 2; Peak oviposition was observed during the first 30 days P < 0.001) were significantly higher in C. montrouzieri in the P. citri group (F = 62.95; d.f. = 2, 78; offered P. citri on pumpkin vs. F. virgata on pumpkin P < 0.001) but only after 60 days in both F. virgata

4 © 2014 Blackwell Verlag GmbH H. Wu et al. C. montrouzieri as a predator of F. virgata

Table 3 Reproduction and longevity of Cryptolaemus montrouzieri when offered Ferrisia virgata reared on pumpkin fruits (F. virgata + pumpkin) or cotton leaves (F. virgata + cotton), or Planococcus citri reared on pumpkin fruits (P. citri + pumpkin)

P. citri + pumpkin F. virgata + pumpkin F. virgata + cotton Parameter (n = 40) (n = 24) (n = 17)

Pre-oviposition period (days)1 4.52 Æ 0.13c 8.90 Æ 0.76a 6.94 Æ 0.60b Oviposition period (days) 2 99.65 Æ 4.80b 79.00 Æ 5.15c 114.06 Æ 11.65a Fecundity (eggs/female)1 1195.30 Æ 62.40a 433.79 Æ 48.96c 861.06 Æ 80.27b Oviposition rate (eggs/female/day) 2 12.21 Æ 0.39a 5.78 Æ 0.69c 8.04 Æ 0.65b Fertility (larvae/female/day)1 10.92 Æ 0.35a 5.13 Æ 0.59c 7.29 Æ 0.59b Egg hatch (%) 3 89.48 Æ 0.83a 88.82 Æ 1.57a 90.66 Æ 1.10a Female proportion of the progeny 3 0.44 Æ 0.01a 0.42 Æ 0.02a 0.46 Æ 0.02a Female longevity (days)1 144.65 Æ 4.94a 168.17 Æ 12.88a 161.50 Æ 8.86a Male longevity (days) 2 193.73 Æ 11.14a 219.54 Æ 14.94a 167.88 Æ 13.89a

Data represent means Æ SE. n indicates the number of reproducing females observed. Means within a row followed by the same letter are not signifi- cantly different (P > 0.05; 1Mann–Whitney U-test, 2Tukey test, or 3Wald v2 test).

Fig. 1 Age-dependent fecundity (means Æ SE) of Cryptolaemus montrouzieri when offered Ferrisia virgata reared on pump- kin fruits (F. virgata + pumpkin) or cotton leaves (F. virgata + cotton), or Planococcus citri reared on pumpkin fruits (P. citri + pump- kin). The data represent the average number of eggs laid per female every 30 days (P > 0.05; Tukey test) (number of reproducing females per treatment: n = 24, 17 and 40, respectively). groups (F = 35.33; d.f. = 2, 78; P < 0.001). After 90 nutritional requirements (Evans et al. 1999). In the and 120 days, however, fecundity was similar present laboratory study, F. virgata and P. citri reared between the group offered P. citri on pumpkin and on pumpkins were equally suitable prey for the pre- F. virgata on cotton leaves, but both groups had imaginal stages of C. montrouzieri in terms of total higher egg numbers than the group given F. virgata developmental time and survival rates. However, on pumpkin (90 days: F = 7.83; d.f. = 2, 78; P when using pumpkin as a host, predators given = 0.001) (120 days: F = 6.23; d.f. = 2, 78; P = 0.003). F. virgata were heavier in the 2nd and 4th larval instar By day 150, fecundity in all three groups had and the pupal stage than those given P. citri. On the declined, and mean values were similar (F = 2.72; other hand, P. citri appeared to be a better prey than d.f. = 2, 78; P = 0.072). F. virgata to sustain reproduction of C. montrouzieri. Likewise, Cabral et al. (2006) reported that the aphids Aphis fabae Scopoli and Myzus persicae (Sulzer) were Discussion equally suitable to the larval stages of Coccinella unde- Food quality is one of the most important factors cimpunctata L. but differed in their value to sustain influencing the developmental and reproductive per- reproduction. Zhang et al. (2012) also noted that formance of a predator, and its natural prey may lar- M. persicae and Chaitophorus populeti (Panzer) yielded gely differ in nutritional quality (Zhang et al. 2012). similar developmental performance in the ladybird In the field, C. montrouzieri appears to be an opportu- Propylea japonica (Thunberg), but had a different nistic predator that feeds on a wide range of mealybug influence on reproductive parameters and adult lon- species (Jiang et al. 2009), but this behaviour may gevity. Hodek (1962) and Hodek and Honek (1996) not clearly indicate prey suitability and predator described the characteristics that distinguish essential

© 2014 Blackwell Verlag GmbH 5 C. montrouzieri as a predator of F. virgata H. Wu et al. prey from alternative prey for ladybirds, with the for- Hopkins et al. 2009). Likewise, allelochemicals mer being those that promote successful pre-imaginal expressed in cotton leaves or pumpkin fruits may development and reproduction, and the latter being have accumulated in the mealybugs feeding on these those that do not permit development or reproduc- hosts, which in turn may have affected the develop- tion, but only serve as a source for survival. Based on ment and reproduction of C. montrouzieri. Tritrophic these definitions, our data demonstrate that F. virgata effects with a negative impact on the predator’s biol- is an essential or ‘complete’ prey as it supports both ogy have been demonstrated for a number of coccin- development and reproduction of C. montrouzieri ellid predators feeding on homopteran prey. For (Michaud 2005). instance, Le Ru€ and Mitsipa (2000) reported that The effect of host plant on the suitability of F. virgat- development and reproduction of Exochomus flaviven- a as a prey for C. montrouzieri, in terms of its develop- tris Mader were greatly affected when offered the cas- mental and reproductive performance, was not sava mealybug, Phenacoccus manihoti Matile-Ferrero, unequivocal. Whereas offering the predator F. virgata reared on four resistant plants. Similarly, Adalia bi- on cotton leaves prolonged total development, it punctata L. fed on M. persicae collected from plants yielded greater fecundity as compared with a diet of with no or low levels of glucosinolates had higher fit- F. virgata maintained on pumpkin fruits. Nonetheless, ness than those fed on M. persicae from plants with on all diets, total developmental times (22–23 days) high levels of glucosinolates (Francis et al. 2001). in our study were consistent with those reported in a Results from experiments conducted by Pratt et al. study by Ghorbanian et al. (2011), who offered (2008) confirm that the presence of sinigrin in Brassica C. montrouzieri P. citri reared on leaves at 27°C nigra (L.) Koch results in the cabbage aphid Brevicoryne (23.1 days) and much shorter than those observed by brassicae (L.) becoming unsuitable as prey for A. bi- Solangi et al. (2012), who fed the predator on P. solen- punctata larvae. Host plants may, however, also posi- opsis on potato sprouts at 28°C (37.6 days). Further, tively affect the outcome of biological control via their values of pre-oviposition period, oviposition period chemical traits. For instance, Du et al.(2004) investi- and total fecundity on F. virgata reared on pumpkin gated three cotton cultivars with low, medium and or cotton leaves in our study were comparable with high gossypol contents on the development, repro- those reported by Ghorbanian et al. (2011) (5.6 days, duction and survival of Aphis gossypii Glover and its 70.4 days and 433.1 eggs, respectively) and Solangi predator P. japonica. Their results demonstrated that et al. (2012) (9.9 days, 76.4 days and 486.9 eggs, high gossypol content in host cotton had an antibiotic respectively). Whereas developmental parameters effect on A. gossypii but showed a positive effect on were similar, fecundity levels of C. montrouzieri pre- growth and development of P. japonica at the third sented with F. virgata on cotton leaves in our study trophic level. were much higher than those observed in above- Although cotton leaves as a host for F. virgata mentioned studies. yielded better fecundity of C. montrouzieri as com- The factors underlying the differential suitability of pared to pumpkin fruits, the practical advantages of F. virgata as affected by its plant host as a prey for pumpkin fruits as host plant material for maintaining C. montrouzieri are unknown. One hypothesis is that a colony of the predator should not be ignored. In the nutritional profile of F. virgata reared on the two Asia, C. montrouzieri is mass reared mostly on live host plants was different which in turn may have mealybugs such as P. citri reared on pumpkins affected the predation rate, development and survival (Chacko et al. 1978; Babu and Azam 1987; Li 1993). of the predator (Zhang et al. 2012). Indeed, Giles However, we observed that P. citri prefers to assem- et al. (2002) demonstrated that the fatty acid compo- ble and produce large amounts of honeydew and sition of the pea aphid Acyrthosiphon pisum (Harris) wax when maintained on pumpkin fruits, which can varies depending on its host plant species, and that quickly lead to rotting of the fruits. Compared with this variation affects the performance of its predator P. citri, F. virgata prefer to disperse and aggregations Coccinella septempunctata L. However, suitability of a are therefore usually smaller. In this way, the pump- herbivorous prey for its predator is not only governed kins can keep longer and reproduce more mealybugs. by its ability to extract nutrients from its host plant, The method using F. virgata reared on pumpkin fruits but also by antinutritional factors, which may be can reduce the cost of mass rearing C. montrouzieri taken up from the plant. Secondary metabolites from and at the same time allows to avoid inadvertent its host plant may render a herbivore less palatable or adaptation to P. citri as a laboratory host, which may nutritionally suitable as prey or may even cause toxic contribute to better biological control of F. virgata effects in its predator (Duffey 1980; Price et al. 1980; outbreaks.

6 © 2014 Blackwell Verlag GmbH H. Wu et al. C. montrouzieri as a predator of F. virgata

Our laboratory experiments demonstrated the suc- Dixon AFG, 2000. predator-prey dynamics: ladybird cessful development of C. montrouzieri on F. virgata and biological control. Cambridge University reared on both pumpkin and cotton leaves, and a Press, Cambridge, UK. positive effect of cotton as a host plant for the mealy- Du L, Ge F, Zhu S, Parajulee MN, 2004. Effect of cotton bug on the reproductive capacity of the ladybird. cultivar on development and reproduction of Aphis gos- These findings indicate a potential role for C. mont- sypii (Homoptera: Aphididae) and its predator Propylaea rouzieri as a biological control agent of F. virgata in japonica (Coleoptera: Coccinellidae). J. Econ. Entomol. – cotton fields. However, as the outcome of a biological 97, 1278 1283. control programme can be influenced by several biotic Duffey SS, 1980. Sequestration of plant natural products by insects. Annu. Rev. Entomol. 25, 447–477. and abiotic factors (Collier and Van Steenwyk 2004; Evans EW, Stevenson AT, Richards DR, 1999. Essential Frank 2010), further investigations in the field would versus alternative foods of insect predators: benefits of a be necessary to determine the efficiency of C. mont- mixed diet. Oecologia 121, 107–112. rouzieri as a biological control agent of the striped Francis F, Haubruge E, Hastir P, Gaspar C, 2001. Effect of mealybug as an emerging cotton pest. aphid host plant on development and reproduction of the third trophic level, the predator Adalia bipunctata Acknowledgements (Coleoptera: Coccinellidae). Environ. Entomol. 30, 947– 952. This research was supported by grants from the Frank SD, 2010. Biological control of pests using National Basic Research Program of China (973 Pro- banker plant systems: past progress and future direc- gram) (Grant No. 2013CB127605), National Natural tions. Biol. Control 52, 8–16. 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