Research Report

Comparative Study of Different Diets Efficiency on Some Biological Parameters of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae)  

Mahmoud Jokar , Mehdi Zarabi
1 Department of Entomology and Plant Pathology, Abureihan Campus of Agriculture, University of Tehran, IRAN
2 Department of Life Sciences Engineering, Faculty of New Science and Technology, University of Tehran, Tehran- IRAN
Author    Correspondence author
Molecular Entomology, 2014, Vol. 5, No. 1   doi: 10.5376/me.2014.05.0001
Received: 11 Dec., 2013    Accepted: 08 Jan., 2014    Published: 28 Jan., 2014
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Jokar and Zarabi, 2013, Comparative Study of Different Diets Efficiency on Some Biological Parameters of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae), Molecular Entomology, Vol.5, No.1 1-9 (doi: 10.5376/me.2014.05.0001)


Green lacewing, Chrysoperla carnea (Stephens) is a major, cosmopolitan predator of different pests. This study surveyed relative consumption of three diets: eggs of flour moth, Anagasta kuehniella (Zeller), artificial diet (consists of honey, yeast and water), and semi artificial diet (consists of honey, essential amino acid, Hen’s yolk egg powder, extracting of flour moth’s body, A, D, E and B vitamin groups, yeast and water), on developmental time (T),weight, longevity and mortality percentage of larvae and pupae and fecundity, fertility and sex ratio of female. All experiments were conducted at (25±5)℃, (60±5)% RH, and photoperiod of 16:8 (L: D).Results showed significant differences (p<0.01) between diets in different parameters except for egg Incubation period and sex ratio. The lowest developmental time (T) 29.79±1.57 (day) was belonged to semi artificial diet. Larvae and pupae longevity were 12.29±0.29, 8.08±0.39; 19.46±0.76, 3.77±0.74 and 10.07±0.3, 7.15±0.34 (days) in diets respectively. The lowest and highest mortality percentage of larvae and pupae on semi artificial and artificial diets were 4%, 0%, 42% and 38% respectively. The highest weights of larvae and pupae (3.68±0.25 mgr and 9.46±0.16 mgr) were observed on semi artificial diet. The fecundity and fertility rates were 410.25±9.33, 150±4.02 and 470.25±9.8; 370.98±6.7, 94.5±3 and 383.83±4.6 (egg/female) respectively. According to these results the semi artificial diet was the most accurate diet for mass rearing of predator.

Artificial diet; Anagasta kuehniella (Zeller); Biological parameters growth; Chrysoperla carnea (Stephens); Mass rearing; Semi artificial diet

The green lacewings, Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) is a cosmopolitan predator nested in a wide range of agricultural habitats. Earlier, many authors such as DeBach and Hagen (1964), Henry (1979; 1985 and 1992), and Brooks et al., (1994) have discussed about the role of this predator in controlling agricultural insect pests. Today, Approximately 85 companies produce up to 125 natural-enemy species in order to manage different pests, which one of the most common is green lacewings (Van Lenteren, 2003). Augmentative biological control methods are dependent upon the production of large numbers of high quality natural enemies with the lowest cost (Glenister and Hoffmann, 1998; Nordlund, 1998; Smith and Nordlund, 1999 and 2000). In this method, biocontrol agents producers often culture natural enemies on their natural preys (or hosts), which need to maintain on their host plants. Certainly, maintaining of three trophic levels need high labor costs and costs associated with operating and maintaining separate spaces and equipment to produce each trophic level. Thus, reducing some of the rearing costs like eliminating live plants could be an important commercial approach (De Clercq, 2004). For this reason, many preys of predators like different lepidopterans can be reared effectively on diets that are devoid of any living plant material. Several predatory preys can be produced simply on relatively cheap foods. Recently, the egg stage of a few species has been used as factitious prey by some commercial insectaries to produce generalist predators including coleopterans (e.g., lady beetles), and neuropterans (e.g., lacewings) (Cranshaw et al., 1996; Van Lenteren, 2003). Artificial diets must ensure two fundamental factors: the nutritional requirements of predators and the reproductive ability with high quality (Cohen, 2004). Also, there are some biological parameters such as developmental time, survival rate, oviposition rate (i.e., fecundity), oogenesis rate, longevity, and predation potential and body size (weight or length), that are important parameters to gauge the impact (i.e., potential benefit) of factitious prey or an artificial diet for predator mass rearing. These parameters are used to estimate the quality of commercially-produced predators (Penn et al., 1998; Grenier and DeClercq, 2003; Van Lenteren et al., 2003a; Callebaut et al., 2004). The eggs of the Mediterranean flour moth, Anagasta kuehniella (Zeller) (Lepidoptera: Pyralidae), as factitious prey were tested to show the suitability to mass rearing of natural enemies (Hamasaki and Matsui, 2006). Prepupae of the alfalfa leaf cutting bee (Megachilero tundata Fabricius (Hymenoptera: Megachilidae), a factitious prey could be suitable diet for the larval stages of C. carnea (Uddin et al., 2005). A. kuehniella eggs are one of the most favorable factitious preys to culture larvae stages of another Chrysopid, Dichochrysa prasina (Burmeister) (Neuroptera: Chrysopidae) which cause high survival rates and shortened developmental times (Pappas et al., 2007). However, the next important step in cost-effective rearing of predators includes the utilization of an artificial diet that eliminates the use of the prey. There are three classifications of artificial diets, based on the degree; holidic diets, in which all constituents are known in chemical (i.e., molecular) structure, meridic diets, in which most of the constituents are known chemically, and oligidic diets, in which few of the constituents are known chemically (Dougherty, 1959). Using of artificial diets for mass rearing of C. carnea is generally based on holidicand meridic method (Dougherty, 1959). There are worldwide presented works on biological parameters of C. carnea which fed on factitious and artificial diets (Zaki, 1999; Singh and Varna, 1989; Tauber et al., 1973). Eggs of A. kuehniella and Sitotroga cerealella (Olivier) (
Lepidoptera: Gelechiidae) are the most commonly used preys to mass rearing of Chrysoperla species in insectariums. Production and storage methods are well established for these prey species (Lόpez-Arroyo et al., 1999). These preys sub serve rapid growth and development, high fecundity and good survival in commercially produced C. carnea (Lόpez-Arroyo et al., 1999). Choi et al., (2000) reported the successfully feeding of Chrysopa pallens (Rambur) on artificial diet containing lyophilized beef liver, silkworm pupae powder (1%). Lee and Lee (2005) was reared C. pallens on artificial diet and evaluated biological parameters. Zaki et al., (2001) demonstrated that C. carnea reared on semi-artificial diet based on the algae, Chlorella vulgaris (Beyerinck) (Chlorellales: Chlorellaceae). Sattar et al., (2007) studied biological parameters of C. carnea on artificial diets (consists of different concentration of Ground beef, Ground beef liver, powder hen eggs, Sucrose (sugar), Honey, Brewer’s yeast, Propionate, Potassium sorbet, Streptomycin, Sulphate, Chlortetracycline, Agar, Distilled water, Acetic acid, and Vitamin solution) which were included brewer's yeast and vitamin solution. Ulhaq et al., (2006) surveyed the effects of Hen's egg derivatives on the biology of adult’s C. carnea and compared them with standard diet (including sugar, yeast extract, honey, distilled water, and casein). Present study evaluated the potential benefits of two new artificial and semi artificial diets in comparing with a factitious prey (A. kuehniella eggs) for mass rearing of C. carnea according to some important biological parameters in laboratory condition.

1 Materials and Methods
1.1 Rearing of predator
C. carnea adults were originally collected from the experimental source of Tehran University Lab. (Pakdasht, Tehran, Iran). They were maintained on polyester cylinder tubes that inside spreads with scalar papers and spout covered with mesh. All cultures were kept in laboratory condition 25 ± 5℃, 60±5% RH and photoperiod of 16:8 (L: D). The adults were fed drop-likely with artificial diet on plastic board (3×15 cm).
Eggs were collected daily by razor blade and transferred to experimental dishes as colony sources. New-born larvae moved to petri-dishes separately, and fed by different diets daily.
1.2 Rearing of flour moth
Wheat flour was firstly freezed at -20℃ for five days to kill eggs or larvae of other pests. Then, this sterile flour put on packages and covered with mesh layer for air ventilation. 24-h-old males and females moth were transferred form a source (Iranian Research Institute of Plant Protection, Tehran-IRAN), and released to flour packages until 24 h to establish the new colonies and removed. New emerged adults were captured by electrical aspirator and transferred into plastically funnel which its lower part covered by mesh layer. The females pushed ovipositors through the opening layer and laid their eggs. Eggs were been collected from a paper below mesh layer by soft brush daily to freeze until applying in the experiments.
1.3 Preparing artificial and semi artificial diets
Artificial diet was a mixture of honey, yeast, and water (in proportion to 1, 1, 2) and semi artificial diet was a mixture of honey, essential amino acid, yolk egg powder, extracting of flour moth’s body, A, D, E and B vitamin groups, yeast, and water (10%, 5%,15%, 10%, 2.5%, 10% and 47.5%).
1.4 Releasing larval predator
Newborn larvae of C. carnea were separately released in different petri-dishes (7.5×1.5 cm) enclosed of treatments (freezed egg of flour moth, small drops of artificial and semi artificial diets) (N=4). All diets replaced with fresh ones daily.
1.5 Estimating biological parameters
One hundred C. carnea eggs collected from 30 pairs of adults (24-h-old). They kept in two plastic petri-dishes (covered with fine muslin cloth for air ventilation) until hatching. A piece of filter paper was been placed at the bottom of the petri-dishes and a few drops of water were added to maintain necessary humidity. Dishes kept in an Incubator. All data enclosed the number of hatched eggs and their incubation period; 1st, 2nd and 3rd larval instars and pupal duration times; and the percentage of immature mortality calculated carefully each 8 (h) until the appearance of new generation. Different larval instars were distinguished by residue of exuviate. 4-days-old larvae put in refrigerator at 4℃ for 20 min to be completely immobile and then weighted. Female and male were been distinguished by their genital organs at the end of pupal stage for evaluating the new generation sex ratio. In addition, mean generation time (T) [(∑xlxmx)/R0; the sum of development time from the egg stage to half of the life expectation of females after sexual maturation] which is one of important biological parameters, calculated by Carey (1993).
1.6 Laboratory incubator
The incubator (RI28 Shellab, 30.8 Cubic.Ft) provided uniform temperature in this large space by integrating a highly responsive microprocessor with an appropriately sized heating element. An independent secondary temperature controller offers the added security of over temperature protection. The air circulation system creates a one-pass circulation pattern that provides both exceptional temperature uniformity and rapid heat recovery.
1.7 Statistical analysis
One way ANOVA followed by Tukey’s HSD post hoc test was used to compare biological traits on different diets. Significant differences were considered at the level of 1% (p<0.01). All data analyzed by SAS version 9.1, (SAS Institute Inc., 2002) software. Because mortality data was percentage value, were using arcsine transforming (Arcsin√x). After Normal distribution and mortality data analyzed using of Variance with ANOVA and checked by Tukey’s test in SPSS Software at completely randomized design of treatments (ten replicates in each treatment) (SPSS Inc, 1993).
2 Results
2.1 The developmental times
The length of 1st, 2nd and 3rd larval instars was significantly different among different diets (Table 1).

Table 1 Immature duration (Day) (Mean ± SD) of C. carnea reared on three diets under laboratory conditions

The minimum larval duration (3.09±0.18 d) was belonged to 1st instars which were reared on semi artificial diet and the maximum one (8.5±0.16 d) was observed in 2nd instars which was reared on artificial diet. Also, the
incubation period of eggs showed no significant difference between diets (Table 1). Duration of immature stages related to feeding of different diets is shown in Table1. The lowest amount of total larval duration observed on semi artificial diet (10.07±0.3 d) and A. kuehniella eggs (12.29±0.29 d) while the artificial diet showed the longest immature duration time (20.02±0.81 d). The same pattern were observed on the developmental times (T) which the parameter are calculated by (Carey, 1993), shown in Figure 1.

Figure 1 Developmental times (T) of C. carnea on different diets

The important point is that papal duration showed no significant difference with other treatments on artificial diet. The main reason was pupal mortality at early pupal stage which caused to decrease total mean duration (Table1 and Table 2).

Table 2 Percentage mortality (%) and (Transformed mean ± SE) of C. carnea reared on three diets under laboratory conditions

2.2 Mortality percentage of larvae and pupae
The percentage mortality and Transformed percentage at larval and pupal stages showed in Table 2. The highest mortality percentage 42 and 38 (%) were observed in artificial diet, while in rest of others it was similar. But significant difference between diets displayed by Transformed percentage. The results of one-way ANOVA at larval and pupal stages were P value = 0.0436, F=4.371 and P value = 0.0003, F= 4.366.
2.3 Larval and pupa weight
The weight of larvae (4-days-old) and pupae were influenced significantly by the quantities of different diets. It showed significant differences (p<0.01) between stages and diets. Max weights of larvae 3.68±0.15 (mgr.) and pupae, 9.46±0.16 (mgr.) were belonged to semi artificial diet (Figure 2).


Figure 2 Mean weight of immature stages of C. carnea

2.4 Pre-oviposition period
In this study, our result showed overlapping between flour moth eggs and semi artificial diet that exhibited the same pre-oviposition period (4.43±0.65 and 4.37±0.55 d) (Figure 3). The adult oviposition process showed similar process to factitious prey (flour moth eggs) and semi artificial diet in this study in comparison to the artificial diet. The peak of oviposition observed during 10-15 days and the end of it was at 19-22 days (Figure 4).


Figure 3 Mean of pre-oviposition period of C. carnea adults on different diets

Figure 4 Fluctuation of oviposition rate of C. carnea adults on different diets

2.5 Fecundity and fertility
The lowest and highest average number of eggs (150.5±4.02 no.) and (470.25±9.8 no.) (eggs/female) were laid by females fed on artificial and semi artificial diets, respectively (Figure 5). Also the fertility of eggs showed significant differences (p<0.01) between different diets. The lowest fertility (offspring/female) was observed in females, which were fed on artificial diet (Figure 5).

Figure 5 Mean fecundity and fertility rates of females C. carnea

2.6 Sex ratio
The sex ratio of new generation adults were 13:12, 14:11 and 12:13 (female: male) on flour moth eggs, semi artificial diet and artificial diet respectively. It showed no significant difference between kinds of food and amounts of sex ratio (close to 50%:50%) (Table 3).

Table 3 Comparing sex ratio, fecundity, fertility of C. carnea on diets

3 Discussion
3.1 The developmental times
The essential factor for suitable growth and development of C. carnea is the type and amount of predator larval feeding (Zheng et al., 1993b; Obrycki et al., 1989). Hence in this research the mean total larval and pupal periods of lacewing observed on semi artificial diet is the best choice for a good growth of adults and their predatory potential. Our results are very close to Ulhaq et al., (2006) work which reported total larval and pupal periods on artificial diet (hen’s egg yolk) as 13.84±0.20 and 6.33±0.40 (d), respectively. Also, present results of immature stages durations (egg, larvae and pupa) on factitious prey (flour moth eggs) are similar to the results of Uddin et al., (2005) on (Prepupae of alfalfa leaf cutting bee, M. rotundata) (4, 10.9±0.1 and 9.08±0.1 d), and Iqbal Nawaz Khan et al., (2005) on (eggs of S. cerealella) (larval period 11.64± 0.22 d and pupal period 8.48 ± 0.38 d). The mean duration of 1st, 2nd and 3rd larval instars of 3.87±0.31, 4.06±0.4 and 4.36±0.28 (d), respectively, recorded for the flour moth eggs fed larvae of C. carnea are the same as results by Iqbal Nawaz Khan et al., (2005) estimated 4.48 ± 0.17, 2.96 ± 0.3 and 4.20 ± 0.25 (d), respectively for the mention instars of larvae fed on eggs of S. cerealella, results of mean duration of 1st, 2nd and 3rd larval instars is not similar to other work like Nasreen et al., (2004) (1.5-2, 2.83-4.83 and 6.33-7.83 d, respectively) which may related to egg of different moth species which is used in experiments.
3.2 Immature mortality
Syed et al., (2008) evaluated larval and pupal mortality of C. carnea on egg of S. cerealella (1st=0, 2nd=5, 3rd=5 and pupal=10%), Sattar et al., (2007) reported when predator fed on two artificial diets the results were as followed LD= 14.25,65 (%) and PD=17.33, 74.9 (%) as similar as present studies. Lee and Lee (2005) reported immature mortality of C. pallens on artificial diet (1st=0.6, 2nd=0, 3rd=0.4 and pupal= 11%) differs from our finding on semi artificial diet which is related to different composition of artificial diets and predator’s species. Artificial diet was used in Lee et al., (2005) as similar as present semi artificial diet but it is contained of some common Antibiotics (penicillin and streptomycin) which may affect in predator’s development.
3.3 Larval and pupal weights
Because experiments on this mentioned parameter of C. carnea have not been investigated, we cited to similar experiments but we do it on other species of green-lacewing and moth eggs. Nasreen et al., (2004) reported that larval predator’s weight when fed on S. cerealella eggs was 4.2 to 8.4 (mgr.), Sattar et al., (2010) estimated that pupal predator’s weight was 8.1 and 8.2 (mgr.) on S. cerealella eggs and kind of artificial diet (DMRT®), respectively, and Tavares et al., (2011) evaluated that larvae’s weight of C. externa (Neuroptera: Chrysopidae) on A. kuehniella eggs was 1.74±0.03 to 5.06±0.1 (mgr.) the same as our results.
3.4 Pre-oviposition period
Atlihan et al., (2004) studied that this period on different prey densities of S. cerealella eggs was 6.7±0.58 to 8.2±0.37 (d), Nawaz et al., (2008) recorded that the pre-oviposition period on control artificial diet treatment (Honey, water and yeast ) was 6.08 (d) that is very close to our result. But Sattar et al., (2010) showed different results such as (3.25±0.16 to 4.9±0.14 d) (2.37±018 d) (3.12±0.22 to 3.37±0.18 d) because of different level of protein's concentration in their artificial diet, rearing on S. cerealella eggs, and at 24-32 0C, respectively.
3.5 Fecundity and fertility
Hagen (1950) showed that the fecundity rate of C. carnea which fed on a protein free diet will be very low which we found it in our results when fed on artificial diet too. According to Sundby (1958) who reported the average number of egg per female and hatching rate of predator on synthetic artificial diet were 473±87.3 (no. of eggs) and 67 (%) which is very close to present result (470.25±9.33 No. egg/female and 81%). Pappas et al., (2007) evaluated egg hatchability of D. prasina reared on eggs of A. kuehniella at five constant temperatures and a photoperiod of 16:8 (L:D) as 75.6±2.8 to 87.3±2.5 % which was similar to present result. It shows that the similarity is because of the same nutritional value between two studies, which these materials are as follow: honey, yeast, ascorbic acid, cholesterol and protein resources. Nawaz et al., (2008) reported that the fecundity per female on artificial diet (vitamin E, water, honey and yeast) is 180.49 (no. of eggs) which is far from our result (150.5±4.02 no. of eggs). It seems that this difference is related to the higher amount of the vitamin E in previous study than in present finding. Also results of the process of oviposition in Uddin et al., (2005) when C. carnea was reared on flour moth eggs were similar to present research (The peak of oviposition observed in Uddin et al., (2005) during 9-12 days and the end of it was at 20-25 days). So, based upon present experiments, the semi artificial diet showed the best result for the highest oviposition rate of female in comparison to the other diets under the same laboratory conditions. Semi artificial diet consists of components and each component has the promoting effect on fecundity. As reported by Hill (1989), sugar is the most important component in diet formula for the insects that has pronounced effect on the egg production. Similarly, McEwen and Kidd (1995) had recommended yeast and sugar for maximum egg production. Honey is also a very important component regarding fecundity. McEven and Kidd (1995) and Kubota and Shiga (1995) analyzed that a mixture of honey and autolysate yeast is a suitable diet for production of fertile eggs. Last but not the least component is yolk that is the most important one. Milevoj (1999) reared adults of C. carnea on adult diet consisting of milk, eggs, fruit sugar and yeast and found a favorable effect on fecundity. In addition, higher fecundity was observed in semi artificial diet because it is loaded by different proteins (amino acids) (Norioka et al., 1984).Vitamin A, Niacin, Riboflavin (B12), Pantothenic acid, Thiamin, Pyridoxine, Folic acid, Vitamin E and D are present in large quantities of egg yolk powder in semi artificial diet. Similarly Folic acid, which is particularly more important for egg productions, is much higher in Hen’s yolk powder of semi artificial diet. Egg yolk powder in semi artificial diet, also has high amounts of saturated, mono unsaturated, polyunsaturated oils and lipids for egg production. It makes a lot of cholesterol level (1075 mg per 100 g) in semi artificial diet too (Rolfes et al., 1978). Thus we used all these components in our semi artificial diet formula and get similar results in the highest fecundity rate of females. In addition, because of abundant caloric value (303 calories per 100 g) in semi artificial diet, predator can provide essential energy for completing life duration in a short time.
3.6 Sex ratio
Iqbal Nawaz Khan et al., (2005) demonstrated that the sex ratio of new born adults when their larvae fed on egg of S. cerealella was 56%, which is close to our result (52%). He suggested that food did not affect the sex ratio. Uddin et al., (2005) and Zheng et al., (1993a) obtained that 52% of emerged adults are females. All mentioned results justify present finding.
4 Conclusion
Finally, according to our results, the semi artificial diet is the best diet for mass rearing in comparison to the other diets, because of low incubation, larval and pupal periods which cause a complete short life cycle, high fecundity and fertility and producing a quantity of eggs which establish an strong colony in insectariums.
We are most grateful to Dr. Gh.Golmohammadi, Dr. Katy.Kheradmand and Dr. H. Ghajarie Najarbashi for supporting this research.
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