Next Article in Journal
Effect of Sex, Age and Temperature on the Functional Response of Macrolophus pygmaeus Ramber and Nesidiocoris tenuis Reuter (Heteroptera: Miridae) on Eggs of Tuta absoluta
Previous Article in Journal
Target Enzymes of Origanum majorana and Rosmarinus officinalis Essential Oils in Black Cutworm (Agrotis ipsilon): In Vitro and In Silico Studies
Previous Article in Special Issue
Diet Affects the Temperature–Size Relationship in the Blowfly Aldrichina grahami
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Insects
Volume 15
Issue 7
10.3390/insects15070484
insects-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Effects of Two Prey Species Combinations on Larval Development of the Predatory Ladybird Cheilomenes propinqua

by
Andrey N. Ovchinnikov
1,
Antonina A. Ovchinnikova
1,
Sergey Y. Reznik
1,* and
Natalia A. Belyakova
2
1
Zoological Institute, Russian Academy of Sciences, Universitetskaya 1, 199034 St. Petersburg, Russia
2
All-Russia Institute of Plant Protection, Russian Academy of Sciences, Podbelskogo 3, 196608 St. Petersburg, Russia
*
Author to whom correspondence should be addressed.
Insects 2024, 15(7), 484; https://doi.org/10.3390/insects15070484
Submission received: 24 May 2024 / Revised: 20 June 2024 / Accepted: 27 June 2024 / Published: 28 June 2024
(This article belongs to the Collection Science of Insect Rearing Systems)
Browse Figures
Versions Notes

Abstract

:

Simple Summary

The selection of an appropriate diet is a key component of methods for the mass rearing of biocontrol agents. It is known that feeding on mixed, alternating, or changing foods often favor insect development. We investigated the effects of various combinations of high-quality (the green peach aphid) and low-quality (eggs of the grain moth) foods on the development of a predatory ladybird Cheilomenes propinqua. The benefits of mixed foods to larval development were only found in some treatments with limited supplies of aphids. Feeding on various combined diets never resulted in higher survival, faster development, or a larger size of emerging adults than those observed for feeding on unlimited amounts of aphids. We conclude that if necessary (for example, in the case of temporary shortage or a lack of aphids in mass rearing facilities or in the case of preventing release of adults for biological control of pests in greenhouses), C. propinqua larvae can be fed with grain moth eggs by replacing, mixing, or alternating with aphids, although this will result in a decrease in pre-adult survival, rate of development, and the size of emerging adults. On the other hand, even a minimal addition of aphids can have a substantial positive effect on larvae fed with grain moth eggs.

Abstract

Feeding on mixed, alternating, or changing diets often favor insect development. With the aim to optimize mass rearing and use for the biological control of insect pests, we investigated the effects of various combinations of high-quality (the green peach aphid Myzus persicae) and low-quality (eggs of the grain moth Sitotroga cerealella) foods on the larval development of a predatory ladybird Cheilomenes propinqua. In the first experiment, eggs and aphids were mixed in different proportions; in the second experiment, larvae switched from feeding on aphids to feeding on eggs. Although the beneficial additive effect of mixed foods was detected in some treatments with limited diets, feeding on various combinations of eggs with aphids never resulted in higher survival, faster development, or a larger size of emerging adults than those observed for feeding on unlimited amounts of aphids. For the practice of biological control, we conclude that, if necessary (for example, in the case of temporary shortage or a lack of aphids in mass rearing facilities or in the case of preventing release of C. propinqua adults in greenhouses), C. propinqua larvae can be fed with grain moth eggs by replacing, mixing, or alternating with aphids, although this will inevitably result in a proportional decrease in pre-adult survival, rate of development, weight, and size of the emerging adults. On the other hand, even a minimal addition of aphids can have a substantial positive effect on larvae fed with grain moth eggs.

1. Introduction

The selection of an appropriate diet is a key component of methods for the mass and laboratory rearing of biocontrol agents [1,2,3,4,5]. From an economic point of view, this selection is often a special case of a general ‘price–quality’ schema [6], that is, a choice between highly preferred and most suitable but more expensive natural foods, and relatively cheap but usually much less preferred and less suitable factitious diets. In such situations, many authors have investigated the potential of mixed diets including two or several foods of different qualities [7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27]. Much more rarely have alternating [27,28] and changing (switching) [16,29,30,31] diets been tested. Often [7,8,9,10,11,13,14,16,20,22,24,27], although far from always [15,17,18,19,23,25,28], a substantial positive additive effect was observed in these studies: feeding on mixed, alternating, or changing diets resulted in better survival, faster development and maturation, larger individuals, higher fecundity, etc. than feeding on each of their components.
Polyphagous predatory ladybirds are widely used for the biological control of insect pests particularly because of their broad food specificity: one and the same agent can be used against various pests [1,2,3,4,32,33,34]. Indeed, both in laboratory and under natural conditions, many ladybird species can feed on very different animal and plant substances [4,34,35,36,37,38]. However, although different foods can be consumed, their relative suitability can vary drastically. Hodek [35,36] suggested that all acceptable foods of predatory coccinellids could be roughly divided into (1) ‘essential’ foods that ensure the successful completion of larval growth and the development, maturation, mating, normal oogenesis and oviposition by females, and (2) ‘alternative’ foods that can be used merely as a source of energy for the long-term survival of adults. Under natural conditions, the essential prey of different coccinellid predators are most often aphids, soft scales, thrips, mites, and other foods rich in proteins whereas alternative foods are floral nectars, fruit juices, and other plant substances high in carbohydrates. Moreover, essential foods can differ markedly in their preference and suitability for larval development and the reproduction of adult ladybirds [4,8,20,35,36,38,39,40,41,42,43]. As above-mentioned, the laboratory and mass rearing of the natural prey of ladybirds is usually a costly process because of the necessity of growing their host plants. Therefore, factitious (not natural) essential foods, in particular, the eggs of easily reared lepidopteran pests of stored products such as the Mediterranean flour moth, Ephestia kuehniella Zeller, and the Angoumois grain moth, Sitotroga cerealella (Olivier), are often used [8,10,20,35,36,38,39,40,42,43,44].
Over the past few years, we have studied a predatory ladybird Cheilomenes propinqua vicina Mulsant (=Cydonia (Cheilomenes) vicina Mulsant) that is widely distributed in subtropical and tropical regions of Africa and Southwest Asia [45]. This polyphagous predator, often reaching high population densities, is rightly considered by many authors as an important natural enemy of various agricultural insect pests. In particular, it was recorded as a predator of Aphis gossypii Glover on pear trees in Egypt [46], on guava trees in South Africa [47], eggplants in India [48]; citrus psylla Trioza erytreae (Del Guercio) in South Africa [49]; mealybugs on guava trees in Egypt [50]; the cotton mealybug Phenacoccus solenopsis Tinsley on various agricultural plants in Israel [51]; mealybugs and green scales on coffee plants in Tanzania [52]; Coccidae infesting fruit trees in Egypt [53]; whiteflies on cassava in Kenya [54]; various insect pests of grapevine [55]; and aphids, mealybugs, and soft scales on various cultural plants in Egypt [56,57,58], Sudan [59], Benin [60], and India [48]. Such a broad range of prey including a number of important pests of protected crops, wide habitat specificity, and large geographic range allow the hope that C. propinqua can be successfully used as an effective agent for biological control in greenhouses. In addition, C. propinqua larvae and adults show a rather high voracity: when feeding on A. gossypii, the larvae of this relatively small (adult body length 4–5 mm) ladybird consumed a total of about 500 aphids during their development whereas the females consumed 40–80 aphids per day with a total of about 2000 individuals per female [43,61,62,63]. Indeed, pilot trials showed that C. propinqua is able to successfully control Aphis fabae Scop on kalanchoe crops in greenhouse conditions [61].
Moreover, preliminary biological studies have shown that this predatory ladybird combines rapid development (10–11 days from the egg to adult stage under the optimal conditions) with high fecundity (15–30 eggs per day with a total fecundity of about 1000 eggs per female), suggesting a high potential for mass rearing [43,61,62,63]. However, the development of optimal methods for the mass rearing and application of a biocontrol agent requires basic information on its biological peculiarities. Earlier studies concerned the influence of temperature, aphid prey species, and its host plant on the rate of C. propinqua pre-adult development, adult size and longevity, female maturation, and fecundity [57,64]. Influences of photoperiod, temperature, and diet on the induction of reproductive (adult) diapause [43], the transportation and storage potential of females [65], and on the prey search activity of adults [66] have also been investigated. A special study was devoted to the comparison of the pre-adult mortality, rate of development, fecundity, net reproduction rate, rate of increase, and other biological parameters in individuals fed on different prey species [59]. In these studies, C. propinqua larvae and adults were fed either by preferred high-quality essential prey species such as aphids Aphis fabae Scop. [63], A. gossypii Glover [57,59], A. nerii Boyer de Fonscolomb [59,64], Melanaphis sacchari Zehntner [59], and Myzus persicae (Sulzer) [43,65,66] or by also essential but much less preferred and less suitable low-quality food such as the eggs of the grain moth S. cerealella [43,65,66]. The effects of mixed, alternating, or changing diets on C. propinqua larvae and adults have not been investigated, although these approaches have been successfully used with many other mass-reared insects from different orders [7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31].
It should be also mentioned that mixed diets can be interesting to biocontrol practitioners in two quite different aspects. First, as noted above, feeding on mixtures of different foods can be a promising method for the laboratory and mass rearing of C. propinqua. Second, it is expected that C. propinqua could be used for the biological control of aphids in greenhouses by the so-called ‘standing army’ method, that is, preventing release of adults not after but before the substantial increase in pest population density [33,67,68,69,70,71,72,73,74,75]. This approach is currently considered very promising, but its application usually requires the regular supplementation of factitious food to promote the survival of the released biocontrol agents at low pest population density or even in the absence of pests (potential prey). In the case of C. propinqua, grain moth eggs could be used for this supplementation, whereby the ladybirds would feed on the eggs with the possible addition of some quantity of aphids or other high-quality prey. Therefore, we have quite recently studied the effects of mixed diets (combinations of eggs of the grain moth S. cerealella and the green peach aphid M. persicae in different proportions) on the reproductive maturation and fecundity of C. propinqua females. Mixed diets of this type (low-quality food with the addition of different proportions of high-quality prey) have been used in a number of earlier studies [20,76,77]. Our previous experiments revealed that some of the tested mixed diets can be considered as promising foods for C. propinqua females, although the economic feasibility of this method is not clear yet [78]. With regard to basic entomology, the authors of recent reviews on the ecophysiology of predatory ladybirds noted that the additive effects of mixed diets were found only in some of the studies on this subject, and the reasons of this variability are also still not clear [4,18,23,34,35,37]. Therefore, any new data on this topic can be used for further meta-analysis.
The aim of the present study was to evaluate the suitability of mixed and changing diets consisting of different proportions of green peach aphids and grain moth eggs for C. propinqua pre-adult development and the influence of these diets on the biological parameters of the emerged adults. The working hypothesis of our study was that mixed food will be the optimal diet for the development of C. propinqua.

2. Materials and Methods

2.1. Insects

The experiments were performed in 2023–2024 with a laboratory population of C. propinqua that originated from 42 adults collected in September 2015 in Alexandria, Egypt (31.200391° N, 29.9155046° E) and then reared at the Biocontrol Laboratory, All-Russian Institute of Plant Protection on the wheat aphid (Schizaphis graminum Rond.) at a temperature of about 24 °C and the photoperiod of L:D = 16:8 (hereafter, light and dark periods in h are given). Before the experiments, the ladybirds were reared for about three years at the Laboratory of Experimental Entomology, Zoological Institute RAS at a temperature of 25 °C and L:D = 16:8 on the green peach aphid M. persicae, which were reared on Vicia faba L. seedlings.

2.2. Experimental Design

2.2.1. General Methods

At the start of each experiment, a group of about 100 larvae hatched over 24 h from eggs laid by 40–50 C. propinqua females of the main laboratory population was reared at 25 °C and L:D = 16:8 on the green peach aphid in transparent plastic containers (27 × 38 × 27 cm) covered with cotton cloth. After emergence, adults were sexed using morphological differences of the terminal sternites: males have a straight margin of the last abdomen sternite while females have a convex distal margin [79,80,81]. In addition, females have a distinct black area along the anteromedian margin of the head [82]. Then, the adults were kept in Petri dishes (90 × 15 mm) at the same temperature and day length in groups of 6–10 individuals (equal number of males and females) and fed one of the two diets: (1) larvae and adults of the green peach aphid M. persicae on a V. faba seedling (hereafter ‘aphids’) and (2) eggs of the Angoumois grain moth S. cerealella glued by 30% sugar solution to a piece of hard paper and an Eppendorf tube filled with water and plugged with a cotton ball (hereafter ‘eggs’). Eggs laid by females fed on each of the two diets were collected daily within 2–4 h after light-on and incubated separately in Petri dishes of the same size under the same conditions. Hatched larvae of the first instar were kept in the same Petri dishes until molt to the second instar. Larvae of the first instar were not fed; the survived individuals cannibalize eggs and other larvae, which is normal for predatory Coccinellidae [35,36,37,38]. Larvae of the second instar were collected daily within 2–4 h after light-on, then reared individually in Petri dishes that were the same size at the same photothermal conditions, and fed on different diets according to the experimental design (see Section 2.2.2 and Section 2.2.3). All other conditions in different treatments of each experiment were exactly the same.
Each larva was checked daily (2–4 h after light-on) for survival and instar change. Instar change was determined by the presence of shed exuvium and by changes in the color, size, shape, and positions of various larval elements of armature on the dorsal and lateral sides of the thoracic and abdominal segments such as the scoli and parascoli (Figure 1). It is known that most coccinellids have four larval stages, and in the first instar larvae, scoli are shorter, having a small number of branches and longer setae [83,84]. The parascolus is shortened, and there is a modified scolus, (a type of branched projection of the body), the length of which is usually no more than three times its width. Each branch of the scolus bears one thick seta at the distal end. Short descriptions of the larval instars (see also Figure 1) are provided, and the terminology of the different structures on the body of larvae follows Gage’s nomenclature [85].
  • First instar larva. Body is elongated, cylindrical, and tapered, with whitish yellow integument. Larval elements of armature are weakly sclerotized. Parascoli are short (about 0.06 mm) and thick.
  • Second instar larva. Body and armature of the body surface are sclerotized, pigmented with whitish yellow areas of body. Parascoli are about 0.14 mm, well sclerotized, darker than those on the first instar.
  • Third instar larva. Larvae are similar to the second instar in structure and color, body shape is cylindrical and slightly elongated; parascoli are about 0.2 mm, of the same color as the integument.
  • Fourth instar larva. Tegument is dark brown with well-demarcated whitish yellow areas of body. Parascoli are brighter colored, larger (0.3–0.4 mm), and more sclerotized than those of the third instar.
Pupation and adult emergence were also recorded every day at the same time (2–4 h after light-on). Freshly emerged adults were immediately weighted with an analytical electronic balance (OHAUS PA-64C) with an accuracy of 0.1 mg and sexed. Then, the maximum body width (with closed elytra) was determined using an MSP-2 stereomicroscope with an accuracy of 0.05 mm as an estimation of adult size. Thus, for each experimental treatment (that is for each tested diet), the survival and mean time of development from the second larval instar to the adult stage and the mean size and weight of emerging adults were determined. Considering that size and weight are closely correlated with the fecundity and voracity of predatory ladybirds [4,14,41,86,87,88,89], we can conclude that the combination of the parameters recorded in our study can be used as a proxy for both the potential of intensive mass rearing and the efficiency of application for the biological control of insect pests.

2.2.2. The First Experiment (Mixed Diets)

In the first ‘mixed diets’ experiment, each larva was fed on the same diet throughout its life. In different treatments, different mixed and pure diets were used. All larval diets consisted of one or both of the two prey species: ‘aphids’ (larvae and/or adults of the green peach aphid M. persicae) and ‘eggs’ (eggs of the Angoumois grain moth S. cerealella). Eggs (if any) were always provided in excess, whereas aphids in certain diets were limited. This can be explained by the fact that in mass rearing, eggs are considered as a relatively cheap, low-quality factitious diet in contrast to aphids, which are a high-quality but much more expensive food source [78]. Regarding preventing colonization, in greenhouses, eggs can be regularly supplemented in sufficient quantity, whereas the population density of aphids (pests) is expected to be unpredictable and usually low, if not zero. Therefore, the different diets included four levels of aphid content: zero, low (5–10% of the average daily demand for a given day of larval development), medium (about 50% of the average daily demand), and high (unlimited, or more exactly substantially higher than the average daily demand for a given day of development). It should be noted that when planning our experiments, we did not use the physiological (larval instars) but absolute (days) time scale. The reason for this is that the physiological time scale, although more natural, would be too complicated for a practical application. Therefore, it should be considered that our data are valid for the temperature of 25 °C, whereas lower or higher temperatures would require a corresponding elongation or shortening of the time scale. Thus, based on the average daily demands determined in our (unpublished) pilot tests, the quantities of aphids and eggs included in the mixed diets were determined (Table 1). The grain moth eggs were glued by a 30% sugar solution to a piece of hard paper (10 × 15 mm); the amounts of grain moth eggs and sugar solution were kept constant for all treatments in the experiment. Larvae fed on all diets that included eggs were offered an Eppendorf tube filled with water and plugged with a cotton ball. Aphids (if any) were provided on a V. faba seedling (10–30 mm in length); if aphids were not included in the diet, an empty (not infested by aphids) V. faba seedling was placed in a Petri dish. In combination, two diets of maternal females and seven larval diets led to 14 treatments in the first experiment. Each treatment was performed on 52–58 larvae with a total of 775 individuals, 532 of which (41–51 per treatment, with the exception of the LA diet) developed to the adult stage.

2.2.3. The Second Experiment (Changing Diets)

In the second ‘changing diets’ experiment, all larvae were fed on pure (unmixed) diets (either eggs or aphids) and both foods were always provided in excess. However, the diet was not constant throughout the period of development: initially, the larvae fed on aphids and then switched to feeding on eggs. The difference between the experimental treatments was in the duration of the period of feeding on aphids: 1, 2, 3, 4, or 5 days. In addition, two controls were performed: (1) larvae that constantly fed on eggs (the duration of the period of feeding on aphids was zero) and (2) larvae that constantly fed on aphids (the duration of the period of feeding on aphids was more than 5 days). As shown by our (unpublished) pilot experiments and confirmed by the present study, C. propinqua larval development from the second instar larva to the pupal stage at 25 °C lasted for 7–10 days, depending on diet. In particular, in larvae constantly fed on aphids, this period constituted about 7 days. As in the first experiment, aphids were provided on a V. faba seedling (10–30 mm in length), and the grain moth eggs were glued by a 30% sugar solution to a piece of hard paper (10 × 15 mm). All larvae fed on eggs were also offered an Eppendorf tube filled with water and plugged with a cotton ball and an empty (not infested by aphids) V. faba seedling. In combination, two diets of maternal females and seven larval diets (five experimental treatments and two controls, see Table 2) led to 14 treatments. Each treatment of the second experiment was performed on 56–67 larvae with a total of 846 individuals, 668 of which (42–54 per treatment) reached the adult stage.

2.3. Statistical Analysis

Statistical analysis was performed with SYSTAT 10.2 (Systat Software Inc., Richmond, VA, USA). Non-parametric data were analyzed with the chi-square test (when necessary, the Mantel–Haenszel adjustment was used). Parametric data were not normally distributed and were therefore ranked before ANOVA. Single pairwise comparisons of the parametric data were made with the Kruskal–Wallis test; multiple pairwise comparisons with Tukey’s HSD test on ranked data. Other details of statistical analysis are given in the figures and tables.

3. Results

3.1. The First Experiment (Mixed Diets)

3.1.1. Pre-Adult Survival and Sex

A pairwise chi-square test conducted separately for the seven larval diets showed that the influence of the food of maternal females (either aphids or eggs) on the survival of their progeny from the second instar larva to the adult stage was not statistically significant (p > 0.05 for all larval diets). Analysis of the pooled data for all diets (chi-square test with the Mantel–Haenszel adjustment, larval diet was used as a strata variable) showed the same result: χ2 = 1.48, df = 1, n = 775, p = 0.224. Therefore, the data for survival with the two female diets were pooled for further statistical analysis. The influence of larval diet, in contrast, was highly statistically significant for the total data of the experiment: χ2 = 303.9, df = 6, n = 775, p < 0.001. Indeed, as seen in Figure 2A, almost all of the larvae fed on the LA diet died, whereas more than half of the larvae fed on other diets survived to the adult stage. Among them, the highest survival was recorded for the larvae fed on diets with an unlimited supply of aphids (EHA and HA) and the lowest for those fed on grain moth eggs without or with the minimum addition of aphids (E and ELA). Mortality structure, as shown by the chi-square analysis of the total data, was also dependent on the larval diet: χ2 = 152.3, df = 3, n = 243, p < 0.001. The general pattern, however, was similar in all treatments of the experiment: the highest mortality occurred at the first and second larval instars (Figure 3A). The influence of maternal diet on the structure of mortality was not statistically significant: χ2 = 1.1, df = 3, n = 243, p = 0.776.
The proportion of females in the total progeny was 49.3%, which was not significantly different from the equal distribution: χ2 = 0.12, df = 1, n = 532, p = 0.729. Mantel–Haenszel chi-square analysis with the larval diet used as a strata variable showed that the male/female ratio was not dependent on the diet of maternal females: χ2 = 0.39, df = 1, n = 532, p = 0.533. Then, the data for the two maternal diets were pooled, and the chi-square analysis of these data showed that the influence of larval diet was also not statistically significant: χ2 = 2.24, df = 5, n = 532, p = 0.815.

3.1.2. Time of Development

Three-way ANOVA of the total data (Table 3) showed that the time of C. propinqua development from the second larval instar to the adult stage was significantly dependent on both the maternal and larval diets, whereas the influence of sex as well as all interactions were not statistically significant. Hence, the data for males and females were pooled for further statistical analysis. As seen in Figure 4A, the rate of development showed the same pattern of dependence on larval diet as survival (see Figure 2A): the fastest development was recorded for the larvae fed on diets with an unlimited supply of aphids (EHA and HA) and the slowest for those fed on grain moth eggs without or with the minimum addition of aphids (E and ELA), whereas larvae that received the medium daily supply of aphids (EMA and MA) showed intermediate results. With regard to maternal diet, larvae hatched from the eggs laid by females fed on grain moth eggs on average developed somewhat faster than those hatched from the eggs laid by females fed on green peach aphids, although in the pairwise comparisons, this difference was statistically significant for only two larval diets (Table 3 and Figure 4A).

3.1.3. Size and Weight of Emerging Adults

Three-way ANOVA of the total data (Table 3) showed that the weight and size of the emerging C. propinqua adults strongly depended on the larval diet and sex of an individual; the interaction of these two factors was also significant, whereas the influence of maternal diet and all other interactions were not statistically significant. Hence, the data on the progeny of females fed on different diets were pooled for further statistical analysis. As seen in Figure 5A and Figure 6A, the size and weight of the males and females showed a similar pattern of dependence on larval diets. Feeding only on eggs (E diet) resulted in the emergence of the smallest and lightest individuals. The addition of the minimum amount of aphids (ELA diet) caused a slight increase in adult size and weight, although this difference was only statistically significant for females. The treatment with the medium amount of aphids (MA diet) yielded somewhat larger and heavier adults, and again, the addition of eggs (EMA diet) resulted in an increase in size and weight (in this case, the difference was statistically significant for both males and females). The largest and heaviest individuals emerged from larvae fed on a high (practically unlimited) amount of aphids (HA diet); the addition of eggs to the unlimited amount of aphids (EHA diet) did not cause any significant changes in adult size and weight (Figure 5A and Figure 6A).

3.2. The Second Experiment (Changing Diets)

3.2.1. Pre-Adult Survival and Sex

Analysis of the total data (chi-square test with the Mantel–Haenszel adjustment, larval diet was used as a strata variable) showed that the influence of the food of the maternal females (either aphids or eggs) on the survival of their progeny from the second instar larva to the adult stage was not statistically significant: χ2 = 1.09, df = 1, n = 846, p = 0.296. Pairwise chi-square tests conducted separately for the seven larval diets also did not reveal any statistically significant difference (p > 0.05 for all cases). Therefore, data for the two female diets were pooled for further statistical analysis. The influence of larval diet, based on the total data of the experiment, was highly statistically significant: χ2 = 33.5, df = 6, n = 846, p < 0.001. As seen in Figure 2B, when the number of days of feeding on aphids increased from 0 to 3, the pre-adult survival gradually increased from 64.7 to 83.4% and then remained stable around this level. Further analysis showed that the mortality structure was not significantly dependent on the maternal diet: χ2 = 4.1, df = 3, n = 178, p = 0.253. Treatments with different larval diets, as seen in Figure 3B, slightly differed in the structure of mortality, but this difference was not statistically significant: χ2 = 25.8, df = 18, n = 178, p = 0.105.
Females constituted 49.7% of the total progeny, which was not significantly different from the equal distribution: χ2 = 0.02, df = 1, n = 668, p = 0.877. Mantel–Haenszel chi-square analysis with the larval diet used as a strata variable showed that the proportion of females in the progeny was not dependent on the maternal diet: χ2 = 0.47, df = 1, n = 668, p = 0.495. Therefore, the data for the two maternal diets were pooled for chi-square analysis of the total data, which showed that the influence of larval diet was also not statistically significant: χ2 = 7.0, df = 6, n = 668, p = 0.322.

3.2.2. Time of Development

Three-way ANOVA of the total data of the second experiment showed that time of C. propinqua development from the second larval instar to the adult stage significantly depended on the larval diet, whereas the influence of the diet of maternal females was not statistically significant (Table 4). In addition, males developed somewhat faster than females, but (as demonstrated by statistically insignificant interactions) both sexes showed the same pattern of differences between larval diets. As seen in Figure 4B, the time of pre-adult development decreased with the number of days when the larvae fed on aphids. In contrast to pre-adult survival, a gradual uniform increase in the rate of pre-adult development occurred over the whole range of the used diets (comp. Figure 2B and Figure 4B).

3.2.3. Size and Weight of Emerging Adults

Three-way ANOVA of the total data (Table 4) showed that the weight and size of emerging C. propinqua adults strongly depended on the larval diet and sex of an individual; the interaction of larval and maternal diets was marginally significant, whereas the direct influence of maternal diet and all other interactions were not statistically significant. The non-significant interaction of the sex and diet factors suggest that the patterns of weight and size dependence on larval diets in the males and females were similar. This can also be clearly seen in Figure 5B and Figure 6B: both the size and weight of the emerging males and females increased with the number of days of feeding on aphids. Furthermore, for the duration of pre-adult development, this effect was gradual and uniform over the whole range of diets studied.

4. Discussion

First, we conclude that the working hypothesis of our study was only partly confirmed. As clearly indicated by the results of the first experiment, feeding on various mixtures of high-quality (green peach aphids) and low-quality (grain moth eggs) foods never resulted in higher pre-adult survival, faster pre-adult development, or a larger size and weight of emerging adults than those observed for unlimited feeding on aphids. The quality of mixed foods was mostly determined by the contents of aphids. In particular, as seen in Figure 2A, Figure 4A, Figure 5A and Figure 6A, the results obtained with feeding on a practically unlimited number of aphids (HA diet) were not significantly different from those with the EHA diet (unlimited number of aphids with an addition of unlimited number of the grain moth eggs). Thus, based on the results of the whole experiment, the additive effect of mixed diets was not detected. However, on the other hand, in some combinations of the limited diets, a significant positive additive effect was shown. For example, when larvae that hatched from eggs laid by females fed on aphids were then fed with the ELA diet (eggs and low quantity of aphids), the time of their development was significantly shorter than those of larvae fed with the E diet (only eggs), whereas larvae fed on the LA diet (only low quantity of aphids) failed to reach the adult stage (Figure 4A). Moreover, the emerged females in the ELA treatments were larger (Figure 5A) and heavier (Figure 6A) than those in the E treatments. Similarly, the males and females that developed from larvae fed with the EMA diet (eggs and medium quantity of aphids) were larger (Figure 5A) and heavier (Figure 6A) than those developed from larvae fed with the E diet (only eggs) and MA diet (medium quantity of aphids). Thus, in some treatments with limited diets, the additive effect of mixed foods was detected.
The experiment with changing diets yielded similar results. The survival, rate of development, adult size, and adult weight gradually increased with the number of days of feeding on aphids. The patterns of these effects differed between the above-mentioned parameters, but the best results were always obtained with the ladybirds constantly fed on aphids, although the difference from the individuals that fed on aphids for 5 days was not always statistically significant.
Some of the earlier studies also failed to demonstrate any significant positive effect produced by mixed, alternating, or changing diets. For example, experiments with larvae of the seven spotted ladybird Coccinella septempunctata L. fed on three cereal aphid species (alone or in combination) showed that the survival, rate of pre-adult development, prepupal, and adult weight of individuals fed on a mixed diet were not higher (in some cases even significantly lower) than those for ladybirds fed on the best of pure (unmixed) diets [15]. The same conclusion was later made from a study on the same predator but other aphids: no benefit from the mixing of aphid species was found, and the quality of the mixed diets was determined by the quality of the constituent species [18]. The rate of development of Hippodamia convergens (Guerin-Meneville) larvae fed on various mixtures of two aphids (Schizaphis graminum (Rondani) and Rhopalosiphum padi (L.)) and the weight of the emerged adults were not higher than those of individuals fed on the same quantity of each of the two prey species [19]. Larval survival of two aphidophagous ladybirds, H. convergens and Harmonia axyridis (Pallas), fed on a mixture of green peach aphids and eggs of the Colorado potato beetle, was significantly lower than when the larvae were fed only with green peach aphids, although in both cases, the aphids were provided in excess [23]. Brumoides foudrasii (Mulsant) females fed on high-quality natural food, mealybugs Ferrisia dasylirii (Cockerall), had more mature oocytes than females fed on the mixture of F. dasyliri and the low-quality factitious food, flower pollen [17]. However, another recent study on H. convergens obtained ambiguous results: larvae fed only on S. graminum showed faster larval development and a higher weight of emerging adults than larvae fed on the mixture of this prey with plant substances (pollen, sugars, and leaves), but when feeding only on aphids was continued through adult life, the preoviposition period was longer and female fecundity was lower than in individuals fed on the mixed diet [25]. Regarding insect predators from other orders, for instance, the longevity and fecundity of Orius laevigatus (Fieber) (Heteroptera, Anthocoridae) females fed on eggs of the grain moth Sitotroga cerealella (Oliv.) alternated with cysts of the brine shrimp Artemia salina Leach were not higher than those of females fed on the more suitable of the two foods, the grain moth eggs [28].
To justify our unfulfilled expectations, we noted that in many other earlier studies conducted on various species of predatory ladybirds such as Adalia bipunctata (L.) [9,10], Coccinella septempunctata L. [13], C. transversalis (F.) [11], C. transversoguttata Brown [13], Harmonia axyridis (Pallas) [8,12,20,24], Heteroneda billardieri (Crotch) [7], Hippodamia variegata (Goeze) [22], Oenopia conglobata contaminata (Menetries) [14], and Propylea japonica (Thunberg) [16] feeding on mixed or changing diets resulted in higher rates of survival, development, and maturation, larger individuals, and higher fecundity than feeding on each of their components.
Moreover, as noted above, the results of our study cannot be considered as definitely negative. Indeed, the first experiment showed that about 70% of the larvae fed on the ELA diet (the grain moth eggs plus a low quantity of aphids) developed to adults, whereas practically all larvae fed only on a low quantity of aphids (LA diet) failed to reach the adult stage (Figure 1A). Similarly, as seen in Figure 5A and Figure 6A, adults that emerged from the larvae fed on the EMA diet (eggs plus medium quantity of aphids) were significantly heavier and larger than those that emerged from the larvae fed only on a medium quantity of aphids (MA diet). Hence, the possibility of feeding on low-quality food (grain moth eggs) can at least partly compensate for the shortage of high-quality food (aphids). Although this will result in a proportional decrease in pre-adult survival, the rate of development, and the size of emerging adults, these parameters will still be higher than those in the absence of grain moth eggs.
Thus, we conclude for the practice of laboratory and mass rearing that if necessary (for example, in the case of temporary shortage or a lack of aphids), C. propinqua larvae can be fed with grain moth eggs by replacing, mixing, or alternating with aphids, although this will inevitably result in a proportional decrease in the pre-adult survival, rate of development, and size of the emerging adults. In the case of preventing release of C. propinqua adults for the biological control of pests in greenhouses, larvae hatched from the laid eggs will be able to feed on both aphids or other high-quality prey and supplemented factitious food (the grain moth eggs), but the shortage of high-quality food will lead to the above-mentioned negative consequences. On the other hand, even a minimal addition of aphids can have a substantial positive effect on the development of larvae fed with grain moth eggs. Regarding basic entomology, it is interesting to note that in our study, a significant additive effect was only found in the treatments with a limited supply of high-quality food.

Author Contributions

Conceptualization, N.A.B. and S.Y.R.; Methodology, S.Y.R., A.N.O., A.A.O. and N.A.B.; Investigation, A.N.O. and A.A.O.; Data curation, A.A.O. and A.N.O.; Writing—original draft preparation, S.Y.R., A.N.O. and N.A.B.; Writing—review and editing, A.N.O., A.A.O. and N.A.B.; Visualization, S.Y.R. and A.N.O.; Project administration, N.A.B.; Funding acquisition, S.Y.R. and N.A.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was partly funded by the state research project ‘Taxonomy, morphology, ecophysiology, and evolution of insects’ (# 122031100272-3) from the Ministry of Sciences and High Education of the Russian Federation.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We are thankful to L.S. Ramenskaya and V.V. Tsvetkova (Zoological Institute) for their assistance in the experiments.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Van Lenteren, J.C. IOBC Internet Book of Biological Control, Version 6. 2012. Available online: https://www.iobc-global.org/publications_iobc_internet_book_of_biological_control.html (accessed on 25 May 2023).
  2. Van Lenteren, J.C.; Alomar, O.; Ravensberg, W.J.; Urbaneja, A. Biological control agents for control of pests in greenhouses. In Integrated Pest and Disease Management in Greenhouse Crops; Gullino, M.L., Albajes, R., Nicot, P.C., Eds.; Springer: Cham, Switzerland, 2020; pp. 409–439. [Google Scholar]
  3. Van Lenteren, J.C.; Bueno, V.H.; Klapwijk, J.N. Augmentative Biological Control. In Biological Control: Global Impacts, Challenges and Future Directions of Pest Management; Mason, P.G., Ed.; Csiro Publishing: Clayton, Australia, 2021; pp. 90–109. [Google Scholar]
  4. Riddick, E.W. Benefits and limitations of factitious prey and artificial diets on life parameters of predatory beetles, bugs, and lacewings: A mini-review. BioControl 2009, 54, 325–339. [Google Scholar] [CrossRef]
  5. Thompson, S.N. Nutrition and culture of entomophagous insects. Annu. Rev. Entomol. 1999, 44, 561–592. [Google Scholar] [CrossRef]
  6. Thomas, M. Heuristic price theory: A model of pluralistic price evaluations. Consum. Psychol. Rev. 2023, 6, 75–91. [Google Scholar] [CrossRef]
  7. Badrulhadza, A.; Velasco, L.R.I.; Medina, C. Suitability of non-natural prey during the larval growth of Heteroneda billardieri (Crotch), a potential predator of mango leafhopper. J. Trop. Agric. Food Sci. 2019, 47, 15–24. [Google Scholar]
  8. Berkvens, N.; Bonte, J.; Berkvens, D.; Deforce, K.; Tirry, L.; De Clercq, P. Pollen as an alternative food for Harmonia axyridis. BioControl 2008, 53, 201–210. [Google Scholar] [CrossRef]
  9. Bonte, M.; Samih, M.A.; De Clercq, P. Development and reproduction of Adalia bipunctata on factitious and artificial foods. BioControl 2010, 55, 485–491. [Google Scholar] [CrossRef]
  10. De Clercq, P.; Bonte, M.; Van Speybroeck, K.; Bolckmans, K.; Deforce, K. Development and reproduction of Adalia bipunctata (Coleoptera: Coccinellidae) on eggs of Ephestia kuehniella (Lepidoptera: Phycitidae) and pollen. Pest Manag. Sci. 2005, 61, 1129–1132. [Google Scholar] [CrossRef]
  11. Evans, E.W. Egg production in response to combined alternative foods by the predator Coccinella transversalis. Entomol. Exp. Appl. 2000, 94, 141–147. [Google Scholar] [CrossRef]
  12. Evans, E.W.; Gunther, D.I. The link between food and reproduction in aphidophagous predators: A case study with Harmonia axyridis (Coleoptera: Coccinellidae). Eur. J. Entomol. 2005, 102, 423–430. Available online: https://www.eje.cz/pdfs/eje/2005/03/13.pdf (accessed on 15 May 2024). [CrossRef]
  13. Evans, E.W.; Stevenson, A.T.; Richards, D.R. Essential versus alternative foods of insect predators: Benefits of a mixed diet. Oecologia 1999, 121, 107–112. [Google Scholar] [CrossRef]
  14. Hassani, F.; Shirvani, A.; Rashki, M. Fitness evaluation of Oenopia conglobata contaminata (Menetries) (Col.: Coccinellidae) fed on different diets. Acta Biol. Slov. 2019, 62, 35–43. [Google Scholar] [CrossRef]
  15. Hauge, M.S.; Nielsen, F.N.; Toft, S. The influence of three cereal aphid species and mixed diet on larval survival, development and adult weight of Coccinella septempunctata. Entomol. Exp. Appl. 1998, 89, 319–322. [Google Scholar] [CrossRef]
  16. Li, D.; Chen, P.; Liu, J.; Chi, B.; Zhang, X.; Liu, Y. Artificial rearing of the ladybird Propylea japonica on a diet containing oriental armyworm, Mythimna separata. Entomol. Exp. Appl. 2021, 169, 472–479. [Google Scholar] [CrossRef]
  17. de Lima, M.S.; Pontes, W.J.T.; de Lucena Nóbrega, R. Pollen did not provide suitable nutrients for ovary development in a ladybird Brumoides foudrasii (Coleoptera: Coccinellidae). Divers. J. 2020, 5, 1486–1494. [Google Scholar] [CrossRef]
  18. Nielsen, F.H.; Hauge, M.S.; Toft, S. The influence of mixed aphid diets on larval performance of Coccinella septempunctata (Col., Coccinellidae). J. Appl. Entomol. 2002, 126, 194–197. [Google Scholar] [CrossRef]
  19. Phoofolo, M.W.; Giles, K.L.; Elliott, N.C. Quantitative evaluation of suitability of the greenbug, Schizaphis graminum, and the bird cherry-oat aphid, Rhopalosiphum padi, as prey for Hippodamia convergens (Coleoptera: Coccinellidae). Biol. Control 2007, 41, 25–32. [Google Scholar] [CrossRef]
  20. Reznik, S.Y.; Vaghina, N.P. Effects of photoperiod and diet on diapause tendency, maturation and fecundity in Harmonia axyridis (Coleoptera: Coccinellidae). J. Appl. Entomol. 2013, 137, 452–461. [Google Scholar] [CrossRef]
  21. Rojas, M.G.; Morales-Ramos, J.A.; Riddick, E.W. Use of Tenebrio molitor (Coleoptera: Tenebrionidae) powder to enhance artificial diet formulations for Coleomegilla maculata (Coleoptera: Coccinellidae). Biol. Control 2016, 100, 70–78. [Google Scholar] [CrossRef]
  22. Sayed, S.M.; El Arnaouty, S.A. Effect of corn pollens, as supplemental food, on development and reproduction of the predatory species, Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae). Egypt. J. Biol. Pest Control 2016, 26, 457–461. [Google Scholar]
  23. Snyder, W.E.; Clevenger, G.M. Negative dietary effects of Colorado potato beetle eggs for the larvae of native and introduced ladybird beetles. Biol. Control 2004, 31, 353–361. [Google Scholar] [CrossRef]
  24. Soares, A.O.; Coderre, D.; Schanderl, H. Dietary self-selection behaviour by the adults of the aphidophagous ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae). J. Anim. Ecol. 2004, 73, 478–486. [Google Scholar] [CrossRef]
  25. Stowe, H.E.; Michaud, J.P.; Kim, T. The benefits of omnivory for reproduction and life history of a specialized aphid predator, Hippodamia convergens (Coleoptera: Coccinellidae). Environ. Entomol. 2021, 50, 69–75. [Google Scholar] [CrossRef]
  26. Vahmani, A.; Shirvani, A.; Rashki, M. Biological parameters of Oenopia conglobata (Linnaeus) (Coleoptera: Coccinellidae) feeding on different diets. Int. J. Trop. Insect Sci. 2022, 42, 2241–2247. [Google Scholar] [CrossRef]
  27. Zanuncio, J.C.; Molina-Rugama, A.J.; Serrao, J.; Pratissoli, D. Nymphal development and reproduction of Podisus nigrispinus (Heteroptera: Pentatomidae) fed with combinations of Tenebrio molitor (Coleoptera: Tenebrionidae) pupae and Musca domestica (Diptera: Muscidae) larvae. Biocontr. Sci. Technol. 2001, 11, 331–337. [Google Scholar] [CrossRef]
  28. Pazyuk, I.M.; Reznik, S.Y. On the prospects of rearing the predatory bug Orius laevigatus (Fieber)(Heteroptera, Anthocoridae) on cysts of Artemia salina Leach (Crustacea, Anostraca). Entomol. Rev. 2023, 103, 263–269. [Google Scholar] [CrossRef]
  29. Amzah, B.; Velasco, L.R.I.; Medina, C.D. Effect of diet switching on the reproduction of Heteroneda billardieri (Crotch)(Coleoptera: Coccinellidae). Acta Biol. Malaysiana 2012, 1, 55–61. [Google Scholar] [CrossRef]
  30. Badrulhadza, A.; Velasco, L.R.I.; Medina, C. Effect of diet switching on the larval growth of Heteroneda billardieri (Crotch)(Coleoptera: Coccinellidae), predator of mango leafhopper in the Philippines. J. Trop. Agric. Food Sci. 2018, 46, 137–148. [Google Scholar]
  31. Ponsonby, D.J.; Copland, M.J.W. Aspects of prey relations in the coccidophagous ladybird Chilocorus nigritus relevant to its use as a biological control agent of scale insects in temperate glasshouses. BioControl 2007, 52, 629–640. [Google Scholar] [CrossRef]
  32. Michaud, J.P. Coccinellids in biological control. In Ecology and Behaviour of the Ladybird Beetles (Coccinellidae); Hodek, I., van Emden, H.F., Honěk, A., Eds.; John Wiley & Sons: Chichester, UK, 2012; pp. 488–519. [Google Scholar]
  33. Parrella, M.P.; Lewis, E. Biological control in greenhouse and nursery production: Present status and future directions. Am. Entomol. 2017, 63, 237–250. [Google Scholar] [CrossRef]
  34. Pervez, A. Ecology and Behaviour of Predaceous Ladybird Beetles (Coleoptera: Coccinellidae). In Biodiversity, Environment and Ecosystem Services; Arya, M.K., Ed.; Discovery Publishing House: New Delhi, India, 2023; pp. 12–29. [Google Scholar]
  35. Hodek, I. Food Relationships. In Ecology of Coccinellidae; Hodek, I., Honěk, A., Eds.; Kluwer: Dordrecht, The Netherlands, 1996; pp. 143–238. [Google Scholar]
  36. Hodek, I.; Evans, E.W. Food relationships. In Ecology and Behaviour of the Ladybird Beetles (Coccinellidae); Hodek, I., van Emden, H.F., Honěk, A., Eds.; Wiley-Blackwell: Chichester, UK, 2012; pp. 141–274. [Google Scholar]
  37. Michaud, J.P. On the assessment of prey suitability in aphidophagous Coccinellidae. Eur. J. Entomol. 2005, 102, 385–390. [Google Scholar] [CrossRef]
  38. Nedvěd, O.; Honěk, A. Life History and Development. In Ecology and Behaviour of the Ladybird Beetles (Coccinellidae); Hodek, I., van Emden, H.F., Honěk, A., Eds.; Wiley-Blackwell: Chichester, UK, 2012; pp. 54–109. [Google Scholar]
  39. Chen, J.; Qin, Q.J.; Liu, S.; He, Y.Z. Effect of six diets on development and fecundity of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Afr. Entomol. 2012, 20, 76–84. [Google Scholar] [CrossRef]
  40. De Castro-Guedes, C.F.; de Almeida, L.M.; do Rocio Chiarello Penteado, S.; Moura, M.O. Effect of different diets on biology, reproductive variables and life and fertility tables of Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae). Rev. Bras. Entomol. 2016, 60, 260–266. [Google Scholar] [CrossRef]
  41. Honěk, A. Intraspecific variation in body size and fecundity in insects: A general relationship. Oikos 1993, 66, 483–492. [Google Scholar] [CrossRef]
  42. Mirhosseini, M.A.; Hosseini, M.R.; Jalali, M.A. Effects of diet on development and reproductive fitness of two predatory coccinellids (Coleoptera: Coccinellidae). Eur. J. Entomol. 2015, 112, 446–452. [Google Scholar] [CrossRef]
  43. Reznik, S.; Ovchinnikov, A.; Ovchinnikova, A.; Bezman-Moseyko, O.; Belyakova, N. Photoperiodic, thermal and trophic responses of a predatory ladybird Cheilomenes propinqua. J. Appl. Entomol. 2021, 145, 134–144. [Google Scholar] [CrossRef]
  44. Abdel-Salam, A.H.; Abdel-Baky, N.F. Life table and biological studies of Harmonia axyridis Pallas (Col., Coccinellidae) reared on the grain moth eggs of Sitotroga cerealella Olivier (Lep., Gelechiidae). J. Appl. Entomol. 2001, 125, 455–462. [Google Scholar] [CrossRef]
  45. Kovář, I. Family Coccinellidae Latreille, 1807. In Catalogue of Palaearctic Coleoptera; Löbl, I., Smetana, A., Eds.; Apollo Books: Stenstrup, Denmark, 2007; Volume 4, pp. 568–631. [Google Scholar]
  46. Youssif, M.A.I. Coccinellid species and their insect parasitoids in pear orchards at El-Khattara district, Sharkia Governorate, Egypt. J. Entomol. Zool. Stud. 2019, 7, 780–790. [Google Scholar]
  47. Samways, M.J. Interrelationship between an entomogenous fungus and two ant-homopteran (Hymenoptera: Formicidae-Hemiptera: Pseudococcidae & Aphididae) mutualisms on guava trees. Bull. Entomol. Res. 1983, 73, 321–331. [Google Scholar]
  48. Borkakati, R.N.; Venkatesh, M.R.; Saikia, D.K. Insect pests of Brinjal and their natural enemies. J. Entomol. Zool. Stud. 2019, 7, 932–937. [Google Scholar]
  49. Catling, H.D. The bionomics of the South African citrus psylla Trioza erytreae (Del Guercio) (Homoptera: Psyllidae) 4. The influence of predators. J. Entomol. Soc. S. Afr. 1970, 3, 341–348. [Google Scholar]
  50. Adly, D.; Fadl, H.A.; Mousa, S.F.M. Survey and seasonal abundance of mealybug species, their parasitoids and associated predators on guava trees in Egypt. Egypt J. Biol. Pest Control 2016, 26, 657–664. [Google Scholar]
  51. Spodek, M.; Ben-Dov, Y.; Mondaca, L.; Protasov, A.; Erel, E.; Mendel, Z. The cotton mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) in Israel: Pest status, host plants and natural enemies. Phytoparasitica 2018, 46, 45–55. [Google Scholar] [CrossRef]
  52. Magina, F.L.; Kilambo, D.L.; Maerere, A.P.; Teri, J.M. Innovative strategies for control of coffee insect pests in Tanzania: A review. Huria J. Open Univ. Tanzan. 2016, 22, 63–72. [Google Scholar]
  53. Badary, H. Ecological aspects of Sassetia spp. (Coccidae: Coccoidae: Hemiptera) and thier natural enemies in Egypt. Egypt. Acad. J. Biol. Sci. A Entomol. 2011, 4, 163–174. [Google Scholar] [CrossRef]
  54. Atuncha, H.; Ateka, E.; Amata, R.; Mwirichia, R.; Kasina, M.; Mbevi, B.; Wakoli, E. Evaluation of predation potential of coccinellids on cassava whiteflies. J. Entomol. Nematol. 2013, 5, 84–87. [Google Scholar] [CrossRef]
  55. Ghanim, A.A.; Abou-El-naga, A.A.; El-Serafi, H.A.; Jabbar, A.S. Studies on the population densities of certain insect pests attacking grapevine trees and their associated predators in Mansoura district. J. Plant Prot. Pathol. 2015, 6, 1089–1104. [Google Scholar] [CrossRef]
  56. Bayoumy, M.H.; Michaud, J.P. Cannibalism in two subtropical lady beetles (Coleoptera: Coccinellidae) as a function of density, life stage, and food supply. J. Insect Behav. 2015, 28, 387–402. [Google Scholar] [CrossRef]
  57. Abdel-Salam, A.H.; El-Serafi, H.A.; Bayoumy, M.H.; Abdel-Hady, A.A. Effect of temperature and aphid-host plant variety on performance and thermal requirements of Coccinella undecimpunctata L. and Cheilomenes propinqua isis (Mulsant). J. Plant Prot. Pathol. 2018, 9, 375–380. [Google Scholar]
  58. Ramadan, M.M.; Hassan, M.A.; Afifi, M. Ecological studies on the Peach green aphid, Myzus persicae and its natural enemies. J. Plant Prot. Pathol. 2022, 13, 29–35. [Google Scholar] [CrossRef]
  59. Mahmoud, A.K.; Yousif, N.E.; Satti, A.A. Effect of three aphid species on the life tables data of the coccinellid predator, Cheilomenes propinqua vicina (Mulsant). Environ. Nat. Resour. Int. J. 2016, 1, 49–55. [Google Scholar]
  60. Sæthre, M.G.; Godonou, I.; Hofsvang, T.; Tepa-Yotto, G.T.; James, B. Aphids and their natural enemies in vegetable agroecosystems in Benin. Int. J. Trop. Insect Sci. 2011, 31, 103–117. [Google Scholar] [CrossRef]
  61. Nordey, T.; Boni, S.B.; Agbodzavu, M.K.; Mwashimaha, R.; Mlowe, N.; Ramasamy, S.; Deletre, E. Comparison of biological methods to control Aphis fabae Scopoli (Hemiptera: Aphididae) on kalanchoe crops in East Africa. Crop Prot. 2021, 142, 105520. [Google Scholar] [CrossRef]
  62. El-Heneidy, A.H.; El-Serafy, H.A.; Mohamed, N.E.; Elbanna, E.H.E. Biological characteristics of two coccinellid predators when reared on Aphis gossypii Glover and an artificial diet under laboratory condition. J. Plant Prot. Pathol. 2021, 12, 575–578. [Google Scholar] [CrossRef]
  63. Yarpuzlu, F.; Uygun, N. Effects of different temperatures on development and fecundity of a predatory beetle, Cheilomenes propinqua (Mulsant) (Coleoptera: Coccinellidae). Türkiye Biyol. Mücadele Derg. 2010, 1, 97–107. [Google Scholar]
  64. El-Batran, L.A.; Ghanim, A.A.; Shanab, L.M.; Ramadan, M.M. Thermal requirements for development of Aphis nerii Boyer de Fonscolombe and its predator Cydonia vicina isis Muls. J. Plant Prot. Path. 2015, 6, 825–837. [Google Scholar] [CrossRef]
  65. Reznik, S.Y.; Ovchinnikov, A.N.; Bezman-Moseyko, O.S.; Samartsev, K.G.; Belyakova, N.A. Storage potential of the predatory ladybird Cheilomenes propinqua in relation to temperature, humidity, and factitious food. Insects 2022, 13, 613. [Google Scholar] [CrossRef]
  66. Ovchinnikov, A.; Reznik, S.; Bezman-Moseyko, O.; Belyakova, N. Walking activity of a predatory ladybird, Cheilomenes propinqua: Impacts of photoperiod, temperature, and starvation. BioControl 2022, 67, 513–522. [Google Scholar] [CrossRef]
  67. Messelink, G.J.; Bennison, J.; Alomar, O.; Ingegno, B.L.; Tavella, L.; Shipp, L.; Palevsky, E.; Wäckers, F.L. Approaches to conserving natural enemy populations in greenhouse crops: Current methods and future prospects. BioControl 2014, 59, 377–393. [Google Scholar] [CrossRef]
  68. Brenard, N.; Sluydts, V.; De Bruyn, L.; Leirs, H.; Moerkens, R. Food supplementation to optimize inoculative release of the predatory bug Macrolophus pygmaeus in sweet pepper. Entomol. Exp. Appl. 2018, 166, 574–582. [Google Scholar] [CrossRef]
  69. Brenard, N.; Sluydts, V.; Christianen, E.; Bosmans, L.; De Bruyn, L.; Moerkens, R.; Leirs, H. Biweekly supplementation with Artemia spp. cysts allows efficient population establishment by Macrolophus pygmaeus in sweet pepper. Entomol. Exp. Appl. 2019, 167, 406–414. [Google Scholar] [CrossRef]
  70. Kozlova, E.G.; Krasavina, L.P.; Orlova, G.S. Experience of biocontrol use in cucumber protection from the complex of greenhouse pests. Zashchita Karantin Rastenii 2019, 11, 39–42. (in Russian). [Google Scholar]
  71. Sade, A.; Steinberg, S.; Salinger-Bubnov, M.; Gilboa, E.; Klempert, G.; Roitman, N.; Grosman, A. Improved western flower thrips control through artemia-based early introduction of Orius laevigatus in commercial pepper greenhouses. IOBC/WPRS Bull. 2019, 147, 39–46. [Google Scholar]
  72. Dader, B.; Colomer, I.; Adan, A.; Medina, P.; Vinuela, E. Compatibility of early natural enemy introductions in commercial pepper and tomato greenhouses with repeated pesticide applications. Insect Sci. 2020, 27, 1111–1124. [Google Scholar] [CrossRef] [PubMed]
  73. Kruidhof, H.M.; Elmer, W.H. Cultural Methods for Greenhouse Pest and Disease Management. In Integrated Pest and Disease Management in Greenhouse Crops; Gullino, M.L., Albajes, R., Nicot, P.C., Eds.; Springer: Cham, Switzerland, 2020; pp. 285–330. [Google Scholar]
  74. Benson, C.M.; Labbe, R.M. Exploring the role of supplemental foods for improved greenhouse biological control. Ann. Entomol. Soc. Am. 2021, 114, 302–321. [Google Scholar] [CrossRef]
  75. Woelke, J.B.; Bouw, M.; Cusumano, A.; Messelink, G.J. Lygus rugulipennis on chrysanthemum: Supplemental prey effects and an evaluation of trap plants. J. Appl. Entomol. 2023, 147, 157–166. [Google Scholar] [CrossRef]
  76. Toft, S. The quality of aphids as food for generalist predators: Implications for natural control of aphids. Eur. J. Entomol. 2005, 102, 371–383. [Google Scholar] [CrossRef]
  77. Zaslavskiy, V.A.; Semyanov, V.P.; Vaghina, N.P. Food as a cue factor controlling adult diapause in the lady beetle Harmonia sedecimnotata (Coleoptera, Coccinellidae). Entomol. Rev. 1998, 78, 774–779. [Google Scholar]
  78. Ovchinnikov, A.N.; Ovchinnikova, A.A.; Reznik, S.Y.; Belyakova, N.A. Signal and nutritional effects of mixed diets on reproduction of a predatory ladybird, Cheilomenes propinqua. Insects 2023, 14, 587. [Google Scholar] [CrossRef]
  79. Ünlü, A.G.; Obrycki, J.J.; Bucher, R. Comparison of native and non-native predator consumption rates and prey avoidance behavior in North America and Europe. Ecol. Evol. 2020, 10, 13334–13344. [Google Scholar] [CrossRef]
  80. Stellwag, L.; Losey, J.E. Sexual dimorphism in North American Coccinellids: Sexing methods for species of Coccinella L. (Coleoptera: Coccinellidae) and implications for conservation research. Coleopt. Bull. 2014, 68, 271–281. [Google Scholar] [CrossRef]
  81. McCornack, B.P.; Koch, R.L.; Ragsdale, D.W. A simple method for in-field sex determination of the multicolored Asian lady beetle Harmonia axyridis. J. Insect Sci. 2007, 7, 10. [Google Scholar] [CrossRef] [PubMed]
  82. Rogers, C.E.; Jackson, H.B.; Eikenbary, R.D.; Starks, K.J. Sex determination in Propylea 14-punctata (Coleoptera: Coccinellidae), an imported predator of aphids. Ann. Entomol. Soc. Am. 1971, 64, 957–959. [Google Scholar] [CrossRef]
  83. Celli, N.G.R.; Almeida, L.M.; Basílio, D.S.; Castro, C.F. The way to maturity: Taxonomic study on immatures of Southern Brazilian Coccinellini (Coleoptera: Coccinellidae) species important in biological control. Zoologia 2021, 38, e64154. [Google Scholar] [CrossRef]
  84. LeSage, L. Coccinellidae (Cucujoidea). In Immature Insects; Stehr, F.W., Ed.; Kendall/Hunt: Dubuque, IA, USA, 1991; Volume 2, pp. 485–494. [Google Scholar]
  85. Gage, J.H. The larvae of Coccinellidae. Ill. Biol. Monogr. 1920, 6, 23–294. [Google Scholar]
  86. Bista, M.; Omkar. Effects of body size and prey quality on the reproductive attributes of two aphidophagous Coccinellidae (Coleoptera) species. Can. Entomol. 2013, 145, 566–576. [Google Scholar] [CrossRef]
  87. Kajita, Y.; Evans, E.W. Relationships of body size, fecundity, and invasion success among predatory lady beetles (Coleoptera: Coccinellidae) inhabiting alfalfa fields. Ann. Entomol. Soc. Am. 2010, 103, 750–756. [Google Scholar] [CrossRef]
  88. Khan, A.A. Stage-specific functional response of predaceous ladybird beetle, Harmonia eucharis (Mulsant)(Coleoptera: Coccinellidae) to green apple aphid, Aphis pomi De Geer (Hemiptera: Aphididae). J. Biol. Control 2010, 24, 222–226. [Google Scholar]
  89. Kundoo, A.A.; Khan, A.A. Coccinellids as biological control agents of soft bodied insects: A review. J. Entomol. Zool. Stud. 2017, 5, 1362–1373. [Google Scholar]
Insects 15 00484 g001
Figure 1. Cheilomenes propinqua larvae of different instars. 1—first instar larva, 2—second instar larva, 3—third instar larva, 4—fourth instar larva. (A)—lateral view, (B)—dorsal view. Photos by A.N. Ovchinnikov.
Figure 1. Cheilomenes propinqua larvae of different instars. 1—first instar larva, 2—second instar larva, 3—third instar larva, 4—fourth instar larva. (A)—lateral view, (B)—dorsal view. Photos by A.N. Ovchinnikov.
Insects 15 00484 g001
Insects 15 00484 g002
Figure 2. Influence of diet on the survival of Cheilomenes propinqua larvae from the second instar to the adult stage. Diets are indicated below the x-axis. (A) The first (mixed diets) experiment; abbreviations of diets: E—eggs of the grain moth, ELA—eggs of the grain moth and low quantity of aphids, EMA—eggs of the grain moth and medium quantity of aphids, EHA—eggs of the grain moth and high quantity of aphids, LA—low quantity of aphids, MA—medium quantity of aphids, HA—high quantity of aphids (see Table 1 for more detailed description of diets). (B) The second (changing diets) experiment; the numbers below the x-axis indicate the number of days when the larvae fed on aphids before the switch to feeding on eggs (see Table 2 for a more detailed description of diets). Data shown are percents and 95% confidence intervals. Sample sizes are indicated above the bars. Bars of the same graph with different letters are significantly different (p < 0.05 by the chi-square test).
Figure 2. Influence of diet on the survival of Cheilomenes propinqua larvae from the second instar to the adult stage. Diets are indicated below the x-axis. (A) The first (mixed diets) experiment; abbreviations of diets: E—eggs of the grain moth, ELA—eggs of the grain moth and low quantity of aphids, EMA—eggs of the grain moth and medium quantity of aphids, EHA—eggs of the grain moth and high quantity of aphids, LA—low quantity of aphids, MA—medium quantity of aphids, HA—high quantity of aphids (see Table 1 for more detailed description of diets). (B) The second (changing diets) experiment; the numbers below the x-axis indicate the number of days when the larvae fed on aphids before the switch to feeding on eggs (see Table 2 for a more detailed description of diets). Data shown are percents and 95% confidence intervals. Sample sizes are indicated above the bars. Bars of the same graph with different letters are significantly different (p < 0.05 by the chi-square test).
Insects 15 00484 g002
Insects 15 00484 g003
Figure 3. Influence of diet on the structure of Cheilomenes propinqua mortality. Diets are indicated below the x-axis. (A) The first (mixed diets) experiment; abbreviations of diets: E—eggs of the grain moth, ELA—eggs of the grain moth and low quantity of aphids, EMA—eggs of the grain moth and medium quantity of aphids, EHA—eggs of the grain moth and high quantity of aphids, LA—low quantity of aphids, MA—medium quantity of aphids, HA—high quantity of aphids (see Table 1 for more detailed description of diets). (B) The second (changing diets) experiment; the numbers below the x-axis indicate the number of days when the larvae fed on aphids before the switch to feeding on eggs (see Table 2 for more detailed description of diets). Data shown are the percentages of different stages of development in the total number of individuals that died before reaching the adult stage: the second instar larvae (L2), the third instar larvae (L3), the fourth instar larvae (L4), and pupae (P). Sample sizes are indicated above the bars.
Figure 3. Influence of diet on the structure of Cheilomenes propinqua mortality. Diets are indicated below the x-axis. (A) The first (mixed diets) experiment; abbreviations of diets: E—eggs of the grain moth, ELA—eggs of the grain moth and low quantity of aphids, EMA—eggs of the grain moth and medium quantity of aphids, EHA—eggs of the grain moth and high quantity of aphids, LA—low quantity of aphids, MA—medium quantity of aphids, HA—high quantity of aphids (see Table 1 for more detailed description of diets). (B) The second (changing diets) experiment; the numbers below the x-axis indicate the number of days when the larvae fed on aphids before the switch to feeding on eggs (see Table 2 for more detailed description of diets). Data shown are the percentages of different stages of development in the total number of individuals that died before reaching the adult stage: the second instar larvae (L2), the third instar larvae (L3), the fourth instar larvae (L4), and pupae (P). Sample sizes are indicated above the bars.
Insects 15 00484 g003
Insects 15 00484 g004
Figure 4. Influence of maternal and larval diets on time of Cheilomenes propinqua development from the second instar to the adult stage. (A) The first (mixed diets) experiment; abbreviations of diets: E—eggs of the grain moth, ELA—eggs of the grain moth and low quantity of aphids, EMA—eggs of the grain moth and medium quantity of aphids, EHA—eggs of the grain moth and high quantity of aphids, LA—low quantity of aphids, MA—medium quantity of aphids, HA—high quantity of aphids (see Table 1 for more detailed description of diets). (B) The second (changing diets) experiment; the numbers below the x-axis indicate the number of days when larvae fed on aphids before the switch to feeding on eggs (see Table 2 for a more detailed description of the diets). Maternal diets are indicated above the graph, larval diets below the x-axis. Data shown are the means and SD. Sample sizes are indicated above the bars. The effect of larval diet: bars of the same graph with the same filling labeled by different letters are significantly different (p < 0.05 by Tukey’s HSD test on the ranked data). The effect of maternal diet: asterisks show a significant difference between the neighboring bars (*—p < 0.05, ***—p < 0.001 by the Kruskal–Wallis non-parametric test).
Figure 4. Influence of maternal and larval diets on time of Cheilomenes propinqua development from the second instar to the adult stage. (A) The first (mixed diets) experiment; abbreviations of diets: E—eggs of the grain moth, ELA—eggs of the grain moth and low quantity of aphids, EMA—eggs of the grain moth and medium quantity of aphids, EHA—eggs of the grain moth and high quantity of aphids, LA—low quantity of aphids, MA—medium quantity of aphids, HA—high quantity of aphids (see Table 1 for more detailed description of diets). (B) The second (changing diets) experiment; the numbers below the x-axis indicate the number of days when larvae fed on aphids before the switch to feeding on eggs (see Table 2 for a more detailed description of the diets). Maternal diets are indicated above the graph, larval diets below the x-axis. Data shown are the means and SD. Sample sizes are indicated above the bars. The effect of larval diet: bars of the same graph with the same filling labeled by different letters are significantly different (p < 0.05 by Tukey’s HSD test on the ranked data). The effect of maternal diet: asterisks show a significant difference between the neighboring bars (*—p < 0.05, ***—p < 0.001 by the Kruskal–Wallis non-parametric test).
Insects 15 00484 g004
Insects 15 00484 g005
Figure 5. Influence of sex and larval diet on the weight of Cheilomenes propinqua emerging adults. (A) The first (mixed diets) experiment; abbreviations of diets: E—eggs of the grain moth, ELA—eggs of the grain moth and low quantity of aphids, EMA—eggs of the grain moth and medium quantity of aphids, EHA—eggs of the grain moth and high quantity of aphids, LA—low quantity of aphids, MA—medium quantity of aphids, HA—high quantity of aphids (see Table 1 for more detailed description of diets). (B) The second (changing diets) experiment; the numbers below the x-axis indicate the number of days when the larvae fed on aphids before the switch to feeding on eggs (see Table 2 for a more detailed description of diets). Sex is indicated above the graph, larval diets below the x-axis. Data shown are the means and SD. Sample sizes are indicated above the bars. The effect of larval diet: bars of the same graph with the same filling labeled by different letters are significantly different (p < 0.05 by the Tukey’s HSD test on ranked data).
Figure 5. Influence of sex and larval diet on the weight of Cheilomenes propinqua emerging adults. (A) The first (mixed diets) experiment; abbreviations of diets: E—eggs of the grain moth, ELA—eggs of the grain moth and low quantity of aphids, EMA—eggs of the grain moth and medium quantity of aphids, EHA—eggs of the grain moth and high quantity of aphids, LA—low quantity of aphids, MA—medium quantity of aphids, HA—high quantity of aphids (see Table 1 for more detailed description of diets). (B) The second (changing diets) experiment; the numbers below the x-axis indicate the number of days when the larvae fed on aphids before the switch to feeding on eggs (see Table 2 for a more detailed description of diets). Sex is indicated above the graph, larval diets below the x-axis. Data shown are the means and SD. Sample sizes are indicated above the bars. The effect of larval diet: bars of the same graph with the same filling labeled by different letters are significantly different (p < 0.05 by the Tukey’s HSD test on ranked data).
Insects 15 00484 g005
Insects 15 00484 g006
Figure 6. Influence of sex and larval diet on the size of Cheilomenes propinqua emerging adults estimated by the maximum body width. (A)—the first (mixed diets) experiment; abbreviations of diets: E—eggs of the grain moth, ELA—eggs of the grain moth and low quantity of aphids, EMA—eggs of the grain moth and medium quantity of aphids, EHA—eggs of the grain moth and high quantity of aphids, LA—low quantity of aphids, MA—medium quantity of aphids, HA—high quantity of aphids (see Table 1 for more detailed description of diets). (B)—the second (changing diets) experiment; the numbers below the x-axis indicate the number of days when larvae fed on aphids before the switch to feeding on eggs (see Table 2 for more detailed description of diets). Sex is indicated above the graph, larval diets—below the x-axis. Data shown are the means and SD. Sample sizes are indicated above the bars. The effect of larval diet: bars of the same graph with the same filling labeled by different letters are significantly different (p < 0.05 by Tukey’s HSD test on the ranked data).
Figure 6. Influence of sex and larval diet on the size of Cheilomenes propinqua emerging adults estimated by the maximum body width. (A)—the first (mixed diets) experiment; abbreviations of diets: E—eggs of the grain moth, ELA—eggs of the grain moth and low quantity of aphids, EMA—eggs of the grain moth and medium quantity of aphids, EHA—eggs of the grain moth and high quantity of aphids, LA—low quantity of aphids, MA—medium quantity of aphids, HA—high quantity of aphids (see Table 1 for more detailed description of diets). (B)—the second (changing diets) experiment; the numbers below the x-axis indicate the number of days when larvae fed on aphids before the switch to feeding on eggs (see Table 2 for more detailed description of diets). Sex is indicated above the graph, larval diets—below the x-axis. Data shown are the means and SD. Sample sizes are indicated above the bars. The effect of larval diet: bars of the same graph with the same filling labeled by different letters are significantly different (p < 0.05 by Tukey’s HSD test on the ranked data).
Insects 15 00484 g006
Table 1. Composition of diets used in the first (mixed diets) experiment (daily rations are given).
Table 1. Composition of diets used in the first (mixed diets) experiment (daily rations are given).
Time of the Experiment 1Diets (Full Names and Abbreviations Used in the Present Paper)
Eggs (E)Eggs and Low Quantity of Aphids (ELA)Eggs and Medium Quantity of Aphids (EMA) Eggs and High Quantity of Aphids (EHA)Low Quantity of Aphids (LA)Medium Quantity of Aphids (MA)High Quantity of Aphids (HA)
1st dayEggs in excessEggs + 1 aphid larvaEggs + 2 adult aphidsEggs + aphids in excess1 aphid larva2 adult aphidsAphids in excess
2nd dayEggs in excessEggs + 1 aphid larvaEggs + 4 adult aphidsEggs + aphids in excess1 aphid larva4 adult aphidsAphids in excess
3rd dayEggs in excessEggs + 1 aphid larvaEggs + 6 adult aphidsEggs + aphids in excess1 aphid larva6 adult aphidsAphids in excess
4th dayEggs in excessEggs + 1 adult aphidEggs + 8 adult aphidsEggs + aphids in excess1 adult aphid8 adult aphidsAphids in excess
5th dayEggs in excessEggs + 1 adult aphidEggs + 10 adult aphidsEggs + aphids in excess1 adult aphid10 adult aphidsAphids in excess
6th and subsequent daysEggs in excessEggs + 1 adult aphidEggs + 14 adult aphidsEggs + aphids in excess1 adult aphid14 adult aphidsAphids in excess
1 Time of the experiment (days) was counted from molt to the second instar.
Table 2. Diets used in the second (changing diets) experiment (daily rations are given, the food was always provided in excess).
Table 2. Diets used in the second (changing diets) experiment (daily rations are given, the food was always provided in excess).
Time of the Experiment 1Diets (The Number of Days When the Larvae Fed on Aphids)
012345>5
1st dayEggs Aphids Aphids Aphids Aphids Aphids Aphids
2nd dayEggs Eggs Aphids Aphids Aphids Aphids Aphids
3rd dayEggs Eggs Eggs Aphids Aphids Aphids Aphids
4th dayEggs Eggs Eggs Eggs Aphids Aphids Aphids
5th dayEggs Eggs Eggs Eggs Eggs Aphids Aphids
6th and subsequent daysEggs Eggs Eggs Eggs Eggs Eggs Aphids
1 Time of the experiment (days) was counted from molt to the second instar.
Table 3. Influence of the maternal female diet, larval diet, and sex of an individual on various biological parameters of Cheilomenes propinqua (the results of the first experiment: ANOVA test of the ranked data, n = 532, dferr = 508).
Table 3. Influence of the maternal female diet, larval diet, and sex of an individual on various biological parameters of Cheilomenes propinqua (the results of the first experiment: ANOVA test of the ranked data, n = 532, dferr = 508).
Factor or Interaction of Factors and the Number of Degrees of FreedomBiological Parameters
Time of Development from the Second Instar to the Adult StageAdult SizeAdult Weight
Female diet, df = 1F = 17.5, p < 0.001F = 2.3, p = 0.134F = 1.5, p = 0.217
Larval diet, df = 5F = 68.7, p < 0.001F = 152.8, p < 0.001F = 151.7, p < 0.001
Sex, df = 1F = 2.7, p = 0.098F = 433.1, p < 0.001F = 357.7, p < 0.001
Female diet × larval diet, df = 5F = 1.8, p = 0.101F = 0.8, p = 0.576F = 0.4, p = 0.851
Female diet × sex, df = 1F = 0.7, p = 0.415F = 0.0, p = 0.841F = 0.7, p = 0.395
Larval diet × sex, df = 5F = 0.9, p = 0.503F = 7.3, p < 0.001F = 7.8, p < 0.001
Female diet × larval diet × sex, df = 5F = 0.6, p = 0.722F = 1.3, p = 0.255F = 1.6, p = 0.153
Table 4. Influence of the maternal female diet, larval diet, and sex of an individual on various biological parameters of Cheilomenes propinqua (the results of the second experiment: ANOVA test of the ranked data, n = 668, dferr = 640).
Table 4. Influence of the maternal female diet, larval diet, and sex of an individual on various biological parameters of Cheilomenes propinqua (the results of the second experiment: ANOVA test of the ranked data, n = 668, dferr = 640).
Factor or Interaction of Factors and the Number of Degrees of FreedomBiological Parameters
Time of Development from the Second Instar to the Adult StageAdult SizeAdult Weight
Female diet, df = 1F = 1.74, p = 0.187F = 0.7, p = 0.437F = 0.3, p = 0.580
Larval diet, df = 6F = 58.2, p < 0.001F = 85.9, p < 0.001F = 75.8, p < 0.001
Sex, df = 1F = 7.3, p = 0.007F = 426.3, p < 0.001F = 323.6, p < 0.001
Female diet × larval diet, df = 6F = 1.1, p = 0.346F = 2.3, p = 0.036F = 2.2, p = 0.042
Female diet × sex, df = 1F = 0.1, p = 0.893F = 0.7, p = 0.419F = 0.6, p = 0.450
Larval diet × sex, df = 6F = 1.3, p = 0.264F = 1.0, p = 0.432F = 0.9, p = 0.461
Female diet × larval diet × sex, df = 6F = 0.8, p = 0.523F = 0.6, p = 0.760F = 0.4, p = 0.833
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Ovchinnikov, A.N.; Ovchinnikova, A.A.; Reznik, S.Y.; Belyakova, N.A. Effects of Two Prey Species Combinations on Larval Development of the Predatory Ladybird Cheilomenes propinqua. Insects 2024, 15, 484. https://doi.org/10.3390/insects15070484

AMA Style

Ovchinnikov AN, Ovchinnikova AA, Reznik SY, Belyakova NA. Effects of Two Prey Species Combinations on Larval Development of the Predatory Ladybird Cheilomenes propinqua. Insects. 2024; 15(7):484. https://doi.org/10.3390/insects15070484

Chicago/Turabian Style

Ovchinnikov, Andrey N., Antonina A. Ovchinnikova, Sergey Y. Reznik, and Natalia A. Belyakova. 2024. "Effects of Two Prey Species Combinations on Larval Development of the Predatory Ladybird Cheilomenes propinqua" Insects 15, no. 7: 484. https://doi.org/10.3390/insects15070484

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop