Background

The spread of insecticide strains of stored-product pests and environmental problems connected with chemical control, like the effect of methyl bromide on the ozone layer, has led to intensify the researches for alternative control methods such as biological control (Rees 2003). Predatory mites of the family Phytoseiidae are of economic importance because they are efficient bio-agents that can be used against insect and mite pests in many crops in the open fields and in the greenhouses worldwide (Fouly et al. 2013).

Many phytoseiid species are facultative predators (generalists), not only on spider mites but also on other sources of food such as whiteflies, pollen (Fouly and Hassan 1991-1992; Gnanvossous et al. 2005; and Al-Shammery 2011), and thrips (van Houten et al. 2005; Messelink et al. 2005; and Winner et al. 2008). The two phytoseiid mites Neoseiulus cucumeris (Oud.) and Neoseiulus barkeri (Hughes) are known to play a natural important role in controlling the spider mites of the family Tetranychidae and Eriophyidae as well as the whiteflies and thrips on vegetables (Fouly et al. 2011).

The Mediterranean flour moth, Anagasta (Ephestia) kuehniella (Keller) (Pyralidae) and Sitotroga cerealella (Oliv.) (Gelechiidae), are serious cosmopolitan pests of stored grain products (Rees 2003). Eggs and larvae of A. kuehniella are widely utilized as a substitute host/prey to the laboratory-reared parasitoid and predatory species for biological control (Hamasaki and Matsui 2006 and Paust et al. 2008). The cotton leafworm, Spodoptera littoralis (Boisduval) (Noctuidae), is one of the most important agricultural insect pests in the Middle East. It attacks many crops including cotton, alfalfa, peanut, potatoes, lettuce, celery, pepper, and tomato (Mohamed 2003).

The present study was conducted to evaluate the potential of two phytoseiid predatory mites, Neoseiulus cucumeris and N. barkeri, of consuming alternative sources of food such as different insect eggs. The effect of insect eggs on different biological aspects as well as life table parameters of both phytoseiid predators was studied under laboratory conditions.

Materials and methods

Cultures of the phytoseiid predatory mites

Samples from both predatory mites, N. cucumeris and N. barkeri, were collected from leaves of kidney bean (Phaseoulus vulgaris L.), growing at a private farm at Hail District, Saudi Arabia, in 2017. Collected plant leaves were placed in cellophane bags, with small pieces of cotton wool soaked in ether and transferred directly to the laboratory of Department of Biology, College of Science, Hail University, Saudi Arabia, for direct examination, using a stereoscopic binocular. A pure culture from each of N. cucumeris and N. barkeri was maintained by feeding them on mobile stages of the two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), in separate climatic rooms at 27 ± 1 °C and 65 ± 5% RH and photoperiod of 10:14 h (L:D). Predatory mites were reared on detached hibiscus leaf discs, Hibiscus mutabilis L. (5 cm in diameter), which were placed underside upon a wet cotton wool layer in plastic trays. The wet cotton wool prevented the mites from escaping and maintained the leaf freshness by adding drops of water when needed. The phytoseiid mite species were identified by Dr. Ahmad H. Fouly, Professor of Acarology at Faculty of Agriculture, Mansoura University, Egypt.

Cultures of Anagasta (Ephestia) kuehniella and Sitotroga cerealella

Laboratory colonies from each of A. kuehniella and S. cerealella were maintained separately in plastic cylinders, filled with 100 g of a standard diet (43.5% wheat flour, 43.5% maize meal, 3.0% yeast, and 10% glycerin). Adults naturally do not feed (Norris and Richards,1934). To establish the colonies, three pairs of moths from each species were introduced into a cylinder to lay eggs and then were deposited onto the standard diet. Two crumpled paper towels (25 × 25 cm) were placed in each cylinder for pupation. Ten cylinders/hosts were used. Eggs were collected from 20 pairs of moths in a plastic container (20 × 16 × 10 cm), lined with two porous plastic sheets (20 × 5 cm) as an ovipositional surface.

Culture of Spodoptera littoralis

S. littoralis colony was established by field collections from P. vulgaris growing in a private farm in Hail District. The larvae were fed on leaves of castor bean. Fresh clean leaves were supplied daily. Pre-pupae were removed and placed in wooden cages (70 × 90 × 50 cm) with wire gauze sides (2 mm meshes). The floor of these cages was covered by a layer of fine autoclaved coarse sawdust, to be always moist, as relatively high humidity is essential for the formation of the cocoons. Emerging adults were fed on (10% sugar) solution and offered fresh castor bean leaves to serve as an ovipositional site (Adham et al. 2009). Deposited egg batches were transferred daily to the rearing units of the predatory mites.

Experimental technique

For individual rearing, newly deposited eggs of each of N. barkeri and N. cucumeris were transferred from the culture to leaf discs of hibiscus, 1 in.2 each. The newly deposited eggs were collected daily for a week and divided into three groups, each with 50 eggs. The newly hatched larvae were confined singly on a leaf disc and provided with a surplus amount of one of the tested insect eggs for their whole life span. The first and second groups were provided by S. cerealella and A. kuehniella eggs, while the third one was supplied with S. littoralis eggs. Mites were examined daily until maturity. The numbers of immature stages reached maturity, and their sex ratio was recorded. The newly emerged females were copulated as soon as they emerged and kept at the same conditions during their life span. Number of deposited eggs of each newly adult female was recorded daily. The incubation period of each species of the predatory mites was recorded. All treatments were conducted at 27 ± 1 °C and 65 ± 5% RH.

Statistical analysis

Biological data

Developmental time, duration of female reproductive period, and number of deposited eggs of each mite female were analyzed, using one-way ANOVA, followed by means separation, using LSD test and Duncan multiple range test (Costat Software Program 1990).

Life table parameters

Duration of immature stages, mortality rates, sex ratio, and total number of deposited eggs/females (Fecundity) of N. barkeri and N. cucumeris were estimated daily and used for calculating of life table parameters according to Birch (1948) and Laing (1968) and then by using the Basic Computer Program of Abou-Setta et al. (1986), where the intrinsic rate of natural increase rm was estimated by the equation: Σe-rm LxMx = 1, where x is the age in days, lx the age-specific survival rate (proportion of females alive at age x), and Mx the oviposition rate at age x {(age-specific oviposition) × (proportion of females)}. The net reproductive rate (Ro) was given as Ro = ΣlxMx. The mean generation time (T), in days, was calculated as T = ΣXl × Ml/ΣXlMl and then used as T = ln Ro / rm. The hatchability and survival rate at the lab conditions of 26 °C and 70% RH were used for estimating lx. The proportions of females (number of females/total adults) were used for calculating the Mx values.

Results and discussion

Effects of prey type on predator’s development period

Data presented in Table 1 indicated that insignificant differences among incubation periods of N. cucumeris male when fed on the three preys were found. Total duration of immature stages was significantly longer, when N. cucumeris was fed on S. cerealella eggs than on the other two egg species. In other words, duration of life cycle was significantly longer when N. cucumeris was provided with S. cerealella eggs (16.56 days for male and 15.42 days for female) than the other two kinds of insect eggs. Maximum time of life cycle of N. barkeri occurred for male fed on eggs of S. cerealela (18.82 days), likewise, the minimum time was observed for male fed on eggs of A. kuehniella (9.92 days). The longest life cycle (15.42 days) was obtained for N. cucumeris females fed on eggs of S. cerealella, while the shortest one (9.6 days) was recorded when female of N. cucumeris fed on A. kuehniella eggs (9.66 days) (Table 2). Therefore, it can be concluded that both N. cucumeris and N. barkeri were able to feed and complete their developmental periods on eggs of A. kuehniella, S. littoralis, and S. cerealella as alternative food sources. These results are supported by the findings of El-Sawi and Momen (2005) and Momen and El-Sawi (2008). Contradictory, Romeih et al. (2004) who found that Neoseiulus (Amblyseius) californicus (McGregor) failed to feed on Corcyra cephalonica eggs and could not complete its life cycle. These results also incorporated with Romeih et al. (2004) and Momen and El-Sawi (2008) who reared Euseius scutalis on S. littoralis and S.exigua Huber and Agrotis ipsilon (Hufnagel) eggs as alternative food sources and found that the total developmental time of the immature stages was the shortest on eggs of S. littoralis. Also, Fouly et al. (2013) noticed that Bemisia tabaci gave the longest life cycle of the predatory mite E. scutalis, followed by the immature stages of T. urticae, while plant pollen gave the shortest life cycle. Escudero and Ferragut (2004) found that developmental time was significantly longer when N. californicus and Phytoseiulus persimilis Athias–Henriot were fed on Tetranychus evansi Baker than T. urticae, T. turkestani Ugarov and Nikolski, and T. ludeni Zacher.

Table 1 Duration (in days) of male developmental stages of Neosiulus cucumeris fed on eggs of Anagasta kuehniella, Spodoptera littoralis, and Sitotroga cerealella and incubated at 27 °C and 70% RH
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Table 2 Duration (in days) of male developmental stages of Neosiulus barkeri fed on eggs of Anagasta kuehniella, Spodoptera littoralis, and Sitotroga cerealella and incubated at 27 °C and 70% RH
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Longevity of N. barkeri males was likewise affected by the type of prey. It was significantly longer when the predator was fed on S. cerealella (17.91 days) than the other prey species. However, longevity did not show a significant difference, when the predator was supplied by A. kuehniella (12.42 days) or S. littoralis eggs (12.83 days) (Table 2).

There was a significant difference between the duration of developmental stages, where female life cycle of N. cucumeris was the longest (15.42 days), when it was fed on S. cerealella, and the shortest (9.6 days), when females were fed on A. kuehniella eggs (Table 3). The adult females of N. cucumeris started laying eggs after (3.13, 5.27, and 6.68 days), when reared on eggs of A. kuehniella, S. littoralis, and S. cerealella, respectively. Furthermore, ovipositional period was significantly longer, when the females of N. cucumeris were fed on A. kuehniella eggs than on the other two species. Female longevity was significantly longer (22.92 days), when female was fed on eggs of S. cerealella than the other tested insect eggs.

Table 3 Duration (in days) of Neosiulus cucumeris females fed on eggs of Anagasta kuehniella, Spodoptera littoralis, and Sitotroga cerealella and incubated at 27 °C and 70% RH
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The total duration of life cycle of N. barkeri female was affected by the type of food, where it averaged 16.21, 12.58, and 10.33 days, when the predator was fed on eggs of S. cerealella, S. littoralis, and A. kuehniella, respectively (Table 4). Adult longevity was also influenced by the type of food as it was significantly longer, when N. barkeri female was fed on S. cerealella (25.92 days) followed by S. littoralis (21.85 days) and A. kuehniella (19.19 days), respectively. The longest ovipositional period (12.14 days) was recorded, when the mite female was fed on S. cerealella eggs, while the shortest (10.46 days) was recorded for the female that fed on S. littoralis.

Table 4 Duration (in days) of Neosiulus barkeri females fed eggs of Anagasta kuehniella, Spodoptera littoralis, and Sitotroga cerealella and incubated at 27 °C and 70% RH
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The data also indicated that the fecundity (no. deposited eggs/female) of N. cucumeris and N. barkeri females was highest on eggs of A. kuehniella (25.06 eggs/female, with a daily rate of 2.05 eggs, and 23.26 eggs/female, with a daily rate of 2.04 eggs, respectively) (Table 5). The lowest fecundity was obtained, when the predatory mites were provided by S. cerealella eggs. Similar results were obtained by Momen and El-Sawi (2008) who mentioned that the fecundity of E. scutalis was highest on eggs of S. littoralis and S. exigua and the lowest was on A. ipsilon eggs. Results in Table 5 also showed that there was a significant difference between the total deposited eggs of the two predatory mites by feeding on A. kuehniella and S. cerealella. There was insignificant difference between the total deposited eggs of the two predatory mites, when they were provided by the eggs of S. littoralis. The daily rate of deposited eggs did not show a significant difference between the two predatory mite species, when they fed on eggs of A. kuehniella and S. littoralis. Contradictory, N. cucumeris laid more eggs than N. barkeri when both were supplied by S. cerealella eggs.

Table 5 Total and daily rate of deposited eggs of Neoseiulus cucumeris and N. barkeri fed eggs of Anagasta kuehniella, Spodoptera littoralis, and Sitotroga cerealella and incubated at 27 °C and 70% RH
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Life table parameters of N. cucumeris and N. barkeri

Obtained results showed that the survival percentages of the two phytoseiid mites, N. cucumeris and N. barkerii, reached their highest level of survival (90% and 88%), when both predators were fed on eggs of A. kuehniella, respectively. Feeding on eggs of S. cerealella caused the lowest rate of survival where it was 80% and 82% for N. cucumeris and N. barkeri, respectively (Table 6). Figures 1 and 2 illustrated that Lx values gradually decreased during the ovipositional period. Also, it was found that the type of food had insignificant effect on the sex ratio, where A. kuehniella, S. littoralis, and S. cerealella caused a female proportion of N. cucumeris of 0.58, 0.56, and 0.52%, while these values of N. barkeri were 0.56, 0.52, and 0.52%, respectively  (Table 6).

Table 6 Life table parameters of Neosiulus cucumeris and N. barkeri fed on three different kinds of insect eggs and incubated at 27 °C and 70% RH
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Fig. 1
figure 1

Age-specific survivorship of Neoseiulus barkeri fed eggs of Anagasta kuehniella, Spodoptera littoralis, and Sitotroga cerealella and incubated at 27 °C and 65% RH

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Fig. 2
figure 2

Age-specific survivorship of Neoseiulus cucumeris fed eggs of Anagasta kuehniella, Spodoptera littoralis, and Sitotroga cerealella and incubated at 27 °C and 65% RH

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Fig. 3
figure 3

Age-specific fecundity of Neoseiulus barkeri fed eggs of Anagasta kuehniella, Spodoptera littoralis, and Sitotroga cerealella and incubated at 27 °C and 65% RH

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Fig. 4
figure 4

Age-specific fecundity of Neoseiulus cucumeris fed eggs of Anagasta kuehniella, Spodoptera littoralis, and Sitotroga cerealella and incubated at 27 °C and 65% RH

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The mean generation time (T) was affected by food source; therefore, data showed that the eggs of S. cerealella prolonged the T period of N. cucumeris (23.45 days), while A. kuehniella caused the shortest one (17.42 days). Correspondent values were 35.37 and 25.80 days for N. barkeri (Table 6). Therefore, it can be concluded that A. kuehniella and S. littoralis were more suitable as food sources for both phytoseiid mites, where they shortened the mean generation time.

Feeding on insect eggs generally caused low net reproductive rates Ro of both tested predatory mites, where eggs of A. kuehniella and S. littoralis were more favorable diets, and resulted in 9.027 and 9.470, and 11.840 and 9.360 females/female of N. cucumeris and N. barkeri, respectively. Feeding on S. cerealella eggs caused the lowest Ro value (6.87 and 8.09 females/female) for both predatory mites, respectively (Table 6). Although these values were the highest, they are still lower than the Ro values when both phytoseiid mites were fed on spider mites or plant pollen. Similar results were obtained by Momen and El-Sawi (2008) who mentioned that Ro of E. scutalis was highest on eggs of S. littoralis and S. exigua, and the lowest on A. ipsilon eggs. Concerning the intrinsic rate of natural increase (rm), which is the rate of increase of an insect or mite species under specific physical conditions, in unlimited environment, the effects of increasing density do not need to be considered (Birch 1948). The present data showed that rm is 0.126, 0.110, and 0.085 for N. cucumeris, when fed on A. kuehniella, S. littoralis, and S. cerealella, respectively. Correspondent values were 0.095, 0.075, and 0.059 females, when N. barkeri was provided by the aforementioned preys, respectively. Figures 3 and 4 showed the age specific fecundity (Mx) where most of the deposited eggs of both N. barkeri and N. cucumeris were laid within the first two weeks of their life.

The expected number of new females, which would add daily to the population as represented by the finite rate of increase erm (λ), showed similar results and followed the trend observed with rm values. Again, the finite rate of increase was obviously affected by the type of food, where erm values were at their highest rates, when N. cucumeris and N. barkeri were fed on eggs of A. kuehniella (1.100 and 1.134) and decreased on S. littoralis to reach the lowest rate, on the eggs of S. cerealella (Table 6).

Several authors studied the capability of generalist phytoseiid mites to feed not only on spider mites but also on insects and pollen (Messelink et al. 2005; Winner et al. 2008; Al-Shammery 2011 and Fouly et al. 2011).

Conclusion

In conclusion, the results showed that the two phytoseiid mites, N. cucumeris and N. barkeri, which are considered promising biological control agents of some mites and insect pests, could be reared successfully under laboratory conditions by feeding them on different insect eggs as an alternative food source, especially when their natural preys are scarce.