Abstract
Neoseiulus cucumeris (Oudemans) is a generalist phytoseiid predatory mite widely used as a biological control agent against phytophagous mites, including tetranychid and tarsonemiid species, as well as thrips and whiteflies. Because identifying a suitable diet is a critical first step for the mass rearing of predatory mites, this study evaluated the effects of several enriched diets of Tyrophagus putrescentiae (Schrank) as a factitious prey (alternative food) on the performance of N. cucumeris. The tested diets included bran (B) as a control; wheat flour + bran (BW); yeast + wheat + bran (BWY); dog food + wheat + bran (BWD); yeast + dog food + bran (BDY); and wheat + yeast + dog food + bran (BWDY). The results showed that the intrinsic rate of increase (r) did not differ significantly among diets compared with the control. However, total lifespan and fecundity of N. cucumeris reared on the enriched diets were higher than those reared on the control and BW diets. The predatory mite was reared on the BDY and BWDY diets for ten consecutive generations. After ten generations, females fed the BDY diet showed significant increases in fecundity, gross reproductive rate (GRR), finite rate of increase (λ), and intrinsic rate of increase (r) relative to G1. In contrast, rearing the predatory mite on the BWDY diet for ten generations resulted in significantly shorter female longevity, adult longevity, and total lifespan compared to those fed BDY at G10. Overall, the BDY diet improved the biological performance of N. cucumeris after ten generations compared with the first generation, while long-term feeding on the BWDY diet maintained stable performance. Although the combination of diets appears more costly than a single diet, the resulting stable performance justifies the additional expense. Therefore, the BWDY diet is considered the most suitable option for the long-term mass rearing of N. cucumeris.
Keywords: Long-term rearing, Phytoseiidae, Predatory mite, Mixed diet, Tyrophagus putrescentiae
Subject terms: Ecology, Ecology, Zoology
Introduction
The number of protected cultivations is increasing, while the stable environmental conditions, monoculture, lack of natural enemies, and rapid development of pesticide resistance in greenhouses lead to the outbreak and overflow of pests. The use of chemicals is the most common method for controlling pests, and the extensive use of them has resulted in the development of resistance to almost all the available groups of pesticides, only after a few applications. In addition to having detrimental effects on biodiversity, the use of synthetic pesticides to control phytophagous mites led to the death of non-target organisms and the presence of residues in crops1–3. These side effects necessitate the development of alternative pest control strategies, such as integrated pest management (IPM)-based biocontrol agents for the management of pests. The most important biocontrol agents are predatory mites belonging to the Phytoseiidae family, the second-largest group of biocontrol agents after the hymenopterans that are commercially produced worldwide4.
Neoseiulus cucumeris (Oudemans) (Acari: Phytoseiidae), one of the type III lifestyle generalist phytoseiid predatory mites, is listed among the 25 most commercially used augmentative biocontrol agents worldwide5,6, and it has the ability to develop and reproduce on non-pest prey species and alternative food sources. Before using a predatory mite, it should be reared in high-quality conditions; the most important and actually the first step for mass production of biocontrol agents is to find the most suitable diet. Wide distribution and flexible feeding behaviors of N. cucumeris facilitate mass rearing on alternative foods instead of natural prey. Stored acarid mites are economical alternative foods used for the mass production of the predatory mites7,8.
Tyrophagus putrescentiae (Schrank) (Acari: Acaridae) is a promising diet for mass rearing of the predatory mite N. cucumeris9, although it has been used to rear other phytoseiid predatory mites. Enhancing the nutritional quality of factitious prey (T. putrescentiae) represents an effective strategy for improving the mass-rearing efficiency of Amblyseius swirskii Athias-Henriot (Acari: Phytoseiidae)10. Optimizing macronutrient balance at the prey level, Carpoglyphus lactis L. (Acari: Acaridae), can reliably enhance predator fitness, offering a mechanistic and scalable framework for improving the sustainability and efficiency of predatory mite production in biological control programs11. Research has shown that predator performance cannot be sustained by an excess of protein or carbohydrates alone. Instead, optimal enhancement of A. swirskii developmental speed, fecundity, and population growth depends on diets that provide a well‑balanced nutritional profile providing sufficient protein for reproduction, adequate carbohydrates for energy, and essential micronutrients for physiological regulation. In line with this concept, enrichment of T. putrescentiae diets shortened the development time and increased the fecundity of Neoseiulus barkeri Hughes (Acari: Phytoseiidae)12. Meanwhile, other studies have emphasized that the balance among major nutrient classes rather than the abundance of any single component is a key determinant of predator life-history outcomes13.
Above-mentioned findings reinforce the need for a prey diet that promotes protein biosynthesis without compromising energetic balance conditions best met through multi-source dietary enrichment. Since, in the mass-rearing process of the phytoseiid mites, the nutritional quality of the prey can affect predator’s performance, diets could be expanded to include a much wider range of food sources by combining specific nutrients to actively restore nutritional imbalances in their diets8. The main objective of this study was to evaluate the effects of several enriched diets at the second trophic level, T. putrescentiae, on the performance of N. cucumeris at the third trophic level, as well as to assess the impact of long-term feeding on mixed diets on the predatory mite. The findings provide essential information for optimizing mass-rearing protocols of N. cucumeris.
Materials and methods
Preparation of diets
Wheat flour (Golha Company), wheat bran (Tehran Bakery), yeast (Kimia Enzyme Company), and dog food (Fidar-Patira Company) (5.3% fat, 23.4% protein, 3.3% fiber, 6.8% moisture, and 7.5% ash) were sourced for the experiments. The granular additives, including dog food and yeast, were ground into powder prior to mixing with wheat bran and flour. Almond (Prunus amygdalus L. [Rosaceae]) pollen was personally collected from almond orchards in Shiraz, Fars Province, Iran. The pollen was dried at 37 °C and subsequently stored at − 20 °C for long-term use or at 4 °C for short-term use.
Stock culture of stored product mite, T. putrescentiae
The T. putrescentiae specimens used in this study originated from a laboratory colony at Tarbiat Modares University that was established from a stock culture previously identified by our research group. Species confirmation has already performed based on key morphological characteristics described14. The colony has been consistently maintained under controlled laboratory conditions, and voucher specimens are available in the laboratory. The mites were subsequently reared on 100% wheat bran (B; control) and on the following enriched diets: 20% wheat flour + bran (BW); 20% yeast + 20% wheat flour + bran (BWY); 20% dog food + 20% wheat flour + bran (BWD); 20% yeast + 20% dog food + bran (BDY); and 20% wheat flour + 20% yeast + 20% dog food + bran (BWDY). Rearing of T. putrescentiae was conducted for two to three generations (approximately 20 days) under laboratory conditions. Since the population increase of stored-product mites is greater under conditions of higher temperature, higher humidity, and increased darkness, T. putrescentiae was reared in Plexiglas containers at 27 ± 1 °C, 75% ± 5% RH, and a photoperiod of 8:16 h (L: D) in Plexiglas containers (10 × 7 × 4 cm).
Stock culture ofN. cucumeris
To establish the stock culture, N. cucumeris individuals were obtained from Bio-Planet (Italy) and transferred onto a green plastic sheet (16 × 11 × 0.1 cm) placed on a water-soaked sponge inside a Plexiglas container (30 × 15 × 12 cm). The edges of the plastic sheet were covered with moist tissue paper, which served as a barrier to prevent mite escape. Water was added daily to the containers to prevent desiccation of the sponge and tissue strips. The stock culture of N. cucumeris was maintained in a growth chamber at 25 ± 1 °C, 60 ± 5% RH, and a photoperiod of 16:8 h (L: D). To ensure that the predatory mites had no prior exposure to the experimental diets, almond pollen, recognized as a suitable and economical diet for the long-term rearing of N. cucumeris7, was provided as food twice per week.
Experimental setup
The experimental units were quite similar to the stock culture rearing units but smaller. The 3-cm-diameter units consisted of green plastic sheets (3 × 3 × 0.1 cm), plastic trays (7 × 5 × 4 cm), and wet sponges. Some cotton fibers were stuck onto the plastic sheet to provide a suitable place for oviposition. About 60 pairs of N. cucumeris were selected randomly from the stock culture and kept in a new experimental unit for less than 24 h to have the same-aged eggs as the predator. The newly laid eggs were transferred to the experimental units individually. After larval emergence, they were fed individually with one of the six reared diets. About 50–70 of all stages of T. putrescentiae were used at 2-day intervals. After adult emergence, females were coupled with the males of the same treatment. If sex ratios deviated from 1:1, surplus individuals of the more abundant sex were paired with individuals from the stock colony, while the collected data of the redundant sex were not included in analyses. All replicates (50) of each treatment were monitored daily until the adults’ death. All experiments were conducted for one generation (G1), although both mixed diets (BDY and BWDY) continued to ten generations (G10). All units were kept at 25 ± 1 °C, 65 ± 5% RH, and a photoperiod of 16:8 (L: D) h.
Data analysis
The values of all the life table parameters, including the net reproductive rate (R0), gross reproductive rate (GRR), finite rate of increase (λ), intrinsic rate of increase (r), and mean generation time (T), as well as proportion of individuals of each stage at each age (pxj), age-specific survival rate (lx) (the probability that a newborn will survive to age x, calculated by pooling all the surviving individuals of different stages), age-stage-specific fecundity (fxj), and age-specific fecundity (mx) were calculated according to the age-stage, two-sex life table procedure15,16 using the TWOSEX-MSChart software17 on different diets. The variances and standard errors of the life table parameters were determined using the bootstrap procedure (100,000 samples)18. Multiple comparisons among different diets were carried out using the paired bootstrap test19. All figures were prepared using Microsoft Office Excel 2017.
Results
Comparison between the first generation of the treatments
Although the durations of the egg, larval, and protonymphal stages did not differ significantly among treatments, the deutonymphal stage was significantly longer in mites fed the control, BWD, BDY, and BWDY diets. The total preadult period of the predator was significantly shorter on the BWDY diet than on the BW and BWY diets. N. cucumeris exhibited the shortest adult longevity and total lifespan (from birth to death) when fed the control and BW diets. The longest adult preoviposition period (APOP) was observed in mites fed the BDY diet, which did not differ significantly from the control, whereas the shortest total preoviposition period (TPOP) occurred in mites reared on the BWDY diet, with no significant differences compared with the control, BWY, and BWD diets. Fecundity and the number of oviposition days of N. cucumeris were significantly higher in the control and BW treatments than in the other diets tested. The preadult survival rate did not differ significantly among treatments. Similarly, no significant differences were detected among diets for the gross reproductive rate (GRR), net reproductive rate (R0), intrinsic rate of increase (r), or finite rate of increase (λ). However, the mean generation time (T) of N. cucumeris fed the BDY diet differed significantly from that of the control (Table 1).
Table 1.
Duration of different life stages (days), fecundity (eggs/female), and population growth parameters (mean ± SE) of Neoseiulus cucumeris fed on Tyrophagus putrescentiae reared on six dietary treatments in generation 1.
| Diet | Control | BW | BWD | BWY | BDY (G1) | BWDY(G1) |
|---|---|---|---|---|---|---|
| Egg (day) |
2.3 ± 0.144a (n = 25) |
2.2 ± 0.139a (n = 27) |
2.3 ± 0.135a (n = 24) |
2.2 ± 0.150a (n = 32) |
2.2 ± 0.089a (n = 36) |
2.0 ± 0.120a (n = 31) |
| Larva (day) |
1.0 ± 0.000a (n = 25) |
1.0 ± 0.000a (n = 27) |
1.0 ± 0.000a (n = 24) |
1.0 ± 0.000a (n = 32) |
1.0 ± 0.000a (n = 36) |
1.0 ± 0.000a (n = 31) |
| Protonymph (day) |
2.0 ± 0.039a (n = 25) |
1.9 ± 0.050a (n = 27) |
1.9 ± 0.059a (n = 23) |
2.0 ± 0.054a (n = 32) |
1.8 ± 0.062a (n = 36) |
1.8 ± 0.060a (n = 31) |
| Deutonymph (day) |
1.4 ± 0.099d (n = 25) |
2.0 ± 0.036a (n = 27) |
1.6 ± 0.105bcd (n = 22) |
1.8 ± 0.089ab (n = 32) |
1.6 ± 0.083 cd (n = 36) |
1.7 ± 0.093bc (n = 31) |
| Total preadult (day) |
6.7 ± 0.109bc (n = 25) |
7.1 ± 0.138a (n = 27) |
6.8 ± 0.157abc (n = 22) |
7.0 ± 0.171ab (n = 32) |
6.6 ± 0.138bc (n = 36) |
6.5 ± 0.137c (n = 31) |
| Female longevity (day) |
22.6 ± 2.300c (n = 14) |
22.0 ± 3.878c (n = 16) |
45.7 ± 4.964a (n = 14) |
34.3 ± 1.902b (n = 18) |
41.7 ± 3.612ab (n = 18) |
39.6 ± 5.018ab (n = 17) |
| Male longevity (day) |
25.5 ± 3.810b (n = 11) |
36.3 ± 4.297ab (n = 11) |
36.8 ± 5.716ab (n = 8) |
42.3 ± 3.429a (n = 14) |
43.4 ± 4.186a (n = 18) |
37.7 ± 5.598ab (n = 14) |
| Adult longevity (day) |
23.9 ± 2.081b (n = 25) |
27.8 ± 3.146b (n = 27) |
42.5 ± 3.802a (n = 22) |
37.38 ± 1.946a (n = 32) |
42.6 ± 2.737a (n = 36) |
38.7 ± 3.683a (n = 31) |
| Total life span (day) |
30.6 ± 2.062b (n = 25) |
34.9 ± 3.130b (n = 27) |
49.2 ± 3.814a (n = 22) |
44.38 ± 1.959a (n = 32) |
49.2 ± 2.715a (n = 36) |
45.3 ± 3.709a (n = 31) |
| APOP (day) |
2.3 ± 0.171ab (n = 13) |
2.1 ± 0.061b (n = 16) |
2.0 ± 0.000b (n = 14) |
2.1 ± 0.055b (n = 18) |
2.6 ± 0.182a (n = 16) |
2.1 ± 0.109b (n = 16) |
| TPOP (day) |
9.0 ± 0.247abc (n = 13) |
9.4 ± 0.154a (n = 16) |
8.9 ± 0.217abc (n = 14) |
8.8 ± 0.255bc (n = 18) |
9.1 ± 0.135ab (n = 18) |
8.5 ± 0.179c (n = 16) |
| Oviposition days |
15.4 ± 1.413b (n = 13) |
12.8 ± 1.516b (n = 16) |
22.9 ± 1.939a (n = 14) |
22.1 ± 0.896a (n = 18) |
21.8 ± 0.879a (n = 18) |
22.0 ± 1.351a (n = 17) |
| Fecundity (eggs/female) |
26.9 ± 3.103b (n = 14) |
27.3 ± 3.426b (n = 16) |
45.6 ± 3.996a (n = 14) |
39.8 ± 1.729a (n = 18) |
44.4 ± 1.726a (n = 18) |
43.7 ± 4.035a (n = 17) |
| Preadult Survival % |
100 ± 0.000a (n = 25) |
100 ± 0.000a (n = 27) |
92 ± 0.057a (n = 24) |
100 ± 0.000a (n = 32) |
94 ± 0.036a (n = 38) |
100 ± 0.000a (n = 31) |
| GRR (eggs/individual) |
19.52 ± 4.695a (n = 25) |
20.16 ± 4.457a (n = 27) |
32.11 ± 5.526a (n = 24) |
23.11 ± 3.792a (n = 32) |
22.72 ± 3.924a (n = 38) |
28.08 ± 5.033a (n = 31) |
| R0 (eggs/individuals) |
15.04 ± 3.166a (n = 25) |
16.19 ± 3.256a (n = 27) |
26.62 ± 5.140a (n = 24) |
22.41 ± 3.629a (n = 32) |
21.03 ± 3.690a (n = 38) |
24.00 ± 4.486a (n = 31) |
| r (day− 1) |
0.1684 ± 0.015a (n = 25) |
0.1761 ± 0.012a (n = 27) |
0.1926 ± 0.014a (n = 24) |
0.1836 ± 0.012a (n = 32) |
0.1748 ± 0.012a (n = 38) |
0.1847 ± 0.0135a (n = 31) |
| λ (day− 1) |
1.1835 ± 0.017a (n = 25) |
1.1926 ± 0.015a (n = 27) |
1.2125 ± 0.017a (n = 24) |
1.2017 ± 0.015a (n = 32) |
1.1911 ± 0.014a (n = 38) |
1.2030 ± 0.016a (n = 31) |
| T (day) |
15.96 ± 0.407bc (n = 25) |
15.69 ± 0.564c (n = 27) |
16.95 ± 0.401abc (n = 24) |
16.87 ± 0.435abc (n = 32) |
17.34 ± 0.313a (n = 38) |
17.12 ± 0.458ab (n = 31) |
APOP, adult preovipositional period; TPOP, total preovipositional period (from egg to first oviposition); The means followed by different letters in the same row are significantly different (P < 0.05, Paired bootstrap).
Tyrophagus putrescentiae reared on bran+ wheat (BW), bran+ wheat + dog food (BWD), bran+ wheat+ yeast (BWY), bran + dog food+ yeast (BDY), bran+ wheat + dog food + yeast (BWDY); Control (wheat bran).
The first adult appeared on day 5 when fed on the diet of BWY. Females fed on the BWD diet lived more days, whereas the last female died after 86 days, while females fed on control and BWY lived fewer days, and the last female died at the age of 50 and 55 days, respectively. However, males fed on BDY and BWDY lived more days, the last one died at the age of 85 days for both treatments (Fig. 1). Based on the fecundity curves, the highest daily fecundity was observed with the diet of BDY (2.8 eggs/female) at the age of 15 days, while the lowest was with the treatments of BWY (2 eggs/female) at the age of 12 days (Fig.2).
Fig. 1.
Proportion of individuals of each stage at each age (pxj) of Neoseiulus cucumeris fed on Tyrophagus putrescentiae reared on bran+ wheat (BW), bran+ wheat + dog food (BWD), bran+ wheat+ yeast (BWY), bran + dog food+ yeast (BDY), bran+ wheat + dog food + yeast (BWDY); Control (wheat bran); Generation (G).
Fig. 2.
Age-specific survivorship (lx), age-specific fecundity (mx), and age-stage-specific fecundity (fxj) of Neoseiulus cucumeris fed on Tyrophagus putrescentiae reared on bran+ wheat (BW), bran+ wheat + dog food (BWD), bran+ wheat+ yeast (BWY), bran + dog food+ yeast (BDY), bran+ wheat + dog food + yeast (BWDY); Control (wheat bran); Generation (G).
Comparison between the generations (G1-G10) of the mixed diets
At the first generation, the durations of APOP and TPOP were significantly shorter when the predatory mite fed on BWDY, while other parameters including, the stage longevities, fecundity, and population parameters did not have any significant difference between BDY and BWDY, as shown in both Tables 1 and 2. However, after ten generations of rearing on BWDY, the durations of egg, female longevity, adult longevity, and total lifespan were significantly shorter, and the duration of protonymph was longer than ten generations of rearing on BDY. There was no significant difference between larva, deutonymph, preadult period, male longevity, oviposition parameters, and population growth parameters for both BDY and BWDY in G10 (Table 2).
Table 2.
Multi-generational (G1 and G10) comparison of the duration of different life stages (days), fecundity (eggs/female), and population growth parameters (mean ± SE) of Neoseiulus cucumeris fed on Tyrophagus putrescentiae reared on mixed diets (BDY and BWDY).
| Diet | BDY (G1) | BDY (G10) | BWDY(G1) | BWDY(G10) |
|---|---|---|---|---|
| Egg (day) |
2.2 ± 0.089aA (n = 36) |
2.2 ± 0.106aA (n = 28) |
1.9 ± 0.120aA (n = 31) |
1.8 ± 0.137bA (n = 28) |
| Larva (day) |
1.0 ± 0.000aA (n = 36) |
1.0 ± 0.000aA (n = 28) |
1.0 ± 0.000aA (n = 31) |
1.0 ± 0.000aA (n = 28) |
| Protonymph (day) |
1.8 ± 0.062aA (n = 36) |
1.6 ± 0.090bA (n = 28) |
1.9 ± 0.060aA (n = 31) |
2.0 ± 0.051aA (n = 28) |
| Deutonymph (day) |
1.6 ± 0.083aA (n = 36) |
1.4 ± 0.095aA (n = 26) |
1.7 ± 0.093aB (n = 31) |
1.3 ± 0.088aA (n = 28) |
| Total preadult (day) |
6.6 ± 0.138aA (n = 36) |
6.2 ± 0.122aB (n = 26) |
6.5 ± 0.137aA (n = 31) |
6.1 ± 0.146aB (n = 28) |
| Female longevity (day) |
41.7 ± 3.612aB (n = 18) |
56.4 ± 4.596aA (n = 18) |
39.6 ± 5.018aA (n = 17) |
38.9 ± 4.935bA (n = 18) |
| Male longevity (day) |
43.4 ± 4.186aA (n = 18) |
36.9 ± 8.408aA (n = 8) |
37.7 ± 5.598aA (n = 14) |
33.9 ± 4.431aA (n = 10) |
| Adult longevity (day) |
42.6 ± 2.737aA (n = 36) |
50.4 ± 4.359aA (n = 26) |
38.7 ± 3.683aA (n = 31) |
37.1 ± 3.521bA (n = 28) |
| Total life span (day) |
49.2 ± 2.715aA (n = 36) |
56.6 ± 4.368aA (n = 26) |
45.3 ± 3.709aA (n = 31) |
43.2 ± 3.478bA (n = 28) |
| APOP (day) |
2.6 ± 0.182aA (n = 16) |
2.2 ± 0.089aA (n = 18) |
2.1 ± 0.109bA (n = 16) |
2.1 ± 0.055aA (n = 18) |
| TPOP (day) |
9.1 ± 0.135aA (n = 18) |
8.5 ± 0.215aB (n = 18) |
8.5 ± 0.179bA (n = 16) |
8.3 ± 0.194aA (n = 18) |
| Oviposition days |
21.8 ± 0.879aA (n = 18) |
22.7 ± 0.883aA (n = 18) |
22.0 ± 1.351aA (n = 17) |
21.7 ± 1.745aA (n = 18) |
| Fecundity (eggs/female) |
44.4 ± 1.726aB (n = 18) |
49.8 ± 2.041aA (n = 18) |
43.7 ± 4.035aA (n = 17) |
45.2 ± 3.393aA (n = 18) |
| Preadult Survival % |
94 ± 0.036aA (n = 38) |
93 ± 0.045aA (n = 28) |
100 ± 0.000aA (n = 31) |
97 ± 0.034aA (n = 29) |
| GRR (eggs/individual) |
22.72 ± 3.924aB (n = 38) |
37.55 ± 4.745aA (n = 28) |
28.08 ± 5.033aA (n = 31) |
34.41 ± 5.482aA (n = 29) |
| R0 (eggs/individuals) |
21.03 ± 3.690aA (n = 38) |
32.04 ± 4.706aA (n = 28) |
24.00 ± 4.486aA (n = 31) |
28.06 ± 4.570aA (n = 29) |
| r (day− 1) |
0.1748 ± 0.012aB (n = 38) |
0.2131 ± 0.012aA (n = 28) |
0.1847 ± 0.0135aA (n = 31) |
0.2097 ± 0.012aA (n = 29) |
| λ (day− 1) |
1.1911 ± 0.014aB (n = 38) |
1.2376 ± 0.014aA (n = 28) |
1.2030 ± 0.016aA (n = 31) |
1.2333 ± 0.015aA (n = 29) |
| T (day) |
17.34 ± 0.313aA (n = 38) |
16.23 ± 0.347aB (n = 28) |
17.12 ± 0.458aA (n = 31) |
15.85 ± 0.433aB (n = 29) |
APOP, adult preovipositional period; TPOP, total preovipositional period (from egg to first oviposition). The means followed by different lowercase letters within the same row are comparisons between the corresponding generations of two diets. The means followed by different capital letters in the same row are comparisons among different generations of each diet (P < 0.05, Paired bootstrap).
Tyrophagus putrescentiae reared on bran + dog food + yeast (BDY), bran+ wheat + dog food + yeast (BWDY); Control (wheat bran); Generations (G).
When N. cucumeris fed on BDY for ten generations, the periods of preadult, TPOP, and T were significantly shorter than those when fed for one generation on the diet, while the parameters of female longevity, fecundity, GRR, r, and λ were significantly lower at the first generation. When the predatory mite fed on BWDY for ten generations, the periods of preadult and T were significantly shorter, and the duration of deutonymph was longer than individuals of G1, and other parameters including the durations of the stages, oviposition, and population parameters showed no significant difference between the first and 10th generations of BWDY diet (Table 2).
The first adult appeared on day 6 in G1, and on day 5 in G10 by feeding on both diets of BDY and BWDY. In G1, females feeding on the BWDY diet lived more days (84 days) than females of BDY, whereas males lived 85 days for both diets. In G10, males and females fed on BDY lived more days (72 and 98 days, respectively) than on the BWDY diet (Fig. 1). Based on the fecundity curves, the highest daily fecundity was observed in the diet of BDY (2.8 eggs/female) at the age of 15 days in G1 and (3.17 eggs/female) at the age of 10 days in G10 (Fig. 2 ).
Discussion
An important characteristic of phytoseiid mites is their ability to use alternative food sources. Carpoglyphus lactis (L.), Thyreophagus entomophagus (Laboulbene), Acarus siro L., Lepidoglyphus destructor (Schrank), and Tyrophagus putrescentiae are some of the astigmatid mite species used as alternative food in the commercial mass production of several species of phytoseiid predators9,20. These factitious prey rear on some economic diets such as bran, flour, yeast in darkness and high humidity. Tyrophagus putrescentiae appears to be promising for mass rearing of N. cucumeris either as a solo diet or as part of a mixed diet9. In the present study, the effects of some enriched diets of T. putrescentiae, as well as long-term feeding on mixed diets were determined on the performance of N. cucumeris.
Since the fecundity, development, and survival rate are reflected in the intrinsic rate of increase (r), this parameter can be used as a reliable criterion to indicate the suitability of diets used for rearing the phytoseiid generalist predators. According to demographic theory, when r is greater than zero, the food is suitable for population growth21. The results showed that r values of N. cucumeris on almost all diets had no significant difference in comparison with the base diet (control) in G1; however, total lifespan and fecundity of the predatory mites reared on enriched diets were greater than those of the control and BW diets, which indicated that the enriched diets are more suitable for the performance of the predatory mite. There are some records that the enriched base diet of factitious prey resulted in increasing the fecundity of phytoseiid mites; for example, the reproduction of A. swirskii was higher when it was fed with the enriched prey, T. putrescentiae20, and feeding on an enriched diet of C. lactis, resulted in the highest reproductive rate of the predatory mite A. swirskii11,22.
The range of r value in the present study was from 0.168 to 0.193 day[-1 in G1, while the value of this parameter has been reported to be lower than our findings when N. cucumeris was fed on prey reared on some oily seeds such as almond, flax, pumpkin, and sunflower23. In addition, the recorded r was lower than reported one when N. cucumeris fed on enriched prey T. putrescentiae by pollen grains of saffron, cattail, and date, as well as the seeds of chickpea and mung bean8. However, the intrinsic rate of increase of N. cucumeris reared on diets of BWD, BWY, and BWDY was more than the previously recorded value of r 8,23.
Diet mixing is common among generalist predatory mites24,25, and the benefits deriving from this have been mainly attributed to the ability of species to feed on different types of prey containing different amounts of nutrients and thus actively restores nutritional imbalances in their diets26. In the present study, the performance of N. cucumeris fed on mixed diets (BDY and BWDY) has no difference in comparison with other diets and the control, while after ten generations, the total pre-adult period of both mixed diets was shorter than that in G1. A short pre-adult period is a good feature for biocontrol agents by leading to a shortening of generation duration and consequently increasing the population growth potential of the predator. In addition, the parameters of GRR, r, λ, and fecundity after long-term rearing on a BDY diet were increased significantly; it appears adaptation on this mixed diet improved the performance of the predatory mite. Similar to our findings, the astigmatid mites T. entomophagus, A. siro, and L. destructor were more suitable diets for oviposition of the predatory mite A. swirskii when they were reared on dog food + wheat bran + yeast compared to those reared on wheat bran + yeast20. Dog food contains macro and micro elements, fiber, essential amino acids, and fatty acids27, and yeast can break down sugar and carbohydrates in foods such as wheat flour or bran and make them more available to predators.
Although no information is available in the literature regarding the biochemical composition of diets fed to N. cucumeris, some research works are found regarding other phytoseiid species. Marked enhancements in reproductive performance were observed in A. swirskii females when fed on T. putrescentiae reared on enriched diets10. The improved reproductive output under these diets appears to reflect an optimized nutritional balance, combining carbohydrate-rich components with both plant- and animal-derived supplements. These results emphasize that optimizing prey diet composition is a crucial step toward improving metabolic efficiency, reproductive performance, and ultimately, the sustainability of predatory mite mass-rearing systems within integrated pest management frameworks. The developmental and adult longevity performance of A. swirskii was also strongly influenced by the nutritional composition of its factitious prey, C. lactis11. The link between nutritional quality and population dynamics has been previously attributed to the C/N ratio of prey tissue, where optimal ratios facilitate both growth and reproductive outputs in predatory insects. Moreover, while protein plays a dominant role in reproduction, as discussed earlier, carbohydrates and lipids may be equally important for metabolic energy and fecundity sustainability across generations. Optimizing the nutritional composition of diets for C. lactis significantly alters its biochemical makeup and, in turn, the demographic performance of A. swirskii. In addition, neither high protein nor high carbohydrate content alone is sufficient to support all aspects of predator performance. Rather, diets that offered a balanced profile containing adequate levels of protein for reproduction, carbohydrates for energy, and micronutrients for physiological regulation are most effective in enhancing development rate, reproductive output, and overall population growth11.
Although the intrinsic rate of increase did not differ significantly among diets compared with the control, the total lifespan and fecundity of predatory mites reared on enriched diets were higher than those of mites reared on the control diet. Moreover, after ten generations, fecundity, gross reproductive rate (GRR), intrinsic rate of increase (r), and finite rate of increase (λ) increased significantly in mites fed the BDY diet, whereas the preadult period and mean generation time (T) were significantly reduced in mites fed the BWDY diet. Overall, diet enrichment improved the performance of the predatory mite, and mixed diets proved to be more suitable for the long-term rearing of N. cucumeris, likely due to their higher diversity of macro- and micronutrients. Although the combination of diets appears more costly than a single diet, the resulting stable performance justifies the additional expense.
Acknowledgements
The support of this research by the Department of Entomology, Tarbiat Modares University is greatly appreciated.
Author contributions
Shima Yazdanpanah: Writing – original draft, Software, Methodology, Investigation, Data curation, Conceptualization. Yaghoub Fathipour: Writing – review & editing, Validation, Supervision, Project administration, Methodology, Funding acquisition, Data curation, Conceptualization.
Funding
This study was financially and technically supported by Tarbiat Modares University.
Data availability
The data that support the findings of this study are available from the corresponding authors, [SY and YF], upon reasonable request.
Declarations
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Contributor Information
Shima Yazdanpanah, Email: shimayazdanpanah@modares.ac.ir.
Yaghoub Fathipour, Email: fathi@modares.ac.ir.
References
- 1. Ziad, B. Evaluation of three pesticides against phytophagous mites and their impact on phytoseiid predators in an eggplant open-field. Acarologia57, 529–539 (2017). [Google Scholar]
- 2.Lorenzon, M., Pozzebon, A. & Duso, C. Biological control of spider mites in North-Italian vineyards using pesticide resistant predatory mites. Acarologia58, 98–118 (2018). [Google Scholar]
- 3.Malagnini, V., Baldessari, M., Duso, C., Pozzebon, A. & Angeli, G. Side-effects of a number of insecticides on predatory mites in apple orchards. Acarologia63, 17–28 (2023). [Google Scholar]
- 4.Yang, J., Lv, J., Liu, J., Xu, X. & Wang, E. Prey preference, reproductive performance, and life table of Amblyseius tsugawai (Acari: Phytoseiidae) feeding on Tetranychus urticae and Bemisia tabaci. Sys Appl. Acarol. 24, 404–413 (2019). [Google Scholar]
- 5.McMurtry, J. A., de Moraes, G. J. & Sourassou, N. F. Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Sys Appl. Acarol. 18, 297–320 (2013). [Google Scholar]
- 6.McGregor, R., Crisp, K. & Castiglia, C. Feeding lifestyles of the Phytoseiidae revisited: searching for a factitious rearing host for Neoseiulus fallacis (Acari: Phytoseiidae). Biocontrol65, 593–599 (2020). [Google Scholar]
- 7.Yazdanpanah, S., Fathipour, Y., Riahi, E. & Zalucki, M. P. Mass production of Neoseiulus cucumeris (Phytoseiidae): an assessment of fifty generations reared on almond pollen. J. Econ. Entomol.114 (6), 2255–2263 (2021). [DOI] [PubMed] [Google Scholar]
- 8.Yazdanpanah, S. & Fathipour, Y. How enriched diet of the second trophic level (Tyrophagus putrescentiae) affects the performance of the third trophic level (Neoseiulus cucumeris): the role of pollens and legumes. Bull. Entomol. Res.114 (6), 869–875 (2024). [DOI] [PubMed] [Google Scholar]
- 9.Krasavina, L. & Trapeznikova, O. Assessment of different species of fodder mites for mass rearing of the predatory mites Amblyseius swirskii and Neoseiulus cucumeris (Mesostigmata, Phytoseiidae) under laboratory conditions. Plant. Protec News. 103 (3), 177–181 (2020). [Google Scholar]
- 10.Pishgar, E., Yazdanpanah, S. & Fathipour, Y. How to improve mass production of the predatory mite Amblyseius swirskii (Acari: Phytoseiidae) by enhancing its factitious prey Tyrophagus putrescentiae (Acari: Acaridae) quality using animal-based supplements. J. Econ. Entomol.118 (6), 2821–2831 (2025). [DOI] [PubMed] [Google Scholar]
- 11.Jahanbazi, M., Zibaee, A. & Fathipour, Y. Nutritional management of Carpoglyphus lactis diets enhances Amblyseius swirskii performance for biological control. Sci. Rep.16, 1266 (2026). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Huang, H. et al. Impact of proteins and saccharides on mass production of Tyrophagus putrescentiae (Acari: Acaridae) and its predator Neoseiulus barkeri (Acari: Phytoseiidae). Biocontrol Sci. Technol.23, 1231–1244 (2013). [Google Scholar]
- 13.Barry, K. L. & Wilder, S. M. Macronutrient intake affects reproduction of a predatory insect. Oikos122, 1058–1064 (2013). [Google Scholar]
- 14.Fayaz, B. A., Khanjani, M. & Rahmani, H. Tyrophagus putrescentiae (Schrank) (Acari: Acaridae) from Western Iran with a key to Iranian species of the genus. Acarina24 (1), 61–76 (2016). [Google Scholar]
- 15.Chi, H. & Liu, H. Two new methods for the study of insect population ecology. Bull. Inst. Zool. Acad. Sinica. 24, 225–240 (1985). [Google Scholar]
- 16.Chi, H. Life-table analysis incorporating both sexes and variable development rates among individuals. Environ. Entomol.17, 26 (1988). [Google Scholar]
- 17.Chi, H. TWO SEX-MSChart: a computer program for the age-stage, two-sex life table analysis. 202 Edition. (2025). http://zenodo.org/records/7484085 (Accessed December 2025).
- 18.Huang, Y. B. & Chi, H. Age-stage, two-sex life tables of Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae) with a discussion on the problem of applying female age-specific life tables to insect populations. Insect Sci.19 (2), 263–273 (2012). [Google Scholar]
- 19.Reddy, G. V. & Chi, H. Demographic comparison of sweet potato weevil reared on a major host, Ipomoea batatas, and an alternative host, I. triloba. Sci. Rep.5 (1), 11871–11879 (2015). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Pirayeshfar, F., Safavi, A., Moayeri, S., Messelink, G. J. & H.R. & Provision of astigmatid mites as supplementary food increases the density of the predatory mite Amblyseius swirskii in greenhouse crops, but does not support the omnivorous pest, western flower thrips. Biocontrol66, 511–522 (2021). [Google Scholar]
- 21.Chen, Q. et al. Age stage, two-sex life table of Parapoynx crisonalis (Lepidoptera: Pyralidae) at different temperatures. PLoS ONE. 12 (3), e0173380 (2017). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.San, P. P., Tuda, M., Nakahira, K. & Takagi, M. Optimal rearing medium for the population growth of the predatory mite, Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae). Egypt. J. Biol. Pest Control. 30 (1), 130 (2020). [Google Scholar]
- 23.Yazdanpanah, S. & Fathipour, Y. Exploring the oilseed plant-mediated effects on biological attributes of the predatory mite Neoseiulus cucumeris through its factitious prey Tyrophagus putrescentiae. Biocontrol Sci. Technol.35 (8), 898–908 (2025). [Google Scholar]
- 24.Samaras, K., Pappas, M. L., Fytas, E. & Broufas, G. D. Pollen provisioning enhances the performance of Amblydromalus limonicus on an unsuitable prey. Front. Ecol. Evol.7 (2), 122 (2019). [Google Scholar]
- 25.Han, Y. et al. Effects of various nectar and pollen plants on the survival, reproduction, and predation of Neoseiulus bicaudus. Insects15 (3), 190 (2024). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Mayntz, D., Raubenheimer, D., Salomon, M., Toft, S. & Simpson, S. J. Nutrient-specific foraging in invertebrate predators. Science307 (5706), 111–113 (2005). [DOI] [PubMed] [Google Scholar]
- 27.Swanson, K. S., Carter, R. A., Yount, T. P., Aretz, J. & Buff, P. R. Nutritional Sustainability of Pet Foods. Adv. Nutr.4, 141–150 (2013). [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available from the corresponding authors, [SY and YF], upon reasonable request.