Oviposition selection, prey preference and release strategies enhance the combined aphid control effects of Aphidoletes aphidimyza and Aphidius gifuensis

doi:10.21203/rs.3.rs-4650195/v1

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Oviposition selection, prey preference and release strategies enhance the combined aphid control effects of Aphidoletes aphidimyza and Aphidius gifuensis

https://doi.org/10.21203/rs.3.rs-4650195/v1

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Aphidius gifuensis and Aphidoletes aphidimyza are widely used in agriculture to control Myzus persicae using inundative biological control (IBC). However, it is not clear whether intraguild predation (IGP) can be overcome to achieve stable aphid control when both predators and parasitoids are released simultaneously for M. persicae control. In this work, we evaluated the oviposition site selection and prey preference of predatory gall midges or parasitoids in the presence of intragroup species, and the efficiency of aphid control in greenhouse greenhouses after releasing them in various methods. Predatory gall midge will avoid laying eggs on plants with only parasitic aphids, but A. gifuensis has no obvious parasitism options under predatory gall midge larval activity. Intraguild predation has no significant effect on predation preference in A. aphidimyza, but significantly alters parasitism preference in A. gifuensis. In addition, among all treatments in the greenhouse experiment, the best aphid control was achieved by releasing A. aphidimyza for 8 days followed by the A. gifuensis treatment, while the treatment of releasing A. gifuensis for 8 days followed by A. aphidimyza was less effective in controlling aphids than the treatment of releasing only A. aphidimyza. These results suggest that simultaneous release of A. gifuensis and A. aphidimyza for peach aphid control is synergistic, but is significantly affected by the mode of release. It may prove valuable for the development improved augmentative release strategies for these two natural enemies.

biological control

Myzus persicae

intraguild predation

predator

parasitoid

interspecific interaction

Myzus persicae (Sulzer) (Hemiptera: Aphididae) is a highly destructive worldwide agricultural pest that can complete its development on more than 400 plant species in more than 40 families (Bass et al. 2014; Xu and Gray 2020), and is a mediator insect for more than 100 plant viruses (Margaritopoulos et al. 2020). It is now one of the most widely distributed and resistant species in the world, having developed resistance to almost all insecticides used (Bass et al. 2014). To control peach aphids in solanaceous crops, growers release large quantities of reared Aphidius gifuensis Ashmead (Hymenoptera: Braconidae) and Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae) for timely control of aphids in the crop (inundative biological control). However, when using several natural enemies to control a pest, it is vital to understand the nature of natural enemy interactions and apply them to a reasonable combination of organisms in order to maximize ecosystem services. (Cardinale et al. 2003; Wilby et al. 2005). Therefore, how they coexist in ecosystems when sharing resources is a key question that needs to be addressed to understand ecosystem functioning (Chailleux et al. 2017).

Oviposition behavior is an important component of many ecological aspects of insects, including population dynamics, life history evolution, host specificity, and biological control of pests (Almohamad et al. 2009; Amiri-Jami et al. 2016). The link between adult oviposition selection and larval performance is a key factor in the evolution of oviposition behavior (Craig et al. 1989; Thompson 1988). Adults' oviposition sites impact hatchling larvae's ability to find food (Sadeghi and Gilbert, 2001; Sentis et al. 2012), as well as the intensity of intraspecific and interspecific disturbance (Fréchette et al. 2007; Messelink et al. 2011). This is especially important for footless larvae with limited foraging ability (Peckarsky et al. 2000; Thompson 1988). Previous studies have found that the presence of intraspecific or interspecific competitors is one of the important factors affecting egg-laying selection in female insects (Almohamad et al. 2008; Messelink et al. 2011; Amiri-Jami et al. 2016). Interspecific intraguild predation may affect the stabilization of predator populations (Godfray and Pacala 1992) or adversely affect the foraging and egg-laying performance of individual predators (Agarwala et al. 2003; Rosenheim et al. 1995). Not only do such interactions result in predators severely influencing the fate of parasitoid wasp larvae (Hassanzadeh-Avval et al. 2018; Sánchez-Hernández et al. 2020), but parasitoids similarly influence the egg-laying choices of predators (Almohamad et al. 2008). However, the current oviposition selection of A. gifuensis and A. aphidimyza is not reported.

The efficiency of biological control by natural enemies is influenced by the intraguild predator relative preference for intraguild and extraguild prey (Naranjo, 2007; Chailleux et al. 2013). This is because specific prey can provide benefits to predator health such as increased egg production, development to adulthood, and faster development time (Stasek et al. 2018). However, the selection of prey by predators and parasitoids depends on prey physiology (body thickness) and defensive behaviors (kicking, pulling, leaving, dropping), which can vary depending on the age stage of the prey (Shrestha et al. 2015; Humphreys and Ruxton 2018). This results in predators or parasitoids usually showing a preference for prey of a specific age (Yazdani et al. 2015; Mohammadpour et al. 2019). When predators are used in combination with parasitoids, this will weaken intraguild predation if they have differential preferences for prey of different ages and vice versa. Thus, understanding the stage preferences of predators and parasitoids for shared prey can help in developing biological control programs.

In the use of predators and parasitoids for biological control, although the results of indoor experiments suggest that interspecific competition between them can be intense, these natural enemies are not always detrimental to biological control when mixed and released into the greenhouse or outdoors (Aigbedion-Atalor et al. 2021; Chailleux et al. 2017; Messelink et al. 2013). For example, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) feeds on aphids or mummies parasitized by Aphelinus asychis Walker (Hymenoptera: Aphelinidae), but at mixed release H. axyridis can complement A. asychis biological control of aphids rather than disrupting this through intraguild predation control (Snyder et al. 2004). Previous studies have shown that the negative effects of intraguild predation can be attenuated by altering the timing of predator and parasitoid wasp releases (Mohammadpour et al. 2020). Thus, although A. aphidimyza and A. gifuensis share the same ecological niche and similar biological habits when controlling M. persicae on baked tobacco (Boulanger et al. 2019; Yang et al. 2009), which can undergo asymmetric intragroup predation. However, the effectiveness of aphid control may be greatly increased by mixed releases, due to spawning selection and prey preference between them, as well as reasonable timing of releases.

We predicted that (1) A. aphidimyza and A. gifuensis would avoid laying their eggs wherever possible where there is interspecific competition; (2) predators and parasitoids differ in their preference for prey of different ages, and that they would change their preference for prey of the same age when there is interspecific competition; and (3) that the release of both species in the greenhouse in a different way could improve their biological control effectiveness.

Plant material and insect rearing

Selected roasted tobacco seedlings (MS k326) were reared M. persicae and experimental seedlings. A. aphidimyza, A. gifuensis, and the tobacco aphid were obtained from the Natural Enemy Breeding Center, Evolution Town, Fenggang County, Zunyi City, Guizhou Province (27°46′28.43″N, 107°41′18.53″E). A. aphidimyza was harvested in 2018 from a tobacco base in Leshan Town, Zunyi City, Guizhou Province (27°38′29.47″N, 106°40′12.58″E), and both A. gifuensis and M. persicae were collected in Evolution Town, Fenggang County, Zunyi City, Guizhou Province (27°46′ 28.43″N, 107°41′18.53″E), and both natural enemies were populations reared by M. persicae. All tobacco seedlings and insect populations were kept in an artificial climate chamberat 25°C ± 1°C, 65% RH, 14: 10 L: D regime.

Acquisition of different instar aphid nymphs and parasitized aphids

To obtain aphid nymphs at various instar stages, a tobacco leaf disc (6 cm in diameter) was kept at the bottom of a Petri dish (6 cm in diameter) containing 1% agar gel. Each Petri dish contained 20 M. persicae adults, which subsequently were taken out after 24 h. Newly molted first-instar nymphs were transferred to detached tobacco leaves (each leaf measuring < 500 cm²), with the leaf base kept moistened in water. The aphid nymphs were reared until they reached the desired instar stage required for our experiment.

To produce a diverse population of day-old parasitized aphids, each Petri dish was populated with 30 first-instar nymphs of M. persicae (held for 1 h before the subsequent test). Then, two fully mated females of A. gifuensis were introduced into the Petri dish. After 24 h, the parasitized M. persicae were transferred onto the surface of detached tobacco leaves (each leaf measuring < 500 cm²), where they were reared to obtain parasitized aphids of different ages. The leaf bases were submerged in water to maintain moisture levels. Depending on the timing of the parasitization of M. persicae, we identified three parasitism periods: three days old (parasitized but not yet undergoing mummification), six days old (imminent mummification), nine days old (mummification).

Oviposition site selection by Aphidoletes aphidimyza and Aphidius gifuensis

Experimental experiments were conducted under controlled settings of 25°C and 65% R.H. Thirty parasitized aphids (3 days old, 6 days old, and 9 days old) and healthy aphids were transferred to four three-leaf stage tobacco seedlings, and 9 days old parasitized aphids were glued to the tobacco leaves with Elmer's glue. After 3 h of aphid colonization, four tobacco seedlings were randomly placed on four corners of a 25*15*15 cm rectangular nylon mesh fabric cage (100 mesh). Afterwards, one fully mated female adult A. aphidimyza was transferred to the mesh cage. After 48 h, the number of A. aphidimyza eggs on the tobacco seedlings of different treatments was recorded and the experiment was repeated 15 times.

The parasitism behavior of A. gifuensis under the risk of intragroup predator activity was studied on three-leaf stage tobacco plants, placed in cages made from nylon gauze (100 mesh, 25*15*15 cm). The experiment was set up with two treatments: (i) Intraguild predator predation trace (PT) treatment, which thirty 2nd-3rd instar aphids and five A. aphidimyza 3rd instar larvae that were introduced intobacco seedling; (ii) Intraguild predator activity trace (CT) treatment, where only five A. aphidimyza 3rd instar larvae that were starved for 6 h were introduced in tobacco seedlings; (iii) Control tobacco seedlings were also introduced with only thirty 2nd-3rd instar aphids. After 24 h, aphids and predator larvae were removed from the tobacco seedlings and the predated aphid carcasses were retained. Then, 30 2nd instar aphids were introduced to each tobacco seedling. After the aphids had colonized for 3 h, the seedlings were transferred to a nylon mesh cage, and then one A. gifuensis that had fledged within 24 h and was fully mated was introduced into the cage. After 24 h, A. gifuensis was removed and to prevent aphid escape, aphids from each treatment were transferred to petri dishes for incubation. The number of mummies was counted after 10 days, and the leaf in the petri dishes was replaced every 1–2 d. Each treatment was replicated 11 times.

Preference experiment

The experiment was conducted in Petri dishes (Φ = 60 mm, h = 30 mm), and 30 aphids were picked into each dish based on the single-day predation of Aphidoletes aphidimyza and the optimal holding capacity of the dish. Fifteen 1st and 3rd instar aphids (or parasitized aphids and healthy aphids) were picked and placed in petri dishes, and aphids were allowed to colonize for 1 h and then transferred to a single-head predator to start preference testing. The following are combinations of preference tests: (i) 1st instar nymph aphid + 3rd instar nymph aphid + 1st (2nd, or 3rd ) instar larva of predator; (ii) 1st instar nymph aphid + 3rd instar nymph aphid + 1st (2nd, or 3rd ) instar larva of predator + Aphidius gifuensis adults; (iii) 4th instar nymph aphid + 5th days old parasitized aphid + 1st (2nd, or 3rd ) instar larva of predator. Each treatment was replicated 15 times. natural enemies were removed after 24 h. The number of aphids preyed upon was recorded, and aphids not moving and considered dead when gently touched with a brush. Correct natural aphid mortality under same settings without unleashing natural enemies.

Preference for A. gifuensis the experiments were done in Petri dishes (Φ = 80 mm, h = 33 mm), and 40 aphids were picked into each dish based on the single-day parasitism of A. gifuensis and the optimal holding capacity of the dish. The 'Imago Activity (IA)' treatment consisted of a mated A. aphidimyza adult, which was allowed to mate for 12 h, placed in a Petri dish. PT and CT treated as above. After 6 h, the aphid nymphs and A. aphidimyza larvae were removed from the Petri dishes, and the predated aphid carcasses or A. aphidimyza adults were retained. Aphids were allowed to colonize for 1 h and then transferred to a single mated adult A. gifuensis to start preference testing. The following treatments set up under were as follows: (i) 1st instar nymph aphid + 3rd instar nymph aphid + A. gifuensis adults; (ii) PT (CT, or IA) + 1st instar nymph aphid + 3rd instar nymph aphid + A. gifuensis adults. Each treatment was repeated 15 times and no new aphids were added midway through all treatments. After 24 h, 1st and 3rd instar aphids from different treatments were incubated separately. The number of mummies was recorded after the incubation was continued for 10 days, during which time the tobacco leaves were replaced every 1–2 d.

Using the β-Manly preference index to analyze prey preferences of natural enemies (Manly 1974; Chesson 1983), which was calculated for A. aphidimyza (1) and A. gifuensis (2) by the following formula:

\({\beta }_{i} = \frac{\text{l}\text{o}\text{g}\left(\frac{{e}_{i}}{{A}_{i}}\right)}{\text{log}\left(\frac{{e}_{i}}{{A}_{i}}\right) + \text{l}\text{o}\text{g}\left(\frac{{e}_{j}}{{A}_{j}}\right)}\) (Manly, 1974; Pehlivan et al., 2017) (1)

\({\beta }_{i} = \frac{\text{l}\text{o}\text{g}\left(\frac{{n}_{i}+0.001}{{A}_{i}}\right)}{\text{log}\left(\frac{{n}_{i+0.001}}{{A}_{i}}\right) + \text{l}\text{o}\text{g}\left(\frac{{n}_{j+0.001}}{{A}_{j}}\right)}\) (Manly, 1974; Pehlivan et al., 2017) (2)

Where β_i is the preference for prey type i; A_i and A_j are the number of prey types i and j, respectively, at the beginning of the experiment; e_i and e_j are the number of prey types i and j, respectively, at the end of the experiment, n_i and n_j are the number of unparasitized aphids for type i and type j prey, respectively. The value of β_i will fall between 0 and 1, with values greater than 0.5 indicating preferences.

Greenhouse experiment

The greenhouse test was started on May 30, 2022, in the seedling shed of Fenggang County Natural Enemy Breeding Center, which has three fans and a skylight on the roof to provide effective ventilation at high noon temperatures. Tobacco seedlings were transplanted into plastic pots (28 cm in diameter) containing a special substrate for tobacco seedlings and a yellow soil mixture (2:1), and were placed to grow until seven-leaf stage in 85*85*140 cm screen cages with a cover made of 100-mesh nylon mesh, one seedling per cage. After that, 1, 4 and 5 adult aphids were introduced to the penultimate 1, 2 and 3 leaves of each plant, respectively. The number of aphids on each plant was counted 5 days after aphid inoculation, when there were approximately 200 aphids and natural enemies were introduced. Six different treatments were considered: (i) Introduction of only 4 pairs of A. aphidimyza (AA); (ii) Introduction of only 4 pairs of A. gifuensis (AG); (iii) Simultaneous introduction of 4 pairs of A. gifuensis and 4 pairs of A. aphidimyza (AAG); (iv) Introduction of 4 pairs of A. aphidimyza followed 8 days later by 4 pairs of A. gifuensis (FAAG); (v) Introduction of 4 pairs of A. gifuensis followed 8 d later by 4 pairs of A. aphidimyza (FAGA); (vi) No release of natural enemies (Control). Natural enemy insects from each treatment were mated for at least 20 h prior to release, and were introduced into the mesh cages at around 6 pm in the evening. Each treatment was replicated 5 times. The number of aphids on the plants was recorded every 4 d, using counter-assisted counting (GEDUN). The day of introduction of the predator or parasitic was recorded as 0 d. After that, the number of predatory gall mosquito larvae was recorded once a day, and the number of aphids mummified was recorded every 4 d. The number of stipe aphids recorded each time was cumulative because it was difficult to separate the newly emerged mummies from the previous stipe aphids. Throughout the test, climatic conditions in the greenhouse were recorded using a digital thermometer (JR900, Medtec) placed 1 m above the ground.

Statistical analysis

In oviposition selection experiments, Generalized Linear Mixed Models (GLMM) were used to analyze the number of predatory gall midge eggs or the number of aphids being parasitized. Logarithmic conversion log (x + 1) prior to analysis. The different treatments were fixed factors and the females in each replicate were randomized. Differences between pairs of fixed factors were tested at the 5% level using the Least Significant Difference Fisher 's LSD (Least Significant Difference) approach.

The one-sample t-test was used to compare the difference between Manly's index and 0.5 (P < 0.05), and the test was also used to compare the difference in predation by A. aphidimyza larvae on older or younger aphids in the presence of A. gifuensis adults (P < 0.05). One-way analysis of variance (ANOVA) was used to compare differences in parasitization of 1st (or 3rd) instar aphids by A. gifuensis between treatments, and when significant differences existed (P < 0.05), multiple comparisons were made at the 0.05 level using Tukey's HSD test.

The use of generalized linear mixed models (GLMM) was used to analyze the number of M. persicae, mummies, predatory gall midge larvae, and parasitism rates of parasitoids, which were log-transformed (log (x + 1)) prior to analysis. Treatments were fixed factors, time was randomized, and each GLMM was linked using a normal distribution with a constant function, with pairwise comparisons using Least Significant Difference Fisher 's (LSD, P < 0.05) for fixed-factor levels where differences existed. Abbott's formula (100 × (1-(treatment/control)) was applied to calculate the percentage reduction of M. persicae across treatments (Abbott 1925; Bouagga et al. 2018). Differences in percent aphid reduction between treatments were compared using the nonparametric Kruskal-Wallis test (H-test), and when significant differences existed (P < 0.05), pairwise comparisons of two independent samples were made using the Mann-Whitney test (U-test). All data were analyzed using SPSS 26.0 (IBM Corporation, Armonk, NY, USA), and graphs were created with SigmaPlot 14.0 (Systat Software, San Jose, CA, USA).

Oviposition site selection by Aphidoletes aphidimyza and Aphidius gifuensis

There was significant oviposition selection by predatory gall midge for tobacco seedlings in the presence of parasitized aphids of different days old (GLMM: F_3,56 = 60.45, P < 0.001) (Fig. 1a). Predatory gall mosquitoes chose to lay significantly fewer eggs (P < 0.001) on tobacco seedlings with only advanced parasitized aphids, and did not choose to lay eggs on seedlings with only mummified aphids, compared to the control. Mean egg production of predatory gall midge was significantly reduced in tobacco seedlings that were parasitized by aphids only at 3 days old (P = 0.021), 6 days old (P < 0.001), or 9 days old, compared to those in which only healthy aphids were present. Larval activity of predatory gall mosquitoes did not significantly affect parasitism selection of parasitoid A. gifuensis (GLMM: F_2,30 = 0.50, P = 0.609) (Fig. 1b), where A. gifuensis parasitized slightly less under the PT treatment than the control and CT treatments.

Preference experiment

The natural mortality of both 1st and 3rd instar aphids in the preference experiment did not exceed 3%. Thus, aphid mortality was caused by the experimental treatments.

Predation by 2nd instar larvae of A. aphidimyza on 3rd instar aphids(t = 2.14, P = 0.042)and 3rd instar larvae of predatory gall midge on 1st instar aphids was significantly lower (t = 3.00, P = 0.006) when A. gifuensis adults were present (Table 1). However, regardless of the presence or absence of A. gifuensis adults, the 1st, 2nd, and 3rd instar larvae of predatory gall mosquitoes preferred to feed on 1st instar wakame, with Manly's indices significantly higher than 0.5, with the 3rd instar larvae having the highest Manly's index (Table 1). In addition, except for the 1st instar larvae of predatory gall midge, the Manly's indices of 2nd and 3rd instar larvae on healthy aphids were 0.78 and 0.72, respectively, which were significantly higher than 0.5 (Table 2).

Table 1

Manly’s index of preference and predatory capacity of 1st and 3rd instar nymph of *Myzus persicae* by the *Aphidoletes aphidimyza* larval (24 h)
Aphidoletes aphidimyza larval	Aphidius gifuensis adult	Number of aphids consumed (Mean ± SE)		Manly’s index (β₁) (Mean ± SE)
Aphidoletes aphidimyza larval	Aphidius gifuensis adult	1st instar nymph	3rd instar nymph	1st instar nymph	t	df	P
1st instar	Not	2.9 ± 0.3 a	1.6 ± 0.3 a	0.65 ± 0.05	3.119	14	0.008
1st instar	Yes	2.3 ± 0.3 a	1.2 ± 0.2 a	0.66 ± 0.06	2.871	14	0.012
2nd instar	Not	3.4 ± 0.5 a	2.3 ± 0.3 a	0.59 ± 0.04	2.377	14	0.032
2nd instar	Yes	3.0 ± 0.4 a	1.3 ± 0.2 b	0.67 ± 0.06	3.159	14	0.007
3rd instar	Not	5.3 ± 0.4 a	1.9 ± 0.3 a	0.76 ± 0.03	8.298	14	< 0.001
3rd instar	Yes	4.3 ± 0.3 b	1.4 ± 0.2 a	0.77 ± 0.03	8.909	14	< 0.001

Different lowercase letters in the table indicate that the presence or absence of A. gifuensis adult had a significant effect on predation by A. aphidimyza of the same larval stage on M. persicae of the same age (Student’s t-test, P < 0.05). A one-sample t-test was used to compare the Manly index with 0.5, with P < 0.05 indicating a significant difference.

Table 2

Manly’s index of preference and predatory capacity of parasitized and unparasitized nymph of *Myzus persicae* by the *Aphidoletes aphidimyza* larval
Aphidoletes aphidimyza larval	Number of aphids consumed (Mean ± SE)		Manly’s index (β₁) (Mean ± SE)
Aphidoletes aphidimyza larval	Unparasitized nymph	Parasitized nymph	Unparasitized nymph	t	df	P
1st instar	1.9 ± 0.3	0.9 ± 0.1	0.57 ± 0.08	0.868	14	0.400
2nd instar	3.2 ± 0.4	1.1 ± 0.3	0.78 ± 0.06	4.512	14	< 0.001
3rd instar	3.7 ± 0.3	1.5 ± 0.2	0.72 ± 0.03	6.354	14	< 0.001

A one-sample t-test was used to compare the Manly index with 0.5, with P < 0.05 indicating a significant difference.

For the parasitoid A. gifuensis, we found significant differences in the number of 1st instar of parasitized aphids between treatments (F_3,56 = 10.69, P < 0.001), whereas there was no statistically significant difference in the number of parasitized aphids against the 3rd instar aphids (F_3,56 = 2.58, P = 0.063) (Table 3). Manly's β-index showed significant preference for parasitizing 1st instar aphids in both control and IA treatments of A. gifuensis, whereas CT and PT treatments of A. gifuensis did not show a significant preference for 1st instar aphids (Table 3).

Table 3

Parasitism and Manly index of 1st and 3rd instar nymph of *Myzus persicae* by *Aphidius gifuensis* under *Aphidoletes aphidimyza* larval predation traces (PT), crawling traces (CT) and imago presence (IA) (24 h)
—	Number of aphids consumed (Mean ± SE)		Manly’s index (β₁) (Mean ± SE)
—	1st instar nymph	3rd instar nymph	1st instar nymph	t	df	P
CK	14.5 ± 0.8 a	10.6 ± 0.9 a	0.63 ± 0.05	2.717	14	0.017
CT	11.2 ± 0.7 b	10.1 ± 0.7 a	0.55 ± 0.04	1.276	14	0.223
PT	9.1 ± 0.7 b	10.6 ± 0.8 a	0.44 ± 0.03	-2.086	14	0.056
IA	14.3 ± 0.5 a	7.8 ± 0.9 a	0.74 ± 0.03	6.929	14	< 0.001

Data in the table were mean ± SE, Different letters in the same column indicate a significant difference between the treatment according to Tukey’s test (p < 0.05). A one-sample t-test was used to compare the Manly index with 0.5, with p < 0.05 indicating a significant difference.

greenhouse experiment

Temperature and humidity variations throughout the greenhouse experiment are shown in Fig. 2.

There was no significant difference (ANOVA: F_5,24 = 0.19, P = 0.965) in the number of aphids between treatments prior to the introduction of released natural enemies (Fig. 3a). However, M. persicae populations differed significantly between treatments throughout the survey period After the release of predatory gall midge and tobacco aphid cocoon wasp (GLMM: F_5,264 = 93.84, P < 0.001) (Fig. 3a). Among them, the most significant increase in aphid numbers was observed in the control (Control), which was significantly higher than AA (t = 10.77, P < 0.001), AAG (t = 15.11, P < 0.001), FAAG (t = 16.20, P < 0.001), and the introduction of A. gifuensis8d followed by A. aphidimyza (FAGA: t = 7.86, P < 0.001). But the difference with AG was not significant (t = 1.17, P = 0.245). Meanwhile, the FAAG treatment of M. persicae had the lowest number of M. persicae, which was significantly lower than the AA, AG, and FAGA treatments (t = -5.43, P < 0.001; t = -15.03, P < 0.001; and t = -8.34, P < 0.001), whereas the difference with the AAG treatment was not significant (t = -1.09, P = 0.278) (Fig. 3a). The difference in percentage reduction of M. persicae among treatments was significantly significant (H (4) = 24.113, P < 0.001). In particular, the percentage of aphid reduction in AG treatment was 17.5% significantly lower than AA (79.1%, U = 16.50, P = 0.005), AAG (86.8%, U = 22.75, P < 0.001), FAAG (89.1%, U = 25.75, P < 0.001), and FAGA (66.7%, U = 11.88, P = 0.042) treatments (Fig. 3b).

In this experiment, A. aphidimyza were able to colonize under different treatments and persist until the end of the experiment. In this case, F₁ generation predator larvae began to emerge on the 3d after the introduction of natural enemies, while F₂ generation larvae began to emerge on the 18th day after the introduction. Both F₁ generation larvae and F₂ larvae of predatory gall midge were significantly different between treatments (GLMM: F₁: F_3,136 = 17.245, P < 0.001; F₂: F_3,156 = 22.824, P < 0.001) (Fig. 4).

In the present study, mummies began to emerge at d 7–8 after natural enemy introduction, and adults of the F₁ generation of A. gifuensis began to emerge at d 11 after natural enemy introduction (Fig. 5a). The number of mummies differed significantly between treatments throughout the survey period (GLMM: F_3,156 = 58.15, P < 0.001) and parasitism rate (GLMM: F_3,156 = 7.01, P < 0.001) (Fig. 5). The AG had the highest number of mummies, which was significantly higher than the AAG and FAAG (t = 11.36, P < 0.001; t = 6.71, P < 0.001), and did not differ significantly from the FAGA (t = 0.61, P = 0.542), while the AAG had the lowest number of mummies. In addition, the FAGA had the highest parasitization rate and the AG the lowest among all treatments (Fig. 5b).

Despite the asymmetric intraguild predation of A. aphidimyza with A. gifuensis (Liu et al. 2020; Messelink et al. 2013) and the presence of commensal biological habits (Boulanger et al. 2019; Yang et al. 2009), but our results suggest that control of M. persicae can be significantly enhanced when co-released. In the laboratory results showed a clear tendency for A. aphidimyza to selectively lay eggs on seedlings with unparasitized M. persicae, and A. gifuensis also parasitized slightly more on seedlings without predator activity than on those with predator activity, which is similar to our first prediction. A. aphidimyza and A. gifuensis have preferences for prey of different ages, and when interspecific competition exists, they change some of their preferences thereby diminishing this risk, confirming our second conjecture. Finally, the results of the greenhouse experiment showed that releasing the release of two natural enemies at different times improved the control of M. persicae, the best results were obtained by FAAG.

Often female insects choose a relatively suitable or safer place to lay their eggs in response to potential risks. In our system, A. aphidimyza laid significantly more eggs on seedlings with only healthy aphids than on seedlings with only parasitized aphids, and A. aphidimyza did not choose to lay eggs on seedlings with only mummified aphids. Pineda et al. (2007) and Almohamad et al.(2008) similarly found that Episyrphus balteatus (De Geer) (Diptera: Syrphidae) laid more eggs on healthy aphids than on parasitized or mummies. Reasons for the occurrence of spawning selection in A. aphidimyza may include. First, A. aphidimyza females may have the ability to sense parasitized aphids and mummies. de Azevedo et al. (2018) showed that A. aphidimyza is able to sense Metarhizium brunneum Petch. (Hypocreales: Clavicipitaceae) and chooses to lay its eggs where the fungus is absent. Second, there may be differences in honeydew produced by different states of aphids. Mohl et al. (2020) found that honeydew quality directly affects the health of A. aphidimyza adults or has a repellent effect on their foraging behavior. Since aphids are parasitized to secrete honeydew of reduced quality and concentration (Tena et al. 2018; Wäckers et al. 2008), oviposition selection occurs in A. aphidimyza adults in order to optimize the survival of their offspring.

During prey sharing between a predator and a parasitoid wasp, the predator exerts persistent intimidation on the parasitoid wasp (Martinou et al. 2010), and persistent intimidation has been shown to be a unique mechanism among asymmetric intraguild species (Ruxton 2000). When parasitoids are at risk of predation, parasitoids can utilize semiochemicals to sense spatial and temporal information about the presence of a predator and may reduce output costs or divert foraging effort to finding patches more suitable for offspring survival (Nakashima et al. 2004). However, our study found that A. gifuensis did not show significant avoidance in the activity trajectories of predatory gall midge larvae compared to controls. This may be because some aphid predators avoid foraging at patches with traces of the same chemical (Yasuda et al. 2000; Agarwala et al. 2003), so even patches with predator-associated chemicals may be a no-enemy space, and here it does not necessarily mean that there is a real risk.

The present study found that A. aphidimyza larvae showed a significantly higher preference for 1st instar M. persicae than 3rd instar, and this preference did not change even in the presence of A. gifuensis adults. In contrast, A. gifuensis also parasitized 1st instar M. persicae significantly more than 3rd instar tobacco aphids in the absence of predator activity. Similar prey preferences exist for other predators or parasitoids (Hassanzadeh-Avval et al. 2018; Shrestha et al. 2015; Rasool et al. 2022). This may be related to differences in size and mobility of aphids at different stages, with senior aphids typically being larger and more sensitive than younger aphids, and therefore more difficult to capture. Also, it may be related to the aphid's own defense, which has been reported to be more pronounced in higher-aged aphids than lower-aged aphids among different species (Velasco-Hernandez et al. 2017). Russel (1972) found that relative size between Anthocoris nemorum (Linnaeus) (Heteroptera: Anthocoridae) and prey determined capture rates by natural enemies, with smaller prey facing a greater risk of capture.

In our study, we found that larvae of A. aphidimyza preyed on healthy aphids significantly more than parasitized aphids. This is similar to the result that A. aphidimyza preferred to prey on M. persicae not parasitized by Aphidius matricariae (Haliday) (Hymenoptera: Braconidae) (Aparicio et al. 2020). It is possible that chemical changes are induced in the aphid surface layer after aphids are parasitized (Lebreton et al. 2010; Kryukov et al. 2022), and that multifunctional predators seem to be able to recognize parasitized prey based on these external cues (Naranjo 2007; Moral et al. 2017; Coelho et al. 2022). In addition, intraguild predator preferences for parasitized and unparasitized prey depend on a variety of factors, including type, growth stage of intraguild prey (Kutuk et al. 2011), and density and degree of cuticle hardening of extraguild prey (Chailleux et al. 2013; Toosi et al. 2019).

In the present study, A. aphidimyza activity traces significantly affect the parasitism preference of A. gifuensis on M. persicae of different ages. Among them, A. aphidimyza adults exacerbated the preference of A. gifuensis for younger aphids, whereas A. aphidimyza larval activity traces weakened this preference, while A. aphidimyza larval feeding traces altered parasitoid wasp preference for younger aphids. It is possible that A. aphidimyza similarly prefers to prey on lower M. persicae, and that A. gifuensis reduces or alters the amount of parasitism on co-preferred prey in order to avoid predation on its offspring. Meisner et al. (2011) found that Aphidius ervi Haliday (Hymenoptera: Braconidae) can reduce the risk of offspring predation by avoiding parasitizing aphids under H. axyridis activity trails. Almohamad and Hance (2014) also found that A. ervi showed avoidance responses to aphid patches with traces of E. balteatus larvae.

Intraguild predation between predators and parasitoids is prevalent (Prieto et al. 2018; Pirzadfard et al. 2020; Xue et al. 2012), and this interspecific interaction may influence the success of pest biological control (Doker et al. 2021; Jonsson et al. 2017). However, our greenhouse experiments showed that the combined release of A. aphidimyza and A. gifuensis in greenhouses was significantly more effective against M. persicae than the release of a single natural enemy. Previous studies have similarly found that A. aphidimyza significantly enhances aphid suppression when used in conjunction with Aphidius colemani (Viereck) (Hymenoptera: Braconidae) or A. matricariae (Messelink 2013; Aparicio 2020). In addition, similar phenomena exist between other predators and parasitoids (Chailleux et al. 2013; Cabello et al. 2015; Aigbedion-Atalor et al. 2021). This suggests that intraguild predation between predators and parasitoids, even though it exists, is not always detrimental to the control of the target pest when released jointly. It may be that there are behaviors between them that weaken intraguild predation. For example, most predators prefer to feed on unparasitized prey (Pehlivan et al. 2017; Mohammadpour et al. 2019; Aparicio et al. 2020), Predators prefer to lay eggs on plants with aphids that are unparasitized or recently parasitized(Fréchette et al. 2006; Yu et al. 2019), parasitized wasps can recognize or sense predators and show avoidance behaviors towards prey patches with predator cues (Battaglia et al. 1995; Almohamad and Hance 2014; Xia et al. 2021), and parasitized prey can quickly escape the threat of predation through measures such as dropping (Humphreys and Ruxton 2018). Our study also found that FAAG treatment had the best aphid control among all treatments and was significantly better than all other treatments except AAG treatment. However, the FAGA treatment was significantly less effective in controlling aphids than the AA treatment. Sánchez-Hernández et al. (2020) found that the simultaneous release of predators and parasitoids reduced the predation risk of focal prey when alternative prey were present, but not when they were released sequentially. This suggests that different release methods can affect the interaction between predators and parasitoids, and thus the success of pest biological control.

A. aphidimyza reproduced for two generations and A. gifuensis reproduced for three generations during this experiment, which is similar to previous descriptions of the life histories of the two natural enemies (Zhang et al. 2014; Wang et al. 2019). Among all the treatments, the number of A. aphidimyza larvae was significantly lower in the F₁ generation in the FAGA treatment than in the other treatments, whereas the opposite was true in the F₂ generation, which may be related to the variation in the number of aphids on the plants. Previous studies have found that egg-laying by A. aphidimyza increases with increasing aphid density on the plant (Gou et al. 2020), and that predatory gall midge adults can use aphid honeydew as a cue to find the optimal location for egg-laying (Choi et al. 2004). Yu et al. (2019) showed that H. axyridis laid significantly fewer eggs on plants with parasitized aphids than on plants with healthy aphids.

Chailleux et al. (2013, 2017) found that predators have an effect on the population dynamics of parasitoids when predators and parasitoids coexist. In this greenhouse experiment, the number of mummies was significantly higher in the AG and FAGA treatments than in the AAG and FAAG treatments, with the lowest number of mummies in the AAG treatment. This suggests that both predators and different modes of release can have an effect on A. gifuensis parasitizing M. persicae. The effects of other predators and parasitoids on biological control when released in different sequences have been similarly reported (Sánchez-Hernández et al. 2020). These data suggest that biological control can be enhanced by modifying natural enemy releases.

In the equilibrium theory prediction of the intraguild predator, biological defense is only disrupted if the intraguild prey is a better competitor for shared prey than the intraguild predator (Holt and Polis 1997; Janssen et al. 2006). Although these predictions may not be directly applicable to the dynamics of natural enemies on shorter time scales (Briggs and Borer, 2005), predatory gall midge may have been a better aphid-controlling natural enemy insect than A. gifuensis in our experiments. Messelink et al. (2013) found that Orius majusculus (Reuter) (Hemiptera: Anthocoridae) is a better competitor for aphids than A. colemani. Although intraguild predators may reduce intraguild prey densities, they generally do not disrupt control of shared prey (Vance-Chalcraft et al. 2007; Bouagga et al. 2018; Aigbedion-Atalor et al. 2021), and our results are in consistent.

Overall, the potential negative effects of intraguild predation on biological control can be compensated by positive factors when A. aphidimyza and A. gifuensis are released in combination, thus showing synergistic effects, but the mode of release affects their aphidic control effects. Since different release sequences may increase the risk of interspecific competition and reduce the efficiency of pest management (Sánchez-Hernández, 2020), the best way to avoid this problem is to determine the optimal release of these biological control agents. The best aphid control in this experiment was achieved by releasing A. aphidimyza for 8 days followed by A. gifuensis treatment (FAAG). However, despite our initial exploration of optimal release methods based on the biology of the two natural enemies, the FAAG treatments in this experiment were not necessarily optimal for them. Therefore, future experiments will continue to explore in depth, including release time, appropriate release ratio, release interval, and improvement of aphid fly and aphid coccinellid wasp acclimatization in the field.

Acknowledgments: We thank the Zunyi Natural Enemy Insect Breeding Center for experimental conditions.This research work was supported by Zunyi Branch Tobacco Company (Project: 2020xm05; 2021520300200081; 2022XM11; 2022520300270188), and the Guizhou Province Science and Technology Innovation Talent Team Project (Qian Ke He Pingtai Rencai–CXTD [2021]004).

Author Contributions: Conceptualization, Y.-X. F., X. W., X.-X. S., M.-F. Y.; methodology, X.-F. Y., X. W., M.-F. Y., C.-Y. H.; software, X. W., X.-X. S; investigation, Y.-X. F., X. W., X.-X. S, H.-Z. W; data curation: Y.-X. F., X. W.; writing-original draft preparation, Y.-X. F., X. W.; writing—review and editing, M.-F.Y., C.-Y. H.; Supervision: M.-F. Y. and C.-Y. H.; project administration: M.-F. Y., G.-J. Y.; funding acquisition: Y.-X. F., M.-F. Y., G.-J. Y., W.-H. Z. All authors have read and agreed to the published version of the manuscript.

Availability of data and materials: The datasets used and/or analyzed during the study are available from the corresponding author on reasonable request.

Ethics approval and consent to participate: Not applicable.

Consent for publication: The authors consent for publication.

Conflict of interest: The authors declare no conflict of interest.

Data availability:Data are available from the first author on reasonable request.

Agarwala BK, Bardhanroy P, Yasuda H, Takizawa T (2003) Effects of conspecific and heterospecific competitors on feeding and oviposition of a predatory ladybird: a laboratory study. Entomol Exp Appl 106 (3):219-226. https://doi.org/10.1046/j.1570-7458.2003.00021.x
Aigbedion-Atalor PO, Hill MP, Ayelo PM, Ndlela S, Zalucki MP, Mohamed SA (2021) Can the combined use of the mirid predator Nesidiocoris tenuis and a braconid larval endoparasitoid Dolichogenidea gelechiidivoris improve the biological control of Tuta absoluta?. InSects 12:1004-1016. https://doi.org/10.3390/insects12111004
Almohamad R, Hance T (2014) Encounters with aphid predators or their residues impede searching and oviposition by the aphid parasitoid Aphidius ervi (Hymenoptera: Aphidiinae). Insect Sci 21:181-188. https://doi.org/10.1111/1744-7917.12037
Almohamad R, Verheggen FJ, Haubruge E (2009) Searching and oviposition behavior of aphidophagous hoverflies (Diptera: Syrphidae): A review. Biotechnol Agron Soc 13:467-481. https://api.semanticscholar.org/CorpusID:55400601
Almohamad R, Verheggen FJ, Francis F, Hance T, Haubruge E (2008) Discrimination of parasitized aphids by a hoverfly predator: Effects on larval performance, foraging, and oviposition behavior. Entomol Exp Appl 128(1):73-80. https://doi.org/10.1111/j.1570-7458.2007.00664.x
Amiri-Jami AR, Sadeghi H, Gilbert F, Moravvej G, Asoodeh A (2016) Oviposition preference of aphidophagous hoverflies toward oviposition site quality: The presence of intra- and interspecific competitor, glucosinolate content, and prey species. J Asia-Pac Entomol 19(2):275-280. https://doi.org/10.1016/j.aspen.2016.02.002
Aparicio Y, Gabarra R, Arno J (2020) Interactions among Myzus persicae, predators and parasitoids may hamper biological control in Mediterranean peach orchards. Entomol Gen 40(3):217-228. https://doi.org/10.1127/entomologia/2020/0946
Bass C, Puinean AM, Zimmer CT, et al (2014) The evolution of insecticide resistance in the peach potato aphid, Myzus persicae. Insect Biochem Mol Biol 51:41-51. https://doi.org/10.1016/j.ibmb.2014.05.003
Battaglia D, Pennacchio F, Romano A Tranfaglia A (1995) The role of physical cues in the regulation of host recognition and acceptance behavior of Aphidius ervi Haliday (Hymenoptera: Braconidae). J Insect Behav 8(6):739-750. https://doi.org/10.1007/BF02009503
Bouagga S, Urbaneja A, Perez-Hedo M (2018) Combined use of predatory mirids with Amblyseius swirskii (Acari: Phytoseiidae) to enhance pest management in sweet pepper. J Econ Entomol 111(3):1112-1120. https://doi.org/10.1093/jee/toy072
Boulanger FX, Jandricic S, Bolckmans K, Wackers FL, Pekas A (2019) Optimizing aphid biocontrol with the predator Aphidoletes aphidimyza, based on biology and ecology. Pest Manag Sci 75(6):1479-1493. https://doi.org/10.1002/ps.5270
Briggs CJ, Borer ET (2005) Why short-term experiments may not allow long-term predictions about intraguild predation. Ecol Appl 15(4):1111-1117. https://doi.org/10.1890/04-1776
Cabello T, Bonfil F, Gallego JR, Fernandez FJ, Gamez M, Garay J (2015) Can interactions between an omnivorous hemipteran and an egg parasitoid limit the level of biological control for the tomato pinworm?. Environ Entomol 44:12-26. https://doi.org/10.1093/ee/nvu017
Cardinale BJ, Harvey CT, Gross K, Ives AR (2003) Biodiversity and biocontrol: Emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem. Ecol Lett 6:857-865. https://doi.org/10.1046/j.1461-0248.2003.00508.x
Chailleux A, Bearez P, Pizzol J, Amiens-Desneux E, Ramirez-Romero R, Desneux N (2013) Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest Tuta absoluta. J Pest Sci 86(6):533-541. https://doi.org/10.1007/s10340-013-0498-6
Chailleux A, Droui A, Bearez P, Desneux N (2017) Survival of a specialist natural enemy experiencing resource competition with an omnivorous predator when sharing the invasive prey Tuta absoluta. Ecol. Evol 7(1):8329-8337. https://doi.org/10.1002/ece3.3396
Chesson J (1983) The estimation and analysis of preference and its relatioship to foraging models. Ecology 64(5):1297–1304. https://doi.org/10.2307/1937838
Choi M, Roitberg BD, Shani A, Raworth DA, Lee G (2004) Olfactory response by the aphidophagous gall midge, Aphidoletes aphidimyza to honeydew from green peach aphid, Myzus persicae. Entomol Exp Appl 111(1):37-42. https://doi.org/10.1111/j.0013-8703.2004.00151.x
Coelho RS, Pec M, Rodrigues Silva AL, Penaflor MFGV, Marucci RC (2022) Predation potential of the earwig Euborellia annulipes on fruit fly larvae and trophic interactions with the parasitoid Diachasmimorpha longicaudata. J Appl Entomol 147(2):147-156. https://doi.org/10.1111/jen.13091
Craig TP, Itami JK, Price PW (1989) A strong relationship between oviposition preference and larval performance in a shoot-galling sawfly. Ecology 70(6):1691-1699. https://doi.org/10.2307/1938103
de Azevedo AGC, Stuart RM, Sigsgaard L (2018) Presence of a generalist entomopathogenic fungus influences the oviposition behaviour of an aphid-specific predator. Biocontrol 63(5):655-664. https://doi.org/10.1007/s10526-018-9889-1
Doker I, Revynthi AM, Kazak C, Carrillo D (2021) Interactions among exotic and native phytoseiids (Acari: Phytoseiidae) affect biocontrol of two-spotted spider mite on papaya. Biol Control 163(1):104758. https://doi.org/10.1016/j.biocontrol.2021.104758
Fréchette B, Dixon A, Alauzet C, Boughenou N, Hemptinne JL (2006) Should aphidophagous ladybirds be reluctant to lay eggs in the presence of unsuitable prey?. Entomol Exp Appl 118(2):121-127. https://doi.org/10.1111/j.1570-7458.2006.00366.x
Fréchette B, Rojo S, Alomar O, Lucas R (2007) Intraguild predation between syrphids and mirids: Who is the prey? Who is the predator?. Biocontrol 52:175-191. 10.1007/s10526-006-9028-2
Gou JY, Wang XQ, Huang CY, Wang XY, Liu MH, Li B et al (2020) Research on the oviposition selection of Aphidoletes aphidimyza (Rondani). Chn Plant Prot 40(6):5-10. https://kns.cnki.net
Hassanzadeh-Avval M, Sadeghi-Namaghi H, Fekrat L (2018) Prey preference and prey switching in Anthocoris minki Dohrn (Hemiptera: Anthocoridae). J Asia-Pac Entomol 21(4):1116-1121. https://doi.org/10.1016/j.aspen.2018.08.007
Holt RD, Polis GA (1997) A theoretical framework for intraguild predation. Am Nat 149(4):745-764. https://doi.org/10.1086/286018
Humphreys RK, Ruxton GD (2018) Dropping to escape: A review of an under-appreciated antipredator defence. Biol Rev 94:575-589. https://doi.org/10.1111/brv.12466
Janssen A, Montserrat M, HilleRisLambers R, Roos AMD, Sabelis MW (2006) Intraguild predation usually does not disrupt biological control. Progress in Biological Control 3:21-44. https://doi.org/10.1007/1-4020-4767-3_2
Jonsson M, Kaartinen R, Straub CS (2017) Relationships between natural enemy diversity and biological control. Curr Opin Insect Sci 20:1-6. https://doi.org/10.1016/j.cois.2017.01.001
Kryukov VY, Chernyak EI, Kryukova N et al (2022) Parasitoid venom alters the lipid composition and development of microorganisms on the wax moth cuticle. Entomol Exp Appl 170(10):852-868. https://doi.org/10.1111/eea.13219
Kutuk H, Yigit A, Alaoglu O (2011) Intraguild predation of Serangium parcesetosum (Coleoptera: Coccinellidae), on whitefly Bemisia tabaci (Homoptera: Aleyrodidae) parasitized by Eretmocerus mundus (Hymenoptera: Aphelinidae). Biocontrol Sci Techn 21(8):985-989. https://doi.org/10.1080/09583157.2011.590880
Lebreton S, Christides JP, Bagneres AG, Chevrier C, Darrouzet E (2010) Modifications of the chemical profile of hosts after parasitism allow parasitoid females to assess the time elapsed since the first attack. J Chem Ecol 36(5):513-521. https://doi.org/10.1007/s10886-010-9781-7
Liu JF, Wang XQ, Beggs JR, Ou HD, Yu XF, Shen XX et al (2020) Consuming parasitized aphids alters the life history and decreases predation rate of aphid predator. InSects 11(12): 889. https://doi.org/10.3390/insects11120889
Manly B (1974) A model for certain types of selection experiments. Biometrics 30(2): 281–294. https://doi.org/10.2307/2529649
Margaritopoulos JT, Kati AN, Voudouris CC, Skouras PJ, Tsitsipis JA (2020) Long-term studies on the evolution of resistance of Myzus persicae (Hemiptera: Aphididae) to insecticides in Greece. B Entomol Res 111(1):1-16. https://doi.org/10.1017/S0007485320000334
Martinou AF, Raymond B, Milonas PG, Wright DJ (2010) Impact of intraguild predation on parasitoid foraging behaviour. Ecol Entomol 35(2):183-189. https://doi.org/10.1111/j.1365-2311.2009.01171.x
Meisner M, Harmon JP, Harvey CT, Ives AR (2011) Intraguild predation on the parasitoid Aphidius ervi by the generalist predator Harmonia axyridis: The threat and its avoidance. Entomol Exp Appl 138(3):193-201. https://doi.org/10.1111/j.1570-7458.2010.01090.x
Messelink GJ, Bloemhard CMJ, Cortes JA, Sabelis MW, Janssen A (2011) Hyperpredation by generalist predatory mites disrupts biological control of aphids by the aphidophagous gall midge Aphidoletes aphidimyza. Biol Control 57(3):246-252. https://doi.org/10.1016/j.biocontrol.2011.02.013
Messelink GJ, Bloemhard CMJ, Sabelis MW, Janssen A (2013) Biological control of aphids in the presence of thrips and their enemies. Biocontrol 58(1):45-55. https://doi.org/10.1007/s10526-012-9462-2
Mohammadpour M, Hosseini M, Karimi J, Hosseininaveh V (2019) Effect of age-dependent parasitism in eggs of Tuta absoluta (Lepidoptera: Gelechiidae) on intraguild predation between Nabis pseudoferus (Hemiptera: Nabidae) and Trichogramma brassicae (Hymenoptera: Trichogrammatidae). J Insect Sci 19(3):27-33. https://doi.org/10.1093/jisesa/iez040
Mohammadpour M, Hosseini M, Michaud JP, Karimi J, Hosseininaveh V (2020) The life history of Nabis pseudoferus feeding on Tuta absoluta eggs is mediated by egg age and parasitism status. Biol Control 151:104401. https://doi.org/10.1016/j.biocontrol.2020.104401
Mohl EK, Stenoien CM, Heimpel GE (2020) The effects of host plant species on adult oviposition and larval performance of the aphid predator Aphidoletes aphidimyza. Ecol Entomol 45:606-616. https://doi.org/10.1111/een.1283
Moral RA, Hinde J, Demetrio CGB (2017) Half-Normal plots and overdispersed models in R: The hnp package. J Stat Softw 81(10):1-23. https://doi.org/10.18637/jss.v081.i10
Nakashima Y, Birkett MA, Pye BJ, Pickett JA, Powell W (2004) The role of semiochemicals in the avoidance of the seven-spot ladybird, Coccinella septempunctata, by the aphid parasitoid, Aphidius ervi. J Chem Ecol 30(6):1103-1116. https://doi.org/10.1023/B:JOEC.0000030266.81665.19
Naranjo SE (2007) Intraguild predation on Eretmocerus sp nr emiratus, a parasitoid of Bemisia tabaci, by three generalist predators with implications for estimating the level and impact of parasitism. Biocontrol Sci Techn 17(6):605-622. https://doi.org/10.1080/09583150701408816
Peckarsky BL, Taylor BW, Caudill CC (2000) Hydrologic and behavioral constraints on oviposition of stream insects: Implications for adult dispersal. Oecologia 125(2):186-200. https://doi.org/10.1007/s004420000446
Pehlivan S, Kurtulus A, Alinc T, Atakan E (2017) Intraguild predation of Orius niger (Hemiptera: Anthocoridae) on Trichogramma evanescens (Hymenoptera: Trichogrammatidae). Eur J Entomol 114(1):609-613. https://doi.org/10.14411/eje.2017.074
Pineda A, Morales I, Marcos-García MA, Fereres A (2007) Oviposition avoidance of parasitized aphid colonies by the syrphid predator Episyrphus balteatus mediated by different cues. Biol Control 42(3):274-280. https://doi.org/10.1016/j.biocontrol.2007.05.017
Pirzadfard S, Zandi-Sohani N, Sohrabi F, Rajabpour A (2020) Intraguild interactions of a generalist predator, Orius albidipennis, with two Bemisia tabaci parasitoids. Int J Trop Insect Sci 40(2):259-265. https://doi.org/10.1007/s42690-019-00075-w
Prieto JD, Trotta V, Nardo ED, Forlano P, Fanti P, Battaglia D (2018) Intraguild predation between Macrolophus pygmaeus and Aphidius ervi. B Insectol 71(1):113-120. https://api.semanticscholar.org/CorpusID:90737688
Rasool B, Mehmood Z, Ahmad MF, Iqbal J, Younis T, Munir R (2022) Host instars preference, density-dependent parasitism and behavioral perspective of parasitoids (Aphidius colemani, Aphidius matricariae and Aphelinus abdominalis) in Aphis glycines and Aphis gossypii. Rev Bras Entomol 66(1): e20210045. https://doi.org/10.1590/1806-9665-rbent-2021-0045
Russel RJ (1972) Defensive responses of the aphid Drepanosiphum platanoides in encounters with the bug Anthocoris Nemorum. Oikos 23(2):264-267. https://doi.org/10.2307/3543415
Ruxton GD (2000) The differing effects of interference on individuals of different rank. Ecol Lett 2(1):4-5. https://doi.org/10.1046/j.1461-0248.1999.21047.x
Sadeghi H, Gilbert F (2001) Aphid suitability and its relationship to oviposition preference in predatory hoverflies. J Anim Ecoly 69(5):771-784. https://doi.org/10.1046/j.1365-2656.2000.00433.x
Sánchez-Hernández C, Desneux N, Bao-Fundora L, Ramirez-Romero R (2020) Alternative extraguild prey modifies focal extraguild prey consumption and parasitism but not intraguild predation intensity. Biol Control 153:104475. https://doi.org/10.1016/j.biocontrol.2020.104475
Sentis A, Lucas E, Vickery WL (2012) Prey abundance, intraguild predators, ants and the optimal egg-laying strategy of a furtive predator. J Insect Behav 25(6):529-560. https://doi.org/10.1007/s10905-012-9320-1
Shrestha G, Skovgard H, Steenberg T, Enkegaard A (2015) Preference and life history traits of Aphelinus abdominalis (Hymenoptera: Aphelinidae) when offered different development stages of the lettuce aphid Nasonovia ribisnigri (Hemiptera: Aphididae). Biocontrol 60(4):463-471. https://doi.org/10.1007/s10526-015-9661-8
Snyder WE, Ballard SN, Yang S, Clevenger GM, Miller TD, Ahn JJ et al (2004) Complementary biocontrol of aphids by the ladybird beetle Harmonia axyridis and the parasitoid Aphelinus asychis on greenhouse roses. Biol Control 30(2):229-235. https://doi.org/10.1016/j.biocontrol.2004.01.012
Stasek DJ, Radl JN, Crist TO (2018) The functional response and prey preference of generalist Nabis (Hemiptera: Nabidae) predators to leafhopper prey (Hemiptera: Cicadellidae). Can Entomol 150(2):190-200. https://doi.org/10.4039/tce.2017.68
Tena A, Senft M, Desneux N, Dregni J, Heimpel GE (2018) The influence of aphid-produced honeydew on parasitoid fitness and nutritional state: A comparative study. Basic Appl Ecol 29:55-68. https://doi.org/10.1016/j.baae.2018.04.003
Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47(1):3-14. https://doi.org/10.1007/BF00186709
Toosi M, Rasekh A, Osawa N (2019) Effects of intraguild predation on the life history traits and progeny of the ladybird beetle Hippodamia variegate. B Insectol 72(2):161-168. https://api.semanticscholar.org/CorpusID:204867229
Vance-Chalcraft HD, Rosenheim JA, Vonesh JR, Osenberg CW, Sih A (2007) The influence of intraguild predation on prey suppression and prey release: A meta-analysis. Ecology 88(11):2689-2696. https://doi.org/10.1890/06-1869.1
Velasco-Hernandez MC, Desneux N, Ramirez-Martinez MM, Cicero L, Ramirez-Romero R (2017) Host species suitability and instar preference of Aphidius ervi and Aphelinus abdominalis. Entomol Gen 36(4):347-367. https://doi.org/10.1127/entomologia/2017/0500
Wäckers FL, van Rijn PCJ, Heimpel GE (2008) Honeydew as a food source for natural enemies: Making the best of a bad meal?. Biol Control 45(2):176-184. https://doi.org/10.1016/j.biocontrol.2008.01.007
Wang XQ, Wang XY, Yu XF, Huang CY, Shen XX, Yang XC et al (2019) Morphological ontogeny of Aphidoletes aphidimyza (Rondani). Chn J Appl Entomol 56(4):832-839. https://doi.org/10.7679/j.issn.20951353.2019.097
Wilby A, Villareal SC, Lan LP, Heong KL, Thomas MB (2005) Functional benefits of predator species diversity depend on prey identity. Ecol Entomol 30(5):497-501. https://doi.org/10.1111/j.0307-6946.2005.00717.x
Xia PL, Yu XL, Li ZT, Feng Y (2021) The impacts of Harmonia axyridis cues on foraging behavior of Aphidius gifuensis to Myzus persicae. J Asia-Pac Entomol 24(1):278-284. https://doi.org/10.1016/j.aspen.2020.12.008
Xu Y, Gray SM (2020) Aphids and their transmitted potato viruses: A continuous challenges in potato crops. J Integr Agric 19(2):367-375. https://doi.org/10.1016/S2095-3119(19)62842-X
Xue Y, Bahlai CA, Frewin A et al (2012) Intraguild predation of the aphid parasitoid Aphelinus certus by Coccinella septempunctata and Harmonia axyridis. Biocontrol 57(5):627-634. https://doi.org/10.1007/s10526-012-9439-1
Yang S, Yang SY, Zhang CP, Wei JN, Kuang RP (2009) Population dynamics of Myzus persicae on tobacco in Yunnan Province, China, before and after augmentative releases of Aphidius gifuensis. Biocontrol Sci Techn 19(2):219-228. https://doi.org/10.1080/09583150802696525
Yasuda H, Takagi T, Kogi K (2000) Effects of conspecific and heterospecific larval tracks on the oviposition behaviour of the predatory ladybird, Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 97 (4):551–553. https://doi.org/10.14411/eje.2000.085
Yazdani M, Feng Y, Glatz R, Keller MA (2015) Host stage preference of Dolichogenidea tasmanica (Cameron, 1912) (Hymenoptera: Braconidae), a parasitoid of Epiphyas postvittana (Walker, 1863) (Lepidoptera: Tortricidae). Austral Entomol 54(3):325-331. https://doi.org/10.1111/aen.12130
Yu XL, Feng Y, Feng ZJ et al (2019) Effects of mummy consumption on fitness and oviposition site selection on Harmonia axyridis. Insect Sci 27(5):1-10. https://doi.org/10.1111/1744-7917.12724
Zhang J, Zhang LS, Chen HY, Li YY, Liu Y (2014) Screening host aphids for mass rearing of Aphidius gifuensis (Hymenoptera: Aphidiidae). Chn J Biol Control 30(1):32-37. https://doi.org/10.3969/j.issn.2095-039X.2014.01.005.

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Oviposition selection, prey preference and release strategies enhance the combined aphid control effects of Aphidoletes aphidimyza and Aphidius gifuensis

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Abstract

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Introduction

Materials and methods

Plant material and insect rearing

Acquisition of different instar aphid nymphs and parasitized aphids

Oviposition site selection by Aphidoletes aphidimyza and Aphidius gifuensis

Preference experiment

Greenhouse experiment

Statistical analysis

Results

Oviposition site selection by Aphidoletes aphidimyza and Aphidius gifuensis

Preference experiment

greenhouse experiment

Discussion

Declarations

References

Additional Declarations

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Version 1