Influence of Cold Exposure for Different Durations on Laboratory-Reared Habrobracon hebetor (Say) (Hymenoptera: Braconidae)
Henan Collaborative Innovation Center for Grain Storage Security, School of Food and Strategic Reserves, Henan University of Technology, Zhengzhou 450001, China
*
Author to whom correspondence should be addressed.
Diversity 2025, 17(4), 253; https://doi.org/10.3390/d17040253
Submission received: 2 February 2025
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Revised: 27 March 2025
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Accepted: 28 March 2025
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Published: 31 March 2025
(This article belongs to the Special Issue Integrated Pest Management and Its Role in Biodiversity Conservation)
Abstract
:Biological control by releasing a large number of parasitoids has been an effective strategy for coping with stored-product pest insects. Habrobracon hebetor (Say) (Hymenoptera: Braconidae) has strong control capabilities over Lepidoptera pests. Exploring the optimum storage temperature, life stage, and cold storage period of H. hebetor is of great importance for the utilization of parasitoids. In this context, the survival, parasitism, and fecundity of H. hebetor were evaluated after 10, 20, 30, 40, 50, and 60 d of exposure at −5, 0, 5, 10, and 15 °C for H. hebetor eggs, larvae, pupae, and adults, and the survival, parasitism, and fecundity of H. hebetor individuals that had been maintained at normal rearing condition were taken as a control. The cold exposure duration dramatically affected the development and survival of eggs, larvae, and pupae of H. hebetor, regardless of the temperatures tested. Habrobracon hebetor eggs, larvae, and pupae failed to develop into the next life stage at −5, 0, and 5 °C. Habrobracon hebetor eggs, larvae, pupae, and adults failed to survive after 10 d exposure at −5 and 0 °C. The parasitism rate, fecundity and oviposition duration of H. hebetor adults that originated from eggs, larvae, pupae, and adults after different cold storage durations markedly decreased with increasing cold storage duration. The highest parasitism rate of adults was 34.12% after exposure at 5 °C for 10 d, which was not significantly different from the control (31.86%). The maximum level of egg production of H. hebetor adults developed from initial larvae exposed at 15 °C for 10 d and 20 d were 344.67 and 340.67 eggs/female, respectively, which were not significantly different from the control (392.00 eggs/female). When H. hebetor larvae were stored at 15 °C for 10 and 60 d, the oviposition duration of newly emerged adults reached the maximum and minimum levels recorded, with 17.00 and 0.83 d, respectively. These results provide empirical support for the large-scale production and storage of H. hebetor.
1. Introduction
Augmentative release of parasitic wasps has been an important strategy for coping with stored-product pest insects [1]. In this context, the parasitic wasps must be produced shortly before release due to their relatively short life, which inevitably increases the rearing cost of natural enemies and biological control costs [2]. Cold storage may be a useful strategy to store natural enemies on a large scale and for long intervals [3], which ensures a stable supply of sufficient and high quality parasitic wasps whenever they are needed.
Habrobracon hebetor (Say) (Hymenoptera: Braconidae) can effectively parasitize many species of Lepidoptera pests that attack stored cereals, beans, oilseeds, dried fruits, and medicinal materials [4,5,6,7,8]. Several studies have reported the influence of cold exposure on H. hebetor lifespan and fertility. The survival of H. hebetor pupae decreases when stored at 4 °C for more than 20 d [9]. Habrobracon hebetor pupae can be maintained for 15 d at 4 °C and 80% relative humidity [10]. The adults can be stored at 8 °C for approximately 2 months [11]. Storing pupae at 5 ± 1 °C for more than 30 d results in reducing the parental parasitism, but has no impact on their offspring parasitism [12]. A small number of adults of H. hebetor die or have deformed wings when stored at 10 °C for more than 30 d. The proportion of newly emerged adults with wing deformities increases after 40 d of cold storage of pupae [13]. When reared and stored at 20 °C for 8 weeks or less, the wasp’s developmental duration, survival, and parasitism ability are similar to those of individuals that were reared at 30 °C [14].
To date, most studies have focused on the effects of cold storage on H. hebetor pupae or adults, but there is little research on the performance of eggs and larvae after cold storage. Thus, the purpose of this research was to explore the survival, emergence, parasitism, and oviposition duration of H. hebetor over a range of exposure intervals and low temperatures for different life stages of the parasitoid. The optimal cold storage temperature, storage duration, and life stage were evaluated, in order to provide the inferences necessary for the large-scale production and release protocols of H. hebetor.
2. Materials and Methods
2.1. Experimental Insects
The Ephestia elutella (Lepidoptera: Pyralidae) and H. hebetor colonies have been maintained in the Stored-products Insect Control Laboratory in Henan University of Technology for more than 5 years. Ephestia elutella late-instar larvae were supplied to rear H. hebetor. Ephestia elutella was reared on a diet (50% wheat bran, 30% corn grit, 10% soybean powder, 5% glycerol, and 5% honey water) at 30 ± 2 °C, 75 ± 5% relative humidity (RH), and 12 h:12 h (Light:Dark). To obtain E. elutella late-instar larvae as hosts for raising H. hebetor, approximately three hundred newly emerged moths were transferred to 100 g rearing diet for 1 d, then the moths were removed, and the diet was maintained in a culture chamber for 33 d at rearing conditions mentioned above.
Five pairs of H. hebetor adults (1-d-old, female:male = 1:1) were released into one plastic box (top diameter: 7.3 cm, bottom diameter: 5.5 cm, and height: 3.5 cm) containing 25 late-instar E. elutella larvae. Then, the H. hebetor adults were removed from the plastic box after 24 h. There were 3–6 eggs on each E. elutella larva. The eggs were maintained for 2, 5, and 10 d at rearing conditions mentioned above. Eggs, larvae and pupae of the parasitoid on E. elutella larvae, and H. hebetor adults used in the experiments were 1, 2, 3, and 1-d old, respectively. Eggs (1-d old) of the parasitoid were obtained within 1 d after H. hebetor laided eggs on E. elutella larvae. The larvae of the parasitoid were obtained after H. hebetor eggs had hatched on E. elutella larvae for 2 d. The pupae of the parasitoid were obtained after H. hebetor larvae had pupated on E. elutella larvae for 3 d. The adults of the parasitoid were obtained after H. hebetor pupae had emerged on E. elutella larvae for 1 d. The wasp takes 11.94 ± 0.02 d to complete its life cycle at 30 °C. Habrobracon hebetor larvae lived on the host. The life stages of the host larvae were determined by the number of molts.
2.2. Cold Storage Procedure for H. hebetor
Thirty H. hebetor eggs, larvae, and pupae on E. elutella larvae, female and male adults were randomly selected, respectively, and placed in plastic boxes (top diameter: 6.6 cm, bottom diameter: 5.4 cm, height: 3.8 cm). Then, the plastic boxes were maintained at −5, 0, 5, 10, and 15 °C, 75 ± 5% RH, and 0 h:24 h (Light:Dark) for 10, 20, 30, 40, 50, and 60 d, respectively. Their life stage and survival were observed after the termination of different cold exposure durations, respectively. After cold exposure durations, all life stages of H. hebetor were maintained at rearing conditions mentioned above, and the newly emerged adults were counted. Each mated female wasp was offered daily 50 host larvae until it died. The paralyzed host larvae, and the eggs laid by the female wasps and their oviposition duration were counted and recorded. The survival, emergence, parasitism, and oviposition duration of H. hebetor individuals that had been maintained at normal rearing condition were taken as a control. Each experimental treatment was repeated three times. All experimental treatments (5 temperatures × 4 life stages × 6 storage durations = 120 treatment combinations) were tested three times at the same time each.
2.3. Statistics
The number of eggs laid by H. hebetor was converted by log10(x + 1) scale. The percentages of survival and parasitism of H. hebetor were converted to arcsine square-root values. Three-way ANOVA analysis with temperature, insect life stage, cold exposure duration as fixed variables was applied to compare the differences among different experimental treatments. The assumptions of data normality were checked before statistics. Repeated measures analysis of variance was conducted by SPSS23.0. A minimum value (0.001) was assigned to each zero value before analysis.
Habrobracon hebetor survival rate and parasitism rate were calculated using the following formulas:
Survival rate (%) = (the total number of newly emerged adult H. hebetor or live adult H. hebetor after cold exposure/The total number of initial H. hebetor individuals at the beginning of cold exposure) × 100
Parasitism rate (%) = (the number of parasitized E. elutella late-instar larvae with eggs/The total number of initial E. elutella late-instar larvae) × 100
3. Results
3.1. Impacts of Different Low-Temperature Exposure Durations on Different Life Stages of H. hebetor
The different low-temperature exposure durations markedly affected the development of H. hebetor (Table 1). The eggs of H. hebetor could not develop into larvae at −5, 0, 5, and 10 °C, but they did develop into larvae and pupae after 10 d and 50 d of exposure at 15 °C, respectively. The H. hebetor larvae could not develop into pupae at −5, 0, and 5 °C, but they did develop into pupae after 20 d and 10 d of cold storage at 10 and 15 °C, respectively. The pupae of H. hebetor could not develop into adults at −5, 0, and 5 °C, but they did develop into adults after 50 d of cold storage at 10 and 15 °C.
3.2. Impacts of Different Low-Temperature Exposure Durations on Survival of Different Life Stages of H. hebetor
The survival rate of H. hebetor significantly decreased with increasing cold storage durations (df = 5, 240; F = 0.65; p < 0.01; Table 2). The eggs, larvae, pupae, and adults of H. hebetor died when stored at −5 and 0 °C for more than 10 d. Moreover, the eggs of H. hebetor also died after of 10 d of exposure at 5 and 10 °C. Female adults of H. hebetor could not survive after of 10 d of cold storage at 5 °C. The maximum survival rates of H. hebetor were 18.33% (exposure at 15 °C for 10 d for eggs), 32.50% (exposure at 15 °C for 10 d for larvae), 48.33% (exposure at 15 °C for 10 d for pupae), 92.50% (exposure at 15 °C for 20 d for female), and 34.17% (exposure at 5 °C for 10 d for male).
3.3. Impacts of Different Low-Temperature Exposure Durations on the Parasitism Rate of H. hebetor
The parasitism rate of H. hebetor adults originated from initial eggs, larvae, pupae, and adults after different cold storage durations significantly decreased with increasing cold storage durations (df = 5, 240; F = 2.39; p = 0.02; Table 3). The highest parasitism rate of H. hebetor adults originated from initial eggs (cold storage at 15 °C for 20 d), larvae (cold storage at 15 °C for 20 d), and pupae (cold storage at 15 °C for 10 d) were 22.72%, 29.73%, and 22.20%, respectively. The highest parasitism rates of H. hebetor adults after cold storage at 5 °C and 10 °C for 10 d were 34.12% and 30.44%, respectively, which were not significantly different from the control (31.86%).
3.4. Impacts of Different Low-Temperature Exposure Durations on Egg Production of H. hebetor
The fecundity of H. hebetor adults originated from initial eggs, larvae, pupae, and adults after different cold storage durations significantly decreased with increasing cold storage duration (df = 5, 240; F = 1.08; p < 0.01). The egg production of H. hebetor adults developed from initial eggs reached its maximum level (195.67 eggs/female) at 15 °C for 20 d exposure (Table 4). Also, the maximum level of egg production of H. hebetor adults developed from initial larvae exposed at 15 °C for 10 d and 20 d were 344.67 and 340.67 eggs/female, respectively, which were not significantly different from the control (392.00 eggs/female).
3.5. Impacts of Different Low-Temperature Storage Durations on Oviposition Duration of H. hebetor
The oviposition duration of H. hebetor adults originated from initial eggs, larvae, pupae, and adults after different cold storage durations significantly decreased with increasing cold storage times (df = 5, 240; F = 7.71; p < 0.01; Table 5). When the eggs of H. hebetor were stored at 15 °C for 10 to 50 d, the oviposition duration of newly emerged H. hebetor adults ranged from 4.33 d to 15.67 d. When the larvae of H. hebetor were stored at 15 °C for 10 to 60 d, the oviposition duration of newly emerged H. hebetor adults ranged from 0.83 d to 17.00 d. When the pupae of H. hebetor were stored at 15 °C for 10 and 60 d, the oviposition duration of newly emerged H. hebetor adults ranged from 1.00 d to 15.67 d. In general, the maximum oviposition duration of H. hebetor adults originated from eggs, larvae, and pupae after different cold storage durations were 15.67, 17.00, and 16.00 d, respectively, but there were no significant differences from the control (15.00 d).
4. Discussion
Low-temperature storage is a useful method for mass production and application of H. hebetor [15]. The current research results showed that the insect life stage, temperature and period of low-temperature storage had remarkable effects on H. hebetor development, parasitism ability and egg production. Habrobracon hebetor eggs, larvae, pupae, and adults should not be stored at −5, 0, and 5 °C. When stored at or below 10 °C for more than 10 d, the eggs of H. hebetor could not survive, which is similar to the research results of Huang (1990) [16]. The current research results showed that H. hebetor larvae were more suitable for cold storage than pupae. The survival rate of pupae of H. hebetor significantly decreased after 10 d of cold storage at 5 °C, which is similar to previous results [9,17], indicating that pupa is not the best life stage for cold storage. Meanwhile, prolonged low-temperature exposure of H. hebetor pupae results in increasing proportion of adult developmental abnormalities [13]. Male adults of H. hebetor are extremely sensitive to low temperatures, and all of them die after more than 60 d cold storage at 10 °C [18]. The cold storage time of H. hebetor adults should not exceed 20 d, which significantly reduce the survival rate and egg production of H. hebetor, which is consistent with previous research findings [10,19,20]. Increasing cold storage time negatively affects the survival rate of each life stage of H. hebetor at 12 °C [20]. This current study showed that all of H. hebetor died after 20 d of cold exposure at temperatures below 5 °C. This is different from Chen et al. (2011) [19]. They found that storing H. hebetor adults at 5 °C for 20 d had no any adverse effects on lifespan and fecundity. Meanwhile, the favorable cold storage condition for adult H. hebetor was 10 °C or higher. This is also different from Seyahooei et al. (2018) [21], who found that 5 °C was favorable for H. hebetor cold storage. The differences may be attributed to different strains of the parasitoid and specific experimental conditions used in different studies.
In addition, storing H. hebetor adults at 5 °C for 10 d had no harmful impacts on their parasitism and egg production. If the parasitoid is gradually acclimated at low temperatures, it may effectively improve their performance after cold exposure [22]. Meanwhile, the host and other nutrients were not provided for H. hebetor adults during the cold storage in the present study. Thus, it deserves to further investigate whether providing nutrients can improve the parasitoid’s performances after low-temperature storage, as it has been already proven in the case of other studies [23,24]. Additionally, diapause is an effective technique to boost chilling adaptation ability of parasitoids [25,26]. Storing diapausing females of H. hebetor at 5 °C for 8 weeks can successfully maintain their performance [27]. Meanwhile, the highest parasitism rates of H. hebetor adults after cold storage at 5 °C and 10 °C for 10 d were 34.12% and 30.44% in this study, respectively, which were similar to the control (31.86%). The potential reasons for why the parasitism rate of H. hebetor adults is better but survival is worse still deserve to be further investigated.
5. Conclusions
Cold exposure significantly decreased H. hebetor survival and development. H. hebetor parasitism rate, fecundity and oviposition duration substantially decreased with increasing cold exposure duration. Mass rearing protocols should be notably mediated according to life stage at storage. In view of the overall results, the following optimum parameters were found for H. hebetor with regard to life stage, cold storage temperature and cold storage duration: larvae at 15 °C for 20 days. These results are in favor of the large-scale artificial breeding and application of H. hebetor in practice.
Author Contributions
Conceptualization, J.L., C.B., W.L. and Y.G.; methodology, J.L., C.B., W.L., Y.G. and Y.Y.; software, Y.G. and W.L.; validation, Y.G., W.L. and Y.Y.; formal analysis, Y.G., W.L. and Y.Y.; investigation, Y.G., W.L. and Y.Y.; resources, J.L. and C.B.; writing—original draft preparation, J.L., C.B., W.L., Y.G. and Y.Y.; writing—review and editing, J.L., C.B., W.L., Y.G. and Y.Y.; supervision, J.L. and C.B.; project administration, J.L. and C.B.; funding acquisition, J.L. All authors have read and agreed to the published version of this manuscript.
Funding
This work was supported by the 14th Five-Year Plan National key R & D Project (No. 2021YFD2100604).
Institutional Review Board Statement
The study did not require ethical approval, because the H. hebetor belongs to common insects.
Data Availability Statement
Data are available upon request.
Acknowledgments
The authors sincerely thank Christos G. Athanassiou from the University of Thessaly, Greece for reviewing the previous version of this manuscript.
Conflicts of Interest
The authors have declared that no competing interests exist.
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Table 1.
The developmental stage changes in initial H. hebetor eggs, larvae, and pupae after cold storage at −5, 0, 5, 10, and 15 °C for 10, 20, 30, 40, 50, and 60 d, respectively.
Table 1.
The developmental stage changes in initial H. hebetor eggs, larvae, and pupae after cold storage at −5, 0, 5, 10, and 15 °C for 10, 20, 30, 40, 50, and 60 d, respectively.
| Initial Life Stage | Temperature (°C) | Life Stage After Cold Storage for Different Durations (d) | |||||
|---|---|---|---|---|---|---|---|
| 10 | 20 | 30 | 40 | 50 | 60 | ||
| Egg | −5 | Egg | Egg | Egg | Egg | Egg | Egg |
| 0 | Egg | Egg | Egg | Egg | Egg | Egg | |
| 5 | Egg | Egg | Egg | Egg | Egg | Egg | |
| 10 | Egg | Egg | Egg | Egg | Egg | Egg | |
| 15 | Larva | Larva | Larva | Larva | Pupa | Pupa | |
| Larva | −5 | Larva | Larva | Larva | Larva | Larva | Larva |
| 0 | Larva | Larva | Larva | Larva | Larva | Larva | |
| 5 | Larva | Larva | Larva | Larva | Larva | Larva | |
| 10 | Larva | Larva, Pupa | Larva, Pupa | Pupa | Pupa | Pupa | |
| 15 | Pupa | Pupa | Pupa | Pupa | Pupa | Pupa, Adult | |
| Pupa | −5 | Pupa | Pupa | Pupa | Pupa | Pupa | Pupa |
| 0 | Pupa | Pupa | Pupa | Pupa | Pupa | Pupa | |
| 5 | Pupa | Pupa | Pupa | Pupa | Pupa | Pupa | |
| 10 | Pupa | Pupa | Pupa | Pupa | Pupa, Adult | Adult | |
| 15 | Pupa | Pupa | Pupa | Pupa | Adult | Adult | |
Table 2.
Survival rate (%) of eggs, larvae, pupae, and adults of H. hebetor after cold storage at −5, 0, 5, 10, and 15 °C for 10, 20, 30, 40, 50, and 60 d, respectively.
Table 2.
Survival rate (%) of eggs, larvae, pupae, and adults of H. hebetor after cold storage at −5, 0, 5, 10, and 15 °C for 10, 20, 30, 40, 50, and 60 d, respectively.
| Initial Life Stage | Temperature (°C) | Cold Storage Duration (d) | |||||
|---|---|---|---|---|---|---|---|
| 10 | 20 | 30 | 40 | 50 | 60 | ||
| Egg | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 10 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 15 | 18.33 ± 3.47 eA | 9.17 ± 1.60 eB | 5.00 ± 0.97 cBC | 2.50 ± 1.60 cC | 2.50 ± 1.60 cC | 0 | |
| Larva | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 8.33 ± 2.15 fA | 5.00 ± 2.15 eA | 0 | 0 | 0 | 0 | |
| 10 | 26.67 ± 4.91 dA | 34.17 ± 4.17 cA | 9.17 ± 0.83 cB | 0 | 0 | 0 | |
| 15 | 32.50 ± 4.38 cdeA | 28.33 ± 2.15 cA | 25.00 ± 8.44 aAB | 11.67 ± 2.15 bB | 10.83 ± 3.70 bBC | 9.17 ± 5.67 aC | |
| Pupa | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 10.00 ± 4.91 fA | 5.00 ± 2.15 eB | 0 | 0 | 0 | 0 | |
| 10 | 26.67 ± 4.082 dA | 19.17 ± 1.60 dA | 20.00 ± 4.08 bA | 8.33 ± 2.15 bcB | 8.33 ± 0.96 bB | 0 | |
| 15 | 48.33 ± 7.76 bcA | 47.50 ± 7.38 bA | 27.50 ± 5.83 aB | 18.33 ± 2.15 aB | 17.50 ± 5.34 aB | 13.33 ± 3.04 aB | |
| Adult female | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 36.67 ± 8.71 cdA | 0 | 0 | 0 | 0 | 0 | |
| 10 | 58.33 ± 5.85 bA | 45.83 ± 5.83 bB | 0 | 0 | 0 | 0 | |
| 15 | 90.00 ± 2.36 aA | 92.50 ± 3.44 aA | 20.00 ± 12.25 bB | 0 | 0 | 0 | |
| Adult male | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 34.17 ± 6.44 cdA | 0 | 0 | 0 | 0 | 0 | |
| 10 | 5.83 ± 4.79 fB | 21.67 ± 2.15 dA | 0 | 0 | 0 | 0 | |
| 15 | 0 | 0 | 0 | 0 | 0 | 0 | |
| Egg | 30 (Control) | 83.89 ± 5.97 aA | |||||
| Larva | 87.87 ± 7.74 aA | ||||||
| Pupa | 94.12 ± 1.92 aA | ||||||
Note: The data are the mean ± standard error. Data followed by different lowercase letters in each column, and data followed by different capital letters in each row indicate significant difference according to Tukey’s test at p < 0.05.
Table 3.
The parasitism rates (%) of H. hebetor adults originated from initial eggs, larvae, pupae, and adults after cold storage at −5, 0, 5, 10, and 15 °C for 10, 20, 30, 40, 50, and 60 d on E. elutella late-instar larvae.
Table 3.
The parasitism rates (%) of H. hebetor adults originated from initial eggs, larvae, pupae, and adults after cold storage at −5, 0, 5, 10, and 15 °C for 10, 20, 30, 40, 50, and 60 d on E. elutella late-instar larvae.
| Initial Life Stage | Temperature (°C) | Cold Storage Duration (d) | |||||
|---|---|---|---|---|---|---|---|
| 10 | 20 | 30 | 40 | 50 | 60 | ||
| Egg | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 10 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 15 | 20.21 ± 0.67 cA | 22.72 ± 1.67 abA | 13.54 ± 1.26 bB | 0 | 0 | 0 | |
| Larva | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 12.59 ± 1.165 dA | 8.00 ± 0.33 cB | 0 | 0 | 0 | 0 | |
| 10 | 27.7 ± 1.89 bA | 21.65 ± 0.40 abA | 3.33 ± 0.71 dB | 0 | 0 | 0 | |
| 15 | 29.11 ± 1.21 aA | 29.73 ± 1.24 aA | 5.49 ± 1.02 cB | 0.67 ± 0.33 aC | 0 | 0 | |
| Pupa | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 4.59 ± 0.32 eA | 0.78 ± 0.40 dB | 1.00 ± 0.58 dB | 0 | 0 | 0 | |
| 10 | 18.17 ± 1.79 cA | 16.05 ± 0.48 bA | 7.27 ± 1.28 cB | 0 | 0.33 ± 0.33 aC | 0 | |
| 15 | 22.20 ± 4.22 cA | 17.02 ± 6.37 bA | 18.74 ± 1.40 aA | 0 | 0 | 0 | |
| Adult | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 34.12 ± 0.16 a | 0 | 0 | 0 | 0 | 0 | |
| 10 | 30.44 ± 0.46 aA | 22.93 ± 0.67 abB | 0 | 0 | 0 | 0 | |
| 15 | 27.43 ± 1.02 bA | 26.04 ± 1.76 aA | 18.34 ± 1.56 aB | 0 | 0 | 0 | |
| Adult | 30 (Control) | 31.86 aA | |||||
Note: The data are the mean ± standard error. Data followed by different lowercase letters in each column, and data followed by different capital letters in each row indicate significant difference according to Tukey’s test at p < 0.05.
Table 4.
The number of eggs laid by H. hebetor adults originated from initial eggs, larvae, pupae, and adults after cold storage at −5, 0, 5, 10, and 15 °C for 10, 20, 30, 40, 50, and 60 d.
Table 4.
The number of eggs laid by H. hebetor adults originated from initial eggs, larvae, pupae, and adults after cold storage at −5, 0, 5, 10, and 15 °C for 10, 20, 30, 40, 50, and 60 d.
| Initial Life Stage | Temperature (°C) | Cold Storage Duration (d) | |||||
|---|---|---|---|---|---|---|---|
| 10 | 20 | 30 | 40 | 50 | 60 | ||
| Egg | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 10 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 15 | 157.00 ± 6.08 dA | 195.67 ± 17.65 cA | 91.33 ± 12.77 bB | 0 | 0 | 0 | |
| Larva | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 53.67 ± 10.27 fA | 31.33 ± 7.69 fB | 0 | 0 | 0 | 0 | |
| 10 | 185.00 ± 9.29 cA | 89.67 ± 15.19 eB | 13.33 ± 3.76 cC | 0 | 0 | 0 | |
| 15 | 344.67 ± 6.23 bA | 340.67 ± 6.23 aA | 5.00 ± 1.00 dB | 0 | 0 | 0 | |
| Pupa | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 37.33 ± 1.45 gA | 0.67 ± 0.33 gB | 1.00 ± 0.58 dB | 0 | 0 | 0 | |
| 10 | 193.33 ± 33.18 cdB | 262.67 ± 28.26 bA | 1.67 ± 0.88 dC | 0 | 0 | 0 | |
| 15 | 228.67 ± 57.18 cA | 104.00 ± 52.03 dB | 189.00 ± 21.73 aA | 0 | 0 | 0 | |
| Adult | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 112.00 ± 9.54 e | 0 | 0 | 0 | 0 | 0 | |
| 10 | 430.67 ± 29.17 aA | 269.33 ± 14.53 bB | 0 | 0 | 0 | 0 | |
| 15 | 325.67 ± 10.9 bA | 241.00 ± 21.66 bcB | 82.00 ± 3.51 bC | 0 | 0 | 0 | |
| Adult | 30 (Control) | 392.00 ± 18.25 bA | |||||
Note: The data are the mean ± standard error. Data followed by different lowercase letters in each column, and data followed by different capital letters in each row indicate significant difference according to Tukey’s test at p < 0.05.
Table 5.
The oviposition duration (d) of H. hebetor adults originated from initial eggs, larvae, pupae, and adults after cold storage at −5, 0, 5, 10, and 15 °C for 10, 20, 30, 40, 50, and 60 d.
Table 5.
The oviposition duration (d) of H. hebetor adults originated from initial eggs, larvae, pupae, and adults after cold storage at −5, 0, 5, 10, and 15 °C for 10, 20, 30, 40, 50, and 60 d.
| Initial Life Stage | Temperature (°C) | Cold Storage Duration (d) | |||||
|---|---|---|---|---|---|---|---|
| 10 | 20 | 30 | 40 | 50 | 60 | ||
| Egg | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 10 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 15 | 15.67 ± 0.33 bcA | 14.67 ± 0.33 bA | 10.67 ± 0.33 bB | 6.00 ± 0.58 aC | 4.33 ± 0.33 aC | 0 | |
| Larva | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 9.00 ± 0.00 dA | 7.00 ± 0.00 cA | 0 | 0 | 0 | 0 | |
| 10 | 12.67 ± 0.33 cA | 8.33 ± 0.33 cB | 5.00 ± 0.00 cB | 0 | 0 | 0 | |
| 15 | 17.00 ± 0.00 bA | 15.00 ± 0.00 bA | 5.33 ± 0.33 cB | 2.33 ± 0.33 bBC | 1.33 ± 0.33 aC | 0.83 ± 0.17 aC | |
| Pupa | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 11.67 ± 0.33 cA | 3.67 ± 0.33 dB | 2.33 ± 0.33 dB | 0 | 0 | 0 | |
| 10 | 16.00 ± 1.00 bA | 14.33 ± 0.88 bA | 4.67 ± 0.33 cB | 2.33 ± 0.33 bB | 2.00 ± 0.58 aB | 0 | |
| 15 | 15.67 ± 0.33 bA | 7.67 ± 1.33 cC | 11.33 ± 0.88 aB | 2.17 ± 0.44 bD | 1.67 ± 0.60 aD | 1.00 ± 0.29 aD | |
| Adult | −5 | 0 | 0 | 0 | 0 | 0 | 0 |
| 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| 5 | 11.00 ± 0.00 cA | 0 | 0 | 0 | 0 | 0 | |
| 10 | 21.00 ± 0.00 aA | 18.33 ± 0.33 aA | 0 | 0 | 0 | 0 | |
| 15 | 16.67 ± 0.33 bA | 14.00 ± 0.00 bAB | 11.00 ± 0.58 aB | 0 | 0 | 0 | |
| Adult | 30 (Control) | 15.00 ± 0.33 bA | |||||
Note: The data are the mean ± standard error. Data followed by different lowercase letters in each column, and data followed by different capital letters in each row indicate significant difference according to Tukey’s test at p < 0.05.
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MDPI and ACS Style
Lü, J.; Bai, C.; Guo, Y.; Liu, W.; Yue, Y. Influence of Cold Exposure for Different Durations on Laboratory-Reared Habrobracon hebetor (Say) (Hymenoptera: Braconidae). Diversity 2025, 17, 253. https://doi.org/10.3390/d17040253
AMA Style
Lü J, Bai C, Guo Y, Liu W, Yue Y. Influence of Cold Exposure for Different Durations on Laboratory-Reared Habrobracon hebetor (Say) (Hymenoptera: Braconidae). Diversity. 2025; 17(4):253. https://doi.org/10.3390/d17040253
Chicago/Turabian StyleLü, Jianhua, Chunqi Bai, Yafei Guo, Wenjing Liu, and Yanli Yue. 2025. "Influence of Cold Exposure for Different Durations on Laboratory-Reared Habrobracon hebetor (Say) (Hymenoptera: Braconidae)" Diversity 17, no. 4: 253. https://doi.org/10.3390/d17040253
APA StyleLü, J., Bai, C., Guo, Y., Liu, W., & Yue, Y. (2025). Influence of Cold Exposure for Different Durations on Laboratory-Reared Habrobracon hebetor (Say) (Hymenoptera: Braconidae). Diversity, 17(4), 253. https://doi.org/10.3390/d17040253
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