Phototoxicity of Ultraviolet-A against the Whitefly <i>Bemisia tabaci</i> and Its Compatibility with an Entomopathogenic Fungus and Whitefly Parasitoid

Khan, Muhammad Musa; Fan, Ze-Yun; O’Neill Rothenberg, Dylan; Peng, Jing; Hafeez, Muhammad; Chen, Xin-Yi; Pan, Hui-Peng; Wu, Jian-Hui; Qiu, Bao-Li

doi:https://doi.org/10.1155/2021/2060288

Oxidative Medicine and Cellular Longevity

On this page

Abstract Introduction Materials and Methods Results Discussion Conclusion Data Availability Conflicts of Interest Acknowledgments Supplementary Materials References Copyright Related Articles

Special Issue

Antioxidants and Free Radicals in the Phototoxicity of Drugs and Nanomaterials

View this Special Issue

Research Article | Open Access

Volume 2021 | Article ID 2060288 | https://doi.org/10.1155/2021/2060288

Phototoxicity of Ultraviolet-A against the Whitefly Bemisia tabaci and Its Compatibility with an Entomopathogenic Fungus and Whitefly Parasitoid

Muhammad Musa Khan,^1,2Ze-Yun Fan,^1,3Dylan O’Neill Rothenberg,⁴Jing Peng,¹Muhammad Hafeez,⁵Xin-Yi Chen,¹Hui-Peng Pan,^1,2,3Jian-Hui Wu,^1,2,3and Bao-Li Qiu^1,2,3

Academic Editor: Daoud Ali

Received20 Apr 2021

Accepted09 Jun 2021

Published12 Jul 2021

Abstract

Ultraviolet (UV) radiation significantly affects insect life and, as a result, has been widely used to control different invertebrate pests. The current results demonstrate that when Bemisia tabaci first instar nymphs are exposed to UV-A light for 12, 24, 48, and 72 h, their developmental and biological parameters are negatively affected by UV-A exposure; the effect increased with an increase in exposure time. We hypothesized that UV-A light is compatible with other biological control agents. Results showed that when the entomopathogenic fungus Cordyceps fumosorosea was applied to third instar nymphs of B. tabaci previously exposed to UV-A light, the LC₅₀ was 3.4% lower after 72 h of exposure to UV-A light compared to the control. However, when the fungus was exposed to UV-A light, its virulence decreased with an increase in UV-A exposure time. The parasitism rate of Encarsia formosa against 24 h UV-A-exposed third instar nymphs of B. tabaci increased while the adult emergence from parasitized nymphs was not affected after UV-A light exposure. Parasitism rate was significantly reduced however following E. formosa exposure to UV-A light; but again, adult emergence was not affected from parasitized nymphs. The percentage mortality of E. formosa increased with increasing exposure time to UV-A light. The enzyme activity of SOD, CAT, GST, and AChE and the energy reserve contents were negatively affected due to UV-A exposure. Collectively, this study has demonstrated that UV-A light significantly suppresses the immune system of B. tabaci and that UV-A light is compatible with other biological control agents if it is applied separately from the biological agent.

1. Introduction

Climate change can have various effects on abiotic stress. As a result, it poses a threat to agricultural systems’ long-term viability and productivity. Stress factors, both abiotic and biotic, also play an important role in the life of an insect. There are numerous environmental stresses, such as ozone depletion, increased ultraviolet irradiation, biodiversity destruction, and temperature that impact insects. For many organisms, ultraviolet (UV) radiation is a significant source of stress [1]. UV radiation is currently attracting much attention due to its potentially harmful effects on a variety of species. UV radiation is generally considered a resilient ecological stressor for biological entities [2]. It may damage nucleic acids, membrane fatty acids, and various amino acids [3, 4], resulting in cell toxicity, genetic modifications, and cell signaling pathway modifications [5]. UV exposure shortens an insects’ adult lifespan, increases oviposition rate, and reduces fertility [6, 7]. UV causes the development of reactive oxygen species (ROS), which can damage nucleic acids, membrane lipids, and proteins [4]. These various types of molecule damage have significant biological consequences, such as genetic variation, cytotoxicity, and signaling cell pathway transformation [5].

The whitefly, Bemisia tabaci, is a key pest of many greenhouse vegetables, ornamentals, and also field crops worldwide since the midseventies [8]. This whitefly is polyphagous and leads to serious economic losses [9]. The damage to crops is manifold; the feeding of B. tabaci causes direct damage to plant foliage. In China, for example, B. tabaci MEAM1 is well distributed across 31 provinces or municipalities and causes significant economic losses [10]. Adult and immature whitefly are phloem feeders [11]. Furthermore, B. tabaci acts as a vector of around 150 plant viruses [12].

Insecticides have been the mainstay of controlling B. tabaci in diverse agricultural production systems. Resistance to insecticides resulting in loss of efficacy of many older insecticides has placed excessive pressure on novel products. Alternative control strategies now have a key role in controlling B. tabaci and managing pesticide resistance development. Using biological agents is not only environmentally safe but can also have a significant impact on whitefly management practices. To date, more than 20 species of entomopathogenic fungi are known to infect whitefly. Among these, the entomopathogenic fungus, Cordyceps fumosorosea Zare and Gams (Hyphomycetes), formerly known as Isaria fumosorosea, designated as Cordyceps clade [13], is a well-known fungal species used for whitefly management and has been widely studied [14–17]. C. fumosorosea-based formulations have been commercially available since the 1990s for the management of whitefly [18, 19]. Encarsia formosa Gahan (Hymenoptera: Aphelinidae) also plays an important role in managing B. tabaci [20, 21]. E. formosa is a solitary endoparasitoid that is commercially used as a biocontrol agent for B. tabaci [22, 23]. E. formosa kills 75% of its whitefly host by probing nymphs with its ovipositor and depositing eggs in their bodies. Larvae of E. formosa then feed on the parasitized whitefly internal contents, eating all the organs and leaving only the outer armor in which they pupate from afterwards [24].

UV radiation and other abiotic stressors have a major impact on insect life because they increase the development and accumulation of reactive oxygen species (ROS). These oxygen free radicals increase both the antioxidant potential and oxidant development of cells. They are not harmful at low concentrations and play important roles in cell signaling and defense [25–27]. Multiple biochemical pathways contain carbohydrates, proteins, and lipids as an end product in the energy metabolism of insects [28]. Different physiological processes such as synaptic transmission, morphogenetic behaviors, phospholipid synthesis, sexual maturation, and egg development may be influenced by these carbohydrates, proteins, and lipids (which serve as insect primary energy sources) [29, 30]. As both biological control agents and insect pests share a common habitat [31], it is obvious that the application of UV light has the potential to affect other natural whitefly controlling measures.

The current study was designed to examine the effectiveness of UV-A irradiation against B. tabaci by evaluating both biological and physiological parameters. The risks posed to the entomopathogenic fungus and the whitefly parasitoid by UV-A light were also assessed by evaluating the pathogenicity and percentage parasitism, respectively.

2. Materials and Methods

2.1. Insects, Plants, and Entomopathogenic Fungus

Gossypium hirsutum L. (cotton plants) were raised under glasshouse conditions at South China Agricultural University (SCAU), Guangzhou, in 15 cm diameter plastic pots containing a mixture of soil consisting of 5% clay, 85% peat, and 10% sand to reach the 7–8 expanding leaf stage. Two symmetrical, completely expanded leaves of identical size were used in all experimental replications.

The silverleaf whitefly, B. tabaci Middle East-Asia Minor 1 (formerly known as B. tabaci B biotype), was the B. tabaci species used in this study. Different cotton leaves were caged, and 60 pairs of the whitefly were released into the cage for egg-laying to occur for 24 hours. The adults of the whitefly were then removed after 24 hours, and the plants were kept at a temperature of , relative humidity of 60%, and photoperiod of 14 : 10 (L : D) in an iron-framed and plastic sieve cage () to allow for whitefly development as outlined by Ou et al. [32] (Figure S1).

In 2015, E. formosa was obtained from the Chinese Academy of Agricultural Sciences, Institute of Plant Protection. Under laboratory conditions at SCAU, the parasitoid population was reared at the temperature of , relative humidity of 60%, and a photoperiod of 14 : 10 (L : D) on cotton plants containing third instar whitefly nymphs placed in an iron-framed and plastic sieve cage () as outlined by Ou et al. [32].

C. fumosorosea isolate SP535 was originally isolated from soil obtained from the repository of the Key Laboratory of Biopesticides Innovation and Application of Guangdong Province, SCAU. Potato Dextrose Agar (PDA) media was used to maintain the fungal culture (200 g potatoes, 20 g dextrose, and 20 g agar in 1 L of distilled water) in a glass dish (90 mm Ø) for three weeks under dark conditions at . The methodology followed for maintaining the experimental materials was as outlined by Ou et al. [32].

2.2. UV-A Irradiation Source

A UV-A irradiation source of 15 W power with 360 nm wavelength was used during the experimentation. The UV-A light source was purchased from Shenzhen Guanhongya Photoelectronic Technology Co. Ltd. (Shenzhen, China).

2.3. Effect of UV-A Light on Whitefly Development and Biology

To assess the effect of UV-A on the developmental period and other life table parameters of B. tabaci, first instar nymphs of B. tabaci were used. To obtain a homogeneous first instar nymphal population, cotton plants at the 6-8 expanded leaf stage were used. Leaves were caged, and whitefly adults were released for egg-laying for 24 hours. After removing the adult whiteflies, the plants were kept at and 16 : 8 (L : D) photoperiod for 5-7 days. After the emergence of 80% of first instar nymphs, they were then exposed to UV-A light. A plant containing first instar nymphs was kept under dark conditions before being exposed to UV-A light. The plants containing the first instar nymphs of B. tabaci were exposed to UV-A light for 12, 24, 48, and 72 hours. Similar infested plants which were not exposed to UV light acted as controls. The distance between the UV-light source and the leaf containing the first instar nymphs of B. tabaci was approximately 50 cm. After exposure of 12, 24, 48, and 72 hours, the plants were exposed to normal light. As nymphs reached the second instar, 90 of them were marked on a leaf with each nymph being given a specific number to aid identification. Each marked nymph was taken as a single replication. Individuals were observed each day, and their current instar was recorded until the nymph either developed into an adult or died. Each emerged female was paired with an emerged male from the same treatment and kept in a small petri dish (3 cm) containing agar gel and a (2 cm) cotton leaf disk. The petri dish was observed daily to calculate fecundity and the number of days of female longevity. A new leaf disk was provided daily to avoid the risk of starvation. The remaining males were kept in a petri dish with agar and cotton leaf disk separately to assess their longevity.

2.4. Effect of UV-A Light on Enzyme Activity and Energy Reserves

B. tabaci adults were exposed to UV-A light for 0 (control), 12, 24, 48, and 72 hours. One hundred and fifty adults per treatment per replication were collected. Three technical and three biological replications were established. Collected samples were weighed before homogenization. The total protein content of supernatants from the insect homogenates was determined using bovine albumin serum (BSA) as a norm, as described by Nazir et al. [33].

Adult B. tabaci was homogenized with ice-cold 0.05 M sodium phosphate buffer at room temperature (pH 7.3). At 4°C, the homogenized samples were centrifuged for 10 minutes at 12,000 rpm (rotation per minute). The supernatant was collected and moved to new tubes and centrifuged for 15 minutes at 4°C at 12,000 rpm. For the various enzyme assays, the final supernatants were used for enzyme preparation. Antioxidant enzyme (SOD, POD, CAT, and PPO) and detoxification enzyme (AChE, GST, and P450) activity was determined by the commercially available kits purchased from Nanjing Jiancheng Bioengineering Research Institute. The method followed was as per the instructions provided by the manufacturer.

To estimate the whitefly energy reserve contents after exposure to UV-A light, adults were again exposed to UV-A light as outlined above, and samples were collected. The whole bodies of adult B. tabaci were homogenized in sodium phosphate buffer pH 7.0. The samples were then centrifuged at 4°C for 10 minutes at 10,000 rpm. The collected supernatants were used in further experimentation. For the estimation of energy reserves, commercially available kits to determine cholesterol, glycogen, and triglyceride were purchased from Solarbio Life Science, Beijing, China. The method followed was as per the instructions provided by the manufacturer.

2.5. Effect of UV-A Light on the Virulence of C. fumosorosea against B. tabaci

To determine the virulence of C. fumosorosea against B. tabaci, the progressive concentrations were prepared until the mortality ranged between 10 and 95%. The leaf dip application method was used as outlined by Nazir et al. [33]. In a 250 mL reagent container, a stock suspension of conidia was made containing 100 mL distilled water and 0.05% () Tween 80® by adding the mass sporulating culture. The mixture was shaken vigorously to isolate spores from the hyphal debris. The conidial concentration was determined using an improved Neubauer hemocytometer (Brand GmbH, Wertheim, Germany). The conidial suspensions were diluted in sterilized water containing 0.05% Tween 80 in five separate suspensions (i.e., , , , , and conidia mL^-1). Distilled water containing Tween 80 at 0.05% was used as control. Plants at 7-8 extended leaf stage containing third instar nymphs were used in this experiment. A germination test was performed on a PDA medium before performing bioassays against the whitefly to determine the percentage of viable conidia [34]. Conidial germination was greater than 95% in all bioassays. Plants containing third instar nymphs were kept in the dark for 2 hours and then exposed for 0 (control), 12, 24, 48, and 72 hours to UV-A light. Leaves were dipped into conidial suspensions for 10 seconds and then air-dried on tissue paper for 15 min at room temperature. Each leaf contained 20 third instar nymphs per treatment per replication. Whitefly mortality was recorded after five days of fungal application. The leaves were plucked and placed on Petri plates containing agar gel to maintain leaf moisture and were kept under dark conditions at relative humidity of 90% to stimulate fungal growth to confirm the whitefly mortality due to fungal infection. Percentage mortality was calculated by using the Abbott formula [35].

To assess the effect of UV-A light on the fungus, the fungal culture was exposed to UV-A light for 12, 24, 48, and 72 h. The fungal culture plates were placed in an environmental chamber under dark conditions, and an external UV-A light source was used to expose the fungi. After exposure, treatment with the conidial suspension was undertaken by the method outlined above.

2.6. Effect of UV-A Light on Parasitism of E. formosa against B. tabaci

To determine the effect of UV-A light on the parasitism of E. formosa, cotton plants containing third instar nymphs of B. tabaci (<24 h old) were prepared as outlined above. This experiment was divided into two different parts: (1) whitefly was exposed to UV-A light, and then, E. formosa was released; and (2) E. formosa was exposed to UV-A light and then released onto the whitefly nymphs.

For the first part, cotton plants containing third instar nymphs of whitefly were exposed to UV-A light for 0 (control), 12, 24, 48, and 72 h. Two hundred third instar nymphs (<24 h old) were kept on the leaf, and the remaining nymphs were removed from the leaf using a camel hairbrush. Leaves were caged as shown in Figure S1, and the unexposed parasitoid (<24 h old) with a ratio of 1 : 20 (parasitoid : nymphs) was released into the cages for 24 hours. Each treatment was replicated three times. The number of parasitized nymphs was recorded after ten days. The nymphs that turned brown were considered parasitized. Percentage emergence was then determined by caging the leaves for more than five days. After five days, cages were removed, and the number of emerged adults of E. formosa was counted and recorded. Percentage emergence was determined by using the following formula:

For the second part, the same procedure as outlined above was followed except with the difference that E. formosa (<24 h old) were exposed to UV-A light for 0 (control), 12, 24, 48, and 72 h and then released onto third instar nymphs of B. tabaci.

2.7. Statistical Analysis

The development time of different stages, the survival rate of different stages, the fecundity off, and female whitefly preoviposition duration and adult longevity were all studied using the age-stage two-sex life table model [36, 37]. TWOSEX-MS Chart program was downloaded from the website http://140.120.197.173/Ecology/prod02.htm [38]. Using 100,000 bootstrap replicates, standard errors (SE) and means were measured [40, 41]. In the TWOSEX-MS Chart, the paired bootstrap method was used to compare all treatments [39].

The software PoloPlus (Version: 1.0 (Pacific Southwest Forest and Range Experiment Station, Berkeley, California, USA)) was used to calculate LC₅₀ of C. fumosorosea against B. tabaci. The data of mortality in replications were subjected to test the hypothesis of equality and parallelism via PoloPlus by following the method described by Chang and He [41]. To analyze the parasitism rate among the treatments and enzymatic activity, one-way ANOVA, along with the Tukey post hoc test at , was used to compare the means via SPSS. SigmaPlot 12.0 was used to form graphical work for all parameters. Correlation of enzymatic activity and energy reserves with exposure time to UV-A light was calculated via RStudio v1.3.1056 software with the corrplot package.

3. Results

3.1. Effect of UV-A Light on the Development, Growth, and Dimorphic Parameters of B. tabaci

The effect of UV-A light on the development period of the preadult stages of B. tabaci is shown in Table 1. The presented results demonstrate that the developmental period of the first, second, third, and fourth instars was significantly reduced with increasing UV-A exposure time. The male and female longevity was also reduced at 24, 48, and 72 hours of exposure compared to controls. The APOP (adult preoviposition) was not significantly affected by the UV-A light exposure; the TPOP (total preoviposition period) was significantly reduced at 48 and 72 hours of exposure to UV-A light as compared to the control. Following 72 hours of UV-A exposure also significantly reduced the total fecundity of B. tabaci.

Similarly, results also showed that the fecundity was significantly reduced with the increasing trend of UV-A light exposure compared to the control (Table 2). The effect of UV-A light on the population growth of B. tabaci is given in (Table S1). Results show that (intrinsic rate of increase) and (finite rate of increase) were not affected due to UV-A light exposure. At the same time, (net reproductive rate) was negatively affected by UV-A light exposure after 48 and 72 h. More exposure time lessened the net reproductive rate as compared to the control. The mean generation time was significantly reduced due to UV-A light exposure after 72 hours compared to the control.

The (survival rate of the specific stage) value was reduced in UV-A-exposed B. tabaci. The survival rate of females and males in controls was observed to be 35 and 33 days, 33 and 36 days after 12 hours of exposure, 34 and 34 days after 24 hours of exposure, 30 and 33 days after 48 hours of exposure, and 27 and 33 days after 72 hours of exposure, respectively. Results showed that UV-A light exposure significantly reduced male and female survival rates (Figure S2).

Results for (survival rate of the specific stage), (fecundity of specific age stage), (overall population fecundity), and (total maternity) are shown in Figure S3. The curves are expressed by , which is a simple form of the curves. The results showed that as UV-A light exposure time increased, the survival rate decreased, affecting other reproductive parameters. As the survival curve started to reduce with time, , , and also reduced. In addition, the fecundity value was also reduced in line with a reducing survival rate.

Results of showed that due to UV-A light exposure, the female life expectancy was significantly reduced compared to male life expectancy. In the controls, the life expectancy of females and males was observed at 36.04 and 34 days, respectively. When nymphs were exposed to UV-A light, the male life expectancy after 12, 24, 48, and 72 hours was 34.00, 32.87, 33.89, and 32.99 days, respectively, which was not significantly altered following UV-A exposure. In comparison, a significant reduction in female life expectancy following 12, 24, 48, and 72 hours of exposure was observed: 35.92, 34.00, 30.06, and 27.01 days, respectively (Figure S4).

Results of (reproduction of a specific stage) show how each individual fits into the next population. Results (Figure S5) showed that on the 25^th day, the maximum female reproductive value (106.85) was observed. After exposure to UV-A light for 12, 24, 48, and 72 hours, the reproductive value was 84.39 on the 19^th day, 72.43 on the 19^th day, 60.99 on the 18^th day, and 52.69 on the 15^th day, respectively. Results showed that UV-A light exposure not only reduced the duration of reproduction but also reduced age-specific reproduction.

3.2. Effect of UV-A Light Exposure on the Enzyme Activity and Energy Reserve Contents of B. tabaci

The enzymatic analysis showed that following exposure to UV-A light, a significant reduction in enzyme activity was observed in the exposed treatments compared to the control. The activity of SOD, POD, PPO, GST, and cytochrome P450 and contents of glycogen, triglyceride, and total cholesterol were continuously reduced as the UV-A light exposure time increased. At the same time, no significant effect was observed in CAT and AChE enzyme activity (Figures 1).

(a)

(b)

(c)

(d)

(e)

(f)

(g)

(h)

(i)

(j)

Figure 1

The activity of different enzymes (a) SOD, (b) CAT, (c) POD, (d) PPO, (e) AChE, (f) GST, and (g) cytochrome P450 and contents of different energy reserves (h) glycogen, (i) triglyceride, and (j) total cholesterol of Bemisia tabaci exposed to UV-A light for control (0 h), 12 h, 24 h, 48 h, and 72 hours. The bars are showing the mean value of three replications. Standard error bars are showing the standard deviation of the mean. Lowercase lettering is showing the significance among the treatments at . Similar letters have no significant difference among the treatments.

Results of correlation analysis (Figure 2) of different oxidative and detoxification enzyme activity and energy reserves with UV-A light exposure time demonstrated that, except for PPO, POD, and P450 enzyme activity, all other enzymes had a significant negative correlation with exposure time. These results showed that UV-A light exposure caused depletion of different enzyme activity as the exposure time increased.

3.3. Effect of UV-A Light on the Virulence of C. fumosorosea against B. tabaci

The results of the virulence of C. fumosorosea against B. tabaci are shown in Table 3. The virulence assessment bioassay showed that LC₅₀ in the control (without UV-A exposure) was conidia mL^-1 (-; ; ). As the exposure time of UV-A light increased, the LC₅₀ concentration decreased. The maximum percentage mortality was recorded in the treatment where conidial suspension was applied onto 72 hours of UV-A light-exposed nymphs.

When the fungus was exposed to UV-A light for different time periods, the results showed that with an increase in exposure time, the LC₅₀ also increased. The virulence assessment showed that LC₅₀ in the control (without UV-A exposure) was and after 72 hours of exposure was . The maximum percentage mortality was observed where third instar nymphs of B. tabaci were treated with conidial suspension exposed to UV-A light for 12 hours.

3.4. Effect of UV-A Light on Parasitism of E. formosa against B. tabaci

B. tabaci third instar nymphs firstly exposed to UV-A light and then exposed to E. formosa to assess percentage parasitism showed (Figure 3) that the nymphs exposed 24 hours to UV-A light were parasitized more than the 12, 48, and 72 hours of exposures (; ). The results showed that UV-A light weakened the nymphs of B. tabaci so aiding E. formosa to parasitize more. The resulting percentage emergence was not significantly affected. However, when E. formosa was exposed to UV-A light, its parasitic ability was significantly reduced compared to the control (; ) (Figure 3(a)). The percentage of adult emergence of E. formosa emerging from parasitized nymphs was the same in the control and UV-A light-exposed nymphs (; ). In addition, the percentage of adult emergence was also significantly reduced when the parasitoid was exposed to UV-A light as compared to that in the control (; ) (Figure 3(b)). During the experimentation, it was observed that E. formosa is sensitive to UV-A light. A significant number of E. formosa adults exposed to UV-A light simply died. So, to assess the survival rate of E. formosa, adults were exposed to UV-A light for 12, 24, 48, and 72 hours. Results showed that as the UV-A exposure time increased, the survival percentage significantly decreased, which showed that UV-A light is lethal for E. formosa and so both could not be used together to control B. tabaci (Figure 3(c)).

(a)

(b)

(c)

All the results provide a model that demonstrates UV-A light can be an effective tool to control B. tabaci. UV-A light and biological control agents of B. tabaci could be used together if the UV-A light is applied to the whiteflies before applying the biological control agent. Exposure to UV-A light seriously affected the effectiveness of the biological control agents investigated (Figure 4).

4. Discussion

The current study has demonstrated that due to UV-A light exposure, the nymphal developmental period, preoviposition period, fecundity, female longevity, and other dimorphic parameters of B. tabaci were significantly affected. Results also showed that survival rate, reproduction rate, and life expectancy also reduced with increased UV-A exposure duration. Our present results coincide with Ali et al. [42] who reported that due to UV-A light exposure, the developmental period of immature stages of Mythimna separata (eggs, larvae, and pupa) declined with increased exposure time. The male and female longevity was also reported to decrease with an increase in exposure time. Similarly, Tariq et al. [23] experimented by exposing Dialeurodes citri to UV-A light and reported a significantly shorter developmental time of D. citri immatures (nymphs and pupa) in the F1 generation after adults were exposed to UV-A light. However, both male and female longevity was significantly reduced with exposure time. Zhang et al. [7] also reported an increase in the immature development period of Helicoverpa armigera along with a decrease in male and female longevity as UV exposure time increased. All the stated results confirm that UV-A exposure can significantly affect an insect’s developmental period, but the cause of this change in the developmental period is still unknown.

Different antioxidants are in a complex equilibrium state within an insect species in normal circumstances in order to maintain normal physiological activities. Insects have also developed a complex network of antioxidant enzyme systems [43] and detoxification enzymes [44] to fight against the risk of oxidative stress. In the current study, we observed that due to UV-A light exposure, SOD, POD, and PPO activity was significantly affected. Moreover, the activity of detoxification enzymes was also affected due to UV-A exposure. Many previous studies reported the alteration of enzyme activity when exposed to UV irradiation. Ali et al. [45] reported that UV-A exposure caused oxidative stress in M. separata and altered antioxidant enzymes’ activity. Zhou et al. [46] exposed grain aphid Sitobion avenae to UV-B radiation and reported that the antioxidant enzymes SOD, POD, and CAT were significantly affected. UV exposure resulted in more than 90% reduction in PPO activity after 5 minutes of exposure [47]; when Dendrolimus tabulaeformis were exposed to UV-A light, elevated oxidative stress and disturbed physiological detoxification were recorded [44]. The current study showed that due to UV-A light exposure, a significant decrease in the contents of energy-providing compounds like glycogen, triglyceride, and total cholesterol was observed. It is a basic life history theory that reproduction always costs survival [48]. These two processes share the energy to maintain normal biological function under UV stress [42]. After exposure to UV light, a reduction in these energy reserves justifies a reduction in reproduction and longevity of B. tabaci. However, there is no study available to justify reducing energy reserves due to UV-light exposure; only Ohkawara et al. [49, 50] reported reducing glycogen in humans and minipigs due to UV exposure.

A previous study showed that C. fumosorosea (formerly I. fumosorosea) is an effective biological control agent against B. tabaci, not only being a mycoinsecticide but also in that it exerts oxidative stress in B. tabaci [51]. Santos et al., Wang et al., and Zou et al. [52–54] described that C. fumosorosea is a very efficient and environmentally safe control agent for B. tabaci. However, exposure to solar radiation can strongly affect conidial development, survival, dispersion, dissemination, germination, pathogenesis, and virulence, although its effects often vary from species to species [55–64].

The current study showed that due to UV-A light exposure to B. tabaci, the parasitism rate by E. formosa was increased, but the percentage emergence of parasitoids was not affected. Cochard et al. [65] exposed Aphidius ervi to UV and reported that due to UV-light exposure, a significant change in parasitism by A. ervi was noted, but adult emergence remained unaffected. Our results also showed that UV-A light exposure decreased the parasitism of E. formosa and also caused mortality in E. formosa. It has been reported that UV-light exposure significantly reduced the parasitism of Trichogramma cacoeciae, an egg parasitoid of Lobesia botrana [66]. Indeed, many studies report the toxicity of UV light against different insects [67–71]. Due to cascading effects in the food chain, insects higher up in the food chain are thought to be affected more by environmental stress than those at lower levels. As a result, a change in parasitism rate could be described as an instant stress response [72–74]. The factors that influence parasitoid species composition are difficult to identify, and the reasons why some species react to stress more effectively than others have remained unclear [75].

Due to exposure to high-intensity light or UV light, plants usually respond by producing ROS (reactive oxygen species), which has already been reported as a defense against diseases and pests [76]. The abrupt accumulation of hydrogen peroxide on the pathogen target site makes it toxic for pathogens [77]. ROS is also involved in triggering signaling pathways responsible for the activation of defense mechanisms, for example, the production of secondary metabolites, which are defense compounds [77–79]. In addition, Ouhibi et al. [80] has recently shown that after UV-C light exposure against Botrytis cinerea and Sclerotinia minor, the increased resistance that was observed may include phenolic compounds. It could also be speculated that phytoalexins’ biosynthesis can be due to the increased resistance to UV-C treatments [81, 82]. In UV-C-treated tomato fruit, higher glycoalkaloid alpha-tomatine levels, an antifungal compound, showed resistance against Rhizopus stolonifer [83]. UV-induced resistance to fungi of the genus Penicillium was associated with the accumulation of scoparone and scopoletin phytoalexins in citrus fruits and structural barriers [84]. However, some studies have reported that UV light has a negative impact on the plant’s morphology and physiology; Kakani et al. [85] reported that UV-B light reduced plant height, branch length, leaf area, flower and petal length, petal area, and wax content. However, no reduction in production has been reported regarding exposure to UV light.

5. Conclusion

From the current study, it can be concluded that UV-A light can be used as a B. tabaci management tool. UV-A light affects the adults’ development duration, longevity, and reproduction as well as affecting its physiology by disrupting the enzymatic balance. The UV-A light exposure exerted stress in the B. tabaci and suppressed the immune system, which gave an opportunity to the entomopathogenic fungus to work more efficiently. Therefore, due to the suppression of the immune system, the biological control agent can significantly control B. tabaci better. UV-A light can only be applied before the application of the biological control agent. According to the known literature and current experimental trials, both the entomopathogenic fungus and the parasitoid are sensitive to UV-A application. The literature also documents that UV-light exposure helps plants induce resistance, but no effect on productivity has been recorded. This study has laid the basis for conducting investigations on the application of UV-A light for the management of B. tabaci under semifield or greenhouse conditions.

Data Availability

All the data has already been given in the manuscript and supplementary material.

Conflicts of Interest

The authors have no conflict of interest to declare.

Acknowledgments

The authors thank Dr. Andrew G. S. Cuthbertson (York, UK) for critical comments on an earlier version of the manuscript. The study was supported by the National Key Research and Development Program of China (2019YFD1002100).

Supplementary Materials

Figure S1: caging of cotton leaves during whitefly rearing and experimentation. Figure S2: graphs show (survival rate of the specific stage) of Bemisia tabaci treated at second instar nymph stage exposed to UV-A light. Figure S3: graphs show (survival rate of the specific stage), (fecundity of specific age stage), (overall population fecundity), and (total maternity) values for Bemisia tabaci nymphs exposed to UV-A light. Figure S4: graphs show (life expectancy) values of Bemisia tabaci nymphs exposed to UV-A light. Figure S5: graphs show (reproduction of a specific stage) values for B. tabaci nymphs exposed to UV-A light. Table S1: effect of UV-A light exposure on the population growth parameters () of Bemisia tabaci adults exposed at the nymphal stage. Table S2: percentage mortality of Bemisia tabaci exposed to UV-A light for the different durations and treated with different concentrations of Cordyceps fumosorosea. (Supplementary Materials)

References

V. B. Meyer-Rochow, “Risks, especially for the eye, emanating from the rise of solar UV-radiation in the Arctic and Antarctic regions,” International Journal of Clinical Health, vol. 59, pp. 38–51, 2000.
View at: Google Scholar
M. Schauena, H. T. Hornig-Doa, S. Schomberg, G. Herrmann, and R. J. Wiesner, “Mitochondrial electron transport chain activity is not involved in ultraviolet A (UVA)-induced cell death,” Free Radical Biology and Medicine, vol. 42, no. 4, pp. 499–509, 2007.
View at: Publisher Site | Google Scholar
B. A. Jurkiewicz and G. R. Buettner, “Ultraviolet light-induced free radical formation in skin: an electron paramagnetic resonance study,” Photochemistry and Photobiology, vol. 59, no. 1, pp. 1–4, 1994.
View at: Publisher Site | Google Scholar
G. F. Vile and R. M. Tyrrell, “UVA radiation-induced oxidative damage to lipids and proteins in vitro and in human skin fibroblasts is dependent on iron and singlet oxygen,” Free Radical Biology and Medicine, vol. 18, no. 4, pp. 721–730, 1995.
View at: Publisher Site | Google Scholar
T. J. McMillan, E. Leatherman, A. Ridley, J. Shorrocks, S. E. Tobi, and J. R. Whiteside, “Cellular effects of long wavelength UV light (UVA) in mammalian cells,” Journal of Pharmacy and Pharmacology, vol. 60, no. 8, pp. 969–976, 2008.
View at: Publisher Site | Google Scholar
S. I. Faruki, D. R. Das, and S. Khatun, “Effects of UV-radiation on the larvae of the lesser mealworm, Alphitobius diaperinus (Panzer)(Coleoptera: Tenebrionidae) and their progeny,” Journal of Biological Sciences, vol. 5, no. 4, pp. 444–448, 2005.
View at: Google Scholar
C. Y. Zhang, J. Y. Meng, X. P. Wang, F. Zhu, and C. L. Lei, “Effects of UV-A exposures on longevity and reproduction in Helicoverpa armigera, and on the development of its F1 generation,” Insect Science, vol. 18, no. 6, pp. 697–702, 2011.
View at: Publisher Site | Google Scholar
M. C. Lu, H. R. Chen, and Y. H. Wu, “Current status and future perspectives on natural enemies for pest control in Taiwan,” Biocontrol Science and Technology, vol. 28, no. 10, pp. 953–960, 2018.
View at: Publisher Site | Google Scholar
D. Gerling, “Natural enemies of whiteflies: predators and parasitoids,” Whiteflies: Their Bionomics, Pest Status and Management, pp. 147–185, 1990.
View at: Google Scholar
Y. Q. Liu and S. S. Liu, “Species status of Bemisia tabaci complex and their distribution in China,” Journal of Biosafety, vol. 21, no. 4, pp. 247–255, 2010.
View at: Google Scholar
M. T. Islam and S. Ren, “Effect of sweetpotato whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) infestation on eggplant (Solanum melongena L.) leaf,” Journal of Pest Science, vol. 82, no. 3, pp. 211–215, 2009.
View at: Publisher Site | Google Scholar
P. A. Stansly, S. E. Naranjo, J. K. Brown et al., Bemisia: Bionomics and Management of a Global Pest, Springer Netherlands, New York, 2010.
View at: Publisher Site
R. M. Kepler, J. J. Luangsa-Ard, N. L. Hywel-Jones et al., “A phylogenetically-based nomenclature for Cordycipitaceae (Hypocreales),” IMA Fungus, vol. 8, no. 2, pp. 335–353, 2017.
View at: Publisher Site | Google Scholar
X. Chen, L. Li, Q. Hu et al., “Expression of dsRNA in recombinant Isaria fumosorosea strain targets the TLR7 gene in Bemisia tabaci,” BMC Biotechnology, vol. 15, no. 1, p. 64, 2015.
View at: Publisher Site | Google Scholar
S. Abd-Rabou and A. M. Simmons, “Survey of natural enemies of whiteflies (Hemiptera: Aleyrodidae) in Egypt with new local and world records,” Entomological News, vol. 124, no. 1, pp. 38–56, 2014.
View at: Publisher Site | Google Scholar
G. M. Mascarin, N. N. Kobori, E. D. Quintela, and I. Delalibera, “The virulence of entomopathogenic fungi against Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) and their conidial production using solid substrate fermentation,” Biological Control, vol. 66, no. 3, pp. 209–218, 2013.
View at: Publisher Site | Google Scholar
S. J. Li, X. Xue, M. Z. Ahmed et al., “Host plants and natural enemies of Bemisia tabaci (Hemiptera: Aleyrodidae) in China,” Insect Science, vol. 18, no. 1, pp. 101–120, 2011.
View at: Publisher Site | Google Scholar
A. G. S. Cuthbertson, L. F. Blackburn, D. P. Eyre, R. J. C. Cannon, J. Miller, and P. Northing, “Bemisia tabaci: the current situation in the UK and the prospect of developing strategies for eradication using entomopathogens,” Insect Science, vol. 18, no. 1, pp. 1–10, 2011.
View at: Publisher Site | Google Scholar
M. Faria and S. P. Wraight, “Biological control of Bemisia tabaci with fungi,” Crop Protection, vol. 20, no. 9, pp. 767–778, 2001.
View at: Publisher Site | Google Scholar
T. Dong, B. Zhang, Y. Jiang, and Q. Hu, “Isolation and classification of fungal whitefly entomopathogens from soils of Qinghai-Tibet Plateau and Gansu Corridor in China,” PLoS One, vol. 11, no. 5, pp. 1–12, 2016.
View at: Google Scholar
Y. Argov, Y. Rössler, D. Rosen, and H. Voet, “Stability in the host-parasitoid relationship of Dialeurodes citri and Encarsia lahorensis in the citrus orchard,” BioControl, vol. 48, no. 6, pp. 637–657, 2003.
View at: Publisher Site | Google Scholar
J. S. Hu, D. B. Gelman, and M. B. Blackburn, “Growth and development of Encarsia formosa (Hymenoptera: Aphelinidae) in the greenhouse whitefly, Trialeurodes vaporariorum (Homoptera: Aleyrodidae): effect of host age,” Archives of Insect Biochemistry and Physiology, vol. 49, no. 3, pp. 125–136, 2002.
View at: Publisher Site | Google Scholar
K. Tariq, M. Noor, S. Saeed, and H. Zhang, “The effect of ultraviolet-a radiation exposure on the reproductive ability, longevity, and development of the Dialeurodes citri (Homoptera: Aleyrodidae) F1 generation,” Environmental Entomology, vol. 44, no. 6, pp. 1614–1618, 2015.
View at: Publisher Site | Google Scholar
K. Kos, Ž. Tomanović, H. Rojht, V. Matej, and S. Trdan, “First massive occurrence of greenhouse whitefly parasitoid, Encarsia formosa Gahan (Hymenoptera: Aphelinidae) on greenhouse whitefly, Trialeurodes vaporariorum [Westwood] (Homoptera: Aleyrodidae) in Slovenia,” Acta Agriculturae Slovenica, vol. 93, no. 3, pp. 285–291, 2009.
View at: Google Scholar
Y. Wang, L. W. Oberley, and D. W. Murhammer, “Antioxidant defense systems of two lipidopteran insect cell lines,” Free Radical Biology and Medicine, vol. 30, no. 11, pp. 1254–1262, 2001.
View at: Publisher Site | Google Scholar
H. Kamata and H. Hirata, “Redox regulation of cellular signalling,” Cellular Signalling, vol. 11, no. 1, pp. 1–14, 1999.
View at: Publisher Site | Google Scholar
L. Lijun, L. Xuemei, G. Yaping, and M. Enbo, “Activity of the enzymes of the antioxidative system in cadmium-treated Oxya chinensis (Orthoptera Acridoidae),” Environmental Toxicology and Pharmacology, vol. 20, no. 3, pp. 412–416, 2005.
View at: Publisher Site | Google Scholar
A. Baghban, J. J. Sendi, A. Zibaee, and R. Khosravi, “Effect of heavy metals (Cd, Cu, and Zn) on feeding indices and energy reserves of the cotton boll worm Helicoverpa armigera Hübner (Lepidoptera: Noctuidae),” Journal of Plant Protection Research, vol. 54, no. 4, pp. 367–373, 2014.
View at: Publisher Site | Google Scholar
D. M. Olson, H. Fadamiro, J. G. Lundgren, and G. E. Heimpel, “Effects of sugar feeding on carbohydrate and lipid metabolism in a parasitoid wasp,” Physiological Entomology, vol. 25, no. 1, pp. 17–26, 2000.
View at: Publisher Site | Google Scholar
P. Hogervorst, F. L. Wäckers, and J. Romeis, “Effects of honeydew sugar composition on the longevity of Aphidius ervi,” Entomologia Experimentalis et Applicata, vol. 122, no. 3, pp. 223–232, 2007.
View at: Publisher Site | Google Scholar
M. M. Khan, M. Nawaz, H. Hua, W. Cai, and J. Zhao, “Lethal and sublethal effects of emamectin benzoate on the rove beetle, Paederus fuscipes, a non-target predator of rice brown planthopper, Nilaparvata lugens,” Ecotoxicology and Environmental Safety, vol. 165, pp. 19–24, 2018.
View at: Publisher Site | Google Scholar
D. Ou, L. M. Ren, Y. Liu et al., “Compatibility and efficacy of the parasitoid Eretmocerus hayati and the entomopathogenic fungus Cordyceps javanica for biological control of whitefly Bemisia tabaci,” Insects, vol. 10, no. 12, pp. 1–11, 2019.
View at: Google Scholar
T. Nazir, A. Basit, A. Hanan, M. Z. Majeed, and D. Qiu, “In vitro pathogenicity of some entomopathogenic fungal strains against green peach aphid Myzus persicae (Homoptera: Aphididae),” Agronomy, vol. 9, no. 1, 2019.
View at: Google Scholar
M. Barta, “Pathogenicity assessment of entomopathogenic fungi infecting Leptoglossus occidentalis (Heteroptera: Coreidae),” Czech Mycology, vol. 62, no. 1, pp. 67–78, 2010.
View at: Publisher Site | Google Scholar
W. S. Abbott, “A method of computing the effectiveness of an insecticide,” Journal of Economic Entomology, vol. 18, no. 2, pp. 265–267, 1925.
View at: Publisher Site | Google Scholar
H. Chi and H. Liu, “Two new methods for the study of insect population ecology,” Bulletin of the Institute of Zoology, Academia Sinica, vol. 24, no. 2, pp. 225–240, 1985.
View at: Google Scholar
H. Chi, “Life-table analysis incorporating both sexes and variable development rates among individuals,” Environmental Entomology, vol. 17, no. 1, pp. 26–34, 1988.
View at: Publisher Site | Google Scholar
H. Chi, TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis, vol. 197, 2015, http://140.120.
Y. B. Huang and H. Chi, “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 Science, vol. 19, no. 2, pp. 263–273, 2012.
View at: Publisher Site | Google Scholar
I. Akca, T. Ayvaz, E. Yazici, C. L. Smith, and H. Chi, “Demography and population projection of Aphis fabae (Hemiptera: Aphididae): with additional comments on life table research criteria,” Journal of Economic Entomology, vol. 108, no. 4, pp. 1466–1478, 2015.
View at: Publisher Site | Google Scholar
J. H. Chang and Y. P. He, “The analysis for comparing the pesticide toxicity data using the Polo software,” Acta Agriculturae Zhejiangensis, vol. 26, no. 6, pp. 1552–1557, 2014.
View at: Google Scholar
A. Ali, M. A. Rashid, Q. Y. Huang, and C. L. Lei, “Effect of UV-A radiation as an environmental stress on the development, longevity, and reproduction of the oriental armyworm, Mythimna separata (Lepidoptera: Noctuidae),” Environmental Science and Pollution Research, vol. 23, no. 17, pp. 17002–17007, 2016.
View at: Publisher Site | Google Scholar
G. W. Felton and C. B. Summers, “Antioxidant systems in insects,” Archives of Insect Biochemistry and Physiology, vol. 29, no. 2, pp. 187–197, 1995.
View at: Publisher Site | Google Scholar
W. Wang, C. Gao, L. Ren, and Y. Luo, “The effect of longwave ultraviolet light radiation on Dendrolimus tabulaeformis antioxidant and detoxifying enzymes,” Insects, vol. 11, no. 1, pp. 1–11, 2020.
View at: Google Scholar
A. Ali, M. A. Rashid, Q. Y. Huang, and C. L. Lei, “Influence of UV-A radiation on oxidative stress and antioxidant enzymes in Mythimna separata (Lepidoptera: Noctuidae),” Environmental Science and Pollution Research, vol. 24, no. 9, pp. 8392–8398, 2017.
View at: Publisher Site | Google Scholar
D. Zhou, Y. Du, J. Yang et al., “Effect of UV-B radiation in successive generation on the activity og protective enzymes in the grain aphid, Sitobion avenae (Hemiptera: Aphididae),” Acta Entomologica Sinica, vol. 57, no. 7, pp. 762–768, 2014.
View at: Google Scholar
L. Haddouche, A. Phalak, and R. V. Tikekar, “Inactivation of polyphenol oxidase using 254 nm ultraviolet light in a model system,” LWT - Food Science and Technology, vol. 62, no. 1, pp. 97–103, 2015.
View at: Publisher Site | Google Scholar
G. C. Williams, “Natural selection, the costs of reproduction, and a refinement of lack’s principle,” The American Naturalist, vol. 100, no. 916, pp. 687–690, 1966.
View at: Publisher Site | Google Scholar
A. Ohkawara and K. M. Halprin, “Ultraviolet light and glycogen formation in the human epidermis,” Archives of Dermatology, vol. 95, no. 4, pp. 416–421, 1967.
View at: Publisher Site | Google Scholar
A. Ohkawara, K. M. Halprin, and V. Levine, “Glycogen metabolism following ultraviolet irradiation,” The Journal of Investigative Dermatology, vol. 59, no. 3, pp. 264–268, 1972.
View at: Publisher Site | Google Scholar
J. Tian, H. Diao, L. Liang, C. Hao, S. Arthurs, and R. Ma, “Pathogenicity of Isaria fumosorosea to Bemisia tabaci, with some observations on the fungal infection process and host immune response,” Journal of Invertebrate Pathology, vol. 130, pp. 147–153, 2015.
View at: Publisher Site | Google Scholar
T. T. Santos, E. D. Quintela, G. M. Mascarin, and M. V. Santana, “Enhanced mortality of Bemisia tabaci nymphs by Isaria javanica combined with sublethal doses of chemical insecticides,” Journal of Applied Entomology, vol. 142, no. 6, pp. 598–609, 2018.
View at: Google Scholar
X. Wang, J. Xu, X. Wang et al., “Isaria fumosorosea-based zero-valent iron nanoparticles affect the growth and survival of sweet potato whitefly, Bemisia tabaci (Gennadius),” Pest Management Science, vol. 75, no. 8, pp. 2174–2181, 2019.
View at: Publisher Site | Google Scholar
C. Zou, L. Li, T. Dong, B. Zhang, and Q. Hu, “Joint action of the entomopathogenic fungus Isaria fumosorosea and four chemical insecticides against the whitefly Bemisia tabaci,” Biocontrol Science and Technology, vol. 24, no. 3, pp. 315–324, 2014.
View at: Publisher Site | Google Scholar
J. Rotem, “The role of solar radiation, especially ultraviolet, in the mortality of fungal spores,” Phytopathology, vol. 75, no. 5, pp. 510–514, 1985.
View at: Publisher Site | Google Scholar
N. D. Paul, R. J. Jacobson, A. Taylor, J. J. Wargent, and J. P. Moore, “The use of wavelength-selective plastic cladding materials in horticulture: understanding of crop and fungal responses through the assessment of biological spectral weighting functions,” Photochemistry and Photobiology, vol. 81, no. 5, pp. 1052–1060, 2005.
View at: Publisher Site | Google Scholar
K. K. Newsham, M. N. R. Low, A. R. McLeod, P. D. Greenslade, and B. A. Emmett, “Ultraviolet-B radiation influences the abundance and distribution of phylloplane fungi on pedunculate oak (Quercus robur),” New Phytologist, vol. 136, no. 2, pp. 287–297, 1997.
View at: Publisher Site | Google Scholar
G. U. L. Braga, S. D. Flint, C. D. Miller, A. J. Anderson, and D. W. Roberts, “Both solar UVA and UVB radiation impair conidial culturability and delay germination in the entomopathogenic fungus Metarhizium anisopliae,” Photochemistry and Photobiology, vol. 74, no. 5, p. 734, 2001.
View at: Google Scholar
G. U. L. Braga, S. D. Flint, C. L. Messias, A. J. Anderson, and D. W. Roberts, “Effects of UVB irradiance on conidia and germinants of the entomopathogenic hyphomycete Metarhizium anisopliae: a study of reciprocity and recovery,” Photochemistry and Photobiology, vol. 73, no. 2, p. 140, 2001.
View at: Google Scholar
L. Englander, M. Browning, and P. W. Tooley, “Growth and sporulation of Phytophthora ramorum in vitro in response to temperature and light,” Mycologia, vol. 95, no. 3, pp. 365–373, 2006.
View at: Google Scholar
A. Fourtouni, Y. Manetas, and C. Christias, “Effects of UV-B radiation on growth, pigmentation, and spore production in the phytopathogenic fungus Alternaria solani,” Canadian Journal of Botany, vol. 76, no. 12, pp. 2093–2099, 1998.
View at: Google Scholar
M. P. Santos, L. P. Dias, P. C. Ferreira, L. A. A. P. Pasin, and D. E. N. Rangel, “Cold activity and tolerance of the entomopathogenic fungus Tolypocladium spp. to UV-B irradiation and heat,” Journal of Invertebrate Pathology, vol. 108, no. 3, pp. 209–213, 2011.
View at: Publisher Site | Google Scholar
A. Idnurm, “Light sensing in Aspergillus fumigatus highlights the case for establishing new models for fungal photobiology,” mBio, vol. 4, article e00260, 2013.
View at: Google Scholar
P. Cheng, Z. Ma, X. Wang et al., “Impact of UV-B radiation on aspects of germination and epidemiological components of three major physiological races of Puccinia striiformis f. sp. tritici,” Crop Protection, vol. 65, pp. 6–14, 2014.
View at: Publisher Site | Google Scholar
P. Cochard, T. Galstian, and C. Cloutier, “The proportion of blue light affects parasitoid wasp behavior in LED-extended photoperiod in greenhouses: increased parasitism and offspring sex ratio bias,” Biological Control, vol. 133, pp. 9–17, 2019.
View at: Google Scholar
F. Moreno, I. Pérez-Moreno, and V. Marco, “Effects of Lobesia botrana (Lepidoptera: Tortricidae) egg age, density, and UV treatment on parasitism and development of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae),” Environmental Entomology, vol. 38, no. 5, pp. 1513–1520, 2009.
View at: Publisher Site | Google Scholar
M. Nakajima and H. Yoshida, “Studies on ultraviolet sensitivity in silkworm, with special reference to variations in its killing effect during the larval instar stage,” Japanese Journal of Applied Entomology and Zoology, vol. 15, no. 1, pp. 17–22, 1971.
View at: Publisher Site | Google Scholar
M. Nakajima and H. Yoshida, “Studies on ultraviolet sensitivity in the silkworm, with special reference to the effect of uv-irradiation on melanin formation in the cuticle of the striped silkworm,” Japanese Journal of Applied Entomology and Zoology, vol. 15, no. 2, pp. 51–55, 1971.
View at: Publisher Site | Google Scholar
D. R. A. Wharton, “Ultraviolet repellent and lethal action on the American cockroach,” Journal of Economic Entomology, vol. 64, no. 1, pp. 252–255, 1971.
View at: Publisher Site | Google Scholar
S. H. Cohen, J. A. Sousa, and J. F. Roach, “Effects of UV irradiation on nymphs of five species of cockroaches,” Journal of Economic Entomology, vol. 66, no. 4, pp. 859–862, 1973.
View at: Publisher Site | Google Scholar
S. H. Cohen, J. A. Saousa, J. F. Roach, and J. B. Gingrich, “Effects of UV irradiation on nymphs of Blattella germanica and Periplaneta americana,” Journal of Economic Entomology, vol. 68, no. 5, pp. 687–693, 1975.
View at: Publisher Site | Google Scholar
C. P. Bonsignore, G. Vono, and U. Bernardo, “Environmental thermal levels affect the phenological relationships between the chestnut gall wasp and its parasitoids,” Physiological Entomology, vol. 44, no. 2, pp. 87–98, 2019.
View at: Publisher Site | Google Scholar
W. H. Van Der Putten, M. Macel, and M. E. Visser, “Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 365, no. 1549, pp. 2025–2034, 2010.
View at: Publisher Site | Google Scholar
C. P. Bonsignore and U. Bernardo, “Effects of environmental parameters on the chestnut gall wasp and its complex of indigenous parasitoids,” Science of Nature, vol. 105, no. 3-4, p. 20, 2018.
View at: Publisher Site | Google Scholar
C. P. Bonsignore, G. Vizzari, G. Vono, and U. Bernardo, “Short-term cold stress affects parasitism on the asian chestnut gall wasp Dryocosmus kuriphilus,” Insects, vol. 11, no. 12, p. 841, 2020.
View at: Google Scholar
X. Liu, C. E. Williams, J. A. Nemacheck et al., “Reactive oxygen species are involved in plant defense against a gall midge,” Plant Physiology, vol. 152, no. 2, pp. 985–999, 2010.
View at: Publisher Site | Google Scholar
C. Lamb and R. A. Dixon, “The oxidative burst in plant disease resistance,” Annual Review of Plant Biology, vol. 48, no. 1, pp. 251–275, 1997.
View at: Publisher Site | Google Scholar
J. Dat, S. Vandenabeele, E. Vranová, M. Van Montagu, D. Inzé, and F. Van Breusegem, “Dual action of the active oxygen species during plant stress responses,” Cellular and Molecular Life Sciences, vol. 57, no. 5, pp. 779–795, 2000.
View at: Publisher Site | Google Scholar
J. J. Grant and G. J. Loake, “Role of reactive oxygen intermediates and cognate redox signaling in disease resistance,” Plant Physiology, vol. 124, pp. 24–31, 2000.
View at: Google Scholar
C. Ouhibi, H. Attia, P. Nicot et al., “Effects of nitrogen supply and of UV-C irradiation on the susceptibility of Lactuca sativa L to Botrytis cinerea and Sclerotinia minor,” Plant and Soil, vol. 393, no. 1–2, pp. 35–46, 2015.
View at: Publisher Site | Google Scholar
M. T. Charles, N. Benhamou, and J. Arul, “Physiological basis of UV-C induced resistance to Botrytis cinerea in tomato fruit. III. Ultrastructural modifications and their impact on fungal colonization,” Postharvest Biology and Technology, vol. 47, no. 1, pp. 27–40, 2008.
View at: Publisher Site | Google Scholar
O. Windram, P. Madhou, S. Mchattie et al., “Arabidopsis defense against Botrytis cinerea: chronology and regulation deciphered by high-resolution temporal transcriptomic analysis,” Plant Cell, vol. 24, no. 9, pp. 3530–3557, 2012.
View at: Google Scholar
C. Stevens, V. A. Khan, J. Y. Lu et al., “Induced resistance of sweetpotato to Fusarium root rot by UV-C hormesis,” Crop Protection, vol. 18, no. 7, pp. 463–470, 1999.
View at: Publisher Site | Google Scholar
G. D’Hallewin, M. Schirra, M. Pala, and S. Ben-Yehoshua, “Ultraviolet C irradiation at 0.5 kJ·m-2 reduces decay without causing damage or affecting postharvest quality of Star Ruby grapefruit (C. paradisi Macf.),” Journal of Agricultural and Food Chemistry, vol. 48, no. 10, pp. 4571–4575, 2000.
View at: Publisher Site | Google Scholar
V. G. Kakani, K. R. Reddy, D. Zhao, and A. R. Mohammed, “Effects of ultraviolet-B radiation on cotton (Gossypium hirsutum L.) morphology and anatomy,” Annals of Botany, vol. 91, no. 7, pp. 817–826, 2003.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2021 Muhammad Musa Khan et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies

Views

961

Downloads

771

Citations