Journal of Integrative Agriculture 2018, 17(4): Available online at ScienceDirect

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1 Journal of Integrative Agriculture 18, 17(4: Available online at ScienceDirect RESEARCH ARTICLE Sub-lethal effects of Beauveria bassiana (Balsamo on field populations of the potato tuberworm Phthorimaea operculella Zeller in China YUAN Hui-guo 1*, WU Sheng-yong 1*, LEI Zhong-ren 1, Silvia I. Rondon 2, GAO Yu-lin 1 1 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 1193, P.R.China 2 Department of Crop and Soil Sciences, Hermiston Agricultural Research and Extension Center, Oregon State University, Hermiston, OR 97838, USA Abstract The potato tuberworm Phthorimaea operculella Zeller, is one of the most important potato pests worldwide including China. Several reports indicate that P. operculella could be controlled biologically by the use of beneficial fungus such as Beauveria bassiana (Bals.-Criv Vuill. However, limited information is available under growing conditions in China. Thus, this study evaluated the sub-lethal effects of B. bassiana on the offspring of P. operculella by the age-stage, two-sex life table. First instar larva of P. operculella were treated with conidia ml 1 of the fungus, and several biological parameters were evaluated. The fecundity, duration of the egg stage, all larval stages, pre-adult stage, and total pre-oviposition period, were significantly shorter than the control treatment. Offspring of treated parents, presented a net reproductive rate and mean generation time of per day and days, respectively, compared to per day and days for the untreated ones. This study provides basic information to help understanding the potential long-term effects of entomopathogenic fungi on P. operculella. Keywords: potato tubermoth, sub-lethal effects, biological control, management 1. Introduction The potato tuberworm, Phthorimaea operculella Zeller (Lepidoptera: Gelechiidae, is considered to be one of Received 26 August, 17 Accepted 1 January, 18 YUAN Hui-guo, Tel: ; Fax: , yhgzb123@163.com; Correspondence GAO Yu-lin, Tel: ; Fax: , gaoyulin@ caas.cn * These authors contributed equally to this study. 18 CAAS. Publishing services by Elsevier B.V. All rights reserved. doi: 1.116/S ( the most important potato (Solanum tuberosum L. pests worldwide including China. In recent years, China has been boosting potato production to become the fourth major crop produced in the country following rice, wheat and maize (Zhang et al. 17. Phthorimaea operculella has a close evolutionary relationship with Solanaceous crops that is enhanced by the insect high adaptability to daily and seasonal changes, high reproductive potential, and high survival rate even under extreme temperatures (Dogramaci et al. 8. The pest can thrive under field and storage conditions (Bacon 196; Foot 1974b; Haines 1977; Shelton and Wyman 1979a, b; Briese 1986; Herman et al. 5. In China, P. operculella was first reported in Guangxi in 1937 (Li and Zhang 5; at present, P. operculella is widely distributed in China and mainly occurs in Yunnan, Guizhou and Sichuan (Xu All these regions are key

2 YUAN Hui-guo et al. Journal of Integrative Agriculture 18, 17(4: potato production areas. The pest is difficult to control, and over the years insecticides have been used extensively (Foot 1974a; Trivedi and Rajagopal 1992, however, no resistance to pesticides has been reported yet, but basic line information to determine pesticide susceptibility has already been collected (Dobie 1. P. operculella adults deposit eggs in potato foliage or close to tubers, while the larvae mine leaves, stems, and petioles and excavate tunnels through potato tubers (Rondon et al. 7; Yuan et al. 17. This wider niche ability makes this insect difficult to control. In the U.S. Pacific Northwest, there are many pesticides registered to control P. operculella (Rondon et al. 7, while in China, there are several products that effectively control the pest (Du et al. 6; however, El-kady (11 reported that continuous use of pesticides promoted pesticide resistance in P. operculella and better management program are needed. Under low pesticide input conditions, P. operculella can be controlled effectively by the use of natural enemies (Kroschel and Koch 1996; Coll et al.. Beauveria bassiana (Bals.-Criv Vuill has proved to be an effective biological control agent of P. operculella in the laboratory (Li and Zhang 5. The advantages of using natural products such as B. bassiana are numerous, including being safe to the environment when compared to chemical insecticides, relatively easy to handle and safer to handlers. However, B. bassiana depends on favorable environmental conditions during application and they are heavily humidity dependable (Shah and Pell 3. Microbial control is not yet developed for massive commercial production and more information is still needed to prove the effectiveness of this method (Kroschel and Koch 1996; Sporleder et al. 1. In high pesticide input systems, the effect of pesticides on natural enemies of P. operculella is unknown (Koss 3. Most researches of pesticides have focused on their lethal effects on P. operculella developmental stages (Desneux et al. 7; however, data concerning sub-lethal effects are limited. In general, besides the direct mortality induced by any given pesticide, the sub-lethal effect must be considered for a completely assessment of pesticide impact and effectiveness (Desneux et al. 7. Entomopathogens are a good alternative to pesticides since they contribute to the natural regulation of arthropod populations (Evans 8. Seyed-Talebi et al. (12 studied the sub-lethal effect of B. bassiana on the life table parameters of two-spotted spider mite Tetranychus urticae Koch. They found that the duration of the immature stage was significantly longer on female when compared to male longevity, while oviposition period and fecundity were significantly lower on fungus-treated mites. Hafez et al. (1997 indicated that B. bassiana influence the longevity of P. operculella larvae and adults, however, sub-lethal effects were not thoroughly studied. In potatoes, early studies by Arthurs et al. (8 determined the effects of granulovirus and B. thuringensis for season-long control of P. operculella with mixed results. Quesada-Moraga et al. (4, Latifian et al. (1, and Seyed-Talebi et al. (12 suggested that entomopathogenic fungi should be evaluated further to determine its influence in offsprings life-history, including growth, development and reproduction. Thus, this study was designed to evaluate the sub-lethal effects of B. bassiana on different biological parameters of P. operculella. Information will provide valuable insight regarding the effects of this fungus in P. operculella that could potentially be used in pest management programs. 2. Materials and methods 2.1. Insect colony Following modifications of Gui and Li (3 and Rondon et al. (9 protocols, a colony of P. operculella was established by collecting over 5 adults in the Yunnan Province, China (13.79 E, N. Potato tuberworm adults were reared on potato tubers placed in cylindrical food containers (14 cm diameter 3.5 cm depth which were covered with a fine cheesecloth adjusted with a rubber band. Adults were fed with a 5% sugar suspension which was applied using a small brush applied in a small cotton wick. Also, a round filter paper (5 cm diameter was placed on top of the cheese cloth to be used as oviposition substrate. Eggs were collected daily, and filter paper with eggs was transferred to an empty container until hatching. After hatching, a (6±1 cm-diameter-hemispherical tuber was added as a feeding substrate; tubers were changed every other day. Also, a layer of fine sand was added at the bottom of the container to be used as a pupation substrate. Colony was kept in an environmental chamber (MLR-351H, SANYO Electric Co., Ltd., Moriguchi City, Osaka, Japan at (27±2 C, 12 h L:12 h D, and 8 9% (RH. About every two months, P. operculella adults were added to the colony to prevent introgression and to increase genetic diversity in the confined population. Insects from the colony were used in all bioassays Fungal strain A strain of B. bassiana JLGZL-14, derived from Ostrinia furnacalis (Guenee, was collected in Gongzhuling, Jilin Province, China in 11. The strain was maintained, and conidia were produced on Sabouraud dextrose agar (SDA at (26±1 C under continuous darkness. Conidia were then harvested from one- to three-week-old cultures. Conidial concentrations were determined with a haemocytometer and

3 4 YUAN Hui-guo et al. Journal of Integrative Agriculture 18, 17(4: adjusted with.5% Tween-8 in sterile water. Suspension was diluted to conidia ml 1. Subsample of the conidial suspension was placed in a shaking plate for culture at (26±1 C, 195 r min 1 for 16 h. A haemocytometer was used to count the total number of conidia and conidial germination under the microscope (Li 15. Germination rate of fungal conidia was>9% Bioassays In bioassays, two treatments were used: (1 fungus treated (FT, where first instar P. operculella larvae were dipped for 5 s in a conidial suspension (1 1 7 conidia ml 1, which is the concentration based on the median lethal concentration (LC 5 against 3rd instar larvae of P. operculella in our preliminary test; (2 control treatment (CT, where larvae were dipped in.5% Tween-8. To determine the effect of B. bassiana on P. operculella survival, larvae were collected from filter papers with a small brush and transferred to a Petri dish (7 cm diameter containing 1 ml of conidia suspension for immersion. P. operculella larvae were allowed to dry on a separate filter paper for 5 s and then carefully transferred to a separate Petri dish which was placed over an arena containing a layer of fine sand and two cuboid potato tubers (2 cm 2 cm 2 cm which served as a food source. Larvae of and 5 were used in FT and CT, respectively. Both, fungal and control treatments, were replicated four times. Each arena was placed in an environmental chamber ((27±2 C, RH (8 9%, 12 h L: 12 h D. Once the P. operculella reached the pupae stage, pupae were harvested and used in the life table study. Survival was estimated by counting the number of larvae that reached the pupal stage. Pupae that developed from larvae exposed to B. bassiana are referred to as FT pupae, and those that were treated with sterile water containing Tween-8 are referred to as CT pupae Life table study A sub-sample of FT (n= and CT (n= pupae were sexed and placed in a cylindrical food container (14 cm diameter 3.5 cm depth. For each treatment, about h after adult emergence, egg laying started. A circular filter paper served as oviposition substrate. A sub-sample of forty eggs was separately collected from FT and CT and then placed in containers (3.5 cm in diameter 8 cm depth until hatching. After hatching, a single newly hatched first instar larva was placed in an individual container (3.5 cm in diameter 8 cm depth containing a potato tuber cube (2 cm 2 cm 2 cm that served as a food source. The lid of the container was pricked to allow ventilation and the potato tuber cube was changed every three days. The developmental stage and survival of each P. operculella life stage were recorded daily for each treatment. Each immature stage was determined based on measuring the cephalic capsule. Once the larvae reached the pupal stage; pupae were again separated by sex and transferred to a 6 cm wide 8 cm depth container tighten with a fine cloth adjusted with a rubber band. After emergence, one male and one female were placed together and oviposition was measured by counting daily the number of eggs per filter paper. Filter paper had to be replaced on a daily basis. Adults were fed with sugar suspension. Sixteen couples were separately chosen from fungal and control treatments to assess oviposition. All measurements were made at (27±2 C and a photoperiod of 12 h L:12 h D in a growth chamber Life table analysis Number of days from egg to adulthood, survival, and female daily fecundity were analyzed according to the age-stagetwo-sex life table described by Chi and Liu (1985 and Chi (1988. Data were evaluated using the computer program TWOSEX-MSChart (Chi 12. Following Chi and Liu (1985 protocol, the age-stage-specific survival rate (s xj was determined. In the formula below, x and y were age and stage, respectively. l x was the age-specific survival rate (l x ; f xj was the age-stage-specific fecundity; was the agespecific fecundity (. Also, the intrinsic rate of increase (r, gross reproductive rate (GRR, and net reproductive rate (R were calculated. The intrinsic rate of increase (r was calculated by using the interactive bisection method and the Euler-Lotka equation: e r(x=1 l x =1 (1 x= The net reproductive rate (R, finite rate of increase (k, the mean generation time (T and gross reproductive rate (GRR were calculated as follows: x= R = l x (2 λ=e r (3 T= lnr r GRR= (5 The bootstrap technique (Efron and Tibshirani 1993 was used to estimate the means and standard errors of population parameters (Zhang et al. 15. The differences in the development times, fecundities and the population parameters between the FT and CT were compared by t-test at P<.5. According to the age-stage, two-sex life table (Chi and Liu 1985, the program TIMING-MSChart (4

4 YUAN Hui-guo et al. Journal of Integrative Agriculture 18, 17(4: was used to estimate project population growth (Chi 9. Because bootstrap technique uses random resampling, a small number of replications will generate variable means and standard errors. 3. Results Bioassay tests showed that P. operculella larvae treated with B. bassiana presented a high rate, with mortality of (9.3±2.1%, while mortality rate in the control treatment was (13.8±.7%. Moreover, B. bassiana significantly affected the growth and development of P. operculella offspring, including survival. Table 1 shows the mean number of days for each P. operculella life stages in FT and CT, respectively. The egg, pupal, and teneral stages were significantly different between the FT and CT. The immature stage was significantly higher in FT compared to the CT treatment (P<.5. No differences in longevity were observed between males and females in both treatments (both for P>.5. However, there were significant differences in the mean number eggs per female where untreated females laid a higher number of eggs as compared to treated ones (P<.5. The s xj depicts the probability that an individual will survive to age x and stage j (Fig. 1. The survival rate of 4th instar larvae of P. operculella at FT decreased rapidly and was lower than that of CT larvae. The probability from the 4th instar to pupal of FT (.61 was numerically lower than the CT (.95. The numbers of adult in the FT treatment (.4 were lower than that in CT (.85. The curve of the l x and the is shown in Fig. 2. Also, the daily mean number of offspring produced by females of age x and stage j per day is shown with the f xj (Fig. 2. The l x of FT individuals rapidly declined and the curve decline of the FT is quicker than CT. The of FT individuals is similar than the CT one. In addition, l x of FT was lower than CT. Moreover, the f x of FT treatment had a peak of at 23 d, which is lower than the peak of CT that was 46 at 24 d. The age-stage-specific life expectancy (Fig. 3, which is the expected total time of an individual of age x and stage y, was shorter for FT individuals compared to untreated ones. The age-stage-specific reproductive values (v xj described the contribution of an individual of age x and stage j to the future population. The reproductive value increased at age 21 d and reached a peak of eggs, which is loewer than the peak of CT (12.5 at later time (24 d (Fig. 4. Errors of the r, λ, R and T were calculated in the different treatments by using the bootstrap method (Table 2. Software analysis results showed that R and T were lower in FT (17 per day at 25 d compared to the CT (66 per day at 27 d. 4. Discussion The damage of P. operculella to potato plants mainly occurred during larvae period (Rondon 1. Most researches have been designed to evaluate the effect of B. bassiana on P. operculella by choosing 2nd to 4th instar larvae (Li and Zhang 5; Kaur et al. 11. The virulence of B. bassiana strain JLGZL-14 was tested against 3rd instars in our preliminary test and showed that LC 5 value was conidia ml 1, which was used to evaluate the effect on 1st instar larvae of P. operculella in this study. The bioassays showed that higher susceptibility of 1st as compared to 3rd instars. Although most of 1st instar larvae of P. operculella died from fungal infection in our study, there was still approximately 8% that successfully pupated. This result is consistent with the results reported by Li and Zhang (5. Table 1 Life history table of Phthorimaea operculella Zeller F 1 generation untreated (control or treated with Beauveria bassiana Control Treatment P-value Life stage (d Egg 4.15±.24 (4 a 2.73±.12 (4 b <.1 1st instar larva 3.82±.11 (4 a 1.97±1.42 (39 a <.1 2nd instar larva 3.11±.12 (39 a 3.±. (35 a.23 3rd instar larva 3.43±.28 (39 a 3.15±.12 (33 a.17 4th instar larva 3.85±.13 (39 a 2.5±.16 (28 b <.1 Pupa 7.12±.17 (37 a 5.1±.41 (17 b <.1 Immature 22.51±.51 (37 a 18.27±2.34 (17 b <.1 Adult longevity (d Female 36.33±1.83 (17 a 34.25±1.37 (8 a.53 Male 43.11±7.21 (15 a 36.88±2.67 (8 a <.1 TPOP 1 23± (17 a 21.86±.34 (8 b.46 Mean fecundity (egg female 1 Female 15.65±16.45 (17 a 87.7±23.32 (8 b <.1 1 TPOP was defined as the time between the day an offspring enclosed from the egg and the day of its first oviposition. The number in the bracket represents sample number (n. Data (mean±se with different letters were statistically different between control and treatment (P<.5.

5 6 YUAN Hui-guo et al. Journal of Integrative Agriculture 18, 17(4: Egg L1 L2 L3 l x f x l x L4 Pupa Female Male FT Age-stage-specific survival rate (S xj CT.8.6 Survival rate (l x.4.2 FT CT Fecundity ( Age (d Fig. 1 Age-stage-specific survival rate (s xj of Phtorimaea operculella Zeller untreated or treated with Beauveria bassiana. FT, fungus treated; CT, control treatment; L1 L4 indicate first-, second-, third- and fourth-instar-stage larvae, respectively Age (d Fig. 2 Age-specific survival rate (l x, female age-specific fecundity (f xj, age-specific fecundity of total population (, and age-specific maternity (l x of Phtorimaea operculella Zeller F 1 generation untreated or treated with Beauveria bassiana. FT, fungus treated; CT, control treatment; L1 L4 indicate first-, second-, third- and fourth-instar-stage larvae, respectively. Because of the high reproductive potential of adults (Herman et al. 5; Rondon 1, the B. bassiana-treated larvae that pupated and eclosed as adults would establish the new population and continue to damage potato plants. In addition, the economic damage on potato plants was mainly caused by larval feeding, it is critical to evaluate sub-lethal effects of B. bassiana on P. operculella larva. The age-stage, two-sex life table can accurately and precisely described the survival rate and stage structure, thereby evaluating the sub-lethal effects of B. bassiana on P. operculella. The life table study showed that the survival rate of P. operculella immatures, especially in 4th instar and pupa decreased dramatically in fungal treatment. The overlap of the stage-specific survival curves in the female and male is due to the difference of growth rate between individuals (Chi and Yang 3. In addition, the developmental periods from 1st and 3rd instar larvae were not affected by B. bassiana. Similar results were obtained by Seyed-Talebi et al. (12 who studied the development of all stages of the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae, and found that instars were not affected by fungal infection. However, immature stages (egg+larvae+pupa of FT individuals in our study were shorter than those in CT. It is hypothesized that larvae infected by fungus may have acquired and stored lesser nutrient resources than that of control larvae, which might have affected the development of an insect (Kaur et al. 11. The smaller size in the fungus-treated larvae observed during the test supported the hypothesis. Sub-lethal effects such as reduction in fecundity indicates that the fungus is invading the host (Mulock and Chandler 1. Fewer conclusive studies are available concerning sub-lethal effects of fungal pathogen on reproductive capacity of insects. Our study showed that fungal treatment resulted into significant reduction in reproductive potential. Likewise Seyed-Talebi et al. (12 reported that the fecundity was significantly lower on fungus-treated mites. Wang et al. (14 also found the R for treated whiteflies offspring is lower than that of control, which is consistent with our results. It can also be hypothesized that nutritional deficiency caused by fungal infection can drastically affect the reproduction of females which have high energetic demands.

6 YUAN Hui-guo et al. Journal of Integrative Agriculture 18, 17(4: Egg L1 L2 L3 L4 Pupa Female Male Egg L1 L2 L3 L4 Pupa Female Male FT 6 FT 15 4 Life expectancies (e xj CT Reproductive value (V xj CT Age (d Fig. 3 Age-stage-specific life expectancies (e xj of Phtorimaea operculella Zeller untreated or treated with Beauveria bassiana. FT, fungus treated; CT, control treatment; L1 L4 indicate first-, second-, third- and fourth-instar-stage larvae, respectively. Table 2 Estimated population parameters (mean±se for Phthorimaea operculella Zeller F 1 population untreated (control or treated with Beauveria bassiana Parameter Control Treatment Intrinsic rate of increase (no. d 1.15±.18 a.11±.2 a Finite rate of increase (no. d ±.2 a 1.12±.2 a Net reproductive rate 65.8±27.6 a 17.43±7. b (offspring individual 1 Mean generation time (d 26.51±.31 a 25.±.48 b Different letters indicate significant different between control and treatment (P<.5. We showed that B. bassiana not only has high pathogenicity to P. operculella larvae, but also cause sublethal effects, which include shortening the development period of one generation, reducing the fecundity of female of offspring, and affecting their population parameters. In addition, malformations in offspring wings were observed after fungal treatment. This study provides Age (d Fig. 4 Age-stage-reproductive value (v xj of Phtorimaea operculella Zeller untreated or treated with Beauveria bassiana. FT, fungus treated; CT, control treatment; L1 L4 indicate first-, second-, third- and fourth-instar-stage larvae, respectively. the basic information to help us understand the effects of entomopathogenic fungi on P. operculella larvae and demonstrated that the strain of B. bassiana, JLGZL-14, has potential for control of P. operculella with a concentration of conidia ml 1. Field studies that spray with B. bassiana suspension are necessary to determine their outcome in the suppression of the target pest, P. operculella. 5. Conclusion This study provides the basic information to help us understand the effects of entomopathogenic fungi on P. operculella larvae and demonstrated that the strain of Beauveria bassiana, JLGZL-14, has potential for control of P. operculella with a concentration of conidia ml 1. Acknowledgements The research project was supported by the External Cooperation Program of Yunnan Province, China

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