Irradiation has been recognized and endorsed as a potential phytosanitary measure that could be an alternative to current quarantine treatments. Dosages of 50, 100, 150, 200 and 250 Gy (Grays) were used to irradiate three different life stages (eggs, immatures, and adults) of Planococcus minor (Maskell), focusing on females due to its parthenogenesis ability, with an aim to find the most tolerant stage and the most optimum dose to control P. minor. Cobalt 60 was the source of irradiation used. Irradiation of 150 - 250 Gy has a significant effect on all life stages of P. minor, decreasing its survival rate, percentage adult reproduction, oviposition and fertility rate. The adult was the most tolerant life stage in both mortality and fertility rate. All the different irradiated target life stage groups oviposited eggs but none of the F2 eggs hatched at the most optimum dosage of 150 to 250 Gy.
KEYWORDS: Planococcus minor, Ionizing radiation, Quarantine
Planococcus minor (Maskell) (Hemiptera: Pseudococcidae) is a significant pest of more than 250 host plants in the Afrotropical, Australasian, Nearctic, Neotropical, and Oriental regions (Williams 1985, Ben-Dov 1994, USDA 2000, CAB 2003). P. minor is a phloem feeder, and in general this may cause reduced yield, reduced plant or fruit quality, stunting, discoloration and defoliation. Indirect or secondary damage is caused by sooty mold growth on honeydew produced by this mealybug. Important plant viruses may also be vectored by P. minor (Williams 1985, Cox 1989).
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Ionizing radiation has been recognized as an alternative to methyl bromide for treating agricultural products in order to overcome quarantine barriers in trade (FAO 2003). Several authors have presented reviews of this subject in the last two decades (Burditt 1994, Nation and Burditt 1994, Hallman 1998, 2000, 2001, Johnson and Marcotte 1999). Irradiation treatment does not affect the quality of many commodities, it is comparatively safe to the environment and consumers, and does not need to kill the insects to provide quarantine security. Irradiation has been successfully used for the control of many insect pests such as apple maggot (Rhagoletis pomonella), coddling moth (Cydia pomonella), coconut scale (Aspidiotus destructor) (Follett 2006), carambola fruit borer (Eucosma notanthes) (Lin et al. 2003), huhu beetle, (Prionolplus reticularis) (Lester et al. 2000), rice weevil (Sitophilus zeamais) (Hu et al. 2003), Mango seed weevil (Sternochetus mangiferae) (Follett 2001), and cigarette beetle (Lasioderma serricorne) (Hu et al. 2002). Among insects, Diptera (flies), Coleoptera (beetles), Hemiptera (true bugs) tend to be less radio-tolerant than Lepidoptera (moths and butterflies), although there is a considerable variation among the species that have been tested within these groups (Hallman 2000, Bakri et al. 2005, Follet et al. 2007).
Geography and environmental conditions of Taiwan provide one of the most favorable conditions for P. minor to establish its population. Irradiation continues to be a topic of interest in Taiwan, with several studies published recently on pests of stored products, such as the cigarette beetle, L. serricorne (Hu et al. 2002), rice weevil, S. zeamais (Hu et al. 2003) and the carambola fruit borer, E. notanthes (Lin et al. 2003). In this study, we discuss (1) effects of radiation on the, mortality, development, adult reproduction, oviposited eggs, and fertility of F1 and F2 generation of P. minor, and (2) to identify an effective radiation dose for P. minor.
Materials and Methods
In order to obtain mixed-age colonies for irradiation tests, wild strains of P. minor were collected from Taichung District Agricultural Research and Extension Centre, Council Of Agriculture, Taichung, Taiwan (ROC) in 2006. One hundred mixed immature stages of P. minor were carefully removed from the parent colony using a new soft paint brush (0.5 mm bristles) and equally distributed to uninfested Irish potatoes (Solanum tuberosum). Fresh colonies of P. minor were reared under close laboratory observations at the Insect-Plant Interaction laboratory in National Chung Hsing University, Taichung, Taiwan. A stereo-microscope was used to separate and distribute the immature stages on the outer surfaces of uninfested Irish potatoes. These newly infested Irish potatoes were placed on small petri dishes (d = 6 cm, 42.39 cm³, Alpha Plus Scientific Corporation, Taoyuan, Taiwan) in 500 ml round plastic containers (d = 14 cm, 1846.32 cm³, Day Young Enterprise Company Limited, Chang- Hua, Taiwan) to establish new colonies. Cloth nettings (1521 meshes/ cm², Hsing Guang Hang Company, Taichung, Taiwan) were used as lids of the containers for good aeration. The procedure was repeatedly performed under close laboratory observation to maintain available colonies for the research. Rearing conditions for P. minor during the duration of the experiments were 29 ± 5â„ƒ, photoperiod of 14:10 (L: D) and 70 % relative humidity.
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Under our laboratory conditions a female adult was capable of ovipositing more than 300 eggs. Due to parthenogenesis among these insects, we focused our study on female performance, since it would be biased to assume that the eggs oviposited were results of successful mating. We selected and used eggs that were 7- 14 days old because it took about 7- 14 days for these eggs to hatch to first instar.
In order to study the most irradiation tolerant stage, each irradiation test consisted of mixed life stages of P. minor. Five skin portions comprising of mixed life stages of P.minor colonies were transferred into five respective clean plastic cups (d = 9 cm, 368.79 cm³, Alpha Plus Scientific Corporation, Taoyuan, Taiwan). A slit of approximately 2 cm in length was made on each of the container lid in order to allow aeration. The first cup was irradiated at 50 Gy, the second at 100 Gy, third at 150 Gy, fourth at 200 Gy, and the fifth cup at 250 Gy. A non-irradiated control was handled in the same manner to compare the results. After irradiation, each cup was sealed in separate plastic containers (d = 14 cm, 1846.32 cm³, Day Young Enterprise Company Limited, Chang- Hua, Taiwan). Follett et al. (2007) suggested that generally five doses should be selected and five replicates of at least 30-50 insects should be used. In this study three replicates were irradiated at different time intervals. One hundred insects of each life stage were studied for each replicate of each dose. The irradiation treatment was conducted using a 30 kCi cobalt- 60 hot cell at the Nuclear Science and Technology Development Center, National Tsing Hua University, Hsinchu, Taiwan. The irradiation discs containing respective insect set-ups were rotated ten times per minute to ensure that the irradiated sample received a well-distributed radiation dose with a constant dose rate of 2 kGy/ h for various time intervals in order to obtain 0, 50, 100, 150, 200 and 250 Gy of gamma rays. The absorbed dose was measured using silver dichromate dosimeter. Immediately after irradiation, the irradiated consignments and control were transported back to the Insect-Plant Interaction laboratory in NCHU, Taichung, Taiwan, which is approximately one and a half hours drive away.
Right after arrival to NCHU, one hundred individuals of different life stages were carefully removed from irradiated mixed life stage colonies using a soft paint brush (0.5 mm bristles) and were equally distributed to uninfested potatoes in clean separate plastic containers (d = 14 cm, 1846.32 cm³, Day Young Enterprise Company Limited, Chang- Hua, Taiwan). Each container was separated from other treatments and sealed with cloth nettings (1521 meshes/ cm², Hsing Guang Hang Company, Taichung, Taiwan) as lids. The removal of individual insects from its irradiated parent colony was done with close observation under the microscope mainly due to the small size of P. minor. A separate and new soft paint brush (0.5 mm bristles) was used for every transfer of different individual life stage for every treatment to avoid mixture of life stages or mixture of irradiated insects of different irradiation dosages. Non irradiated control was used for each size class and was handled similarly to treated P. minor. These procedures ensure that no individual life stage is accidentally transferred to a different life stage set up. After irradiation treatment, the insects were held for 4- 8 weeks for observation on mortality rate, percentage of adult reproduction, number of oviposited eggs, and fertility of eggs for the new progeny. Irradiated P. minor which did not lay viable eggs, especially at 150- 250 Gy were observed until they all died, similarly all eggs that did not hatch at 150- 250 Gy were observed until they all died.
All data were subjected to analysis of variance (ANOVA) and regression analysis using the General Linear Model (GLM) procedure of Statistic Analysis System (SAS; SAS Institute, Cary, NC, USA; Version 9.1) followed by Tukey's test. A probability of P < 0.05 was considered significant. The percentage data were transformed into arsine before ANOVA analysis.
The criterion used for survival success in this research was based on the number of eggs that were able to hatch 7- 14 days after irradiation. Irradiated eggs of P. minor which survived to first instar after irradiation decreased from 96 % in the control group to 14 % in 250 Gy (Fig. 1a). Although there was no significant difference (P > 0.05, Tukey test) in mortality rate between 150 and 200 Gy and also between 200 and 250 Gy, significant difference (Y = 88.38 - 0.31x, r2 = 0.95) was achieved with increasing dosages from 50 to 250 Gy (Fig. 1a). Of those individuals which successfully emerged from irradiated eggs, there was no significant difference (P= 0.4392, df = 5, 2, Tukey test) compared with the survivorship to adult stage of the control group (Fig. 1b). However, irradiated P. minor were much weaker, stunted in growth, slow and easily fell off the surfaces of the host commodity upon disturbance (slight movement of the host commodity).
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Percentage (%) of adult reproduction
The criterion used for percentage of adult reproduction in this research was based upon the reproductive success of females that developed from irradiated eggs. In the control group, 90.20 % of females reared from eggs produced eggs themselves. Although increasing dosages of irradiation led to significant decrease (Y = 70.51 - 0.16x, r2 = 0.63) in the number of females that were able to lay eggs, there was no significant difference (P= 0.4392, F = 1.08, Tukey test) in the percentage (%) of adults reproducing among different dosages of irradiation used (Fig. 1c). It was not clear whether the reproduction percentage of these adult females were result of sexual reproduction or parthenogenesis. Adults within the five irradiation treatments that could not lay eggs were believed to be affected by irradiation in comparison to the control group which showed high number of adult females laying eggs.
The oviposited eggs were calculated according to the number of eggs that were laid by reproductive females. The number of eggs oviposited per reproductive adults irradiated as eggs was significantly lower (Y = 295.20 - 1.20x, r2 = 0.90) at all treatment levels in comparison to insects in the control group (Fig. 1d). At 200 Gy, the number of eggs oviposited was insignificant to 150 and 250 Gy even though they were all increasingly low (Fig. 1d). Females that oviposited laid an average of 86.60 eggs at 150 Gy and an average of 82.50 eggs at 250 Gy compared to the control group which laid an average of 311.60 eggs (Fig. 1d). Fig. 1d shows that the lowest irradiation dosage of 50 Gy had a drastic effect on the number of eggs oviposited by reproductive females which survived from the egg stage. All dosages of gamma irradiation had an impact with the amount of eggs oviposited by reproductive females which survived from irradiated eggs compared to the control group.
The impact of irradiation on the fertility of all oviposited eggs showed significant difference (Y = 90.15 - 0.48x, r2 = 0.94) compared to the control group (Fig. 1e). A total of 93.06 % of eggs oviposited in control group hatched to first instar while irradiation halted hatching of eggs at 150 to 250 Gy. At 50 Gy, 62.14 % of eggs hatched which showed significant difference with both the control group and the 41.15 % of eggs that hatched at 100 Gy. The hatch rate significantly decreased with increasing irradiation dosages to 100 Gy. There were low numbers of eggs which did not hatch from 150 to 250 Gy and in turn halted the hatching of eggs to the new generation. The hatch rate of eggs from reproductive females which survived from irradiated eggs significantly decreased with increasing dosages of irradiation compared to the control group.
Irradiated Immature Stages
The number of immature stages which survived irradiation from irradiated immature stages of P. minor decreased with increasing dosages of irradiation (Y = 90.87 - 0.30x, r2 = 0.95). The lowest dose of 50 Gy, showed significant decrease on the survival rate of P. minor to 66.67 % from 97.67 % compared to the control group (Fig. 2a). There was no significant difference between the survival rate of 50 Gy treated immatures compared to survival rate of 100 Gy treated immatures where 63.67 % of survival was recorded (Fig. 2a). The survival rate of immatures at 150 Gy was 43 % thus there was no significant difference between the survival rates of 200 (27.67 %) and 250 Gy (19 %). Irradiated immature stages were stunted in growth and were gravely weak compared to the control group. Some of these immature stages though lived could not survive to adult stage especially under 250 Gy which saw only 84.94 % of those that survived the irradiation developing to adult stage (Fig. 2b). This was significantly low compared to other immature stages irradiated under lower dosages. Although 95.23 % of immature stages irradiated at 200 Gy survived to adult stage, it was insignificant compared to the 250 Gy group and the lower dosage groups (Fig. 2b). There were no significant difference among the control group and irradiated immature stages at 50, 100 and 150 Gy.
Percentage (%) of Adult Reproduction
The number of reproductive females that survived from radiation exposure as immature stages laid eggs at a lower rate with increasing dosages of radiation. All treated immature stages were significantly (Y = 87.17 - 0.24x, r² = 0.78) affected compared to the control group (Fig. 2c). At 50 Gy, the number of reproductive females decreased to 69.60 % from 92.30 % of control group. The effects of 200 Gy was not statistically different from the effects of 250 Gy in relation to percent of adult reproduction (37.30 % and 24.50 %, respectively) and also the effects of 150 Gy were not significantly different from the effects of 100 Gy.
The dose of 50 Gy significantly decreased the number of oviposited eggs to an average of 201 eggs per adult compared to an average of 320 eggs per adult in control group. The number of oviposited eggs significantly decreased (Y = 295.26 - 1.31x, r2 = 0.87) with increasing dosages of irradiation. Each ovipositing adult oviposited an average of only 70 eggs at 250 Gy which was significantly lower compared to the mean average of 320 eggs laid per reproductive adult in the control stage. There was significant difference in the number of oviposited eggs laid by individual reproductive adults in every increasing dosage of irradiation from 50 to 200 Gy. In the 150 Gy group, an average of 95 eggs were laid per adult while adults in the 200 Gy group oviposited (Y = 295.26 - 1.31x, r2 = 0.87) an average of 83 eggs per individual (Fig. 2d).
The impact of irradiation on the fertility rate of all oviposited eggs of the new progeny showed significant difference compared to the control group Y = (91.54 - 0.51x, r2 = 0.94) (Fig. 2e). About 93.31 % of eggs oviposited in control group hatched to F2 immature stages while irradiation halted hatching of eggs at 150 to 250 Gy. At 50 Gy, 64.24 % of eggs hatched which was significantly different from the control and the 100 Gy treated groups (93.31 % and 44.28 %, respectively) to both the control group and the 44.28 % of eggs which hatched at 100 Gy. The dosages from 150 to 250 Gy successfully stop the hatching of eggs to F2 generation.
Mortality/ Survival Rate
Increasing doses of irradiation decreased the survival rate of adults compared to the control group (Y = 96.06 - 0.29x, r2 = 0.98). The dose of 50 Gy decreased the survival rate to 83 % compared to the 97.70 % survival rate of control group (Fig. 3a). Mortality rate at 250 Gy was high with only 26 % survival rate. The dose of 100 Gy decreased the survival rate to 65 % compared to the 47.70 % of 150 Gy group and 37.30 % in 200 Gy group (Fig. 3a). The surviving adults were very weak and stunted compared to the control group.
Percentage (%) of Adult Reproduction
The effect of radiation on reproductive adult stage of P. minor females rapidly decreased the percentage of adult reproduction compared to the number of females that were able to oviposit in the control group (Fig. 3b). Adult females that were exposed from 50 to 250 Gy showed a significant decrease in their capability to oviposit. The percentage of adult reproduction was determined by the number of females that survived and were able to oviposit. Whether the number of females that laid eggs is the result of successful mating was not clear since P. minor is also capable of parthenogenesis. The low number of irradiated females which were capable of laying eggs was not significantly different among different irradiation doses though were comparatively lower compared to the control stage. The 50 Gy (44.65 %) group and 100 Gy (42.36 %) group percentages of adult reproduction were not significantly different from each other, but were twice lower than the control group (Fig. 3b).
The total number of eggs oviposited by individual females rapidly decreased with increasing doses of radiation (Y = 310.48 - 1.25x, r2 = 0.89) (Fig. 3c). The number of eggs oviposited by the 50 Gy treated group, 223.1 eggs, was significantly lower than controls, 327.10 eggs. The 100 Gy dose resulted in an average of 153.20 eggs oviposited per female adults. At 200 and 250 Gy, though the female adults were able to oviposit, the number of eggs laid was significantly lower compared to the effects of the lower dosages of irradiation. Under 250 Gy, ten of the surviving female adults were able to lay an average of 81 eggs which was about 1/3 lower than those laid per female in control group (Fig. 3c).
Similar to treated immature and egg stages, the impact of radiation on the hatch rate of all F2 oviposited eggs of irradiated adults was significantly lower as compared to the control group ( Y= 91.59 - 0.45x, r2 = 0.92)(Fig. 3d). About 92.41 % of eggs oviposited in control group hatched to F2 immature stage while irradiation at 150 to 250 Gy impaired egg hatch. At 50 Gy 68.40 % of eggs hatched which was significantly different to both the control group and the 100 Gy grouping which 92.41 and 49.45 % of eggs hatched, respectively. None of the relatively few eggs produced by insects treated with 150 to 250 Gy hatched (Fig. 3d).
Among insects, many irradiation studies have been performed on Diptera (flies) and Coleoptera (beetles) which tend to be less radio tolerant than Lepidoptera (moths and butterflies), although there is a considerable variation among the species that have been tested within these groups (Hallman 2000, Bakri et al. 2005). Estimates for Hemiptera (scales, mealybugs, aphids and whiteflies) and Thysanoptera (thrips) are based on a small number of studies.
Our focus was similar to studies conducted on other insects such as tephritid fruit flies reported in past papers (Follett et al. 2007), preventing adult emergence may be difficult so adult sterility is the goal. Adult sterility has been the focus of many irradiation treatments in the control of many insect pests (Lester et al. 2000, Follett 2001, 2006, Lin et al. 2003, Hu et al. 2002, 2003).
Our result shows that the increasing doses did not cause 100% mortality in all irradiated life stages, however surviving insects were drastically affected in later performances such as reduced percentage of adult reproduction (ability of female adults to lay eggs), reduced numbers of oviposited eggs, which all finally results in oviposited F2 eggs failing to hatch following treatments at 150 Gy to 250 Gy, thus indicating sterility in adult stage. Unlike other disinfestation techniques, irradiation does not need to kill the pest immediately to provide quarantine security, and therefore live (but sterile or not viable) insects may occur with the exported commodity making inspection for the target pests redundant as a confirmation of treatment application and efficacy (Follett et al. 2007).
Our results show that both, the hatching rate of irradiated eggs and the fertility rate of eggs oviposited by female adults of all irradiated life stages of P. minor, decrease with increasing doses of radiation. Previous studies (Hasan and Khan 1998, Faruki et al. 2007) on other insects also showed that increasing doses of radiation decreased the percent egg hatch. Yang and Sacher (1969) reported a delay in development that was proportional to the radiation doses. Thus, this delay could have a physiological effect on the biological structure of the insect that would affect its later development, possibly resulting to sterility of reproductive adults.
In this study, 150 to 250 Gy was the optimum dosage to sterile adult P. minor. At 150 to 250 Gy, there were no new progeny for all indicated life stages indicating that 150 Gy is sufficient to provide sterility for insects studied in our experiment. Similar result as a baseline to determine the optimum dosage was used by Follett (2006). The optimal dose for male insects to be released in a Sterile Insect Technique (SIT) programme depends on their level of sterility and competitiveness (Helinski et al. 2006). Since parthenogenesis was high among P. minor, females were the main target thus the same standard of sterility was thoroughly considered. Follett et al. (2007) also reported that females are usually more tolerant than males furthermore; sex tolerant stage determination is only performed when the method of reproduction is uncertain.
Our study provides one of the few ground breaking results for the usage of irradiation against Hemiptera insects, particularly Pacific mealybug, P. minor. Our research uniquely focuses on the performances of eggs, immatures and adults especially female because of the high degree of parthenogenesis that occurs. We observed similar parameters on all irradiated life stages, finally identifying that the adult is the most tolerant stage. Irradiation weakens the development, percentage adult reproduction, oviposition and hatching of eggs for P. minor. Furthermore, we conclude that 150 to 250 Gy is the optimum dosage that inhibited the hatching of eggs to a new generation, thus sterilize P. minor. We also studied the effects (unpublished) of irradiation on Custard apple, A. squamosa, a well known host of P. minor, a prospective export commodity in Taiwan. There was no significant damage or destruction found at 250 Gy. Irradiation is cheap, environmental friendly and safe, irradiated food is also safe to consume.
Our study also agrees with the proposed irradiation dose of 250 Gy by Follett et al. (2007) to sterilize or prevent generation turnover in Hemiptera insects. Very few irradiation studies have been performed on Hemiptera insect particularly P. minor, thus more comprehensive studies are needed. This study provides a scaffold to future irradiation studies for Taiwan and abroad and we strongly suggest irradiation as a control measure for P. minor.
We sincerely appreciate everyone who contributed to this research. Two anonymous reviewers also provided valuable input to improve the manuscript. God bless you.
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Fig. 1. Effects of radiation dose on eggs in terms of (1a) hatch rate of eggs (b) survival of 1st instars to adult stage (c) percent (%) reproduction of adults which developed from irradiated eggs, (d) number of oviposited eggs of adults which developed from irradiated eggs, (e) hatch rate of eggs of adults which developed from irradiated eggs. Data are expressed as mean ± SE; bars without the same letter(s) are significantly different (P < 0.05, Turkey's Test). Equations for the regression lines were Y = 88.38 - 0.31x (r2 = 0.95) for hatch rate of eggs, Y = 100.96 - 0.02x (r2 = 0.21) for survival of 1st instars to adult stage, Y = 70.51 - 0.16x (r2 = 0.63) for percentage of reproduction, Y = 295.20 - 1.20x (r2 = 0.90) for number of oviposited eggs, and Y = 90.15 - 0.48x (r2 = 0.94) for fertility rate.
Fig. 2. Effects of radiation dose on immature stage in terms of (a) survival rate of irradiated immature stages, (b) P. minor immature stages that survived to adult stage from irradiated immature stage, (c) percent (%) of reproduction of adults which developed from irradiated immature stage, (d) number of oviposited eggs of adults which developed from irradiated immature stage, (e) hatch rate of eggs of adults which developed from irradiated immature stage. Data are expressed as mean ± SE; bars without the same letter(s) are significantly different (P < 0.05). Equations for the regression lines were Y = 90.87 - 0.30x (r2 = 0.95) for survival rate of immature stages, Y = 102.22 - 0.05x (r2 = 0.53) for survival of immature stages to adult stage, Y = 87.17 - 0.24x (r2 = 0.78) for percentage of reproduction, Y = 295.26 - 1.31x (r2 = 0.87) for number of oviposited eggs, and Y = 91.54 - 0.51x (r2 = 0.94) for fertility rate.
Fig. 3. Effects of radiation dose on adults in terms of (a) survival rate of irradiated adults, (b) percent (%) of reproduction for irradiated adults, (c) number of oviposited eggs of irradiated adults, (d) hatch rate of eggs oviposited by irradiated adults. Data are expressed as mean ± SE; bars without the same letter(s) are significantly different (P < 0.05). Equations for the regression lines were Y = 96.06 - 0.29x (r2 = 0.98) for survival rate of adults, Y = 73.39 - 0.27x (r2 = 0.78) for percentage of reproduction, Y = 310.48 - 1.25x (r2 = 0.89) for number of oviposited eggs, and Y = 91.59 - 0.45x (r2 = 0.92) for fertility rate.