J. Crop Prot. 2012, 1 (3): 221-228 ______

Sublethal effects of indoxacarb, and on life table parameters of Habrobracon hebetor (Hymenoptera: Braconidae) in pupal stage treatment

Hooshang Rafiee-Dastjerdi*, Mehdi Hassanpour, Gadir Nouri-Ganbalani, Ali Golizadeh and Somaye Sarmadi

Department of Plant Protection, Faculty of Agriculture, University of Mohaghegh Ardabili, Ardabil, Iran.

Abstract: Habrobracon hebetor Say (Hymenoptera: Braconidae) as an ectoparasitoid of larval stage of lepidopterous pests is widely used in biological control programs. In the present research, the effect of field recommended doses of imidacloprid, indoxacarb and deltamethrin were studied on life table parameters of H. hebetor in pupal stage treatment. One hundred, two-day-old pupae were treated with 1 micro liter solution using topical method. The pupae were treated with acetone in the control. Thirty emerged adults in each treatment were transferred individually to a Petri dish along with a male for mating. Three last instar larvae of Anagasta kuehniella (Zeller) (Lepidoptera: Pyralidae) were presented to each female wasp daily as host. The numbers of eggs produced per female per day were counted until all of the females were dead. The gross and net reproductive rates in control, imidacloprid, indoxacarb and deltamethrin were 204.6, 207.7, 209.1 and 112.1 and also 75, 41.3, 64.6 and 14.9, respectively. Intrinsic rates of increase were estimated to be 0.215, 0.154, 0.205 and 0.14 female offspring/female/day, respectively. Deltamethrin and imidacloprid had the most adverse effects on life table parameters of H. hebetor. Intrinsic rate of increase was not significantly affected by indoxacarb. These findings indicated that indoxacarb was relatively safe for H. hebetor and could be an appropriate candidate in integrated chemical and biological control.

Keywords: Life table parameters, demography, , natural enemy

12 Introduction management systems attempt to use natural enemies besides insecticides for pest control. The application of insecticides is the most Integrating the application of insecticides and important factor disrupting biological control of biocontrol agents for pest management requires insect pests in most agricultural systems (Croft, knowledge about impacts of insecticides on natural 1990). Arthropod natural enemies are commonly enemies (Croft, 1990; Dent, 1995; Banks and Stark, more susceptible to insecticide applications 1998). Habrobracon hebetor is used as effective compared to target pests. Integrated pest parasitoid of different lepidopteran pests on field crops and stored products (Navaei et al., 2002). Habrobracon hebetor has been studied as a Handling Editor: Dr. Ali Asghar Talebi biocontrol agent of lepidopteran pests in some ______countries (Gerling, 1971; Brower and Press, * Corresponding author, e-mail: [email protected] 1990; Youm and Gilstrap, 1993; Magro and Received: 21 May 2012; Accepted: 30 July 2012 para, 2001; Abdi-Bastami et al., 2011). Also,

221 Sublethal effects of three insecticides on H. hebetor ______J. Crop Prot. the mass rearing of H. hebetor has been table parameters of H. hebetor in pupal stage initiated in Iran and it has been used to control treatment was determined. Helicoverpa sp. and Ostrinia nubilalis (Hübner) (Navaei et al., 2002). Little information is Biological and life table parameters available on lethal and sublethal effects of Pupae were treated with aqueous solutions of commonly used insecticides on H. hebetor field recommended doses of imidacloprid, (Rafiee-Dastjerdi et al., 2008, 2009a, 2009b, indoxacarb, and deltamethrin by topical method Mahdavi et al., 2011). To understand the (290, 125, and 83 ppm based on active overall effects of insecticides on organisms it ingredient, respectively). Triton X-100 was requires not only an estimation of lethal used as the surfactant at a concentration of 555 concentration of insecticides, but also ppm in the experiment. The controls were evaluation of their sublethal effects (Walthal treated with distilled water plus Triton X-100. and Stark, 1996; Stapel et al., 2000; Stark and The treated pupae were transferred to 90 mm Banks, 2003). Ecotoxicology especially diameter Petri dishes. After the emergence of demographic toxicology is usually considered adult wasps, 60 females and 60 males were let as the best way to evaluate effects of to mate for 24 h in glass tubes. After 24 h, 30 insecticides on organisms. The parameters alive females were randomly selected and defined for the stable population have been transferred individually to plastic Petri dishes recommended to evaluate effects of , (60 mm in diameter). Each female wasp was because it is based on both survivorship and presented three pyralid larvae and provided fecundity parameters (Stark and Wennergren, with honey. The host larvae were supplied daily 1995). There is less knowledge about sublethal for wasp oviposition in new Petri dishes. The effects of chemical insecticides on predators survival of each individual female wasp and its and parasites compared with pest arthropods fecundity was recorded daily. Females were (Croft, 1990). In present study, sublethal effects moved to new Petri dishes every 24 h to of imidacloprid, indoxacarb and deltamethrin determine daily and lifetime fecundity (the were assessed on ectoparasitoid, H. hebetor. number of eggs laid by a female wasp daily and over her lifetime). Daily schedules of mortality Materials and Methods and fecundity were integrated into a life table format (Carey, 1993) and used to calculate life Insects’ resources table parameters. All demographic parameters Adults of H. hebetor were obtained from an were analyzed by the jackknife technique insectarium maintained by Plant Protection (Meyer et al., 1988) to calculate the standard Bureau of Bilehsavar in Ardabil province, Iran. error as a measure of variance for these Habrobracon hebetor was reared on fifth instar demographic parameters. The parameters were larvae of Anagasta kuehniella in the laboratory. analyzed using SAS for Windows® release 9.0 The colony of A. kuehniella was reared on wheat (SAS Institute, 2002). flour in plastic boxes (40 × 25 × 15 cm). Fifth instar larvae of A. kuehniella were used for all Results experiments and rearing the colony. Conditions for rearing and bioassay were 26 ± 1 ˚C, 60 ± 5 Biological parameters of females emerged % RH and a photoperiod of 12: 12 h (L: D). from treated pupa and their progeny The longevity and fecundity data of female Insecticides wasps of H. hebetor emerged from pupa The effect of imidacloprid (Confidor® 350 SC, exposed to the field recommended dose of Gyah company, Iran), indoxacarb (Avaunt® 150 the used insecticides were recorded and are SC, DuPont company, France) and deltamethrin presented in Table 1. Laboratory exposure of (Decis® 2.5 EC, Gyah company, Iran) on life pupae to the field recommended

222 Rafiee-Dastjerdi et al.______J. Crop Prot. (2012) Vol. 1 (3) concentrations of the insecticides (Table 2) (F = 5.04; df = 3; P = 0.01). The significantly affected female longevity (P < highest GRR value was on control; however it 0.05) and the emerged female wasps from was not significantly influenced by the treated pupae with deltamethrin showed imidacloprid and indoxacarb compared to the shortest longevity (Table 1). However control. The female offspring from treated two other insecticides did not significantly and control pupae also showed significant affect the female longevity. Similarly, the difference in net reproductive rate value (R0). fecundity, i.e., the total number of eggs per The R0 value in deltamethrin treatment (14.9) female during its life span, was affected was significantly lower than that of control significantly (P < 0.05). The parasitoids and the two other insecticide treatments. The exposed to recommended dose of respective descending order of R0 value was deltamethrin produced less eggs (98.08 eggs) in control, indoxacarb, imidacloprid and than the control parasitoids (430.60 eggs), deltamethrin treatments. The intrinsic rate of whereas the difference between the increase (rm) was strongly affected in indoxacarb and imidacloprid-treated and offspring from the treated pupae with control parasitoids was not significant recommended doses and there were two (Table 1). The highest and lowest egg statistical groups for intrinsic rate of increase survivorship was recorded in control (0.98) (Table 2). In control and offspring from the and deltamethrin treatment (0.91), pupae treated with indoxacarb, imidacloprid respectively. No significant difference was and deltamethrin, the population increased observed between in sex ratio of offsprings daily by 1.24, 1.23, 1.17 and 1.15 times, in the three insecticide treatments and respectively. The mean generation time (T) control (Table 1). was also found to be significantly different between treatments and the longest mean Life table parameters of offspring generation time was observed in imidacloprid The life table parameters of the H. hebetor (Table 2). In addition, the doubling time (DT) females emerged from treated pupae are significantly differed among treatments and shown in Table 2. The gross reproductive rate its value in deltamethrin and imidacloprid (GRR) was significantly affected by treatments was higher than those observed in insecticide treatments and the lowest GRR indoxacarb and control (Table 2). value was detected in deltamethrin treatment

Table 1 Biological parameters (mean ± SE) of Habrobracon hebetor females emerged from the pupae treated by the field recommended doses of insecticides.

Parameters Female longevity Fecundity Egg survival Sex ratio Treatments (day) (egg number) (%)

Control 29.56 ± 2.34a 430.60 ± 56.02a 0.57 ± 0.03a 0.98

Indoxacarb 31.24 ± 2.27a 397.56 ± 54.75a 0.41 ± 0.05a 0.97

Imidacloprid 24.18 ± 3.03a 325.45 ± 62.55a 0.47 ± 0.04a 0.96

Deltamethrin 11.37 ± 1.85b 98.08 ± 22.14b 0.48 ± 0.05a 0.91 Values within each column followed by different letters are significantly different (Tukey test, P < 0.05)

223 Sublethal effects of three insecticides on H. hebetor ______J. Crop Prot.

Table 2 The life table parameters (mean ± SE) of Habrobracon hebetor exposed to the field recommended doses of insecticides in pupal stage.

Parameters GRR R r λ T DT Treatments 0 m Control 204.62 ± 13.97a 75.03 ± 6.08a 0.215 ± 0.003a 1.240 ± 0.004a 20.03 ± 0.21b 3.21 ± 0.05b

Indoxacarb 209.09 ± 24.71a 64.56 ± 8.33ab 0.205 ± 0.005a 1.228 ± 0.006a 20.25 ± 0.40b 3.37 ± 0.09b

Imidacloprid 207.67 ± 29.63a 41.27 ± 8.37b 0.154 ± 0.009b 1.166 ± 0.010b 24.01 ± 0.76a 4.51 ± 0.27a

Deltamethrin 112.06 ± 11.87b 14.90 ± 3.57c 0.140 ± 0.010b 1.151 ± 0.010b 19.00 ± 0.24b 4.96 ± 0.44a Values within each column followed by different letters are significantly different (Tukey test, P < 0.05); GRR: Gross reproductive rate, R0: Net reproductive rate, rm: Intrinsic rate of population increase, λ: Finite rate of population increase, T: Generation time, DT: Doubling time

Discussion ectoprasitoid, hence all its developmental and adult stages are subjected to insecticides. There The pests and their natural enemies usually are some investigations on sublethal effects of occur in fields simultaneously, so natural insecticides on H. hebeotr (Rafiee et al., 2008; enemies would be subjected to insecticide 2009a; Sarmadi et al., 2010, Mahdavi et al., applications and acquire toxicant by direct 2011), and in related studies mostly adult wasps contact, consuming contaminated food and have been used while other stages like pupae walking over surfaces that have may also be affected. The results of the present residues. For successful implementation of an study showed the remarkable sublethal effects IPM program specially an integration of of insecticides on females emerging from the biological and chemical control, an treated pupae and their progeny. Application of understanding of the effects of pesticides on recommended concentrations of deltamethrin biocontrol agents and insecticides on pupal stage had a considerable effect on the compatibility would be valuable tools (Croft, fecundity and longevity of emerged females 1990). Hence, toxicological studies on natural and that of their progeny (Table 2). The results enemies are necessary (Stark et al., 2004). about deltamethrin effects on female’s Natural enemies surviving after an exposure to fecundity of the present study were in a pesticide dose may suffer sublethal effects agreement with the findings reported by that influence their biological parameters like Sarmadi et al. (2010). They concluded that fecundity, longevity, life span, sex ratio or fecundity of treated adult females with behavioral parameters like host searching deltamethrin was significantly decreased ability, subsequently reduce their effectiveness compared with control; but the adult female as biocontrol agents, resulting in decreased longevity was not. This finding is in pest control (Croft, 1990; Stark et al., 1995; disagreement with our results. The different Staple et al., 2000; Salerno et al., 2002, Stark reactions of pupa and adult could be attributed and Banks, 2003; Desneux et al., 2007; to differences in their physiological status, Hamedi et al., 2010; Hamedi et al., 2011). subsequently their different sensitivity. Different life stages of natural enemies are Importantly, the female longevity and fecundity target to insecticides, hence all stages of natural were not affected by two other tested enemies should be considered in researchers’ insecticides, indoxacarb and imidacloprid. studies. H. hebetor is a very important control These findings reveal that the latter two agent of lepidopterous pests in a variety of insecticides may be relatively compatible with agricultural crops and stored products. It is an H. hebetor.

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Determining the life table parameters has in integrating chemical and biological control in been considered as a better measure of response an IPM program. to insecticides (Forbes and Calow, 1999). In our In conclusion, this research showed that the study, the life table parameters showed three used insecticides had sublethal effects on significant differences in performance and H. hebetor. Deltamethrin and imidacloprid population growth parameters among the negatively affected female wasps’ performance treated and untreated females of H. hebetor and population growth. But Indoxacarb caused (Table 2). Lower female’s fecundity in no major noxious effect on biological deltamethrin treatment resulted lowest gross parameters and all measured population and net fecundity among the treatments. In all parameters compared with control. Therefore, treatments, the net reproductive rates (R0) were indoxacarb has been considered as IPM- considerably lower than the gross reproductive compatible insecticide due to its relatively low rates (GRR) indicating that the survivorship (lx) negative effects on the effectiveness of H. was strongly affected by insecticides. The hebetor. Such information can be used to highest mean generation time (T) was observed predict the potential of indoxacarb in at imidacloprid treatment. It would be harmful combination with H. hebetor in an integrated effect on parasitoid, if an insecticide causes an pest management program. After laboratory increase in its generation time. The mean studies, further attention should be devoted on generation time was not affected by semifield and field experiments to find more deltamethrin and indoxacarb compared with applicable results under field conditions. control. Among the life table parameters, the intrinsic rate of increase (rm) has been Acknowledgments recommended to be used for evaluating the sublethal effects of pesticides, because it The work received financial support from reflects the overall effects on both survivorship Postgraduate Education Bureau of the and fecundity (Stark and Wennergren, 1995). University of Mohaghegh Ardabili Iran, which Higher intrinsic rate of increase (rm) in control is greatly appreciated. compared with the insecticide treatments indicated the adverse effects of insecticides on References this parameter. The considerable reduction value of R0 in females treated with deltamethrin Abdi-Bastami, F., Fathipour, Y., Talebi, A. A. followed by a great reduction in rm value. 2011. Comparison of life table parameters of Moreover, the longest mean generation time (T) three populations of braconid wasp, in imidacloprid treatment caused that rm values Habrobracon hebetor Say (Hym.: between imidacloprid and deltamethrin Braconidae) on Ephestia kuehniella Zell treatments were not significantly different. (Lep.: Pyralidae) in laboratory conditions. Sarmadi et al., (2010) studied the population Applied Entomology and Phytopathology, parameters of H. hebetor when adult females 78 (2): 153-176. (In Persian with English were treated with the same insecticides and abstract) reported that rm values were reduced in Banks, J. E. and Stark, J. D. 1998. What is imidacloprid and deltamethrin treatments. ecotoxicology? An ad-hoc grab bag or an These results were relatively in agreement, but iterdisciplinary science? Integrative Biology. the rm value in indoxacarb treatment was Wiley-Liss, Inc., pp. 195-204. significantly lower than control in their study. Brower, J. H. and Press, J. W. 1990. Interaction In our study the rm value was not significantly of Bracon hebetor (Hymenoptera: affected by indoxacarb. These findings Braconidae) and Trichogramma pretiosum indicated that indoxacarb is relatively safe for H. (Hymenoptera: Trichogrammatidae) in hebetor and could be an appropriate candidate suppressing stored product moth populations

225 Sublethal effects of three insecticides on H. hebetor ______J. Crop Prot.

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227 Sublethal effects of three insecticides on H. hebetor ______J. Crop Prot.

اﺛﺮات زﻳﺮﻛﺸﻨﺪﮔﻲ اﻳﻨﺪوﻛﺴﺎﻛﺎرب، اﻳﻤﻴﺪاﻛﻠﻮﭘﺮﻳﺪ و دﻟﺘﺎﻣﺘﺮﻳﻦ روي ﭘﺎراﻣﺘﺮﻫﺎي ﺟﺪول زﻧﺪﮔﻲ زﻧﺒﻮر ﭘﺎرازﻳﺘﻮﺋﻴﺪ (Habrobracon hebetor (Hymenoptera: Braconidae در ﺗﻴﻤﺎر ﻣﺮﺣﻠﻪ ﺷﻔﻴﺮﮔﻲ

ﻫﻮﺷﻨﮓ رﻓﻴﻌﻲ دﺳﺘﺠﺮدي*، ﻣﻬﺪي ﺣﺴﻦﭘﻮر، ﻗﺪﻳﺮ ﻧﻮري ﻗﻨﺒﻼﻧﻲ، ﻋﻠﻲ ﮔﻠﻲزاده و ﺳﻤﻴﻪ ﺳﺮﻣﺪي

ﮔﺮوه ﮔﻴﺎهﭘﺰﺷﻜﻲ، داﻧﺸﻜﺪه ﻛﺸﺎورزي، داﻧﺸﮕﺎه ﻣﺤﻘﻖ اردﺑﻴﻠﻲ، اردﺑﻴﻞ، اﻳﺮان * ﭘﺴﺖ اﻟﻜﺘﺮوﻧﻴﻜﻲ ﻧﻮﻳﺴﻨﺪه ﻣﺴﺌﻮل ﻣﻜﺎﺗﺒﻪ: [email protected] درﻳﺎﻓﺖ: 1 ﺧﺮداد 1391؛ ﭘﺬﻳﺮش: 9 ﻣﺮداد 1391

ﭼﻜﻴﺪه: زﻧﺒﻮر Habrobracon hebetor Say ﭘﺎرازﻳﺖ ﺧﺎرﺟﻲ ﻻروﻫﺎي ﺗﻌﺪاد زﻳﺎدي از ﺑﺎلﭘﻮﻟﻜﺪارن آﻓﺖ ﻣﻲﺑﺎﺷﺪ ﻛﻪ در ﺑﺮﻧﺎﻣﻪﻫﺎي ﻛﻨﺘﺮل ﺑﻴﻮﻟﻮژﻳﻚ اﺳﺘﻔﺎده وﺳﻴﻌﻲ دارد. در ﻣﻄﺎﻟﻌﻪ ﺣﺎﺿﺮ اﺛﺮات دز ﺗﻮﺻﻴﻪ ﺷﺪه ﻣﺰرﻋﻪاي ﺣﺸﺮهﻛﺶﻫﺎي اﻳﻨﺪوﻛﺴﺎﻛﺎرب، اﻳﻤﻴﺪاﻛﻠﻮﭘﺮﻳﺪ و دﻟﺘﺎﻣﺘﺮﻳﻦ روي ﭘﺎراﻣﺘﺮﻫﺎي ﺟﺪول زﻧﺪﮔﻲ زﻧﺒﻮر ﭘﺎرازﻳﺘﻮﺋﻴﺪ H. hebetor در ﺗﻴﻤﺎر ﻣﺮﺣﻠﻪ ﺷﻔﻴﺮﮔﻲ ﻣﻮرد ﺑﺮرﺳﻲ ﻗﺮار ﮔﺮﻓﺖ. 100 ﺷﻔﻴﺮه دو روزه ﻫﺮ ﻛﺪام ﺑﺎ ﻳﻚ ﻣﻴﻜﺮوﻟﻴﺘﺮ از ﻣﺤﻠﻮلﻫﺎي ﺳﻤﻲ ﺑﻪروش ﻣﻮﺿﻌﻲ ﻣﻮرد ﺗﻴﻤﺎر ﻗﺮار ﮔﺮﻓﺘﻨﺪ. ﺷﺎﻫﺪ ﺗﻨﻬﺎ ﺑﺎ اﺳﺘﻮن ﺗﻴﻤﺎر ﺷﺪ. ﺗﻌﺪاد 30 ﻋﺪد زﻧﺒﻮر ﻛﺎﻣﻞ ﻣﺎده ﻇﺎﻫﺮ ﺷﺪه در ﻫﺮ ﺗﻴﻤﺎر اﻧﺘﺨﺎب و ﺑﻪﻫﻤﺮاه ﻳﻚ ﺣﺸﺮه ﻧﺮ ﺑﻪﺻﻮرت ﺟﺪاﮔﺎﻧﻪ ﺑﻪ داﺧﻞ ﻇﺮوف ﭘﺘﺮي ﭘﻼﺳﺘﻴﻜﻲ ﻣﻨﺘﻘﻞ ﺷﺪﻧﺪ. در ﻫﺮ روز ﺗﻌﺪاد 3 ﻋﺪد ﻻرو ﺳﻦ آﺧﺮ ﺑﻴﺪ آرد (Anagasta kuehniella (Zeller در اﺧﺘﻴﺎر ﻫﺮ زﻧﺒﻮر ﻗﺮار ﮔﺮﻓﺖ. ﺗﻌﺪاد ﺗﺨﻢﻫﺎي ﮔﺬاﺷﺘﻪ ﺷﺪه ﺑﻪ ازاي ﻫﺮ ﻣﺎده ﺗﺎ ﻣﺮگ آﺧﺮﻳﻦ ﻓﺮد ﺷﻤﺎرش ﺷﺪﻧﺪ و ﺗﻌﺪاد ﺗﺨﻢﻫﺎي ﺗﻔﺮﻳﺦ ﺷﺪه، ﺗﻌﺪاد ﻻروﻫﺎ، ﺷﻔﻴﺮهﻫﺎ و ﺣﺸﺮات ﻛﺎﻣﻞ ﺗﻮﻟﻴﺪي در ﻫﺮ ﺗﻴﻤﺎر ﻧﻴﺰ ﻣﺸﺨﺺ ﺷﺪ. ﺳﭙﺲ ﺟﺪاول زﻧﺪﮔﻲ ﺑﻪ روش ﻛﺮي (1993) ﺗﺸﻜﻴﻞ و ﭘﺎراﻣﺘﺮﻫﺎي ﺟﺪول زﻧﺪﮔﻲ ﻣﺤﺎﺳﺒﻪ ﺷﺪﻧﺪ. دﻟﺘﺎﻣﺘﺮﻳﻦ و اﻳﻤﻴﺪاﻛﻠﻮﭘﺮﻳﺪ ﺑﻴﺸﺘﺮﻳﻦ اﺛﺮ ﺳﻮء را روي ﭘﺎراﻣﺘﺮﻫﺎي ﺟﺪول زﻧﺪﮔﻲ زﻧﺒﻮر داﺷﺘﻨﺪ وﻟﻲ اﻳﻨﺪوﻛﺴﺎﻛﺎرب ﺗﺄﺛﻴﺮ ﻣﻌﻨﻲداري ﻧﺪاﺷﺖ. ﺑﺎ ﺗﻮﺟﻪ ﺑﻪ ﻧﺘﺎﻳﺞ ﺑﻪدﺳﺖ آﻣﺪه ﻣﻲﺗﻮان ﮔﻔﺖ ﻛﻪ اﻳﻨﺪﻛﺴﺎﻛﺎرب ﺑﺮاي زﻧﺒﻮر ﻧﺴﺒﺘﺎً اﻣﻦ ﺑﻮده و ﻣﻲﺗﻮاﻧﺪ در ﺑﺮﻧﺎﻣﻪﻫﺎي ﻣﺪﻳﺮﻳﺖ ﺗﻠﻔﻴﻘﻲ آﻓﺎت ﺑﻪﻫﻤﺮاه زﻧﺒﻮر ﭘﺎرازﻳﺘﻮﺋﻴﺪ H. hebetor ﻣﻮرد اﺳﺘﻔﺎده ﻗﺮار ﮔﻴﺮد.

ﻛﻠﻤﺎت ﻛﻠﻴﺪي: ﺟﺪول زﻧﺪﮔﻲ، دﺷﻤﻨﺎن ﻃﺒﻴﻌﻲ، اﺛﺮات زﻳﺮﻛﺸﻨﺪﮔﻲ، دﻣﻮﮔﺮاﻓﻲ

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