Bulletin of Insectology 61 (2): 245-250, 2008 ISSN 1721-8861

Functional response of brassicae at different temperatures and relative humidities

1 2 2 Mitra MOEZIPOUR , Maryam KAFIL , Hossein ALLAHYARI 1Department of Plant Protection, College of Agriculture, University of Technology, Isfahan, Iran 2Department of Plant Protection, College of Agriculture, University of Tehran, Karaj, Iran

Abstract

Trichogrammatid egg are the most promising biological control agents for inundative releases against Lepidopteran pests. Trichogramma brassicae Bezdenko is an egg of the carob moth, Apomyelois (Ectomyelois) ceratoniae (Zeller), in Iranian Pomegranate orchards. Study on the functional response of natural enemies is one of the necessary features for the se- lection of natural enemies for biological control programs. In this study, laboratory tests were conducted to determine the func- tional response of T. brassicae on its factitious host, eggs of angoumois grain moth, Sitotroga cerealella (Olivier), at different temperatures and humidity. The type of functional response of T. brassicae was II at 25 °C and III at 20 and 30 °C (60% relative humidity). A model with indicator variable was used to compare the output parameters in different data sets. Analyses indicated that there is a significant difference in functional response of T. brassicae at 20 and 30 °C. Additional tests showed that changes at relative humidity can change the functional response parameters.

Key words: functional response, egg parasitoids, , laboratory assessment, temperature, humidity.

Introduction and evaluation of efficiency and dynamic models for parasitoids and hosts in the field (Parra et al., 1987). The carob moth, Apomyelois (Ectomyelois) ceratoniae Climatic conditions plays an important role in tritrophic (Zeller) ( Pyralidae), is the key pest of interactions among poikilotherms as it influences the Pomegranate orchards in Iran that was first reported in level of control that natural enemies exert (Huffaker et Kashmar (Khorasan province), in 1972. It also produces al., 1971). Lack of quality control procedures during the significant damage on nut and fruit commodities such as mass production of natural enemies may lead to failures almonds, Pistachios, Macadamias, as well as Pomegran- in biological control (van Lenteren et al., 2003). Corre- ates, stone and pomes fruits in many regions around the lation between values obtained at laboratory testing and world (Botha et al., 2004). This pest continues its dam- field performance is important to be able to select a lim- age when the nuts stored under domestic storage condi- ited set of laboratory criteria that give meaningful in- tions (Mehrnejad, 1995). formation about performance after release (van Lenteren Egg parasitoids of the genus Trichogramma have been et al., 2003). used successfully as inundative biological control agents The functional response is an essential element of dy- against a range of agricultural pests mainly Lepidopter- namics of host-parasitoid association and is an impor- ans and are the most widely used natural enemies in bio- tant determinant of the stability of the system (Oaten logical control world wide (Li et al., 1994). Augmenta- and Murdoch, 1975). Holling (1959; 1966) proposed tive release of mass-reared Trichogrammatid egg parasi- three types of functional responses. In type I, number of toids have been identified as a promising method to re- killed host/prey rise as linear to a plateau; type II, a cur- duce both egg hatching and subsequent damage due to vilinear rise to a plateau which then levels off under the larval feeding (Wajnberg and Hassan, 1994; Smith, influence of handling time or satiation and in type III 1996). Different native species of Trichogramma have predator/parasitoid response by a sigmoid increase in been evaluated for controlling the carob moth in Iranian prey/hosts attacked (Hassell, 2000; Mills and Lacan, Pomegranate orchards (Moezipour, 2006). The most 2004). Functional response tests, shows the potential of widespread species in Iran is Trichogramma brassicae parasitoid/predator ability to suppress the different den- Bezdenko ( Trichogrammatidae) (Azema sity of prey/host. and Mirabzadeh, 2005). The first studies were carried An efficient artificial host must be able to produce out on 1990 in Yazd province. Using Trichogramma high numbers of eggs and its eggs must be accepted by wasps against this pest were also carried out during the the parasitoid (Allahyari et al., 2004). Sitotroga ce- years 1991-93, in Varamin (Tehran province). Accord- realella (Olivier) (Lepidoptera Gelechiidae) is a suitable ing to investigations egg was 37.4 and host for T. brassicae and used for mass rearing of 57.84% in Khorasan and Yazd provinces, respectively. Trichogramma wasps; so we used this host instead of The most promising results were found in Yazd prov- target pest. In this study, we try to find the effect of dif- ince (Moezipour, 2006). ferent temperatures and humidity on the ability of T. The success of Trichogramma species depends on brassicae in parasitizing the host eggs. their efficiency in the field, maintenance and behaviour in laboratory, selection of adequate species and/or line- ages besides thermal requirements, liberation techniques

Materials and methods the parameters of the Holling’s disk equation (equation 2) and Roger’s (1972) random parasitoid equation (equa- Population of Trichogramma wasps were collected from tion 3). Some authors emphasize on the limitation of Pomegranate in Yazd province. We collected individu- Holling’s disk equation, and suggest Rogers’ para- als of Trichogrammatid populations from eggs of the site/predator equation as an alternative, which is more carob moth in Pomegranate orchards in Yazd, Iran (35° appropriate when prey depletion (for a predator) or re- 37” N, 50° 20” E). Based on morphometric analysis encounter (for a parasitoid) occurs during the experi- such as genitalia shape, collected wasps were identified ment. Holling’s disk equation can be used only when as T. brassicae. Antennal characters were used to sepa- Rogers’ model does not enable the researcher to esti- rate female and male Trichogramma individuals. mate valid parameters (see Allahyari et al., 2004).

The T. brassicae colony was reared on eggs (<24 h old) (2) Holling’s model N a = aTN 0 1+ aTh N 0 of the factitious host, were obtained from a culture of S.   aT  cerealella, routinely reared in our laboratory. The (3) Rogers’ model   N a = N0 1− exp−  Trichogrammatids were reared on factitious host, at 25   1+ aTh N0  ± 1 °C, 55 ± 10% RH and 16: 8 (L: D) photoperiod. (4) a = (d + bN ) (1+ cN ) 0 0 Where N is the number of host attacked, N the initial Functional response experiments a 0 number of hosts, T the time of exposure (16 hours), a, The eight egg densities (4, 8, 10, 20, 40, 60, 80 and the rate of successful attack, T the handling time and b, 120 eggs per adult parasitoid), were used. Glass shell h c, d are constant. Comparisons between parameters we- vials (12×100 mm) served as experimental units. For re performed by using an equation with indicator vari- each host density, eggs of factitious host (< 24 h) were ables: placed on a small thick paper and inserted into glass    vial. One-day-old mated female wasps (fed on drop of (5)  []b + Db ( j) T N 0  N a = N 0 1− exp −  20% honey/water) were exposed to different density le-   1+ []b + D ( j) []T + D ( j) N 2  vels of S. cerealella eggs. This experiment was done at   b h Th 0  20, 25 and 30 °C, 60 ± 10% RH, and 16: 8 (L: D) pho- Where j is an indicator variable that takes value 0 for toperiod condition. To determine the effect of relative first data set and 1 for the second data set. The parame- humidity on functional response of T. brassicae, two ters Db and DTh estimate the differences between the da- humidity regimes (45 ± 10% and 85 ± 10% RH) were ta sets in the value of the parameter b and Th, respec- tested at 30 °C. At least 20 replications of each density tively. In other words, for example the handling time for were set up, simultaneously. 20 °C is Th, and for 30 °C is Th + DTh. For finding a dif- After 16 hours the female parasitoids were removed ference between two handling times, it must be proved and host egg were maintained under 25 ± 1 °C and 55 ± that DTh is a significant amount, and it is not equal to 10% RH condition. To determine the number of parasi- zero. If DTh is not significantly different from zero, then tized egg, the number of black eggs was counted. At the difference between Th and Th + DTh is not significant each temperature/humidity, the wasps were reared at and the two handling time are equal from statistical that condition at least for two generations and the third point of view (see Juliano, 2001). generation was used for experiments.

Statistical analysis Results Data analysis for functional response includes two steps. In the first step, the shape (type) of functional re- Functional responses of parasitoid in different condi- sponse must be determined, typically by determining if tions are illustrated in figure 1. At different tempera- the data fit a type ΙΙ or ΙΙΙ functional response. Logistic tures T. brassicae showed different types of functional regression of the proportion of parasitized hosts vs. the response. Results of a logistic regression (table 1) in- initial number of hosts is the most effective way in de- dicated that functional response of T. brassicae popu- termining this. In this first step, we fitted a polynomial lation at 25 °C is type II and at 20 and 30 °C is type function: III. At 25 °C the attack coefficient, a (0.0735 ± 0.011) N exp(P + P N + P N 2 + P N 3 ) and the handling time Th (0.311 ± 0.032) were esti- (1) a = 0 1 0 2 0 3 0 mated from Holling’s disk equation using a nonlinear N 1+ exp(P + P N + P N 2 + P N 3 ) 0 0 1 0 2 0 3 0 least square regression. Where P0, P1, P2, and P3 are the parameters to be esti- At 20 and 30 °C, the Roger’s random parasitoid equa- mated. These parameters can be estimated by using the tion has been used in data analysis. Equation (4) was CATMOD procedure in SAS. The sign of P1 and P2 can substituted in (3) and the data set was fitted to it. Results be used to distinguish the shape of the curves. A posi- of nonlinear least square regression indicated that pa- tive linear parameter (P1) and a negative quadratic pa- rameters c and d were not significantly different from rameter (P2) indicated that functional response is type zero; therefore, we eliminated them from the model and ΙΙΙ, whereas if both parameters are negative, the func- a reduced model was used. tional response is type ΙΙ. Estimated b value, at 20 and 30 °C were 0.0025 ± After determining the type of functional response, pa- 0.0005 and 0.0046 ± 0.0007, respectively and estimated rameters must be estimated. We used nonlinear least handling time (Th) in these temperatures were 0.619 ± square regression (NLIN procedure in SAS) to estimate 0.0281 and 0.425 ± 0.0121, respectively. Estimated con-

246

40 70 o 20oC and 60%RH 25 C and 60%RH 60 Observed Observed Predicted predicted 30 50

40 20 30

20 10 Number of parasitizedNumber of eggs parasitizedNumber of eggs

10

0 0 0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 140 Host density Host density

50 40 30oC and 60%RH 30oC and 45%RH

Observed Observed 40 Predicted Predicted 30

30

20

20

10 Number of parasitizedNumber of eggs 10 parasitizedNumber of eggs

0 0 0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 140 Host density Host density

60 30oC and 85%RH

50 Observed Prdicted

40

30

20 Number of parasitized eggs 10

0 0 20 40 60 80 100 120 140 Host density

Figure 1. Functional response of T. brassicae to different densities of S. cerealella eggs, at different temperature and humidity (symbols: observed; line: predicted by model).

fidence interval for Db and DTh in different data sets can midity regimes. Parameters of these two data sets were be used to compare parameters b and Th. Data analyzing compared to the functional response of wasps in 30 °C by using equation 5 indicated that Db and DTh are sig- and 60% RH. There is significant difference in func- nificant values; therefore, there is significant difference tional response parameters of T. brassicae in 45% and between b and Th in functional response of T. brassicae 60% humidity regimes. Comparison between functional at 20 and 30 °C (table 2). response in 60% and 85% showed that there is just sig- Our results indicated that change in relative humidity nificant difference in Th value. at 30 °C, could not change the type of functional re- sponse of T. brassicae and for each two humidity, it was type III. At 45 ± 10%, estimated b value and handling Discussion time were 0.0017 ± 0.0005 and 0.906 ± 0.068, respec- tively. These values for 85 ± 10% RH, were 0.0025 ± A number of attributes have been proposed as character- 0.001 and 0.728 ± 0.06, respectively. istics of effective biological control agents; these in- The outputs of model 5 showed that relative humidity clude a high intrinsic rate of population increase, a high changes, can not affect the values of functional re- searching efficiency, low handling time, and a tendency sponse parameters of this parasitoid. Based on our re- to aggregate in areas where hosts are common for the sults (table 2), there is not any difference in functional target pest (Hassell, 1978). Differences in killing effi- response of T. brassicae in 45% and 85% relative hu- ciency between two parasitoid or predator populations

247

Table1. Results of logistic regression analysis of the proportion of parasitized eggs by T. brassicae, against initial number of eggs.

Temperature / humidity Coefficient Estimate SE χ2 Value P value 20 °C / 60% RH Constant -0.00984 0.0968 0.01 0.919 " Linear 0.0216 0.00308 48.83 <0.0001 " Quadratic -0.00009 0.000021 16.71 <0.0001 25 °C / 60% RH Constant 0.1282 0.1518 0.71 0.3982 " Linear -0.0796 0.01 60.9 <0.0001 " Quadratic 0.002 0.0002 82.5 <0.0001 " Cubic -7.7 E-6 8.9 E-7 74.45 <0.0001 30 °C / 60% RH Constant -0.0863 0.0936 0.85 0.356 " Linear 0.002 0.0029 0.43 0.512 " Quadratic 0.00007 0.00002 11.22 0.0008 30 °C / 45% RH Constant 0.6219 0.1077 33.32 <0.0001 " Linear 0.016 0.0035 21.24 <0.0001 " Quadratic -0.0005 0.0002 5.18 0.023 30 °C / 85% RH Constant 0.4046 0.155 6.81 0.0091 " Linear 0.0285 0.011 7.39 0.0066 " Quadratic -0.0005 0.0002 8.17 0.0043 " Cubic 3.34 E-6 9.4 E-7 12.59 0.0004

Table 2. Parameters estimated by an equation with indicator variable (5) for different data set: functional response of T. brassicae, in different humidity regimes.

Asymptotic 95% CI Parameter Estimate Asymptotic SE Lower Upper 20 °C and 30 °C b 0.0025 0.0005 0.0016 0.0035 Th 0.6199 0.026 0.569 0.6711 Db 0.00204 0.0009 0.00023 0.0038 DTh -0.1943 0.0292 -0.2518 -0.1369 45% and 60% RH b 0.0017 0.0005 0.00074 0.0026 Th 0.9062 0.0588 0.7905 1.0218 Db 0.00291 0.0009 0.0009 0.0048 DTh -0.4807 0.0606 -0.5999 -0.3614 45% and 85% RH b 0.0017 0.0007 0.00035 0.0029 Th 0.9062 0.0831 0.7427 1.0697 Db 0.0009 0.0011 -0.0013 0.003 DTh -0.1784 0.0983 -0.3719 0.0151 60% and 85% RH b 0.0046 0.0011 0.0024 0.0068 Th 0.4255 0.0188 0.3885 0.4626 Db -0.002 0.0013 -0.0047 0.0006 DTh 0.3023 0.0512 0.2015 0.4031 b: constant must be estimated. Th: handling time. Db: indicator variable estimates the differences between the humidity in the value of the parameter b. DTh: indicator variable estimates the differences between the humidity in the value of the parameter Th.

can be compared by estimation and comparison of func- Trichogramma embryophagum (Hartig), it was reared on tional response parameters (Juliano, 2001). Ephestia kuehniella (Zeller) and S. cerealella eggs. In This research showed that different temperature and both experiments, the functional response was type III relative humidity had a significant effect on the func- and Holling disc equation was used to estimate the pa- tional response of egg parasitoids which must be kept rameters. The results revealed that the type of laboratory constant during the wasps’ selection. host has no important effect on the functional response To determine the effect of host species on the search- of T. embryophagum (Fathipour et al., 2003). Their re- ing efficiency, handling time and functional response of sults encouraged us to use factitious host in this study.

248

In laboratory studies, finding the type I and II func- respectively. In conclusion, high temperature and me- tional response for Trichogramma species is typical dium humidity had a strong impact on the magnitude of (Kfir, 1983; Karimiyan, 1998; Faria et al., 2000; Wang parasitizing capacity and thereby functional response of and Ferro, 1998; Lashgari et al., 2004; Mills and Lacan, tested parasitoid. 2004; Reay-Jones et al., 2006). Shen and Li (1987) The determined optimal temperature could be related found a linear relationship for the Asian corn borer, Os- to the adaptation of this species to condition of their trinia furnacalis (Guenée). In this research, at 25 °C, habitat where they were collected. The optimum relative functional response trials resulted in a strong fit to a humidity in this study (60%) was very higher than the curvilinear type II response. relative humidity of Trichogramma wasps natural habi- The type of functional response of parasitoid/predator tat; therefore we can say that one of the main reasons of may change from one type to another as environmental low wasps efficiency in Pomegranate orchards, is the conditions (temperature mainly) change (Wang and low relative humidity, high relative humidity never oc- Ferro, 1998; Mohaghegh et al., 2001). In our tests, data curred in the habitat that the specimen were collected. from 20 and 30 °C, fit a sigmoid type III response in In this study we could clearly establish a relationship which there is an initial rate of parasitisation followed between the functional response of Tricogramma wasps by a constant rate and then a deceleration of response as and temperature, although parasitoids showed high abil- in the type II model, so these two temperatures, may ity to perform at a wider range of humidity. Thus we lead to accelerate the learning ability of female wasps can increase the parasitoid efficiency with regular irri- and increase the rate of parasitized eggs. Difference in gation and other management strategies as though the adaptation to different environmental condition, may be relative humidity increases at the time of Tricogramma due to effects on the foraging behaviour of the parasi- release. Functional response studies in laboratory could toids (Zhang, 1983). Gou (1986) and Zhang et al. be useful in providing the first step for comparing the (1983) suggested that changes (mainly temperature), efficiency of different species/strains and also provide a may affect the foraging behaviour of the parasitoids. valid means of comparing host finding abilities of can- Trichogramma possibly possess a learning ability to didate natural enemies (Overholt and Smith, 1990). In discriminate parasitized eggs and unparasitized eggs addition to laboratory studies, more attention should be through experience (Wang and Ferro, 1998) which may devoted to semi field and field condition to obtain more result in type III response. Bjorksten and Hoffmann applicable results in the field. (1998) suggested that oviposition experience had a stronger effect on host preference than pre-adult experi- ence (learning through development in rearing host). Acknowledgements Kaiser et al. (1989), suggest that females can learn to associate some olfactory cues with the presence of the The authors would like to express their sincere thanks to host. Dr Y. Fathipour for his kind advice on this manuscript Our results suggested that the optimum temperature and we would like to thank the Biocontrol Research according to the highest value of a (searching ability of Department, Plant Protection Research Institute of Iran parasitoid) and the lowest value of Th (handling time), and Department of Plant Protection, University of Te- was 30 °C (type III). Kalyebi et al. (2005), also stated hran, Karaj, Iran, for providing financial support for this that the optimum temperature for Trichogrammatid research. wasps was around 30 °C. Similar optimal was found for other egg parasitoids reared under constant temperature (Chabi-Olay et al., 2004). Furthermore some research- References ers found type III of functional response for Tricho- gramma species at different conditions in laboratory ALLAHYARI H., FARD P. A., NOZARI J., 2004.- Effects of host (Reay-Jones et al., 2006; Arbab Tafti et al., 2004). on functional response of offspring in two populations of No studies have been conducted to establish the rela- Trissolcus grandis on the Sunn pest.- Journal of Applied En- tionship between host densities and rates of attack tomology, 128: 39-43. (functional response) for T. brassicae at different hu- ARAB TAFTI R., SAHRAGARD A., SALEHI L., ASGARI S., 2004.- Study on functional response of Trichogramma brassicae midity. Although Kalyebi et al. (2005) evaluated the Bezdenko (Hym.: Trichogrammatidae) to different densities influence of relative humidity on functional response of of Sitotroga cerealella Olivier (Lep.: Gelechiidae) eggs.- Trichogramma egg parasitoid but reported humidity and Journal of Agricultural Science, 1: 1-8. its interactions with temperature and strain had no effect AZEMA M., MIRABZADEH A.- 2005.- Issues on different as- on the number of eggs parasitized. pects of applying natural enemies biological control of in- Our research was done at three humidity regimes (45, sect pests.- Sepehr Publication, Iran. 60 and 85% RH). By changing the relative humidity BJORKSTEN T. A., HOFFMANN A. A., 1998.- Separating the ef- from 45 to 60%, wasp instantaneous searching effi- fects of experience, size, egg load and genotype on host re- ciency (a = bN ) increased and handling time (T ) de- sponse in Trichogramma (Hymenoptera: Trichogrammati- 0 h dae).- Journal of Behavior, 11: 129-148. creased. Increasing the relative humidity from 60 to BOTHA J., HARDIE D., HOFFMANN H., 2004.- Carob moth.- 85% does not change the value of a significantly, but Garden note, 21: [online] URL: http://www.agric.wa.gov.au/ increases the Th. This means that high relative humidity content/PW/GARD/GN2004_021.PDF. decrease the ability of the wasp. The maximum parasit- CHABI-OLAYE A., FIABOE’ M. K., SCHULTHESS F., 2004.- Host ism in 60 and 85% relative humidity was 37.6 and 21.9, suitability and thermal requirements of Lathromeris ovicida

249

Risbec (Hymenoptera: Trichogrammatidae) egg parasitoid MOEZIPOUR M., 2006.- Effect of different temperature and of cereal stem borers in Africa.- Biological Control, 30: humidity treatments on some biological parameters of two 617-623. Trichogramma brassicae Bezd. populations, collected from FARIA C. A., TORRES E J. B., FARIAS A. M. E., 2000.- Func- pomegranate orchards of Yazd and Saveh. 161 pp. M.Sc. tional response of Trichogramma pretiosum Riley (Hymen- Thesis, Isfahan University of Technology, Iran. optera: Trichogrammatidae) to Tuta absoluta (Meyrick) MOHAGHEGH J., DE CLERCG P., TIRRY L., 2001.- Functional (Lepidoptera: Gelechiidae) eggs: effect of host age.- Anais response of the predators Podisus maculiventris (Say) and da Sociedade Entomológica do Brasil, 29 (1): 85-93. Podisus nigrispinus (Dallas) (Het.: Pentatomidae) to the beet FATHIPOUR Y., HAGHANI M., ATTARAN M., TALEBI A. A., MO- armyworm, Spodoptera exigua (Hunber) (Lep.: Noctuidae): HARRAMIPOUR S., 2003.- Functional response of Tricho- effect of temperature.- Journal of Applied Entomology, 125: gramma embryophagum (Hym.: Trichogrammatidae) on two 131-134. laboratory hosts.- Journal of Entomological Society of Iran, OATEN A., MURDOCH W. W., 1975.- Functional response and 23 (1): 41-54. stability in predator-prey systems.- The American Naturalist, GUO X., 1986.- Bionomics of Trichogramma ostriniae Pang et 109: 289-298. Chen.- Chinese Journal of Biological Control, 2: 148-152. OVERHOLT W. A., SMITH JR. J. W., 1990.- Comparative HASSELL M. P., 1978.- The dynamics of predator- evaluation of three exotic insect parasites (Hymenoptera: prey system.- Princeton University, Princeton, UK. Braconidae) against the southwestern corn borer( Lepidop- HASSELL M. P., 2000.- The spatial and temporal dynamics of tera: Pyralidae) in corn.- Environmental Entomolgy, 19: host parasitoid interactions.- Oxford University Press, Lon- 345-356. don, UK. PARRA J. R. P., ZUCCHI R. A., SILVEIRA NEOTO S., 1987.- Bio- HOLLING C. S., 1959.- Some characteristic of simple types of logical control of pests through egg parasitoids of the genera predation and parasitism.- Canadian Entomologist, 91: 385- Trichogramma and/or Trichogrammatoidea.- Memorias do 398. Instituto Oswaldo Cruz, 82: 153-160. HOLLING C. S., 1966.- The functional response of invertebrate REAY-JONES F. P. F., ROCHAF J., GOEBEL R., TABONE E., predators to prey density.- Memoirs of the Entomological 2006.- Functional response of Trichogramma chilonis to Society of Canada, 48: 1-86. Galleria mellonella and Chilo sacchariphagus eggs.- Ento- HUFFAKER C. B., MESSENGER P. S., DEBACH P., 1971.- The mologia Experimentalis et Applicata, 118: 229-236. natural enemy component in natural control and the theory ROGERS D. J., 1972.- Random search and insect population of biological control, pp. 16-67. In: Biological control (HUF- models.- Journal of Ecology, 41: 369-383. FAKER C. B., Ed.).- Academic Press, New York, USA. SHEN X., LI Y., 1987.- Correlation of egg mass parasitisation JULIANO, S. A., 2001.- Nonlinear curve fitting: predation and and egg parasitisation of Ostriniae furnacalis by Tricho- functional response curves, pp. 159-189. In: Design and gramma spp.- Chinese Journal of Biological Control, 3: analysis of ecological experiments (CHEINER S. M., GURVEN 136-137. J., Eds).- Chapman & Hall, New York, USA. SMITH S. M., 1996.- Biological control with Trichogramma KAISER L., PHAM-DELEGUE M. H., BAKCHINE E., MASSON C., advances, success, and potential of their use.- Annual Re- 1989.- Olfactory responses of Trichogramma maidis Pint. et view of Entomology, 41: 375-406. Voeg.: Effects of chemical cues and behavioral plasticity.- VAN LENTEREN J. C., HALE A., KLAPWIJK J. N., VAN SCHELT J., Journal of Insect Behavior, 2 (5): 701-712. STEINBERG S., 2003.- Guidelines for quality control of com- KALYEBI A., OVERHOLT W. A., SCHULTHESS F., MUEKE J. M., mercially produced natural enemies, pp. 265-304. In: Qual- HASSAN S. A., SITHANANTHAM S., 2005.- Functional re- ity control and production of biological control agents: the- sponse of six indigenous Trichogrammatid egg parasitoids ory and testing procedures (VAN LENTEREN J.C., Ed.).- (Hym.: Trichogrammatidae) in Kenya: influence of tempera- CABI Publishing, Wallingford, UK. ture and relative humidity.- Biocontrol, 32: 164-171. WAJNBERG E., HASSAN S. A., 1994.- Biological control with KARIMIYAN Z., 1998.- Biology and ecology of Trichogramma egg parasitoids.- CAB International, Oxon, UK. brassicae in rice fields of Guilan province. 150 pp., M.Sc. WANG B., FERRO D. N., 1998.- Functional response of Tricho- Thesis, Guilan University, Iran. gramma ostriniae (Hym.: Trichogrammatidae) under labora- KFIR R., 1983.- Functional response to host density by the egg tory and field conditions.- Environmental Entomology, 27: parasite Trichogramma pretiosum.- Entomophaga, 28: 345- 752-758. 353. ZHANG J., WANG J., LIU G., YAN Y., 1983.- Influences of the LASHGARI A. A., TALEBI A. A., FATHIPOUR Y., MOHARAMI- humidities and temperature-humidity combinations on POUR S., 2004.- Study on the functional response of Tricho- Trichogramma ostriniae Pang et Chen (Hymenoptera: gramma brassicae (Hym.: Trichogrammatidae) on three Trichogrammatidae).- Natural Enemies of , 5: 129- host species in laboratory condition, pp. 35. In: 16th Pro- 134. ceedings of Plant Protection, Tabriz, Iran. LI S.Y., HENDERSON D. E., MEYER J. H., 1994.- Selection of suitable Trichogramma species for potential control of the Authors’ addresses: Mitra MOEZIPOUR (corresponding blackheaded Fire worm infesting cranberries.- Biocontrol, 4: author, [email protected]), Department of Plant 244-248. Protection, College of Agriculture, University of Technology, MEHRNEJAD M. R., 1995.- The carob moth, a pest of pistachio Isfahan, Iran; Maryam KAFIL ([email protected]), Hossein ALLA- nut in Iran.- Acta Horticulturae, 419: 365-372. HYARI ([email protected]), Department of Plant Protection, MILLS N. J., LACAN I., 2004.- Ratio dependence in the func- College of Agriculture, University of Tehran, Karaj, Iran. tional response of insect parasitoids: evidence from Tricho- gramma minutum foraging for eggs in small host patches.- Ecological Entomology, 29: 208-216. Received January 25, 2008. Accepted June 3, 2008.

250