Experience acquisition by Trichogramma australicum Girault (Hymenoptera: Trichogrammatidae)

We investigated experience acquisition (alpha-conditioning) by females of the parasitoid Trichogramma australicum using host eggs of the noctuid moth Helicoverpa armigera (Hübner). We compared the acceptance of a host egg by females with different levels of ovipositional experience. The level of experience was designated using the standard oviposition sequence: (1) host contact (C); (2) host examination (E); (3) drilling (D); (4) full insertion (FI); and (5) oviposition (O). Each treatment consisted of a single experience level, but together these consituted a qualitative behavioural continuum of oviposition experience from naive (N) to experienced wasps. We found that host experience by adult T. australicum females can modify their behaviour. Mean duration of host finding was: N = C > E = D > FI = O. Mean duration of host examination and full insertion were: N = C > E = D = FI = O. Drilling was constant for all experience levels. Experience in drilling of the chorion during the previous host-exposure process represents a critical experience for a female and results in efficient handling and more ready acceptance of a subsequently encountered host egg.     

Effects of deltamethrin on the reproduction of Trichogramma cordubensis (Hymenoptera: Trichogrammatidae)

The influence of deltamethrin on the reproduction of Trichogramma cordubensis, a thelytokous egg parasitoid, was investigated by studying egg maturation and daily fecundity of insecticide treated wasps and offspring emergence rates. The insecticide was applied to the parasitoids at the prepupal stage within its host eggs (Ephestia kuehniella). The total number of parasitized eggs per female during the first 7 days was not significantly influenced by the tested concentrations of deltamethrin. Prevalence of parasitism during this period had a similar pattern between deltamethrin treatments and the control. In addition, the mean number of mature eggs observed per female per day was significantly correlated to mean daily fecundity, regardless of the treatments. Offspring emergence was significantly influenced by the insecticide treatments experienced on their progenitors, decreasing significantly at 48 and 72 h for the highest tested concentration of deltamethrin (23.6 mg [a.i.]/L). Despite that, deltamethrin had no adverse effects on the reproduction of treated wasps, particularly when was applied at the concentration recommended by the manufacturer (12.5 mg [a.i.]/L).     

Temperature-dependent Development of Four Egg Parasitoid Trichogramma Species (Hymenoptera: Trichogrammatidae)

Trichogramma species have been successfully utilized for biocontrol of several lepidopteran pests worldwide. The development, survival and progeny production of two Kenyan species' Trichogramma bournieri Pintureau & Babault and Trichogramma sp. nr. mwanzai Schulten & Feijen (collected from Kenya), Trichogramma evanescens Westwood (Germany) and Trichogramma chilonis Ishii (India) was studied at four constant temperatures (13, 18, 25 and 34°C) with the 011 aim of assessing the relative biotic potential of the two native species for 011 biocontrol of Helicoverpa armigera and Plutella xylostella in Kenya. The study was conducted at the Institute 011 for Biological Control (BBA), Darmstadt, Germany. The Trichogramma species tested showed variations 011 in fertility, developmental time, percent emergence, progeny production and sex ratio 011 at the four temperature regimes. Fertility decreased as temperature increased from 25 to 34°C. 011 T. chilonis and T. evanescens completed development at all temperatures tested, but T. 011 bournieri and T. sp. nr. mwanzai failed to complete development at 13°C. The developmental 011 period for all the species decreased as the temperature increased. The duration of development from 011 oviposition to adult emergence varied from 8 days to 12 weeks shorter at 34°C than at 011 13°C for T. chilonis and T. evanescens . For the various temperatures tested, a linear model was 011 satisfactory for egg to adult development at P = 0.05 for T. chilonis and T. evanescens . The 011 lower temperature thresholds for development and duration in degree-days were 8.83°C and 188 for 011 T. chilonis and 9.23°C and 192 for T. evanescens , respectively. For all temperatures tested, 011 T. sp. nr. mwanzai had the highest preimaginal survivorship. Adult emergence was lower at 13°C and 34°C than at 011 18 and 25°C. The highest fertility (mean ±SE) (50.37 ±2.32 adult 011 female -1 ) and progeny production (44.03 ±2.02 adult female -1 ) was recorded at 25°C for 011 T. evanescens . Sex ratio was biased towards female at all temperatures in T. bournieri and T. chilonis . 011 At all temperatures tested, T . sp. nr. mwanzai produced more males than females. For all species tested, 011 favourable parasitism was between 18 and 25°C. The results from this study will be useful for mass rearing purposes as well as for future field release programmes.     

Temperature and strain effects on reproduction and survival of Trichogramma oleae and Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae)

To assess differences in temperature sensitivity during development, life tables for two lines derived from the species Trichogramma oleae Voegelé and Pointel and a strain of Trichogramma cacoeciae Marchal (Hymenoptera: Trichogrammatidae) were elaborated at 15, 20, 25, 30, 35, 36, and 37°C in the laboratory. Eggs of Ephestia kuehniella Zeller together with a fresh drop of honey were supplied every 2 days until the death of the test females, and the removed host egg batches were placed in the equivalent rearing cabinet. The line ‘2F’ of T. oleae was found to be the most efficient at any range of temperatures except at 20 and 37°C, in comparison to the other tested strains. For all species, no progeny emerged from eggs incubated at 36°C and none of the parasitized eggs turned black at 37°C. The better performance at a broader range of temperatures by T. oleae (line 2 F) might be caused by a shorter history in artificial rearing in comparison to the other strains. Fewer generations at laboratory conditions and frequent multiplication on eggs of its natural host (the olive moth Prays oleae) may have prevented a deterioration in the rearing population of this strain, maintaining its genetic diversity at a higher scale. Applying varying temperature regimes on the rearing stock at regular intervals during the mass production process may help to maintain the essential quality of the biological control agents for field performance at higher temperatures.     

Biological studies on two neotropical egg parasitoid species: Trichogramma nerudai and Trichogramma sp. (Hymenoptera: Trichogrammatidae)

The main biological attributes of two Neotropical egg parasitoids, the arrhenotokous Trichogramma nerudai and the thelytokous Trichogramma sp., were assessed under controlled laboratory conditions. Developmental time from egg to adult, and parasitoid survival, fecundity and fertility were studied using life tables. Results showed that T. nerudai had a faster developmental time than Trichogramma sp. (13.014±0.4019 and 13.595±0.4931 days, respectively). Both species showed similar life table statistics, r_m was 0.222 and 0.225 for T. nerudai and Trichogramma sp., respectively. Parasitoid survival averaged 95% for both species. The results obtained are discussed in the context of selecting one of these natural enemies as a potential biological control agent for the European pine shoot moth Rhyacionia buoliana (Lepidoptera: Tortricidae) in pine forests and the codling moth Cydia pomonella (Lepidoptera: Tortricidae) in apple orchards in Argentina.     

Effect of insecticides on Trichogramma exiguum (Trichogrammatidae: Hymenoptera) preimaginal development and adult survival

The effect of insecticides on Trichogramma exiguum Pinto & Platner emergence, adult survival, and fitness parameters was investigated. Insecticides tested were lambda cyhalothrin, cypermethrin, thiodicarb, profenophos, spinosad, methoxyfenozide, and tebufenozide. All insecticides, with the exception of methoxyfenozide and tebufenozide, adversely affected Trichogramma emergence from Helicoverpa zea (Boddie) host eggs when exposed at different preimaginal stages of development (larval, prepupal, or pupal). Regardless of the developmental stage treated, none of the insecticides tested had a significant effect on the sex ratio or frequency of brachyptery of emerged females. However, the mean life span of emerged T. exiguum females significantly varied among insecticide treatments, and was significantly affected by the developmental stage of parasitoid when treated. Based on LC50 values, spinosad and prophenofos were the most toxic compounds to female T. exiguum adults, followed by lambda cyhalothrin, cypermethrin, and thiodicarb. Insecticides field-weathered for four to 6 d on cotton leaves showed no activity against female T. exiguum adults.     

Ovipositional Synergists and Artificial Diets for Trichogramma australicum Girault (Hymenoptera: Trichogrammatidae)

We studied ovipositional synergists and artificial diets for rearing Trichogramma australicum. Artificial "diet A" included 40% haemolymph of Helicoverpa armigera (Hübner) final instar larvae, 30% of a 10% malt solution in deionised water, 20% chicken egg yolk and 10% Neisenheimer's salt solution with 76 units Penicillin and 76 units Streptomycin/ml diet. Artificial "diet B" was identical except Grace's insect medium® replaced Neisenheimer's salt solution. the number of T. australicum larvae in artificial eggs filled with diet A and diet B was not significantly different (P > 0.05). Significantly fewer (P < 0.05) larvae developed to pupae and adults in artificial eggs filled with diet A. Quantity and quality of artificial diet affected the mortality of T. australicum larvae reared in vitro. Ovipositional synergists included 10% gelatine solution, 10% polyvinyl alcohol solution or 1% agar solution in deionised water. Synergist test-solutions were individually smeared on the external surface of artificial eggs (hemispherical depressions in plastic membrane). Eggs laid and number of T. australicum larvae produced were significantly higher in artificial eggs smeared with gelatine than artificial eggs smeared with polyvinyl alcohol, agar or non-smeared (control) eggs.     

Maternal influence on diapause induction in Trichogramma (Hymenoptera: Trichogrammatidae): the dynamics of photosensitivity

It is known that the prepupal diapause in Trichogramma is dependent on temperature conditions of embryonic and larval development and on the photoperiodic conditions of preimaginal development of maternal females. However, the relative photosensitivity of different preimaginal stages has been never investigated. We studied the position of the photosensitive period over the preimaginal development of maternal females in T. embryophagum Htg. and T. principium Sug. et Sor. by transferring preimaginal stages between diapause‐averting ‘long’ day (L : D = 20 : 4) and diapause‐inducing ‘short’ day (L : D = 12 : 12). Results showed that the influence of maternal photoperiod on progeny diapause was determined during the late pupal stage (last days of preimaginal development at 20°C). During this time, the critical duration of the photoperiodic induction was extremely small: one short or long day caused almost the same effect as the permanent development under these conditions. As a whole, photoperiodic response in Trichogramma was found to be unusually rapid, labile and easily reversible which is probably explained by extremely small size and fast development of these egg parasitoids. The results of this study could be used for elaboration of optimal methods for Trichogramma mass rearing and storage and for prediction of its seasonal cycles under natural conditions.     

Laboratory fecundity as predictor of field success in Trichogramma carverae (Hymenoptera: Trichogrammatidae)

Laboratory fecundity assessments are routinely used to determine the quality of commercially reared Trichogramma egg parasitoids before release for pest control, but there is little information on the relevance of this trait to the field success of Trichogramma. Herein, we characterize the parasitism success of strains of Trichogramma carverae Oatman & Pinto in the laboratory on a factitious (Sitotroga cerealella Olivier) and a natural (Epiphyas postvittana Walker) host. Differences in fecundity of the strains in the laboratory were consistent with a heritability of approximately 10%, allowing ranking of the strains from highest to lowest fecundity. The strains with particularly high and low fecundities were tested for successful parasitism in the field. Results of the field releases show that strain differences in laboratory fecundity did not influence field performance. The implications of this result for fecundity as a quality indicator for commercial stocks are discussed.     

Photo-thermal regulation of diapause in Trichogramma piceum Djur. (Hymenoptera, Trichogrammatidae)

Interaction of the photoperiodic conditions of development of maternal females (day lengths of 2 to 22 h at 20°C) with the thermal regime of development of their progeny (temperature of 12 to 15°C at day length of 12 h) in determination of prepupal diapause in Trichogramma piceum was studied under laboratory conditions. At 15°C the diapause was practically absent. At lower temperatures, the proportion of diapausing prepupae was maximal (25% of larvae at 14°C, 70% of larvae at 13°, and 80% of larvae at 12°C) if the maternal females developed under short day conditions (10–12 h). When maternal females developed at day lengths of 18–20 h, diapause was rarely recorded at all temperatures, while ultra-short (less than 8–10 h) days also caused a decrease in the proportion of diapausing progeny. The right (ecologically important) threshold of this maternal long-day photoperiodic response was about 14–15 h independently of the temperature during the progeny development. These results make it possible to clarify the mechanism of the “maternal photoperiodic correction of the progeny thermal response.” Although the impact of the maternal photoperiodic response can be revealed only within a very narrow thermal range, the relative strength of the diapause-inducing effect of different day lengths is independent of the temperature regimen of the progeny development.     

Development of Trichogramma australicum Girault (Hymenoptera: Trichogrammatidae) in Helicoverpa (Lepidoptera: Noctuidae) host eggs

Abstract Morphological studies of development of the egg parasitoid Trichogramma australicum Girault in the cotton bollworm, Helicoverpa armigera (Hübner), were conducted to provide benchmarks for assessing developmental rates in both natural hosts and artificial diets. Observations of living embryos and histological sections show that embryos proceed rapidly through cleavage and blastoderm formation and show a characteristic pinching or rotation 8 h after deposition. Eggs progressively increase in volume, primarily by increasing in diameter at the widest point. At 29 ± 1°C the duration of the egg stage is 22−24 h, the larval stage 27 h, the prepupal stage 50−52 h, and pupa 85 h. Larvae undergo dramatic shape changes as they ingest food but do not show signs of larval moults, reinforcing observations that there is only one larval instar. Criteria for staging the embryonic and postembryonic development in natural hosts will be used for future studies aimed at developing and refining artificial diets for Trichogramma.     

Acute toxicities and sublethal effects of some conventional insecticides on Trichogramma chilonis (Hymenoptera: Trichogrammatidae)

The acute toxicity of 10 conventional insecticides to adult of Trichogramma chilonis Ishii (Hymenoptera: Trichogrammatidae) was bioassayed by membrane method, and then their sublethal effects on the parasitoid were evaluated in the laboratory. Based on sublethal concentration (LC30) values at 8 h after treatment, we determined that adult T. chilonis were the most susceptible to chlorfenapyr, followed by fipronil, spinosad, avermectins, beta-cypermethrin, and cartap, with lethal concentration (LC)30 values of 0.3133, 0.3269, 1.5408, 3.2961, 6.1469, and 9.021 mg/liter, respectively. The field-recommended concentrations of chlorfluazuron, indoxacarb, Bacillus thuringiensis, and tebufenozide caused <30% mortality of treated adults; therefore, they were used to evaluate sublethal effects on the parasitoid. After treatment with sublethal concentration of fipronil and avermectins, the longevity of treated females (1.2 and 1.6 d) was significantly shortened and fecundity (34.7 and 1.6) was remarkably decreased; consequently, the life-table parameters (R0, r(m), lambda, and T) of T. chilonis were statistically lower than those in the control. Cartap and spinosad also reduced longevity (8 and 7.9 d) and fecundity (110.77 and 117.2) of treated adults, but cartap enhanced the female percentage of F1 offspring (61.6%), resulting a statistical higher R0, r(m), and lambda of treated T. chilonis. In contrast, chlorfluazuron and tebufenozide increased longevity (16.4 and 15.4 d) and fecundity (248 and 256.9) of treated adults but slightly decreased the female percentage of F1 offspring (31.4 and 38.1%). Although chlorfenapyr showed no adverse influence on longevity and fecundity, it remarkably reduced the female percentage of F1 offspring (13.5%), leading to a lower R0, r(m), and lambda of treated T. chilonis. Indoxacarb, B. thuringiensis, and beta-cypermethrin had no obvious sublethal effects on the longevity and fecundity of treated adults. Based on these results, we consider B. thuringienesis, chlorfluazuron, indoxacarb, beta-cypermethrin, and tebufenozide safe to T. chilonis, suggesting that these insecticides are compatible with this parasitoid when being used in the field. However, fipronil, chlorfenapyr, spinosad, and avermectins were very harmful to T. chilonis. Timing of application of these insecticides was critical.     

Pattern of Egg Management by Trichogramma cacoeciae and T. dendrolimi (Hymenoptera: Trichogrammatidae)

The effect of temporary host deprivation on parasitization rates of Trichogramma cacoeciae Marchal and T. dendrolimi Matsumura was investigated. The study was conducted with females that we allowed to engage in 3 days of oviposition after various periods of host deprivation. It seems that the production and management of eggs by the two species is completely different. During the first day of oviposition, parasitization by T. cacoeciae was almost unaffected after 1 to 5 days of host deprivation. As deprivation time increased, however, the number of parasitized hosts decreased from an average of 28.6 ±2.0 hosts provided at emergence to an average of 12.5 ±2.3 hosts when the waiting time was 10 days. The number of hosts parasitized on the first day of parasitization by T. dendrolimi were not affected whatever the waiting test period. During the second or third days of oviposition, the lack of suitable hosts for T. cacoeciae did not depress egg-laying potentiality, whereas a strong reduction in parasitization rates by T. dendrolimi occurred in the next 2 days of oviposition whatever was the waiting period. This leads to ca. 50% reduction in total activity of 3 days of oviposition. Only in T. cacoeciae was it possible to distinguish between ageing and host deprivation. The data suggest that T. dendrolimi is a typical proovigenic species, while T. cacoeciae is neither definitely proovigenic nor synovigenic. A slight decrease in rate of emergence of offspring of T. cacoeciae females that had waited 8 to 10 days for their hosts was observed. As far as biological control is concerned, the efficiency of T. dendrolimi females may be more sensitive to host deprivation than T. cacoeciae.     

Biology and thermal requirements Trichogramma pratissolii Querino & Zucchi (Hymenoptera: Trichogrammatidae) on alternative hosts

The objective of this work was to study the biology and determine the thermal requirements of Trichogramma pratissolii Querino & Zucchi reared on Anagasta kuehniella Zeller (Lepidoptera: Pyralidae) and Corcyra cephalonica Stainton (Lepidoptera: Pyralidae) at 15, 18, 21, 24, 27, 30 and 33 masculineC. The highest percentage of emergence of T. pratissolii was obtained at 27 masculineC on A. kuehniella and from 24 masculineC to 30 masculineC on C. cephalonica. The lower threshold temperature (Tb) and the thermal requirement (K) of T. pratissolii were 12.59 masculineC (Tb) and 122.85 degree-days (K) when reared on A. kuehniella and 11.73 masculineC (Tb) and 139.80 degree-days (K) on C. cephalonica. These results indicate that both A. kuehniella and C. cephalonica are suitable hosts for T. pratissolii mass rearing. The optimal temperature for the immature development and emergence of T. pratissolii on A. kuehniella was 27 masculineC and 24 masculineC to 30 masculineC on C. cephalonica.     

Continuous rearing on Ephestia kuehniella reshaped quality of the parasitoid wasp Trichogramma brassicae (Hymenoptera: Trichogrammatidae)

Continuous mass rearing of Trichogramma brassicae (Bezdenko) at commercial mass-rearing insectaries may affect both quality and performance of natural enemies. In the present study, we studied the quality and performance of a colony of T. brassicae reared for over 45 generations (G) on Ephestia kuehniella Zeller using two-sex life table parameters and parasitism capacity. Our results revealed that although different generations showed no significant difference in terms of female longevity or total life span until G35, G5 and G10 had the highest values of fecundity, gross reproductive rate (GRR), net reproductive rate (R₀), intrinsic rate of natural increase (r), and finite rate of increase (λ). No significant difference in male adult longevity was found among different generations. The longest and shortest mean generation times (T) were found in G10 (13.65 ± 2.31 d) and G45 (13.25 ± 3.37 d), respectively. The finite rate of parasitism (ω) ranged from 0.355 ± 2.332 host/parasitoid/day in G5 to 0.242 ± 0.017 host/parasitoid/day in G45. However, ω did not show any significant difference until G20. These results indicate that T. brassicae wasps held under continuous laboratory rearing declined in quality after 20 generations, and therefore periodical rejuvenation of the colony by adding feral parasitoids is strongly recommended.     

Parasitism in diversified agroecosystems: Phenology ofTrichogramma minutum [Hymenoptera: Trichogrammatidae]

Parasitism ofOstrinia nubilalis egg masses byTrichogramma minutum was observed in maize-bare ground monocultures and polycultures of maize/bean/squash and maize/clover. Parasitism rates were 1.9 times higher in monocultures than in polycultures; seasonal phenology of parasitism, however, was similar in both. Parasitism first occurred during the late whorl/early tassel stage of maize; peak parasitism occurred during the mid to late tassel stage, and then dropped off rapidly. We speculate that direct predation of egg masses, and ammensal preemptive competition for egg masses byColeomegilla maculata may have contributed to the decline in parasitism rates in both monocultures and polycultures during the latter part of the season.      

Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) response to relative humidity with and without host cues

Trichogramma ostriniae is a parasitoid wasp species that is used as a biological control for several lepidopteran agricultural pests. Our study examined the effects of relative humidity (RH) on the behaviour of female T. ostriniae. In Y-tube RH choice assays, wasps generally chose higher RH over lower RH but the latency time taken to make a choice displayed no clear patterns that could be ascribed to the magnitude of the RH difference between arms of the Y-tube. In trials conducted in glass arenas with fixed humidities, the conditional probabilities of transition from searching to interacting with the leaf disk, and from interacting with leaf disks to antennal egg drumming and oviposition, were not significantly different among the RH levels, nor were there differences in latency times. These findings suggest that the level of RH may influence habitat choice but have little effect on search efficacy.     

Temperature effects on induction of parasitization by females of Trichogramma principium (Hymenoptera, Trichogrammatidae)

The effects of temperature on induction and stability of parasitization of less preferred factitious host (the Angoumois grain moth, Sitotroga cerealella) eggs by Trichogramma principium females were studied under laboratory conditions. The percentage of parasitizing females at 15°C was significantly lower than that at 20, 25, and 30°C. At constant temperatures of 15, 20, 25, and 30°C, mean durations of pre-oviposition periods were 6.5, 2.1, 0.9, and 0.6 days, respectively (differences were significant between all regimens). In most of females, parasitization induced by high temperature (25°C) continued after the temperature decrease to 15°C. These results suggest that although emerged females are ready to lay eggs, rather prolonged pre-oviposition period may precede parasitization of less preferred hosts, and the duration of this period may depend on temperature.