Assessment ofTrichogramma species for biological control of forest lepidopteran defoliators

In a laboratory study, we determined the potential of threeTrichogramma (Hymenoptera: Trichogrammatidae) species,T. brassicae Bezdenko,T. minutum Riley andT. nr.sibiricum Sorokina, for biological control against six species of forest lepidopteran pests, black army cutworm, hemlock looper, eastern spruce budworm, western spruce budworm, white-marked tussock moth, and gypsy moth. Females of each parasitoid species were offered eggs from each of the six host species. Parasitization and the effect of the host species on the emerging progeny were examined and recorded.Trichogramma minutum had the broadest host range and successfully parasitized four host species out of the six offered.Trichogramma nr.sibiricum had the narrowest host range and parasitized only two species of hosts. Of the six host species, black army cutworm was the most preferred by all threeTrichogramma species; white-marked tussock moth and gypsy moth were not parasitized by any parasitoids. There was a positive correlation between the size of female offspring and their corresponding egg complement in all three parasitoid species. The developmental time of parasitoids from egg to adult was influenced by both the parasitoid and host species. Our results suggest thatT. minutum has the greatest potential for biological control against various forest lepidopteran pests and that the black army cutworm may be the best target candidate for further study.     

The Oak-silkworm Egg Antheraea pernyi (Lepidoptera: Anthelidae) as a Mass Rearing Host for Parasitoids of the Genus Trichogramma (Hymenoptera: Trichogrammatidae)

The acceptance of 40 different strains of 24 Trichogramma (Hymenoptera: Trichogrammatidae) species for oak-silkworm host eggs, Antheraea pernyi Guerin-Meneville (Lepidoptera: Anthelidae) was tested in laboratory experiments. The oak-silkworm, which is commercially used in China to mass produce Trichogramma dendrolimi Matsumura on a large scale, was accepted for egg laying by 10 out of the 24 species tested but only 3 species (four strains of T. dendrolimi, three strains of T. chilonis Ishii and one strain of T. cacoeciae Marchal) successfully completed development to adult emergence. The number of adults emerged per host egg averaged 83.2, 37.0, 42.3, 53.0 for four different strains of T. dendrolimi; 42.5, 10.0 for two strains of T. chilonis; 24.5 and 0 for two strains of T. cacoeciae.

Seven other Trichogramma species develoedp in A. pernyi eggs, but no adult emergence occurred and no emergence holes on the chorion were found. The number of Trichogramma larvae, pupae, and adults together per host egg averaged 81.7 and 67.4 for two strains of T. embryophagum Hartig; 39.0 for T. japonicum Ashmead; 35.0, 16.7, 19.0, 0 for four strains of T. evanescens Westwood; 18.7, 0, 0, 0 for four strains of T. brassicae Bezdenko; 11.5 for T. piceum Dyurich; 76.4 and 23.0 for two unidentified strains collected in apple and vine orchards in Germany, respectively.

The following 14 Trichogramma species did not parasitize any A. pernyi eggs: T. atopovirilia Oatman & Platner, T. bourarachae Pintureau & Babault, T. buesi Voegél, T. funiculatum Carver, T. ivelae Pang & Chen, T. meyeri Sorokina, T. minutum Riley, T. nerudai Pintureau, T. nubilale Ertle & Davis, T. ostriniae Pang & Chen, T. principium Sugonjaev & Sorokina, T. pretiosum Riley and two further unidentified strains that originated from France and Switzerland.

The results confirmed that A. pernyi is a suitable host for rearing T. dendrolimi and T. chilonis and that the two species T. cacoeciae and T. embryophagum, under optimal conditions, might be possible candidates for rearing.     

Development of a continuous cell line from the insect egg parasitoid,Trichogramma pretiosum (Hymenoptera; Trichogrammatidae)

Summary A cell line (IPLB-TpE1) was established from embryos of the hymenopteran parasitoid,Trichogramma pretiosum Riley. Cultures contain a mixture of attached, elongate spindle-shaped cells and large aggregates of suspended cells. Chromosomes of the cells were typical ofTrichogramma species and isozyme characterization showed patterns similar toT. pretiosum adults, but distinctly different fromHeliothis zea, the lepidopteran host from which parasite eggs were obtained. The cells are capable of growth over a wide range of osmotic pressures with equal growth between 350 and 600 mOsm/kg. Optimal growth was obtained with a pH of 6.5. Doubling time at the 40th passage was 72 h and cultures are currently subcultured at weekly intervals. The mention of a commercial product does not constitute an endorsement by the U. S. Department of Agriculture.     

Egg loads and egg masses: Parasitism ofChoristoneura rosaceana eggs by Trichogramma minutum after inundativerelease in a commercial blueberry field

Inundative releases of Trichogramma minutum Riley were made in a commercialblueberry field in British Columbia, Canada, todetermine the extent of dispersal of adult wasps, andto determine whether complete parasitism of eggswithin egg masses of the target host [oblique-bandedleafroller (OBLR), Choristoneura rosaceana(Harris)] occurred. Three weekly releases of waspswere made from a single release point in the center ofeach field during the flight of first generation OBLRadults. Sticky trap, sentinel egg mass andtarget-host egg mass data all indicated only a limitedrange of dispersal of T. minutum within thefield. In addition, only partial parasitism of eggmasses of the target host occurred even in closeproximity to the release point. We discuss theimportance of determining the response of Trichogramma females to previously-parasitized eggswhen using Trichogramma wasps for biologicalcontrol of lepidopterous species that oviposit largeegg masses.     

Different responses of three predatory mite species toTetranychus urticae,Eriophyes dioscoridis andBrevipalpus pulcher: Evidence for the existence of kairomones and allomones

The responses of 3 phytoseiid mite speciesPhytoseiulus persimilis Athias-Henriot,Phytoseius finitimus Ribaga andAmblyseius gossipi Elbadry to allelochemics emitted by prey mite speciesTetranychus urticae Koch,Brevipalpus pulcher (Canestrini & Fanzago) andEriophyes dioscoridis Soliman & Abou-Awad were studied using a test of two-choice assays. The repellent effect elicited by the tenuipalpid mite,B. pulcher and the eriophyid mite,E. dioscoridis againstP. persimilis could be an evidence for the existence of allomones produced by these 2 prey species. The negative response ofP. persimilis to the different stadia ofB. pulcher and the attraction ofP. finitimus toward the same prey suggest that the volatile semiochemicals produced by this prey act as kairomones forP. finitimus and as allomones forP. persimilis. The strong attraction ofP. finitimus andA. gossipi to the different stadia ofT. urticae and the considerable attraction of either predator toB. pulcher compared to the neutral response toE. dioscoridis reveal that both predators show a hierarchy of preference for the kairomones of the 3 prey species studied.      

Mass production and utilization ofTrichogramma: 10. Control of the codling mothCydia pomonella and the summer fruit tortrix mothAdoxophyes orana [Lep.: Tortricidae]

The effectiveness ofTrichogramma dendrolimi, Trichogramma embryophagum, Trichogramma sp. strain 45 andTrichogramma sp. strain 48 to control the codling mothCydia pomonella L. and the summer fruit tortrix mothAdoxophyes orana F.R. was tested in 4 field trials (1984–1986). Four to sixTrichogramma treatments (depending on the temperature) each at 400 (pillar trees) to 9,000 (round tops) parasites per tree were carried out between June and August to insure the continuous presence ofTrichogramma in the plots. The monitoring was done by examining 3,000 to 10,000 apple fruits per plot. T. dendrolimi reduced the damage ofC. pomonella by 61.35%, ofA. orana by 72.85%.T. embryophagum reduced the damage ofC. pomonella by 50.06%, ofA. orana by 50.8%.Trichogramma strain 45 reduced the damage ofC. pomonella by 41.6% and ofA. orana by 87.9%,Trichogramma strain 48 by 57.2% and 51.2% respectively. The reduction of 67.1% in the number of apple fruits damaged byC. pomonella andA. orana obtained by the inundative releases ofT. dendrolimi in these experiments is considered economically and the use of this species in practice is recommended.      

Selection of suitable trichogramma strains to control the codling mothCydia pomonella and the two summer fruit tortrix mothsAdoxophyes orana,Pandemis heparana [Lep.: Tortricidae]

Simple laboratory methods to select candidateTrichogramma strains for use in biological control were tried. 17 strains were screened for their suitability against the codling mothCydia pomonella L. as well as the 2 summer fruit tortrix mothsAdoxophyes orana F.R. andPandemis heparana Schiff. In one set of experiments, the capacity ofTrichogramma to parasitize each of these target pests was examined, in another set, the preference ofTrichogramma to contact and parasitize the target pests compared to the standard mass rearing hostSitotroga cerealella was assessed in choice experiments. A strain ofTrichogramma dendrolimi from the People's Republic of China was found to have the highest fecundity with all the 4 hosts tested. In choice experiments, however, this strain was shown to have a near equal preference between the target tortrix pestsC. pomonella, A. orana and the replacement hostS. cerealella. 11 localTrichogramma strains collected from fruit orchards and vineyards in different locations in the Federal Republic of Germany were reared separately. Four of these local strains, one identified asT. embryophagum, showed clear preference to the tortrix pestsC. pomonella andA. orana compared toS. cerealella. The preference of one of these strains was particularly strong and amounted to a near total rejection ofS. cerealella eggs in the presence of any of the 2 tortrix pests. The remaining 12 strains had weaker parasitization capacity and/or less preference to the target pests. Four of the strains tested in these experiments, includingT. dendrolimi andT. embryophagum, were mass reared and released in apple orchards between 1984 and 1986. The results of these field experiments are planned to be published in this journal. Mit Unterstützung der Deutschen Forschungsgemeinschaft.     

Host Preferences of Trichogramma pretiosum and the Influence of Prior Ovipositional Experience on the Parasitism of Plutella xylostella and Pseudoplusia includens Eggs

Trichogramma wasps are generalist egg parasitoids used in biological control efforts. In a multi host situation they may preferentially parasitize a non-target host species to the detriment of the control program. Plutella xylostella Linnaeus (Lepidoptera: Plutellidae) is a very serious pest of cabbage, but is only one in a number of species in the ‘cabbageworm’ complex. We investigated the host preferences of Trichogramma pretiosum Riley (Hymenoptera: Chalcidoidea) when offered the eggs of Plutella xylostella and the eggs of Pseudoplusia includens Hübner (Lepidoptera: Noctuidae), another species in the ‘cabbageworm’ complex. Trichogramma pretiosum reared on the eggs of the factitious host Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) parasitized both Plutella xylostella and Pseudoplusia includens eggs under laboratory conditions. For both choice and no-choice experiments, T. pretiosum parasitized significantly more P. xylostella eggs than P. includens eggs. Prior ovipositional experience with one or other of the two host species had no effect on the subsequent parasitism levels of the two host species. The preference for P. xylostella eggs was also not affected by this prior ovipositional experience.     

Environmental variation in physical and chemical cues used by the parasitic wasp,Aphytis melinus, for host recognition

O-caffeoyltyrosine is a host recognition kairomone forAphytis melinus DeBach (Aphelinidae) found in the covers of its host, California red scale,Aonidiella aurantii (Maskell) (Diaspidae). This study tests the hypothesis that the concentration ofO-caffeoyltyrosine and scale cover size are reliable indicators of scale body size, an important component of host quality forA. melinus, over a range of scale rearing conditions. Both scale cover area andO-caffeoyltyrosine concentrations were only qualitatively related to scale body size during the third instar, the scale life stage most suitable forA. melinus. Scale cover area andO-caffeoyltyrosine concentrations were reduced, relative to scale body size, when scale were reared on bark and leaves compared to fruits. Scale cover area andO-caffeoyltyrosine concentration were also relatively reduced when scales were reared in mid-summer compared to spring and fall, and when reared on orange cultivars compared to lemon cultivars in the field. Finally, scale cover area andO-caffeoyltyrosine concentration were reduced when scale were reared at 52% compared to 100% humidity in the laboratory. Scales appear to be chemically conspicuous toA. melinus for a short period of the time in which they are physiologically susceptible. Scales that minimize their cover size and maximize the incorporation rate ofO-caffeoyltyrosine into covers may minimize their conspicuousness toA. melinus. Minimizing scale cover size, but not necessarily incorporation rates, may make scales more vulnerable to predators, however.     

Patch exploitation strategies of parasitoids under indirect intra‐ and inter‐specific competition

1. Insect parasitoids are expected to evolve behavioural strategies to exploit resources in competitive environments optimally. Indirect competition between parasitoids is particularly common because exploited host patches remain available in the environment for other foraging individuals. 2. The effects of indirect competition on the behaviour of two closely related generalist egg parasitoids were investigated: Trichogramma pintoi Voegelé and Trichogramma minutum Riley (Hymenoptera: Trichogrammatidae). Patch residence time, a patch‐leaving mechanism, and progeny sex allocation of females foraging were analysed: (i) alone, (ii) in patches partially parasitised by conspecifics, and (iii) in patches partially parasitised by heterospecifics. 3. Each species responded differently to indirect competition. Trichogramma pintoi females shortened their patch residence times, but they did not adjust their progeny sex ratios. In contrast, T. minutum females did not modify their patch residence times, but they did increase their progeny sex ratios in response to competition. Both Trichogramma species used host rejection, either by antenna rejection or by ovipositor rejection, as a patch‐leaving mechanism. 4. In agreement with a companion study of direct competition using the same model species, the present results indicate that even amongst closely related species, responses to competition can vary considerably.     

The effect of host size on quality attributes of the egg parasitoid,Trichogramma pretiosum

In a study of the quality ofTrichogramma pretiosum Riley (Hymenoptera: Trichogrammidae), we compared female wasps emerging from natural hosts, parasitized in the laboratory or the field with those emerging from factitious hosts used for commercial mass production. Females from the natural hosts were larger, more fecund, and longer lived than those from the factitious hosts. Compared to small females, large female wasps are substantially more fecund when honey (carbohydrate) is available but marginally more fecund when honey is unavailable. The size of a femaleT. pretiosum depends on two factors: the size of the host egg from which it emerges even when the wasp was gregarious, and the number of conspecifics that emerge with it. The similarities in the size distribution of female wasps emerging from natural hosts, in conjunction with the mechanism by whichTrichogramma measure host size and allocate eggs accordingly, suggests the hypothesis that size related components of fitness in femaleT. pretiosum are under strong selection in the field.     

Are egg parasitoids of the genus Trichogramma (Hymenoptera: Trichogrammatidae) promising biological control agents for regulating the invasive Box tree pyralid,Cydalima perspectalis (Lepidoptera: Crambidae)?

The Box tree pyralid, Cydalima perspectalis Walker (Lepidoptera: Crambidae), is an invasive species in Europe, not yet regulated by natural enemies. It is highly destructive to ornamental and native Buxus due to defoliation by larval feeding. The ability of eight Trichogramma species (T. brassicae Bezdenko, T. bourarachae Pintureau & Babault, T. cacoeciae Marchal, T. cordubensis Vargas & Cabello, T. dendrolimi Matsumura, T. evanescens Westwood, T. nerudai Pintureau & Gerding and T. pintoi Voegele) to parasitise and locate eggs of C. perspectalis was assessed in the laboratory. In direct observation tests, all species started to examine and oviposit into exposed eggs. Resulting egg parasitism was low and ranged between 4% and 20% for most of the parasitoid species after three days of exposure. Only T. dendrolimi parasitised significantly more host eggs with parasitism rates above 40%. On average, two to three progeny emerged from one host egg and the resulting sex ratio was female-biased, indicating suitability of the target host for progeny production. In subsequent cage tests on potted Buxus plants, again T. dendrolimi was the most efficient species in locating host eggs on foliage. We conclude that C. perspectalis eggs are attractive to various Trichogramma species. T. pintoi had the highest number of egg encounters and active females. T. dendrolimi females were most able to locate host eggs and to oviposit and produce successfully on them. Nonetheless, further study is needed to clarify the suspected role of potentially egg defensive mechanisms that may impede higher parasitisation in C. perspectalis.     

Freshwater fugu or pufferfishes of the genusTetraodon from the Mekong basin, with descriptions of two new species

The fresh waters of the Mekong basin are inhabited by five species of the pufferfish genusTetraodon Linnaeus, 1758 (sensu lato): the widely distributedT. leiurus Bleeker, 1851; two previously described species endemic to the Mekong,T. baileyi Sontirat, 1989 andT. suvattii Sontirat & Soonthornsathit, 1985; one new species endemic to the Mekong basins.Tetraodon baileyi has now been collected numerous times but only in or near rapids;T. abei, T. barbatus andT. suvattii are often but not exclusively associated with rapids or at least swift flowing streams; whileT. leiurus is found in almost all habitats except rapids.Tetraodon abei andT. barbatus are closely related toT. leiurus, from which they differ most strikingly in coloration.Tetraodon survattii differs from all of the others in having a strongly upturned mouth and light and dark stripes or spots radiating outwards from the eye.Tetraodon baileyi, the most distinctive Mekong pufferfish, has head and body more or less extensively covered with dermal cirri and is entirely scaleless.     

Host specificity and biology ofHeteropsylla spinulosa [Hom.: Psyllidae] introduced into Australia and Western Samoa for the biological control ofMimosa invisa

The biology and host specificity of the psyllidHeteropsylla spinulosa Muddiman, Hodkinson & Hollis collected fromMimosa invisa Von Martius, was studied in Brazil and in Australia. Oviposition was recorded on 19 of 100 plant species tested but nymphs died without feeding, except onM. invisa. H. spinulosa was shown to be specific toM. invisa and was subsequently released and established in Australia and Western Samoa.      

Effects of pre-adult and adult experience on host acceptance in choice and non-choice tests in two strains ofTrichogramma

The effect of adult learning through an oviposition experience, and pre-adult learning through development inside a host was investigated in two strains of an Australian egg parasitoid,Trichogramma nrivelae (Hymenoptera: Trichogrammatidae). Host response was measured in two types of laboratory preference tests. In single host tests, females reared on three lepidopteran hosts (Heliothis punctigera (Noctuidae),Papilio aegeus (Papilionidae), andHypolimnas bolina (Nymphalinae)) were presented host eggs individually, and allowed two ovipositions. Pre-adult experience affected host preference in only one strain, while acceptance of a host was increased in both strains when they had previously oviposited in this host species. An oviposition experience had a stronger effect on host preference than pre-adult experience. In choice tests, pairwise combinations of hosts were arranged in an alternating grid. The ratio of host acceptances to host contacts was computed for the whole test and up to the first oviposition. These indicated that effects of rearing host were weak or absent, but the host chosen initially had a strong effect on host preference. Relative size of the hosts had a strong effect on choice of the first host. The implications of learning inTrichogramma are discussed in relation to host preference testing procedures and the selection of candidate strains for mass rearing and inundative release.     

Flight initiation in the egg parasitoid Trichogramma minutum: Effects of ambient temperature, mates, food, and host eggs

Emergence, preening, and flight initiation were studied in laboratory-reared Trichogramma minutum Riley (Hymenoptera: Trichogrammatidae). Male parasitoids emerged first and flew before females. When both sexes were present in flight cylinders, female parasitoids flew before males. Flight propensity in males was negatively related to the number of emerging females, while flight propensity in females was independent of the number of males present. Ambient temperature significantly affected the propensity and timing of flight; between 70–80% of the parasitoids flew at 25 and 30 °C while less than 4%, mostly males, flew at 20 °C. No flights were observed at 15 °C. The presence of fresh host eggs caused a reduction in the proportion of female parasitoids that flew and a delay in the time to flight for the females that did fly. The presence of food increased the flight propensity of female parasitoids, but did not affect the timing of flight. The relationship between flight behaviour and the efficiency of mass-reared Trichogramma is discussed in terms of its importance for inundative release programmes.     

Allozyme divergence among four species ofPodaechmea s. l. and the status ofUrsulaea (Bromeliaceae, Bromelioideae)

The genetic relationships ofAechmea mexicana, A. lueddemanniana, A. macvaughii andA. tuitensis were investigated using starch gel electrophoresis. Eight enzyme systems encoded by ten putative gene loci were resolved in seventeen populations.Nei's (1978) genetic distances were obtained from allelic frequencies and used with UPGMA algorithm. Results indicate that some populations belonging to different species display genetic similarities closer to each other than to some conspecific populations. Our results do not support the proposed genusUrsulaea (Read & Baensch 1994), sinceA. tuitensis was closer toA. lueddemanniana andA. mexicana than toA. macvaughii.     

Malic enzyme,phosphoglucomutase and phosphoglucose isomerase isozymes inTrichogramma [Hym.: Trichogrammatidae]

ME, PGM and PGI electrophoretic banding patterns in 20 laboratory cultures representing 14 species ofTrichogramma were studied. Variations in PGM were found inT. exiguum, T. marylandense, andT. pretiosum. PGI also showed variation inT. exiguum, T. marylandense, T. minutum, andT. parkeri. However, ME variations were found only inT. pretiosum. Based on progeny analyses, we concluded that ME is a tetramer inTrichogramma with fast and slow alleles at a single locus, and that both PGM and PGI have a single locus and each has four alleles. PGM is a monomer, but PGI is a dimer.

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Résumé Les bandes électrophorétiques de l'enzyme malique, de la P.G.M. et de la P.G.I. ont été étudiées chez 20 souches de laboratoire représentant 14 espèces deTrichogramma. Des variations de la P.G.M. ont été trouvées chezT. exiguum, T. marylandense etT. pretiosum. La. P.G.I. montre aussi des variations chezT. exiguum, T. marylandense, T. minutum etT. parkeri. Par contre, des variations de l'enzyme malique ne sont trouvées que chezT. pretiosum. En nous basant, sur l'analyse de progénitures, nous avons conclu que l'enzyme malique est un tétramère chezTrichogramma comprenant un allèle “lent” et un alléle “rapide”, à un seul locus, et que la P.G.M. et la P.G.I. ont chacune un seul locus à quatre allèles. La P.G.M. est un monomère mais la P.G.I. est un dimère.

     

Effect of fertilized,unfertilized, and UV‐irradiated hosts on parasitism and suitability for Trichogramma parasitoids

Trichogramma spp. (Hymenoptera: Trichogrammatidae) parasitoids have been commonly used as biological control agents in insect pest management. Host quality is believed to influence parasitism, host preference, and suitability for parasitoids. To date, limited studies have compared the parasitism of Trichogramma parasitoids on fertilized, unfertilized, and sterilized host eggs. Hence, we studied the performance of three Trichogramma egg parasitoids, Trichogramma japonicum Ashmead, Trichogramma chilonis Ishii, and Trichogramma leucaniae Pang & Chen, on fertilized, unfertilized, and ultraviolet (UV)‐irradiated fertilized (UVF) eggs of rice moth, Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae). In a no‐choice test, T. japonicum and T. leucaniae parasitized significantly more fertilized or UVF than unfertilized hosts, and T. chilonis parasitized significantly more UVF than either fertilized or unfertilized hosts. In a choice test, all three Trichogramma parasitoids parasitized UVF hosts the most, and unfertilized hosts the least. There were similar percentages of adult emergence and female progeny among fertilized, unfertilized, and UVF hosts for all three Trichogramma parasitoids, except that T. japonicum had significantly lower adult emergence on fertilized hosts. We also found that all three Trichogramma parasitoids developed slower on unfertilized hosts. Regardless of host treatments, T. leucaniae had the longest developmental time and T. chilonis had the shortest. We conclude that Trichogramma parasitoids prefer parasitizing UVF eggs of C. cephalonica without negative effects on their emergence and sex allocation.