Trichogramma

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Trichogramma
Female of Trichogramma dendrolimi on egg of armyworm (Noctuidae), photo was taken by Dr Victor Fursov.jpg
Female Trichogramma dendrolimi on egg of armyworm (Noctuidae)
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Hymenoptera
Family: Trichogrammatidae
Subfamily: Trichogrammatinae
Tribe: Trichogrammatini
Genus: Trichogramma
Westwood, 1833
Species

230+, see text

Trichogramma is a genus of minute polyphagous wasps that are endoparasitoids of insect eggs. [1] Trichogramma is one of around 80 genera from the family Trichogrammatidae, with over 200 species worldwide. [2] [3] [4]

Contents

Although several groups of egg parasitoids are commonly employed for biological control throughout the world, Trichogramma spp. have been the most extensively studied. [5] More than a thousand papers have been published on Trichogramma species, and they are the most used biological control agents in the world. [6]

Trichogramma spp. are also of interest in neuroscience research, having fewer than 10,000 neurons, approaching the theoretical lower limit of the size of an insect brain, yet exhibiting complex behaviors to sustain their lives. [7]

Sensation

Trichogramma have highly developed chemosensory organs due to their need to discriminate host from nonhost in a crowded environment. [3] Zhang et al. 1979 finds 13 sensilla types on the antennae, eyes, mouthparts, wing, leg, and external genitalia of T. dendrolimi . This is considered to generalize to the entire genus, and there may be more still undiscovered. [8]

Parasitism

To locate host eggs, adult females use chemical and visual signals, such as egg shape and colour. [3] After she finds a suitable egg, an experienced female attempts to determine if the egg has previously been parasitized, using her ovipositor and antennal drumming (tapping on the egg surface). Females also use antennal drumming to determine the size and quality of the target egg, which determines the number of eggs the female will insert. [9] A single female can parasitize up to 10 host eggs a day.

Identification

Trichogramma wasps are small and very uniform in structure, which causes difficulty in identifying the separate species. [10] [11] As females are all relatively similar, taxonomists rely upon examination of males to tell the different species apart, using features of their antennae and genitalia. [12] [13]

The first description of a Trichogramma species was in North America in 1871, by Charles V. Riley. He described the tiny wasps that emerged from eggs of the viceroy butterfly as Trichogramma minutum. [3] In taxonomy, original specimens are very important, as they are the basis of reference for subsequent descriptions of species. The original specimens, however, were lost. Riley also described a second species in 1879 as Trichogramma pretiosum, but these specimens were also lost. To correct these errors, entomologists returned to the areas where Riley originally found the species and obtained neotype specimens of T. minutum and T. pretiosum. These specimens are now preserved properly in the United States National Museum. [3] Currently, the number of Trichogramma species is over 200, but as of 1960, only some 40 species of Trichogramma had been described. [14]

Wolbachia in Trichogramma

Wolbachia is a widespread bacterial genus that infects insects' organs, most commonly the reproductive organs. [15] Wolbachia has been observed to alter the host's reproductive success upon infection. [15] Through a series of manipulations, Wolbachia-infected hosts transmit this intracellular bacterium to uninfected individuals. [15] [16] These manipulations include male killing (increasing ratio of infected females that can reproduce), feminization (males become fertile females), parthenogenesis, and cytoplasmic incompatibility. [16] Horizontal transfer of parthenogenesis-inducing Wolbachia, which has been observed in Trichogramma wasps, causes infected females to asexually produce fertile females and nonfunctional males. [17] The effects of this include potential speciation of Trichogramma, if Wolbachia is maintained long enough for genetic divergence to occur and for a new species of asexual wasps to become reproductively isolated. [17]

Transmission of the bacterium through horizontal transfer has been observed within the same species and among different species of Trichogramma, including T. kaykai, T. deion, T. pretiosum, and T. atopovirilia; however, limitations to transmission exist. [16] In vitro successful horizontal transfer is uncommon within Trichogramma, which suggests that the density of Wolbachia must be relatively high inside of the hosts' ovaries. [16] Cytoplasmic incompatibility of the host and bacterium can also be the source of this unsuccessful transfer in-vitro. [16] These limitations in vitro suggest that in nature, horizontal transfer by parthenogenesis-inducing Wolbachia may be a difficult and rare phenomenon. However, when looking at the Wolbachia-host associations, the Trichogramma-Wolbachia form a monophyletic group based on several Wolbachia-specific genes, which may be explained by horizontal transfer of Wolbachia between different species. [16] Therefore, although interspecific horizontal transfer of Wolbachia is limited in vitro, it is likely to occur quite frequently in nature and is not well understood yet.

The effects of Wolbachia in Trichogramma have several evolutionary implications. Commonly, uninfected wasps are unable to breed with infected wasps. [18] Many generations of reproductive isolation of these different groups may result in speciation. [18] In addition, some hosts can evolve with a dependency on Wolbachia for core reproductive functions, such as oogenesis, so that eventually an infection is a requirement for successful reproduction. [18] Finally, Wolbachia can influence gender determination in its hosts so that more females are successfully born. This results in a reversal in sexual selection, where females must compete for male mates, which has evolutionary implications as it exposes different phenotypes to natural selection. [18]

Biological control

Trichogramma spp. have been used for control of lepidopteran pests for many years. They can be considered the Drosophila of the parasitoid world, as they have been used for inundative releases and much understanding today comes from experiments with these wasps. [19] [20]

Entomologists in the early 1900s began to rear Trichogramma spp. for biological control. T. minutum is one of the most commonly found species in Europe and was first mass reared in 1926 on eggs of Sitotroga cerealella . [21] T. minutum has been investigated as a method of biological control of the Choristoneura fumiferana, a major pest of spruce and fir forests. [22]

Nine species of Trichogramma are produced commercially in insectaries around the world, with 30 countries releasing them. Trichogramma wasps are used for control on numerous crops and plants; these include cotton, sugarcane, vegetables, sugarbeets, orchards, and forests. [23] Some of the pests controlled include cotton bollworm ( Helicoverpa armigera ), codling moth ( Cydia pomonella ), lightbrown apple moth ( Epiphyas postvittana ), and European corn borer ( Ostrinia nubilalis ).

Trichogramma species vary in their host specificity. This can lead to nontarget hosts being parasitized. This, in turn, can cause problems by reducing the amount of parasitism of the target host, and depending on the rate of parasitism, nontarget effects could be significant on nontarget host populations. Research is being done on the use of Trichogramma wasps to control populations of spruce bud moth ( Zeiraphera canadensis), which damages white spruce trees. [24]

Trichogramma began to be seriously used in the 1990s in China. Since then some applications have fallen out of use due to the rise of Bt crops because Bt is also toxic to the parasitoid. Future expansion of Bt in China is expected, and this threatens some uses of Trichogramma, however for some crops/pests it remains the better option and so is expected to continue instead of expanded Bt in those applications. Trichogramma will be especially necessary for resistance management if Bt maize/Bt corn is widely adopted. [8]

In 2021 the National Trust in England embarked on a trial of using Trichogramma evanescens , which parasitises clothes moth eggs, in conjunction with pheromones to control common clothes moths, which cause serious damage to carpets, furniture, clothing and other wool and silk objects in historic buildings. [25] The trial was abandoned in 2023; while the microwasps performed well at reducing moth populations in combination with pheromones, they were no better than pheromones alone. [26]

Species used

The most commonly used species for biological control are T. atopovirilia , T. brevicapillum , T. deion , T. exiguum , T. fuentesi , T. minutum , T. nubilale , T. platneri , T. pretiosum , and T. thalense . [3]

T. pretiosum

T. pretiosum is the most widely distributed species in North America. [3] It is a more generalized parasitoid, able to parasitise a range of different species. It has been the focus of many research studies and has been successfully reared on 18 genera of Lepidoptera. T. pretiosum was introduced into Australia in the 1970s as part of the Ord River Irrigation Area IPM scheme. [27] [28]

T. carverae

Trichogramma carverae is mainly used for light brown apple moth and codling moth control, and is predominately used in orchards. [29] In Australia, T. carverae is used for biological control of light brown apple moth in vineyards. Though Australia has its own native Trichogramma species, not much work has been undertaken to use them commercially for biological control within Australia. [30]

Light brown apple moth is common throughout Australia and is polyphagous on more than 80 native and introduced species. The larvae cause the most damage, especially to grape berries, as their feeding provides sites for bunch rot to occur. [31] Losses in the crops can amount up to $2000/ha in one season. It is very predominant in areas such as the Yarra Valley. Insecticide use is not a choice method for most growers, who prefer a more natural means of controlling pests. As a result, Trichogramma wasps were considered a good candidate for biological control, even more so as the moth larvae are difficult to control with insecticide. Moreover, light brown apple moths are relatively vulnerable to egg parasitism, with their eggs being laid in masses of 20–50 on the upper surfaces of basal leaves in grapevines.

Species

List of Trichogramma species

Related Research Articles

<span class="mw-page-title-main">Biological pest control</span> Controlling pests using other organisms

Biological control or biocontrol is a method of controlling pests, whether pest animals such as insects and mites, weeds, or pathogens affecting animals or plants by using other organisms. It relies on predation, parasitism, herbivory, or other natural mechanisms, but typically also involves an active human management role. It can be an important component of integrated pest management (IPM) programs.

<span class="mw-page-title-main">Chalcid wasp</span> Superfamily of wasps

Chalcid wasps are insects within the superfamily Chalcidoidea, part of the order Hymenoptera. The superfamily contains some 22,500 known species, and an estimated total diversity of more than 500,000 species, meaning the vast majority have yet to be discovered and described. The name "chalcid" is often confused with the name "chalcidid", though the latter refers strictly to one constituent family, the Chalcididae, rather than the superfamily as a whole; accordingly, most recent publications (e.g.,) use the name "chalcidoid" when referring to members of the superfamily.

<span class="mw-page-title-main">Parasitoid</span> Organism that lives with its host and kills it

In evolutionary ecology, a parasitoid is an organism that lives in close association with its host at the host's expense, eventually resulting in the death of the host. Parasitoidism is one of six major evolutionary strategies within parasitism, distinguished by the fatal prognosis for the host, which makes the strategy close to predation.

<span class="mw-page-title-main">Tachinidae</span> Family of insects

The Tachinidae are a large and variable family of true flies within the insect order Diptera, with more than 8,200 known species and many more to be discovered. Over 1,300 species have been described in North America alone. Insects in this family commonly are called tachinid flies or simply tachinids. As far as is known, they all are protelean parasitoids, or occasionally parasites, of arthropods, usually other insects. The family is known from many habitats in all zoogeographical regions and is especially diverse in South America.

<i>Manduca quinquemaculata</i> Species of moth

Manduca quinquemaculata, the five-spotted hawkmoth, is a brown and gray hawk moth of the family Sphingidae. The caterpillar, often referred to as the tomato hornworm, can be a major pest in gardens; they get their name from a dark projection on their posterior end and their use of tomatoes as host plants. Tomato hornworms are closely related to the tobacco hornworm Manduca sexta. This confusion arises because caterpillars of both species have similar morphologies and feed on the foliage of various plants from the family Solanaceae, so either species can be found on tobacco or tomato leaves. Because of this, the plant on which the caterpillar is found does not indicate its species.

<span class="mw-page-title-main">Almond moth</span> Species of moth

The almond moth or tropical warehouse moth is a small, stored-product pest. Almond moths infest flour, bran, oats, and other grains, as well as dried fruits. It belongs to the family of snout moths (Pyralidae), and more specifically to the tribe Phycitini of the huge snout moth subfamily Phycitinae. This species may be confused with the related Indian mealmoth or the Mediterranean flour moth, which are also common pantry pests in the same subfamily.

<span class="mw-page-title-main">Parasitoid wasp</span> Group of wasps

Parasitoid wasps are a large group of hymenopteran superfamilies, with all but the wood wasps (Orussoidea) being in the wasp-waisted Apocrita. As parasitoids, they lay their eggs on or in the bodies of other arthropods, sooner or later causing the death of these hosts. Different species specialise in hosts from different insect orders, most often Lepidoptera, though some select beetles, flies, or bugs; the spider wasps (Pompilidae) exclusively attack spiders. More rarely, parasitoid wasps may use plant seeds as hosts, such as Torymus druparum.

<span class="mw-page-title-main">Trichogrammatidae</span> Family of wasps

The Trichogrammatidae are a family of tiny wasps in the Chalcidoidea that include some of the smallest of all insects, with most species having adults less than 1 mm in length, with species of Megaphragma having an adult body length less than 300 μm. The over 840 species are placed in about 80 genera; their distribution is worldwide. Trichogrammatids parasitize the eggs of many different orders of insects. As such, they are among the more important biological control agents known, attacking many pest insects.

<span class="mw-page-title-main">Mediterranean flour moth</span> Species of moth

The Mediterranean flour moth or mill moth is a moth of the family Pyralidae. It is a common pest of cereal grains, especially flour. This moth is found throughout the world, especially in countries with temperate climates. It prefers warm temperatures for more rapid development, but it can survive a wide range of temperatures.

<i>Encarsia formosa</i> Species of wasp

Encarsia formosa is a species of chalcidoid wasp and a well known parasitoid of greenhouse whitefly, one of the first to be used commercially for biological pest control, from the 1920s. They can use at least 15 species of whitefly as a host, including Bemisia tabaci and Aleyrodes proletella.

<span class="mw-page-title-main">Wasp</span> Group of insects

A wasp is any insect of the narrow-waisted suborder Apocrita of the order Hymenoptera which is neither a bee nor an ant; this excludes the broad-waisted sawflies (Symphyta), which look somewhat like wasps, but are in a separate suborder. The wasps do not constitute a clade, a complete natural group with a single ancestor, as bees and ants are deeply nested within the wasps, having evolved from wasp ancestors. Wasps that are members of the clade Aculeata can sting their prey.

<i>Chloridea virescens</i> Species of moth

Chloridea virescens, commonly known as the tobacco budworm, is a moth of the family Noctuidae found throughout the eastern and southwestern United States along with parts of Central America and South America.

Trichogramma brassicae is a species of parasitoid wasps from the Trichogrammatidae family. It mainly parasitizes Lepidopteran hosts in agricultural fields. They are entomaphagous parasitoids that deposit their own eggs inside the host's eggs, consuming the host egg material and emerging upon full development. They are a common biological control species that have been used commercially since the late 1970s. Inundative releases of T. brassicae, recently, can be done by means of drones and integrated control with Bacillus thuringiensis subs. kurstaki were demonstrated effective as chemical insecticide treatments and of course without negative environmental side effects.

<i>Ostrinia furnacalis</i> Species of moth

Ostrinia furnacalis is a species of moth in the family Crambidae, the grass moths. It was described by Achille Guenée in 1854 and is known by the common name Asian corn borer since this species is found in Asia and feeds mainly on corn crop. The moth is found from China to Australia, including in Java, Sulawesi, the Philippines, Borneo, New Guinea, the Solomon Islands, and Micronesia. The Asian corn borer is part of the species complex, Ostrinia, in which members are difficult to distinguish based on appearance. Other Ostrinia such as O. orientalis, O. scapulalis, O. zealis, and O. zaguliaevi can occur with O. furnacalis, and the taxa can be hard to tell apart.

<span class="mw-page-title-main">Naupactini</span> Tribe of beetles

Naupactini is a tribe of broad-nosed weevils. Primarily from the Neotropical realm, reaches highest genus and species diversity in South America. Their size varies from 3.5 to 35 mm long, and its colour patterns are diverse. As well many has colourful iridescent scales, others show opaque scales or setae, and some are subglabrous. In habitats with sparse vegetation or trees absence, the occurrence of flightlessness and parthenogenesis is frequent.

Scirpophaga excerptalis, the white top borer or sugarcane top borer, is a moth in the family Crambidae. It was described by Francis Walker in 1863. It is found in southern Asia from the Indian Subcontinent in the west to southern China in the east, south to New Guinea, possibly Australia and the Solomon Islands.

Trichogramma japonicum is a minute wasp parasitoid from the Trichogrammatidae family in the order Hymenoptera. T. japonicum parasitizes the eggs of many pest species, especially Lepidoptera found in many monocultures. They are entomophagous parasitoids that deposit their eggs inside the host species' egg, consuming the host egg material and emerging from the egg once development is complete. T. japonicum can be found naturally in rice ecosystems, but are dispersed commercially to many monocultures as a biological control. The mitochondrial genomes of T. japonicum are significantly rearranged when comparing it to related insects.

<span class="mw-page-title-main">Meteorinae</span> Subfamily of wasps

Meteorinae is a subfamily of braconid parasitoid wasps; however, since 2015, most scientists have treated this clade as the Tribe Meteorini in Euphorinae. Several species have been used in biological control programs. The name for this group comes from the pupal stage, which, in species attacking Lepidopteran hosts, hangs suspended from a long thread of silk.

<i>Tetrastichus coeruleus</i> Species of wasp

Tetrastichus coeruleus is a gregarious koinobiont wasp which can be used as a biological control agent for the common asparagus beetle.

Andricus mukaigawae is a species of gall wasp native to southeastern Asia. It creates galls on the buds and leaves of oak trees. The galls are sometimes used by other gall wasps unable to create galls of their own, with both species sharing the gall.

References

  1. ↑ Flanders, S; Quednau, W (1960). "Taxonomy of the genus Trichogramma (Hymenoptera, Chalcidoidea, Trichogrammatidae)". BioControl. 5 (4): 285–294. doi:10.1007/bf02372951. S2CID   34509414.
  2. ↑ Consoli FL, Parra JRP, Zucchi RA (2010) 'Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma.' (Springer).
  3. 1 2 3 4 5 6 7 Knutson A (2005) 'The Trichogramma Manual: A guide to the use of Trichogramma for Biological Control with Special Reference to Augmentative Releases for Control of Bollworm and Budworm in Cotton.' (Texas Agricultural Extension Service).
  4. ↑ Sumer, F; Tuncbilek, AS; Oztemiz, S; Pintureau, B; Rugman-Jones, P; Stouthamer, R (2009). "A molecular key to the common species of Trichogramma of the Mediterranean region" (PDF). BioControl. 54 (5): 617–624. doi: 10.1007/s10526-009-9219-8 .
  5. ↑ Upadhyay RK, Mukerji KG, Chamola BP (2001) 'Biocontrol potential and its Exploitation in Sustainable Agriculture: Insect Pests.' (Kluwer Academic/ Plenum Publishers).
  6. ↑ Knutson A (2005) 'The Trichogramma Manual: A guide to the use of Trichogramma for Biological Control with Special Reference to Augmentative Releases for Control of bollworm and Budworm in Cotton.' (Texas Agricultural Extension Service).
  7. ↑ van der Woude, Emma; Smid, Hans M. (September 2017). "Maximized complexity in miniaturized brains: morphology and distribution of octopaminergic, dopaminergic and serotonergic neurons in the parasitic wasp, Trichogramma evanescens". Cell and Tissue Research. 369 (3): 477–496. doi: 10.1007/s00441-017-2642-8 . PMC   5579201 . PMID   28597098.
  8. 1 2 Zang, Lian-Sheng; Wang, Su; Zhang, Fan; Desneux, Nicolas (2021-01-07). "Biological Control with Trichogramma in China: History, Present Status, and Perspectives". Annual Review of Entomology . Annual Reviews. 66 (1): 463–484. doi:10.1146/annurev-ento-060120-091620. ISSN   0066-4170. PMID   32976724. S2CID   221938883.
  9. ↑ Klomp, H; Teerink, B.J.; Wei, Chun Ma (1979). "Discrimination Between Parasitized and Unparasitized Hosts in the Egg Parasite Trichogramma embryophagum (Hym.: Trichogrammatidae): a Matter of Learning and Forgetting". Netherlands Journal of Zoology. 30 (2): 254–27. doi:10.1163/002829679X00412. ISSN   0028-2960.
  10. ↑ Nagarkatti, S; Nagaraja, H (1977). "Biosystematics of Trichogramma and Trichogrammatoidea species". Annual Review of Entomology. 22: 157–176. doi:10.1146/annurev.en.22.010177.001105.
  11. ↑ Thomson, LJ; Rundle, BJ; Carew, ME; Hoffmann, AA (2003). "Identification and characterization of Trichogramma species from south-eastern Australia using the internal transcribed spacer 2 (ITS-2) region of the ribosomal gene complex". Entomologia Experimentalis et Applicata. 106 (3): 235–240. doi:10.1046/j.1570-7458.2003.00029.x. S2CID   84163027.
  12. ↑ Nagarkatti, S; Nagaraja, H (1971). "Redescriptions of some known species of Trichogramma (Hym., Trichogrammatidae), showing the importance of the male genitalia as a diagnostic character". Bulletin of Entomological Research. 61: 13–31. doi:10.1017/s0007485300057412.
  13. ↑ Polaszek, A; Rugman-Jones, P; Stouthamer, R; Hernandez-Suarez, E; Cabello, T; Pino Pérez, M (2012). "Molecular and morphological diagnoses of five species of Trichogramma: biological control agents of Chrysodeixis chalcites (Lepidoptera: Noctuidae) and Tuta absoluta (Lepidoptera: Gelechiidae) in the Canary Islands". BioControl. 57: 21–35. doi:10.1007/s10526-011-9361-y. S2CID   18701180.
  14. ↑ "Chalcids".
  15. 1 2 3 Grenier, Simon; et al. (1998). "Successful horizontal transfer of Wolbachia symbionts between Trichogramma wasps". Proceedings of the Royal Society of London B: Biological Sciences. 265 (1404): 1441–1445. doi:10.1098/rspb.1998.0455. PMC   1689218 .
  16. 1 2 3 4 5 6 Huigens, M. E.; et al. (2004). "Natural interspecific and intraspecific horizontal transfer of parthenogenesis–inducing wolbachia in trichogramma wasps". Proceedings of the Royal Society of London B: Biological Sciences. 271 (1538): 509–515. doi:10.1098/rspb.2003.2640. PMC   1691627 . PMID   15129961.
  17. 1 2 Bourtzis, Kostas; O'Neill, Scott (1998). "Wolbachia Infections and Arthropod Reproduction". BioScience. 48 (4): 287–293. doi: 10.2307/1313355 . JSTOR   1313355.
  18. 1 2 3 4 Charlat, Sylvain; Hurst, Gregory D. D.; Merçot, Hervé (2003-04-01). "Evolutionary consequences of Wolbachia infections". Trends in Genetics. 19 (4): 217–223. doi:10.1016/S0168-9525(03)00024-6. ISSN   0168-9525. PMID   12683975.
  19. ↑ Smith, Sandy M. (1996). "Biological Control with Trichogramma: Advances, Successes, and Potential of Their Use". Annual Review of Entomology . Annual Reviews. 41 (1): 375–406. doi:10.1146/annurev.en.41.010196.002111. ISSN   0066-4170. PMID   15012334. S2CID   33808315. S2CID   96421784.
  20. ↑ BURGIO G., MAINI S., 1995.- Control of European corn borer in sweet corn by Trichogramma brassicae Bezd. (Hym., Trichogrammatidae).- Journal of Applied Entomology, 119 (1): 83-87.
  21. ↑ Flanders, SE (1930). "Mass Production of Egg Parasites of the Genus Trichogramma". Hilgardia. 4 (16): 465–501. doi: 10.3733/hilg.v04n16p465 .
  22. ↑ Smith, S.M.; Hubbes, M.; Carrow, J.R. 1986. Factors affecting inundative releases of Trichogramma minutum Ril. against the spruce budworm. J. Appl. Entomol. 101(1):29–39.
  23. ↑ Hassan, SA (1993). "The mass rearing and utilization of Trichogramma to control lepidopterous pests: Achievements and outlook". Pesticide Science. 37 (4): 387–391. doi:10.1002/ps.2780370412.
  24. ↑ Turgeon, Jean J. "Status of research on the development of management tactics and strategies for the spruce bud moth in white spruce plantations". The Forestry Chronicle. 68 (5): 614–622. doi:10.5558/tfc68614-5.
  25. ↑ "Conservation at Blickling Hall, Norfolk". National Trust. 2022.
  26. ↑ "'Surprising' clothes moths slump of nearly 40% across National Trust houses, possibly helped by record heat and drought, charity's annual insect pests report finds" (Press release). National Trust. 13 February 2023.
  27. ↑ Davies, AP; Zalucki, MP (2008). "Collection of Trichogramma Westwood (Hymenoptera: Trichogrammatidae) from tropical northern Australia: a survey of egg parasitoids for potential pest insect biological control in regions of proposed agricultural expansion". Australian Journal of Entomology. 47 (2): 160–167. doi:10.1111/j.1440-6055.2008.00644.x.
  28. ↑ Davies, AP; Pufke, US; Zalucki, MP (2011). "Spatio-temporal variation in Helicoverpa egg parasitism by Trichogramma in a tropical Bt-transgenic cotton landscape". Agricultural and Forest Entomology. 13 (3): 247–258. doi:10.1111/j.1461-9563.2010.00512.x. S2CID   83477611.
  29. ↑ Llewellyn R (2002) The good bug book: beneficial organisms commercially available in Australia and New Zealand for biological pest control.' (Integrated Pest Management Pty Ltd).
  30. ↑ Glenn, DC; Hercus, MJ; Hoffmann, AA (1997). "Characterizing Trichogramma (Hymenoptera: Trichogrammatidae) species for biocontrol of light brown apple moth (Lepidoptera: Tortricidae) in grapevines in Australia". Annals of the Entomological Society of America. 90 (2): 128–137. doi: 10.1093/aesa/90.2.128 .
  31. ↑ Glenn, DC; Hoffmann, AA (1997). "Developing a commercially viable system for biological control of light brown apple moth (Lepidoptera: Tortricidae) in grapes using endemic Trichogramma (Hymenoptera: Trichogrammatidae)". Journal of Economic Entomology. 90 (2): 370–382. doi: 10.1093/jee/90.2.370 .
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