Trichogramma

Life-forms

Superregnum: Eukaryota
Cladus: Unikonta
Cladus: Opisthokonta
Cladus: Holozoa
Regnum: Animalia
Subregnum: Eumetazoa
Cladus: Bilateria
Cladus: Nephrozoa
Cladus: Protostomia
Cladus: Ecdysozoa
Cladus: Panarthropoda
Phylum: Arthropoda
Subphylum: Hexapoda
Classis: Insecta
Cladus: Dicondylia
Subclassis: Pterygota
Cladus: Metapterygota
Infraclassis: Neoptera
Cladus: Eumetabola
Cladus: Endopterygota
Superordo: Hymenopterida
Ordo: Hymenoptera
Subordo: Apocrita
Superfamilia: Chalcidoidea

Familia: Trichogrammatidae
Genus: Trichogramma
Subgenera: T. (Trichogramma) – T. (Trichogrammanza)

Overview of species: T. acacioi – T. acantholydae – T. achaeae – T. acuminatum – T. adashkevitshi – T. agriae – T. agrotidis – T. aldanense – T. alloeovirilia – T. alpha – T. aomoriense – T. arcanum – T. artonae – T. atopovirilia – T. atropos – T. aurosum – T. australicum – T. bactrianum – T. bellaunionense – T. bennetti – T. bertii – T. bezdencovii – T. bilingensis – T. bistrae – T. bourarachae – T. bournieri – T. brassicae – T. brevicapillum – T. brevifringiata – T. browningi – T. bruni – T. buesi – T. buluti – T. cacaeciae – T. californicum – T. canariensis – T. carina – T. carverae – T. castrensis – T. cephalciae – T. chagres – T. chilonis – T. chilotraeae – T. choui – T. chusniddini – T. closterae – T. clotho – T. colombiense – T. colombiensis – T. cordubense – T. cultellus – T. danaidiphaga – T. danausicida – T. danubiense – T. daumalae – T. deion – T. demoraesi – T. dendrolimi – T. diazi – T. dissimilis – T. distinctum – T. drepanophorum – T. elegantum – T. embryophagum – T. erebus – T. erosicorne – T. esalqueanum – T. ethiopicum – T. euproctides – T. euproctidis – T. evanescens – T. exiguum – T. falx – T. fasciatum – T. flandersi – T. flavum – T. foersteri – T. fuentesi – T. funestum – T. funiculatum – T. fuzhouense – T. galloi – T. gicai – T. guariquensis – T. hebbalensis – T. hesperidis – T. higai – T. ingricum – T. interius – T. inyoense – T. iracildae – T. itsybitsi – T. ivelae – T. jalmirezi – T. japonicum – T. jaxarticum – T. jezoensis – T. julianoi – T. kalkae – T. kaykai – T. kilinceri – T. koehleri – T. kurosuae – T. lachesis – T. lacustre – T. lasallei – T. lenae – T. leptoparameron – T. leucaniae – T. leviculum – T. lingulatum – T. longxishanense – T. lopezandinense – T. maltbyi – T. mandelai – T. manicobai – T. maori – T. marandobai – T. margianum – T. marthae – T. marylandense – T. maxacalii – T. meteorum – T. minutum – T. mirabile – T. mirum – T. misiae – T. mullensi – T. mwanzai – T. nemesis – T. nerudai – T. nestoris – T. neuropterae – T. niveiscapus – T. nomlaki – T. nubilale – T. oatmani – T. obscurum – T. offella – T. oleae – T. ostriniae – T. pallidiventris – T. pangi – T. papilionidis – T. papilionis – T. parkeri – T. parnarae – T. parrai – T. pelovi – T. perkinsi – T. piceum – T. pinneyi – T. pintoi – T. piracicabense – T. platneri – T. poliae – T. polychrosis – T. pratissolii – T. pratti – T. pretiosum – T. primaevum – T. principium – T. psocopterae – T. pusillum – T. raoi – T. retorridum – T. rojasi – T. rossicum – T. santarosae – T. sathon – T. savalense – T. sembeli – T. semblidis – T. semifumatum – T. sericini – T. shchepetilnikovae – T. sibiricum – T. siddiqi – T. silvestre – T. soberania – T. sogdianum – T. sorokinae – T. stampae – T. sugonjaevi – T. taiwanense – T. talitzkii – T. terani – T. thalense – T. trjapitzini – T. tshumakovae – T. tupiense – T. turkestanicum – T. umerus – T. unicum – T. urquijoi – T. ussuricum – T. valentinei – T. valmiri – T. vargasi – T. voegelei – T. yawarae – T. zahiri – T. zeirapherae – T. zucchii
Name

Trichogramma Westwood, 1833: 444

Type species: Trichogramma evanescens Westwood, 1833 (monotypy)
References
Primary references

Westwood, J.O. 1833. Descriptions of several new British forms amongst the parasitic hymenopterous insects. London and Edinburgh philosophical magazine and journal of science (3) 2(12): 443–445. BHL Reference page.

Additional references

Del Pino, M., Hernández-Suárez, E., Cabello, T., Rugman-Jones, P., Stouthamer, R. & Polaszek, A., 2013: Trichogramma canariensis (Insecta: Hymenoptera: Trichogrammatidae) a parasitoid of eggs of the twin-spot moth Chrysodeixis chalcites (Lepidoptera: Noctuidae) in the Canary Islands. Arthropod systematics & phylogeny, 71(3): 169–179. PDF. Reference page.
Nasir, F.M., Büttner, C., Reichmuth, C., Poswal, A., Hagedorn, G. & Schöller, M. 2011. A new species of Trichogramma Westwood (Hymenoptera: Trichogrammatidae) closely related to T. chilonis Ishii from Pakistan. Zootaxa 2790: 41–48. Preview. DOI: 10.11646/zootaxa.2970.1.3 Paywall. Reference page.
Querino, R.B., Mendes, J.V., Costa, V.A. & Zucchi, R.A.. 2017. New species, notes and new records of Trichogramma (Hymenoptera: Trichogrammatidae) in Brazil. Zootaxa 4232(1): 137–143. DOI: 10.11646/zootaxa.4232.1.11. Full article (PDF) Reference page.
Querino, R.B.; Zucchi, R.A. 2003: Six new species of Trichogramma Westwood (Hymenoptera|Trichogrammatidae) from a Brazilian forest reserve. Zootaxa 134: 1–11. Abstract & excerpt Reference page.
Vieira, J.M., Querino, R.B. & Zucchi, R.A. 2014. On the identity of Trichogramma demoraesi Nagaraja (Hymenoptera: Trichogrammatidae), with a checklist and a key to Trichogramma species associated with Erinnyis ello (L.) (Lepidoptera, Sphingidae) in Brazil. Zootaxa 3869(1): 83–89. DOI: 10.11646/zootaxa.3869.1.8 Reference page.
Vieira, J.M., Querino, R.B., Cônsoli, F.L. & Zucchi, R.A. 2015. An integrative taxonomic approach to characterize Trichogramma marandobai (Hymenoptera: Trichogrammatidae). Zootaxa 4021(3): 447–458. DOI: 10.11646/zootaxa.4021.3.4. Preview (PDF) Reference page.

Links

Trichogramma – Taxon details on Global Biodiversity Information Facility (GBIF).

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]

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.

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.[7]
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.[8] 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.[9][10] 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.[11][12]

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.[13]
Wolbachia in Trichogramma

Wolbachia is a widespread bacterial genus that infects insects' organs, most commonly the reproductive organs.[14] Wolbachia has been observed to alter the host's reproductive success upon infection.[14] Through a series of manipulations, Wolbachia-infected hosts transmit this intracellular bacterium to uninfected individuals.[14][15] These manipulations include male killing (increasing ratio of infected females that can reproduce), feminization (males become fertile females), parthenogenesis, and cytoplasmic incompatibility.[15] Horizontal transfer of parthenogenesis-inducing Wolbachia, which has been observed in Trichogramma wasps, causes infected females to asexually produce fertile females and nonfunctional males.[16] 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.[16]

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.[15] 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.[15] Cytoplasmic incompatibility of the host and bacterium can also be the source of this unsuccessful transfer in-vitro.[15] 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.[15] 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.[17] Many generations of reproductive isolation of these different groups may result in speciation.[17] 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.[17] 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.[17]
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.[18][19]

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.[20] T. minutum has been investigated as a method of biological control of the Choristoneura fumiferana, a major pest of spruce and fir forests.[21]

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.[22] 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.[23]

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.[7]
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.[24][25]
T. carverae

Trichogramma carverae is mainly used for light brown apple moth and codling moth control, and is predominately used in orchards.[26] 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.[27]

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.[28] 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
References

Flanders, S; Quednau, W (1960). "Taxonomy of the genus Trichogramma (Hymenoptera, Chalcidoidea, Trichogrammatidae)". BioControl. 5 (4): 285–294. doi:10.1007/bf02372951. S2CID 34509414.
Consoli FL, Parra JRP, Zucchi RA (2010) 'Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma.' (Springer).
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).
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.
Upadhyay RK, Mukerji KG, Chamola BP (2001) 'Biocontrol potential and its Exploitation in Sustainable Agriculture: Insect Pests.' (Kluwer Academic/ Plenum Publishers).
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).
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.
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.
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.
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.
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.
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.
"Chalcids".
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.
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.
Bourtzis, Kostas; O'Neill, Scott (1998). "Wolbachia Infections and Arthropod Reproduction". BioScience. 48 (4): 287–293. doi:10.2307/1313355. JSTOR 1313355.
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.
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.
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.
Flanders, SE (1930). "Mass Production of Egg Parasites of the Genus Trichogramma". Hilgardia. 4 (16): 465–501. doi:10.3733/hilg.v04n16p465.
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.
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.
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.
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.
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.
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).
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.
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.