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Increasing radiation doses in Anastrepha obliqua (Diptera: Tephritidae) larvae improve parasitoid mass-rearing attributes

Published online by Cambridge University Press:  28 June 2022

Jorge Cancino Open the ORCID record for Jorge Cancino [Opens in a new window] ,
Amanda Ayala ,
Laura Ríos ,
Patricia López ,
Lorena Suárez ,
Sergio M. Ovruski  and
Jorge Hendrichs
Jorge Cancino*
Affiliation:
Programa Moscas SADER-IICA, Camino a Cacahoatales S. N., 30860 Metapa de Domínguez, Chis., Mexico
Amanda Ayala
Affiliation:
Programa Moscas SADER-IICA, Camino a Cacahoatales S. N., 30860 Metapa de Domínguez, Chis., Mexico
Laura Ríos
Affiliation:
Facultad de Ciencias Agrícolas, UNACH-Campus IV, 30660 Huehuetán, Chis., Mexico
Patricia López
Affiliation:
Programa Moscas SADER-IICA, Camino a Cacahoatales S. N., 30860 Metapa de Domínguez, Chis., Mexico
Lorena Suárez
Affiliation:
Dirección de Sanidad Vegetal, Animal y Alimentos de San Juan (DSVAA de San Juan), Av. Nazario Benavides 8000 Oeste, Rivadavia, San Juan, Argentina
Sergio M. Ovruski
Affiliation:
LIEMEN, División Control Biológico de Plagas, PROIMI Biotecnología, Avda. Belgrano y Pje. Caseros, T4001MVB San Miguel de Tucumán, Tucumán, Argentina
Jorge Hendrichs
Affiliation:
Insect Pest Control Section, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, IAEA, Vienna, Austria
*
Author for correspondence: Jorge Cancino, Email: jorge.cancino.i@senasica.gob.mx
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Abstract

Doses of 40, 80, 120, and 160 Gy were applied to 5-, 6-, 7-, and 8-day-old Anastrepha obliqua larvae, which were exposed to the Neotropical-native braconids Doryctobracon crawfordi and Utetes anastrephae and the Asian braconid Diachasmimorpha longicaudata. These tests were performed to know the effect of the increase in host radiation on the emergence of the aforementioned parasitoids and the related consequences of oviposition on the host. The study was based on the fact that higher radiation doses may cause a decrease in the host immune activity. There was a direct relationship between the increase in radiation dose and the parasitoid emergence. Both, the weight and the mortality of the host larvae were not affected by radiation. Although the larval weight of the larvae was lower and the mortality was higher in the younger larvae. Both, the number of scars and immature stages per host puparium originated from the younger larvae were lower than those from older larvae. Only U. anastrephae superparasitized more at lower radiation. Superparasitism by D. longicaudata was more frequent at 160 Gy. Qualitative measurements of melanin in the larvae parasitized showed that the levels were lower with increasing radiation. As radiation doses increased, the antagonistic response of the A. obliqua larva was reduced. Host larvae aged 5- and 6-day-old irradiated at 120–160 Gy significantly improve parasitoid emergence. This evidence is relevant for the mass production of the three tested parasitoid species.

Keywords

Fruit fly parasitoidshost immunologyirradiated hostmass rearing of parasitoidsradiation in natural enemies
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 6 , December 2022 , pp. 807 - 817
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Al khalaf, AA and Abdel Baki, SM (2013) Gamma irradiation effects on larvae of the rice moth, Corcyra cephalonica (Staint) (Lepidoptera-Pyralidae). Journal of Entomology and Nematology 5, 45–49.CrossRefGoogle Scholar
Aluja, M and Birke, A (1993) Habitat use by adults of Anastrepha obliqua (Diptera: Tephritidae) in a mixed mango and tropical plum orchard. Annals of the Entomological Society of America 86, 799–812.CrossRefGoogle Scholar
Aluja, M, Guillen, J, Liedo, P, Cabrera, M, de la Rosa, G, Celedonio, H and Mota, D (1990) Fruit infesting tephritids [Dipt.: Tephritidae] and associated parasitoids in Chiapas, Mexico. Entomophaga 35, 39–48.CrossRefGoogle Scholar
Aluja, M, Rull, J, Sivinski, J, Norrbom, AL, Wharton, RA, Macías-Ordóñez, R, Díaz-Fleischer, F and López, M (2003) Fruit flies of the genus Anastrepha (Diptera: Tephritidae) and associated native parasitoids (Hymenoptera) in the tropical rainforest biosphere reserve of Montes Azules, Chiapas, Mexico. Environmental Entomology 32, 1377–1385.CrossRefGoogle Scholar
Aluja, M, Sivinski, J, Ovruski, SM, Guillén, L, López, L, Cancino, J, Torres-Anaya, A, Gallegos-Chan, G and Ruiz, L (2009) Colonization and domestication of seven species of native new world hymenopterous larval–prepupal and pupal fruit fly (Diptera: Tephritidae) parasitoids. BioControl Science and Technology 19, 49–79.CrossRefGoogle Scholar
Aluja, M, Ovruski, SM, Sivinski, J, Córdoba-García, G, Schliserman, P, Núñez-Campero, S and Ordano, M (2013) Inter-specific competition and competition-free space in the tephritid parasitoids Utetes anastrephae and Doryctobracon areolatus (Hymenoptera: Braconidae: Opiinae). Ecological Entomology 38, 485–496.CrossRefGoogle Scholar
Aluja, M, Sivinski, J, Van Driesche, R, Anzures-Dadda, A and Guillen, L (2014) Pest management through tropical tree conservation. Biodiversity and Conservation 23, 831–853.CrossRefGoogle Scholar
Artiaga-López, T, Hernández, E, Domínguez-Gordillo, J, Moreno, DS and Orozco-Dávila, D (2002) Mass production of Anastrepha obliqua at the Moscafrut fruit fly facility, México. In Barnes BN (ed) Proceedings of 6th International Symposium on Fruit Fly of Economic Importance. Irene, South Africa: Isteg Scientific Publications, pp. 389–392.Google Scholar
Ayala, A, Pérez-Lachaud, G, Toledo, J, Liedo, P and Montoya, P (2018) Host acceptance by three native braconid parasitoid species attacking larvae of the Mexican fruit fly, Anastrepha ludens (Diptera, Tephritidae). Journal of Hymenoptera Research 63, 33–49.CrossRefGoogle Scholar
Beckage, NE (2009) Immunology. In Resh, VH and Cardé, RT (eds), Encyclopedia of Insects, 2nd Edn. San Diego, CA, USA: Academic Press, Elsevier Inc., pp. 492–496.CrossRefGoogle Scholar
Boman, HG and Hultmark, D (1987) Cell-free immunity in insects. Annual Review of Microbiology 41, 1095–1103.CrossRefGoogle ScholarPubMed
Cancino, J, Ruiz, L, Gómez, Y and Toledo, J (2002) Irradiación de larvas de Anastrepha ludens (Loew) (Diptera: Tephritidae) para inhibir la emergencia de moscas en la cría del parasitoide Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Folia Entomológica Mexicana 41, 195–208.Google Scholar
Cancino, J, Ruiz, L, Lopez, P and Sivinski, J (2009) The suitability of Anastrepha spp. and Ceratitis capitata larvae as hosts of Diachasmimorpha longicaudata and Diachasmimorpha tryoni: effects of host age and radiation dose and implications for quality control in mass rearing. BioControl Science and Technology 19, 81–94.CrossRefGoogle Scholar
Cancino, J, Ruiz, L, Viscarret, M, Sivinski, J and Hendrichs, J (2012) Application of nuclear techniques to improve the mass production and management of fruit fly parasitoids. Insects 3, 1105–1125.CrossRefGoogle ScholarPubMed
Cancino, J, Ayala, A, Ovruski, SM, Rios, L, López, P and Hendrichs, J (2020) Anastrepha ludens (Loew) (Diptera: Tephritidae) larvae irradiated at higher doses improve the rearing of two species of native parasitoids. Journal of Applied Entomology 144, 866–876.CrossRefGoogle Scholar
Chang, CL, Goodman, CL, Ringbauer, J, Geib, SM and Stanley, D (2016) Larval X-ray irradiation influences protein expression in pupae of the oriental fruit fly. Archives of Insect Biochemistry and Physiology 92, 192–209.CrossRefGoogle ScholarPubMed
Consoli, FL, Parra, JR and Vinson, SB (2000) Estimating parasitoid immature mortality by comparing oviposition and pupal development of Trichogramma galloi Zucchi and T. pretiosum Riley on natural and factitious hosts. Revista Brasileira do Biologia 60, 381–387.CrossRefGoogle Scholar
Córdova-García, G (2008) Mecanismos de defensa de las moscas de la fruta Anastrepha obliqua y Ceratitis capitata (Diptera: Tephritidae) ante el ataque de parasitoides nativos (M. S. thesis dissertation). Universidad Veracruzana, Xalapa, Veracruz, Mexico.Google Scholar
Eben, A, Benrey, B, Sivinski, J and Aluja, M (2000) Host species and host plant effects on preference and performance of Diachasmimorpha longicaudata. Environmental Entomology 29, 87–94.CrossRefGoogle Scholar
Garcia, FRM, Ovruski, SM, Suárez, L, Cancino, J and Liburd, OE (2020) Biological control of tephritid fruit flies in the Americas and Hawaii: a review of the use of parasitoids and predators. Insects 11, 662.CrossRefGoogle ScholarPubMed
González, PI, Montoya, P, Perez-Lachaud, G, Cancino, J and Liedo, P (2007) Superparasitism in mass reared Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Biological Control 40, 320–326.CrossRefGoogle Scholar
Hasan, MM, Yeasmin, L, Athanassiou, CG, Bari, MA and Islam, MS (2019) Using gamma irradiated Galleria mellonella L. and Plodia interpunctella (Hübner) larvae to optimize mass rearing of parasitoid Habrobracon hebetor (Say) (Hymenoptera: Braconidae). Insects 10, 223.CrossRefGoogle ScholarPubMed
Hegazi, E and Khafagi, W (2008) The effects of host age and superparasitism by the parasitoid, Microplitis rufiventris on the cellular and humoral immune response of Spodoptera littoralis larvae. Journal of Invertebrate Pathology 98, 79–84.CrossRefGoogle ScholarPubMed
Hendrichs, J, Bloem, K, Hoch, G, Carpenter, JE, Greany, P and Robinson, AS (2009) Improving the cost-effectiveness, trade and safety of biological control for agricultural insect pests using nuclear techniques. Biocontrol Science and Technology 19, 3–22.CrossRefGoogle Scholar
Hoffmann, MP, Ode, PR, Walker, DL, Gardner, J, van Nouhuys, S and Shelton, AM (2001) Performance of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) reared on factitious hosts, including the target host, Ostrinia nubilalis (Lepidoptera: Crambidae). Biological Control 21, 1–10.CrossRefGoogle Scholar
Hu, JS and Vinson, SB (2000) Interaction between the larval endoparasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae) and its host the tobacco budworm (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 93, 220–224.CrossRefGoogle Scholar
Ibrahim, AG, Palacio, LP and Androhani, I (1994) Biology of Diachasmimorpha longicaudata, a parasitoid of carambola fruit fly (Diptera: Tephritidae). Journal of Tropical Agricultural Science 12, 139–143.Google Scholar
Ideo, S, Watada, M, Mitsui, H and Kimura, MT (2008) Host range of Asobara japonica (Hymenoptera: Braconidae), a larval parasitoid of drosophilid flies. Entomological Science 11, 1–6.CrossRefGoogle Scholar
Jesus-Barros, CR, Adaime, R, Oliveira, MN, Silva, WR, Costa-Neto, SV and Souza-Filho, MF (2012) Anastrepha (Diptera: Tephritidae) species, their hosts and parasitoids (Hymenoptera: Braconidae) in five municipalities of the State of Amapá, Brazil. Florida Entomologist 95, 694–705.CrossRefGoogle Scholar
Jiron, LF (1996) Management guidelines for Anastrepha obliqua associated with mango in Central America. Fruits 51, 25–30.Google Scholar
Kaeslin, M, Reinhard, M, Bühler, D, Roth, T, Wilhelm, RP and Lanzrein, B (2010) Venom of the egg-larval parasitoid Chelonus inanitus is a complex mixture and has multiple biological effects. Journal of Insect Physiology 56, 686–694.CrossRefGoogle ScholarPubMed
Kraaijeveld, AR, Van Alphen, JJM and Godfray, HCJ (2011) The coevolution of host resistance and parasitoid virulence. Parasitology 116(S1), S29–S45.CrossRefGoogle Scholar
Lawrence, P (2005) Morphogenesis and cytopathic effects of the Diachasmimorpha longicaudata entomopoxvirus in host haemocytes. Journal of Insect Physiology 51, 221–233.CrossRefGoogle ScholarPubMed
Liu, H, Jiravanichpaisal, P, Cerenius, L, Lee, BL, Söderhäll, I and Söderhäll, K (2007) Phenoloxidase is an important component of the defense against Aeromonas hydrophila infection in a crustacean, Pacifastacus leniusculus. Journal of Biological Chemistry 282, 33593–33598.CrossRefGoogle Scholar
López, M, Aluja, M and Sivinski, J (1999) Hymenopterous larval-pupal and pupal parasitoids of Anastrepha flies (Diptera: Tephritidae) in México. Biological Control 15, 119–129.CrossRefGoogle Scholar
Mangan, RL, Thomas, DB, Moreno, AT and Robacker, D (2011) Grapefruit as a host for the West Indian fruit fly (Diptera: Tephritidae). Journal of Economic Entomology 104, 54–62.CrossRefGoogle Scholar
Mansour, M and Franz, G (1996) Effect of gamma radiation on phenoloxidase activity in Mediterranean fruit fly (Diptera: Tephritidae) larvae. Journal of Economic Entomology 89, 695–699.CrossRefGoogle Scholar
Marsaro Júnior, AL, Adaime, R, Ronchi-Teles, B, Lima, CR and Pereira, PRVS (2011) Anastrepha species (Diptera: Tephritidae), their hosts and parasitoids in the extreme north of Brazil. Biota Neotropica 11, 117–123.CrossRefGoogle Scholar
Miranda, M, Sivinski, J, Rull, J, Cicero, L and Aluja, M (2015) Niche breadth and interspecific competition between Doryctobracon crawfordi and Diachasmimorpha longicaudata (Hymenoptera: Braconidae), native and introduced parasitoids of Anastrepha spp. fruit flies (Diptera: Tephritidae). Biological Control 82, 86–95.CrossRefGoogle Scholar
Montoya, P, Liedo, P, Benrey, B, Barrera, JF, Cancino, J and Aluja, M (2000 a) Functional response and superparasitism by Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Annals of the Entomological Society of America 93, 47–54.CrossRefGoogle Scholar
Montoya, P, Liedo, P, Benrey, B, Barrera, JF, Cancino, J, Sivinski, J and Aluja, M (2000 b) Biological control of Anastrepha spp. (Diptera: Tephritidae) in mango orchards through augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biological Control 18, 212–224.CrossRefGoogle Scholar
Montoya, P, Cancino, J, Zenil, M, Santiago, G and Gutierrez, JM (2007) The augmentative biological control component in the Mexican national campaign against Anastrepha spp. fruit flies. In Vreysen, MJB, Robinson, AS and Hendrichs, J (eds), Area-Wide Control of Insects Pests: From Research to Field Implementation. Dordrecht, The Netherlands: Springer, pp. 661–670.CrossRefGoogle Scholar
Montoya, P, Cancino, J, Pérez-Lachaud, G and Liedo, P (2011) Host size, superparasitism and sex ratio in mass-reared Diachasmimorpha longicaudata, a fruit fly parasitoid. BioControl 56, 11–17.CrossRefGoogle Scholar
Montoya, P, Pérez-Lachaud, G and Liedo, P (2012) Superparasitism in the fruit fly parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) and the implications for mass rearing and augmentative release. Insects 3, 900–911.CrossRefGoogle ScholarPubMed
Montoya, P, López, P, Cruz, J, López, F, Cadena, C, Cancino, J and Liedo, P (2017) Effect of Diachasmimorpha longicaudata releases on the native parasitoid guild attacking Anastrepha spp. larvae in disturbed zones of Chiapas, Mexico. BioControl 62, 581–593.CrossRefGoogle Scholar
Muhammad, R, Ahmad, Q, Rashidi, SMM and Ahmad, N (2013) Role of irradiated and chilled host Sitotroga cerealella eggs to enhance the parasitic potential of egg parasitoid Trichogramma chilonis (Ishii). Academic Journal of Entomology 6, 133–138.Google Scholar
Murillo, FD, Cabrera-Mireles, H, Barrera, JF, Liedo, P and Montoya, P (2015) Doryctobracon areolatus (Hymenoptera, Braconidae) a parasitoid of early developmental stages of Anastrepha obliqua (Diptera, Tephritidae). Journal of Hymenoptera Research 46, 91–105.CrossRefGoogle Scholar
Murillo, FD, Liedo, P, Nieto-López, MG, Cabrera-Mireles, H, Barrera, JF and Montoya, P (2016) First instar larvae morphology of Opiinae (Hymenoptera: Braconidae) parasitoids of Anastrepha (Diptera: Tephritidae) fruit flies. Implications for interspecific competition. Arthropod Structure & Development 45, 294–300.CrossRefGoogle ScholarPubMed
Nappi, AJ and Ottaviani, E (2000) Cytotoxicity and cytotoxic molecules in invertebrates. BioEssays 22, 469–480.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Nappi, AJ and Vass, E (1993) Melanogenesis and the generation of cytotoxic molecules during insect cellular immune-reactions. Pigment Cell Research 6, 117–126.CrossRefGoogle ScholarPubMed
Nation, JL, Smittle, BJ and Milne, K (1995) Radiation-induced changes in melanization and phenoloxidase in Caribbean fruit fly larvae (Diptera: Tephritidae) as the basis for a simple test of irradiation. Annals of the Entomological Society of America 88, 201–205.CrossRefGoogle Scholar
Orozco-Dávila, D, Artiaga-López, T, Hernández, MR, Domínguez, J and Hernández, E (2014) Anastrepha obliqua (Diptera: Tephritidae) mass-rearing: effect of relaxed colony management. International Journal of Tropical Insect Science 34, 19–27.CrossRefGoogle Scholar
Orozco-Dávila, D, Quintero, L, Hernández, E, Solís, E, Artiaga, T, Hernández, R, Ortega, C and Montoya, P (2017) Mass rearing and sterile insect releases for the control of Anastrepha spp. pests in Mexico – a review. Entomologia Experimentalis et Applicata 164, 176–187.CrossRefGoogle Scholar
Ovruski, S, Aluja, M, Sivinski, J and Wharton, R (2000) Hymenopteran parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the southern United States: diversity, distribution, taxonomic status and their use in fruit fly biological control. Integrated Pest Management Reviews 5, 81–107.CrossRefGoogle Scholar
Poncio, S, Montoya, P, Cancino, J and Nava, DE (2016) Is Anastrepha obliqua (Diptera: Tephritidae) a natural host of the Neotropical parasitoids Doryctobracon crawfordi and Opius hirtus? Austral Entomology 55, 18–24.CrossRefGoogle Scholar
R Core Team (2020) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at https://www.R-project.org/.Google Scholar
Reed, DA, Luhring, KA, StaVord, CA, Hansen, AK, Millar, JG, Hanks, LM and Paine, TD (2007) Host defensive response against an egg parasitoid involves cellular encapsulation and melanization. Biological Control 41, 214–222.CrossRefGoogle Scholar
Ruiz-Arce, R, Barr, NB, Owen, CL, Thomas, DB and McPheron, BA (2012) Phylogeography of Anastrepha obliqua inferred with mtDNA sequencing. Journal of Economic Entomology 105, 2147–2160.CrossRefGoogle ScholarPubMed
Rull Gabayet, JA, Reyes Flores, J and Enkerlin Hoeflich, W (1996) The Mexican national fruit fly eradication campaign: largest fruit fly industrial complex in the world. In McPheron, BA and Steck, GJ (eds), Fruit Fly Pests. A World Assessment of Their Biology and Management. Delray Beach, FL, USA: St Lucie Press, pp. 561–563.Google Scholar
Sang, W, Yu, L, He, L, Ma, WH, Zhu, ZH, Zhu, F, Wang, XP and Lei, CL (2016) UVB radiation delays Tribolium castaneum metamorphosis by influencing ecdysteroid metabolism. PLoS One 11, e0151831.CrossRefGoogle ScholarPubMed
Santos, RPD, Silva, JP and Miranda, EA (2020) The past and current potential distribution of the fruit fly Anastrepha obliqua (Diptera: Tephritidae) in South America. Neotropical Entomology 49, 284–291.CrossRefGoogle ScholarPubMed
SAS Institute (2013) JMP Statistical Discovery Software, Version 11. Cary, NC: SAS Institute Inc.Google Scholar
Silva, JEB, Boleli, IC and Simões, ZLP (2002) Hemocyte types and total and differential counts in unparasitized and parasitized Anastrepha obliqua (Diptera, Tephritidae) larvae. Brazilian Journal of Biology 62, 689–699.CrossRefGoogle ScholarPubMed
Silva, JGV, Dutra VS, Santos, MS, Silva, NM, Vidal, DB, Nink, RA, Guimarães, JA and Araujo, EL (2010) Diversity of Anastrepha spp. (Diptera: Tephritidae) and associated braconid parasitoids from native and exotic hosts in southeastern Bahia, Brazil. Environmental Entomology 39, 1457–1465.CrossRefGoogle ScholarPubMed
Sisterson, M and Averill, AL (2003) Interactions between parasitized and unparasitized conspecifics: parasitoids modulate competitive dynamics. Oecologia 135, 362–371.CrossRefGoogle ScholarPubMed
Sivinski, J, Aluja, M and López, M (1997) The spatial and temporal distributions of parasitoids of Mexican Anastrepha species (Diptera: Tephritidae) within the canopies of fruit trees. Annals of the Entomological Society of America 90, 604–618.CrossRefGoogle Scholar
Sivinski, J, Piñero, J and Aluja, M (2000) The distribution of parasitoid Hymenoptera of Anastrepha fruit flies (Diptera: Tephritidae) along an altitudinal gradient in Veracruz, Mexico. Biological Control 18, 258–269.CrossRefGoogle Scholar
Sivinski, J, Vulinec, K and Aluja, M (2001) Ovipositor length in a guild of parasitoids (Hymenoptera: Braconidae) attacking Anastrepha spp. fruit flies (Diptera: Tephritidae) in southern Mexico. Annals of the Entomological Society of America 94, 886–895.CrossRefGoogle Scholar
Strand, MR and Pech, LL (1995) Immunological basis for compatibility in parasitoid–host relationships. Annual Review of Entomology 40, 31–56.CrossRefGoogle ScholarPubMed
Suárez, L, Buonocore-Biancheri, MJ, Sanchez, G, Cancino, J, Murúa-Bruna, AF, Bilbao, M, Molina, DA, Laria, O and Ovruski-Alderete, SM (2020) Radiation on Medfly larvae of tslVienna-8 genetic sexing strain displays reduced parasitoid encapsulation in mass-reared Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Journal of Economic Entomology 113, 1134–1144.CrossRefGoogle ScholarPubMed
Vinson, SB and Iwantsch, GF (1980) Host regulation by insect parasitoids. The Quarterly Review of Biology 55, 143–165.CrossRefGoogle Scholar
Xu, J, Yang, X, Lin, Y, Zang, L, Tian, C and Ruan, C (2016) Effect of fertilized, unfertilized and UV-irradiated hosts on parasitism and suitability for Trichogramma parasitoids. Entomologia Experimentalis et Applicata 161, 50–56.CrossRefGoogle Scholar