Abstract
Trichogramma species are important natural enemies of Anticarsia gemmatalis Hübner, a key pest of soybean in new world agroecosystems. Development, longevity and parasitism rate of Trichogramma pretiosum Riley, Trichogramma acacioi Brun, Moraes and Soares and Trichogramma rojasi Nagaraja and Nagarkatti were investigated under natural conditions throughout fall and winter in order to determine how these parasitoids survive during the soybean off-season in southern Brazil. All species remained active along the experimental period. Over 90 % of the parasitoids emerged throughout the off-season, except for T. rojasi which showed lower percentage of emergence in April and May. The reproductive activity was not interrupted during fall and winter, indicating that the parasitoids depend on alternative hosts to survive. Parasitoids survived during the off-season combining slow developmental rate with an increase in adult life span, an important adaptation that improves their chances of finding alternative hosts and food sources.
Similar content being viewed by others
References
Avanci MRF, Foerster LA, Cañete CL (2005) Natural parasitism in eggs of Anticarsia gemmatalis Hübner (Lepidoptera, Noctuidae) by Trichogramma spp. (Hymenoptera, Trichogrammatidae) in Brazil. Rev Bras Entomol 49:148–151
Ayres M, Ayres JRM, Ayres DL, Santos AS (2007) BioEstat 5.0 - Aplicações Estatísticas nas Áreas das Ciências Biológicas e Médicas: Sociedade Civil Mamirauá, Belém. CNPq, Brasília, Brazil, p 290
Babendreier D, Kuske S, Bigler F (2003) Overwintering of the egg parasitoid Trichogramma brassicae in Northern Switzerland. BioControl 48:261–273
Boivin G (1994) Overwintering strategies of egg parasitoids. In: Wajnberg A, Hassan SA (eds) Biological control with egg parasitoids. CAB International, Wallingford, UK, pp 219–244
Burbutis PP, Curl GD, Davis CP (1976) Overwintering of Trichogramma nubilale in Delaware. Environ Entomol 5:888–890
Campbell A, Frazer BD, Gilbert N, Gutierrez AP, Mackauer M (1974) Temperature requirements of some aphids and their parasites. J Appl Ecol 11:419–423
Chapman RF (1998) The insects structure and function, 4th edn. Cambridge University Press, New York, USA
Côrrea-Ferreira BS, Moscardi F (1995) Seasonal occurrence and host spectrum of egg parasitoids associated with soybean stink bugs. Biol Control 5:196–202
Curl GD, Burbutis PP (1977) The mode of overwintering of Trichogramma nubilale Ertle and Davis. Environ Entomol 6:629–632
Doetzer AK, Foerster LA (2007) Desenvolvimento, longevidade e reprodução de Trissolcus basalis (Wollaston) e Telenomus podisi Ashmead (Hymenoptera: scelionidae) em condições naturais durante a entressafra da soja no sul do Paraná. Neotrop Entomol 36:233–242
Doetzer AK, Foerster LA (2013) Storage of pentatomid eggs in liquid nitrogen and dormancy of Trissolcus basalis (Wollaston) and Telenomus podisi Ashmead (Hymenoptera: Platygastridae) adults as a method of mass production. Neotrop Entomol 42:534–538
Foerster LA (1996) Efeito da temperatura no desenvolvimento das fases imaturas de Pseudaletia sequax Franclemont (Lepidoptera: Noctuidae). An Soc Entomol Bras 25:27–32
Foerster MR, Foerster LA (2009) Effects of temperature on the immature development and emergence of five species of Trichogramma. BioControl 54:445–450
Foerster MR, Marchioro CA, Foerster LA (2014) Temperature-dependent parasitism, survival, and longevity of five species of Trichogramma Westwood (Hymenoptera: Trichogrammatidae) associated with Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae). Neotrop Entomol 43:176–182
Garcia PV, Wajnberg E, Pizzol J, Oliveira MLM (2002) Diapause in the egg parasitoid Trichogramma cordubensis: role of temperature. J Insect Physiol 48:349–355
Gurr GM, Nicol HI (2001) Effect of food on longevity of adults of Trichogramma carverae Oatman and Pinto and Trichogramma nr brassicae Bezdenko (Hymenoptera: Trichogrammatidae). Aust Entomol 39:185–187
Herms DA (2004) Using degree-days and plant phenology to predict pest activity. In: Krischik V, Davidson J (eds) IPM of Midwest landscapes. University of Illinois, USA, pp 49–50
Ikemoto T, Takai K (2000) A new linearized formula for the law of total effective temperature and the evaluation of line-fitting methods with both variables subject to error. Environ Entomol 29:671–682
Laetemia JA, Laing JE, Corrigan JE (1995) Effect of adult nutrition on longevity, fecundity, and offspring sex ratio of Trichogramma minutum Riley (Hymenoptera: Trichogrammatidae). Can Entomol 127:245–254
Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201
Leather SR, Walters KFA, Bale JS (1993) The ecology of insect overwintering. Cambridge University Press, New York, USA
López JD Jr, Morrison RK (1980) Overwintering of Trichogramma pretiosum in central Texas. Env Entomol 9:75–78
Mansingh A (1971) Physiological classification of dormancies in insects. Can Entomol 9:697–700
Özder N, Saglam O (2005) Overwintering of the egg parasitoids Trichogramma brassicae and T. cacoeciae (Hymenoptera: Trichogrammatidae) in the Thrace region of Turkey. J Pest Sci 78:129–132
Pizzol J, Voegelé J (1988) The diapause of Trichogramma maidis Pintureau and Voegelé in relation to some characteristics of its alternative host Ephestia kuehniella Zell. Boulétreau M. & Bonnot G. (eds) Les insectes parasitoïdes, Colloq INRA, France, 48:93–94
Pratissoli D, Oliveira HN, Polanczyk RA, Holtz AM, Bueno RCOF, Bueno AF, Gonçalvez JR (2009) Adult feeding and mating effects on the biological potential and parasitism of Trichogramma pretiosum and T. acacioi (Hym.: Trichogrammatidae). Braz Arch Biol Technol 52:1057–1062
Rundle BJ, Hoffmann AA (2003) Overwintering of Trichogramma funiculatum Carver (Hymenoptera: Trichogrammatidae) under semi-natural conditions. Env Entomol 32:290–298
Smith SM (1996) Biological control with Trichogramma: advances, successes, and potential of their use. Annu Rev Entomol 41:375–406
Statsoft Inc (2008) Statistica for windows. Statsoft Inc, Tulsa, USA
Thomas MB, Sotherton NW, Coombes DS, Wratten SD (1992) Habitat factors influencing the distribution of polyphagous predatory insects between field boundaries. Ann Appl Biol 120:197–202
Thomsom LJ, Hoffmann AA (2002) Laboratoy fecundity as predictor of field success in Trichogramma carverae (Hymenoptera: Trichogrammatidae). J Econ Entomol 95:912–917
Thomson LJ, Bennett DM, Glenn DC, Hoffmann AA (2003) Developing Trichogramma as a pest management tool. In: Koul O, Dhaliwal GS (eds) Predators and parasitoids. Taylor and Francis, London, UK, pp 65–85
Voegelé J, Pizzol J, Babi A (1998) The overwintering of some Trichogramma species. In: INRA Editions (ed) Trichogramma and other egg parasites, Colloq INRA, France 43:275–282
Winkler K, Wäckers FL, Bukovinszkine-Kiss G, van Lenteren JC (2006) Nectar resources are vital for Diadegma semiclausum fecundity under field conditions. Basic Appl Ecol 7:133–140
Wratten SD (1992) Weeding out the cereal killers. New Sci 1835:31–35
Zaslavski VA, Umarova TY (1982) Photoperiodic and temperature control of diapause in Trichogramma evanescens Westw. (Hymenoptera: Trichogrammatidae). Entomol Rev 60:1–12
Acknowledgments
The authors are grateful to Dr. John Pinto (University of California, Riverside, USA), Dr. Roberto A. Zucchi (Universidade de São Paulo – ESALQ/USP), Dr. Ranyse B. Q. da Silva (Empresa Brasileira de Pesquisa Agropecuária - Embrapa) for the identification of the Trichogramma species, and the two anonymous reviewers for their valuable comments to the manuscript. This research was performed with scholarships provided by the Brazilian National Research Council (CNPq) and Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Dirk Babendreier.
Rights and permissions
About this article
Cite this article
Foerster, M.R., Marchioro, C.A. & Foerster, L.A. How Trichogramma survives during soybean offseason in Southern Brazil and the implications for its success as a biocontrol agent. BioControl 60, 1–11 (2015). https://doi.org/10.1007/s10526-014-9616-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10526-014-9616-5