BioControl

, Volume 59, Issue 3, pp 279–286 | Cite as

Multiparasitism of stink bug eggs: competitive interactions between Ooencyrtus pityocampae and Trissolcus agriope

  • Marzie Mohammadpour
  • M. Amin Jalali
  • J. P. Michaud
  • Mahdi Ziaaddini
  • Hamid Hashemirad
Article

Abstract

Females of Trissolcus agriope (Platygastridae) avoid host (Brachynema signatum) eggs parasitized by conspecifics or Ooencyrtus pityocampae (Encyrtidae), but females of the latter species will superparasitize and multiparasitize, although they mostly attack unparasitized eggs. Females of T. agriope were more efficient in the laboratory and parasitized more hosts in 24 and 48 h. In multiparasitized hosts, O. pityocampae was a superior larval competitor and could complete also development as a facultative hyperparasitoid. When females of both species foraged together, T. agriope parasitized significantly more than O. pityocampae, about 50 % in both cases, although O. pityocampae almost doubled its parasitism rate as the exposure period was lengthened from 24 to 48 h. When O. pityocampae followed T. agriope in sequential foraging bouts, the former species successfully parasitized more hosts than the latter. The advisability of co-releases of both species to improve biological control of first generation B. signatum in Iranian pistachio orchards is discussed.

Keywords

Biological control Brachynema signatum Interspecific competition Intraguild interactions Encyrtidae Scelionidae 

Notes

Acknowledgments

The authors gratefully acknowledge the Pistachio Research Institute of Iran, Rafsanjan, Iran, for the provision of services and facilities essential to completion of this work.

References

  1. Abdul Alim M, Lim UT (2011) Refrigerated eggs of Riptortus pedestris (Hemiptera: Alydidae) added to aggregation pheromone traps increase field parasitism in soybean. J Econ Entomol 104:1833–1839PubMedCrossRefGoogle Scholar
  2. Amarasekare P (2000a) Coexistence of competing parasitoids on a patchily distributed host: local vs. spatial mechanisms. Ecology 81:1286–1296CrossRefGoogle Scholar
  3. Amarasekare P (2000b) Spatial dynamics in a host–multiparasitoid community. J Anim Ecol 69:201–213CrossRefGoogle Scholar
  4. Batchelor TP, Hardy ICW, Barrera JF, Pérez-Lachaud G (2005) Insect gladiators II: competitive interactions within and between bethylid parasitoid species of the coffee berry borer, Hypothenemus hampei (Coleoptera: Scolytidae). Biol Control 33:194–202CrossRefGoogle Scholar
  5. Batchelor TP, Hardy ICW, Barrera JF (2006) Interactions among bethylid parasitoid species attacking the coffee berry borer, Hypothenemus hampei (Coleoptera: Scolytidae). Biol Control 36:106–118CrossRefGoogle Scholar
  6. Battisti A, Ianne P, Milani N, Zanata M (1990) Preliminary accounts on the rearing of Ooencyrtus pityocampae (Mercet) (Hym., Encyrtidae). J Appl Entomol 110:121–127CrossRefGoogle Scholar
  7. Briggs CJ (1993) Competition among parasitoid species on a stage-structured host and its effect on host suppression. Am Nat 141:372–397CrossRefGoogle Scholar
  8. Buschman L, Whitcomb W (1980) Parasites of Nezara viridula (Hemiptera: Pentatomidae) and other hemiptera in Florida. Fla Entomol 63:154–162CrossRefGoogle Scholar
  9. Correa-Ferreira SB (1986) Natural occurrence of the egg parasitoid complex of stink bugs on soybean in Parana, Brazil. An Soc Entomol Bras 5:189–199Google Scholar
  10. Correa-Ferreira SB, Moscardi F (1995) Seasonal occurrence and host spectrum of egg parasitoids associated with soybean stink bugs. Biol Control 5:196–202CrossRefGoogle Scholar
  11. Cusumano A, Peri E, Vinson SB, Colazza S (2011) Intraguild interactions between two egg parasitoids exploring host patches. BioControl 56:173–184CrossRefGoogle Scholar
  12. Cusumano A, Peri E, Vinson SB, Colazza S (2012a) Interspecific extrinsic and intrinsic competitive interactions in egg parasitoids. BioControl 57:719–734CrossRefGoogle Scholar
  13. Cusumano A, Peri E, Vinson SB, Colazza S (2012b) The ovipositing female of Ooencyrtus telenomicida relies on physiological mechanisms to mediate intrinsic competition with Trissolcus basalis. Entomol Exp Appl 143:155–163CrossRefGoogle Scholar
  14. Daane KM, Yokota GY, Krugner R, Steffan SA, da Silva PG, Beede RH, Bentley WJ, Weinberger G (2005) Large bugs damage pistachio nuts most severely during midseason. Calif Agric 59:95–102CrossRefGoogle Scholar
  15. Denoth M, Frid L, Myers JH (2002) Multiple agents in biological control: improving the odds? Biol Control 24:20–30CrossRefGoogle Scholar
  16. Ehler LE (2002) An evaluation of some natural enemies of Nezara viridula in northern California. BioControl 47:309–325CrossRefGoogle Scholar
  17. Grenier S (1994) Rearing of Trichogramma and other egg parasitoids on artifical diets, pp. 73–92. In: Wajnberg E, Hassan SA (eds) Biological control with egg parasitoids. CAB International, Wallingford, UK, p 286Google Scholar
  18. Hashemi Rad H (1999) Identification of egg parasitoid wasps of the green stink bugs (Brachynema spp. and Acrosternum spp.) and study of biology of Trissolcus agriope (Hym.: Scelionidae) in Rafsanjan. M.Sc. thesis, Shahid Chamran University of Ahvaz, Ahvaz, IranGoogle Scholar
  19. Hashemi Rad H (2009) Study on egg parasitoids (T. agriope and Psix sp.) using eggs of four bug species in laboratory conditions. V International Symposium on Pistachios and Almonds 912, Sanliurfa, TurkeyGoogle Scholar
  20. Hoffmann MP, Davidson NA, Wilson LT, Ehler LE, Jones WA, Zalom FG (1991) Imported wasp helps control southern green stink bug. Calif Agric 45:20–22Google Scholar
  21. Kidd D, Amarasekare P (2012) The role of transient dynamics in biological pest control: insights from a host–parasitoid community. J Anim Ecol 81:47–57PubMedCrossRefGoogle Scholar
  22. Masutti L, Battisti A, Milani N, Zanata M, Zanazzo G (1993) In vitro rearing of Ooencyrtus pityocampae (Hym., Encyrtidae), an egg parasitoid of Thaumetopoea pityocampa (Lep., Thaumetopoeidae]. Entomophaga 38:327–333CrossRefGoogle Scholar
  23. Mehrnejad M (2001) The current status of pistachio pests in Iran. Cahiers Options Méditerranéennes 56:315–322Google Scholar
  24. Michailides T, Morgan DP, Doster MA (1994) Diseases of pistachio in California and their significance. Acta Hortic 419:337–344Google Scholar
  25. Nagarkatti S, Giroux KJ, Keeley TP (1991) Rearing Trichogramma nubilale (Hymenoptera: Trichogrammatidae) on eggs of the tobacco hornworm, Manduca sexta (Lepidoptera: Sphingidae). Entomophaga 36:443–446CrossRefGoogle Scholar
  26. Rosenheim JA, Kaya HK, Ehler LE, Marois JJ, Jaffee BA (1995) Intraguild predation among biological-control agents: theory and evidence. Biol Control 5:303–335CrossRefGoogle Scholar
  27. Rosi MC, Isidoro N, Colazza S, Bin F (2001) Source of the host marking pheromone in the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). J Insect Physiol 47:989–995PubMedCrossRefGoogle Scholar
  28. Schmidt GH, Kitt J (1993) Laboratory rearing of Ooencyrtus pityocampae in unfertilized and unlaid eggs of Thaumetopoea species. Naturwissenschaften 80:379–380CrossRefGoogle Scholar
  29. Shepard BM, Elsey KD, Muckenfuss AE, Justo HD Jr (1994) Parasitism and predation on egg masses of the southern green stink bug, Nezara viridula (L.) (Heteroptera: Pentatomidae), in tomato, okra, cowpea, soybean, and wild radish. J Agric Entomol 11:375–381Google Scholar
  30. Takasu K, Hirose Y (1988) Host discrimination in the parasitoid Ooencyrtus nezarae: the role of the egg stalk as an external marker. Entomol Exp Appl 47:45–48CrossRefGoogle Scholar
  31. Tiberi R, Niccoli A, Roversi PF, Sacchetti P (1991) Laboratory rearing of Ooencyrtus pityocampae (Mercet) on eggs of Nezara viridula (L.) and other pentatomids. Redia 74:467–469Google Scholar
  32. Tiberi R, Niccoli A, Sacchetti P (1994) Thaumetopoea pityocampa egg parasitism: modifications resulting from Ooencyrtus pityocampae augmentation. Atti XVII Congresso Nazionale Italiano di Entomologia, Udine, Italy, pp 13–18Google Scholar
  33. Turnbull A, Chant D (1961) The practice and theory of biological control of insects in Canada. Can J Zool 39:697–753CrossRefGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2014

Authors and Affiliations

  • Marzie Mohammadpour
    • 1
  • M. Amin Jalali
    • 1
  • J. P. Michaud
    • 2
  • Mahdi Ziaaddini
    • 1
  • Hamid Hashemirad
    • 3
  1. 1.Department of Plant Protection, Faculty of AgricultureVali-e-Asr University of RafsanjanRafsanjanIran
  2. 2.Department of Entomology, Agricultural Research Center-HaysKansas State UniversityHaysUSA
  3. 3.Department of Plant ProtectionPistachio Research Institute of IranRafsanjanIran

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