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Effect of the Ages of Parasitoid and Host Eggs on Telenomus podisi (Hymenoptera: Platygastridae) Parasitism

  • A P Queiroz
  • B M Favetti
  • R Hayashida
  • M L M Grande
  • M M Neiva
  • A R Panizzi
  • A F BuenoEmail author
Biological Control
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Abstract

This study investigates the influence of parasitoid age and egg age of the hosts Euschistus heros (Fabricius) and Dichelops melacanthus (Dallas) on parasitism of Telenomus podisi Ashmead. Six separate bioassays were conducted: parasitism on eggs of E. heros (bioassay 1) and D. melacanthus (bioassay 2) by T. podisi females of different age (1, 5, and 10 days old); parasitism by T. podisi on eggs of different age (1, 2, 3, 4, and 5 days of embryonic development) of the hosts E. heros (bioassay 3) and D. melacanthus (bioassay 4); preference of T. podisi females for eggs at different embryonic developmental stages (eggs of 1, 2, 3, 4, and 5 days) of the hosts E. heros (bioassay 5) and D. melacanthus (bioassay 6). The age of T. podisi females and their hosts affected parasitism on both E. heros and D. melacanthus eggs. Overall, the parasitism rate was higher in older than younger parasitoids, independent of the tested host species, and host eggs between 1 and 3 days old were similarly parasitized. Thus, in T. podisi mass rearing facilities, it is recommended to use older adults (5 to 10 days old) as mother wasps to increase parasitism on the offered eggs. In addition, when hosts are completely absent in the field, or climatic conditions are unfavorable for release, mass-reared adults can be kept in the laboratory (25°C) for up to 10 days for later release in the field without any impairment of their subsequent parasitism performance.

Keywords

Brown stink bug green-belly stink bug biological control egg parasitoid 

Notes

Acknowledgments

The authors thank Embrapa Soja, the Coordination for the Improvement of Higher Education Personnel (CAPES), and the National Council for Scientific and Technological Development (CNPq) for their financial support and fellowships.

Author Contributions

AP Queiroz, AF Bueno, and AR Panizzi contributed to the study design and wrote the paper. AP Queiroz conducted the sampling. AF Bueno and AR Panizzi contributed reagents/material/analysis tools. AP Queiroz, BM Favetti, R Hayahida, MLM Grande, and MN Neiva conducted the experiments. All authors have read and approved the manuscript.

References

  1. Abram PK (2016) Developmental, morphological, and behavioural plasticity in the reproductive strategies of stink bugs and their egg parasitoids. https://papyrus.bib.umontreal.ca/xmlui/bitstream/handle/1866/13586/Abram_Paul_2016_these.pdf?sequence=4&isAllowed=y. Accessed 26 Aug 2019.
  2. Biever KD (1972) Effect of the temperature on rate of search by Trichogramma and its potential application in field releases. Environ Entomol 1:194–197CrossRefGoogle Scholar
  3. Borges Filho RC, Nava DE, Pratissoli D, Polanczyk RA, Marangon RB, Loiácono M (2017) Biology of Telenomus pachycoris (Hymenoptera: Scelionidae), a parasitoid of eggs of Pachycoris torridus (Hemiptera: Scutelleridae): the effects of egg age, exposure time, and temperature. Florida Entomol 100:375–380CrossRefGoogle Scholar
  4. Bueno AF, Batistela MJ, Bueno RCOF, França-Neto JB, Nishikawa MAN, Filho AL (2011) Effects of integrated pest management, biological control and prophylactic use of insecticides on the management and sustainability of soybean. Crop Prot 30:937–945CrossRefGoogle Scholar
  5. Bueno RCOF, Parra JRP, Bueno AF (2012) Trichogramma pretiosum parasitism of Pseudoplusia includens and Anticarsia gemmatalis eggs at different temperatures. Biol Control 60:154–162CrossRefGoogle Scholar
  6. Bueno AF, Corrêa-Ferreira BS, Roggia S, Bianco R (2015a) Silenciosos e daninhos. Rev Cult 196:25–27Google Scholar
  7. Bueno AF, Bortolotto OC, Pomari-Fernandes A, França-Neto JB (2015b) Assessment of a more conservative stink bug economic threshold for managing stink bugs in Brazilian soybean. Crop Prot 71:132–137CrossRefGoogle Scholar
  8. Burr IW, Foster LA (1972) A test for equality of variances. Mimeo series n° 282. West Lafayette, Purdue University, p 26Google Scholar
  9. Charnov EL, Los-Den Hartogh RL, Jones WT, Van Den Assem J (1981) Sex ratio evolution in a variable environment. Nature 289:27–33PubMedCrossRefGoogle Scholar
  10. Chiesa ACM, Sismeiro MNS, Pasini A, Roggia S (2016) Tratamento de sementes para manejo do percevejo‑barriga‑verde na cultura de soja e milho em sucessão. Pesq Agropec Bras 51:301–308CrossRefGoogle Scholar
  11. Cingolani M, Greco F, Nancy M, Liljesthrom GG (2014) Effect of Telenomus podisi, Trissolcus urichi, and Trissolcus basalis (Hymenoptera: Platygastridae) age on attack of Piezodorus guildinii (Hemiptera: Pentatomidae) eggs. Environ Entomol 43:377–383PubMedCrossRefGoogle Scholar
  12. Cock MJW, van Lenteren JC, Brodeur J, Barratt BIP, Bigler F, Bolckmans K, Cônsoli FL, Haas F, Mason PG, Parra JRP (2010) Do new access and benefit sharing procedures under the convention on biological diversity threaten the future of biological control? BioControl 55:199–218CrossRefGoogle Scholar
  13. Colazza S, Rosi MC (2001) Differences in the searching behavior of two strains of the egg parasitoid Telenomus busseolae (Hymenoptera: Scelionidae). Eur J Entomol 98:47–52CrossRefGoogle Scholar
  14. Cônsoli FL, Kitajima EW, Parra JRP (1999) Ultrastructure of the natural and factitious host eggs of Trichogramma galloi Zucchi and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Int J Insect Morphol 28:211–229CrossRefGoogle Scholar
  15. Corrêa-Ferreira BS, Moscardi F (1995) Seasonal occurrence and host spectrum of egg parasitoids associated with soybean stink bugs. Biol Control 5:196–202CrossRefGoogle Scholar
  16. Corrêa-Ferreira BS, Zamataro CEO (1989) Capacidade reproductiva e longevidade dos parasito’ ides de ovos Trissolcus basalis (Wollaston) e Trissolcus mitsukurii Ashmead (Hymenoptera: Scelionidae). Rev Bras Biol 49:621–626Google Scholar
  17. Corrêa-Ferreira BS, Azevedo J (2002) Soybean seed damage by different species of stink bugs. Agric Forest Entomol 4:145–150CrossRefGoogle Scholar
  18. Cunningham RT, Farias GJ, Nakagawa S, Chambers DL (1971) Reproduction in the Mediterranean fruit fly: depletion of stored sperm in female. Ann Entomol Soc Am 64:312–313CrossRefGoogle Scholar
  19. Fisher RC (1981) Efficiency of parasites in assimilating host tissues into their own. Parasitology 82:33–34Google Scholar
  20. Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton, p 488Google Scholar
  21. Houseweart MW, Jennings DT, Welty C, Southard SG (1983) Progeny production by Trichogramma minutum (Hymenoptera: Trichogrammatidae) utilizing eggs for Choristoneura fumiferana (Lepidoptera: Tortricidae) and Sitotroga cerealella (Lepidoptera: Gelechiidae). Can Entomol 115:1245–1252CrossRefGoogle Scholar
  22. King BH (1987) Offspring sex ratios in parasitoid wasps. Q Rev Biol 62:367–369CrossRefGoogle Scholar
  23. Laumann RA, Moraes MCB, Silva JPD, Vieira AMC, Silveira SD, Borges M (2010) Egg parasitoid wasps as natural enemies of the neotropical stink bug Dichelops melacanthus. Pesq Agropec Bras 45:442–449CrossRefGoogle Scholar
  24. McDougall SJ, Mills NJ (1997) The influence of hosts, temperature and food sources on the longevity of Trichogramma platneri. Entomol Exp Appl 83:195–203CrossRefGoogle Scholar
  25. Michaud JP (2018) Problems inherent to augmentation of natural enemies in open agriculture. Neotrop Entomol 47:161–170PubMedCrossRefGoogle Scholar
  26. Pak GA, Buis HCEM, Heck ICC, Hermans MLG (1986) Behavioural variations among strains of Trichogramma spp.: host-age selection. Entomol Exp Appl 40:247–258CrossRefGoogle Scholar
  27. Panizzi AR (2013) History and contemporary perspectives of the integrated pest management of soybean in Brazil. Neotrop Entomol 42:119–127PubMedCrossRefGoogle Scholar
  28. Panizzi AR, Corrêa-Ferreira BS (1997) Dynamics in the insect fauna adaptation to soybean in the tropics. Trends Entomol 1:71–88Google Scholar
  29. Panizzi AR, Slansky FJR (1985) Review of phytophagous pentatomids (Hemiptera: Pentatomidae) associated with soybean in the Americas. Fla Entomol 68:184–203CrossRefGoogle Scholar
  30. Panizzi AR, Parra JRP, Santos CH, Carvalho DR (2000) Rearing the southern green stink bug using artificial dry diet and artificial plant. Pesq Agropec Bras 35:1709–1715CrossRefGoogle Scholar
  31. Papaj DR (2000) Ovarian dynamics and host use. Annu Rev Entomol 45:423–448PubMedCrossRefGoogle Scholar
  32. Peres WAA, Corrêa-Ferreira BS (2004) Methodology of mass multiplication of Telenomus podisi Ashmead and Trissolcus basalis (Hymenoptera: Scelionidae) on eggs of Euschistus heros (Hemiptera: Pentatomidae). Neotrop Entomol 33:457–462CrossRefGoogle Scholar
  33. Powell JE, Shepard BM (1982) Biology of Australian and United States strains of Trissolcus basalis, a parasitoid of the green vegetable bug Nezara viridula. Austral Ecol 7:181–186CrossRefGoogle Scholar
  34. Pratissoli D, Kloss TG, Zinger FD, Carvalho JR, Vianna UR, Paes JP (2014) Does mating interfere in the biological characteristics of a population of Trichogramma pretiosum? An Acad Bras Ciênc 86:459–464PubMedCrossRefGoogle Scholar
  35. Queiroz AP, Bueno AF, Pomari-Fernandes A, Grande MLM, Bortolotto OC, Silva DM (2017) Quality control of Telenomus remus (Hymenoptera: Platygastridae) reared on the factitious host Corcyra cephalonica (Lepidoptera: Pyralidae) for successive generations. B Entomol Res 107:791–798CrossRefGoogle Scholar
  36. Queiroz AP, Taguti EA, Bueno AF, Grande MLM, Costa C (2018) Host preferences of Telenomus podisi (Hymenoptera: Scelionidae): parasitism on eggs of Dichelops melacanthus, Euschistus heros, and Podisus nigrispinus (Hemiptera: Pentatomidae). Neotrop Entomol 47:543–552PubMedCrossRefGoogle Scholar
  37. Queiroz AP, Favetti BM, Luski PGG, Gonçalvez J, Neves POJ, Bueno AF (2019) Telenomus remus (Hymenoptera: Platygastridae) parasitism on Spodoptera frugiperda (Lepidoptera: Noctuidae) eggs: different parasitoid and host egg ages. Semina Ciên Agr 40:2933–2946Google Scholar
  38. Querino RB, Silva NN, Zucchi RA (2016) Natural parasitism by Trichogramma spp. in agroecosystems of the Mid-North, Brazil. Ciênc Rural 46:1521–1523CrossRefGoogle Scholar
  39. SAS Institute (2009) SAS User’s guide: statistics, Version 8e. SAS Institute, CaryGoogle Scholar
  40. Schwartz A, Gerling D (1974) Adult biology of Telenomus remus (Hymenoptera: Scelionidae) under laboratory conditions. Entomophaga 19:482–492CrossRefGoogle Scholar
  41. Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611CrossRefGoogle Scholar
  42. Silva CC, Laumann RA, Blassioli MC, Pareja M, Borges M (2008) Euschistus heros mass rearing technique for the multiplication of Telenomus podisi. Pesq Agropec Bras 43:575–580CrossRefGoogle Scholar
  43. Slansky F (1986) Nutritional ecology of endoparasitic insects and their hosts: an overview. J Insect Physiol 32:255–261CrossRefGoogle Scholar
  44. Sosa-Gómez DR, Silva JJD (2010) Neotropical brown stink bug (Euschistus heros) resistance to methamidophos in Paraná, Brazil. Pesq Agrop Brasileira 45:767–769CrossRefGoogle Scholar
  45. Sosa-Gómez DR, Corso IC, Morales L (2001) Insecticide resistance to endosulfan, monocrotophos and methamidophos in the neotropical brown stink bug. Euschistus heros (F) Neotrop Entomol 30:317–320CrossRefGoogle Scholar
  46. Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, PrincetonGoogle Scholar
  47. Thomson LJ, Hoffmann AA (2002) Laboratory fecundity as predictor of field success in Trichogramma carverae (Hymenoptera: Trichogrammatidae). J Econ Entomol 95:912–917PubMedCrossRefGoogle Scholar
  48. Thuler RT, Volpe HXL, Bortoli AS, Goulart RM, Viana CLT (2007) Metodologia para avaliação da preferência hospedeira de parasitoides do gênero Trichogramma Westood. Bol Sanid Veg 33:333–340Google Scholar
  49. Valente ECN, Broglio SMF, Passos EMD, Lima ASTD (2016) Performance of Trichogramma galloi (Hymenoptera: Trichogrammatidae) on eggs of Diatraea spp. (Lepidoptera: Crambidae). Pesq Agropec Bras 51:293–300CrossRefGoogle Scholar
  50. van Lenteren JC, Bueno VHP (2003) Augmentative biological control of arthropods in Latin America. Biocontrol 48:123–139CrossRefGoogle Scholar
  51. van Lenteren JC, Tommasini M (2002) Mass production, storage, shipment and quality control of natural enemies. In: Albajes R, Gullino ML, van Lenteren JC, Elad Y (eds) Mass production, storage, shipment and quality control of natural enemies, integrated pest and disease management in greenhouse crops. Springer, Dordrech, pp 276–294Google Scholar
  52. van Lenteren JC, Tommasini MG (2003) Mass production, storage, shipment and release of natural enemies. In: van Lenteren JC (ed) Quality control and production of biological control agents: theory and testing procedures. Cabi, Wallingford, pp 181–189CrossRefGoogle Scholar
  53. van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl 63:39–59CrossRefGoogle Scholar
  54. Vinson SB (1997) Comportamento de seleção hospedeira de parasitoides de ovos, com ênfase na família Trichogrammatidae. In: JRP P, Zucchi RA (eds) Trichogramma e o Controle Aplicado. Fundação de Estudos Agrários Luiz de Queiroz, Piracicaba, pp 67–119Google Scholar
  55. Vinson SB, Iwantsch (1980) Host suitability for insect parasitoids. Annu Rev Entomol 25:397–419CrossRefGoogle Scholar
  56. Wiegart RG, Peterson CE (1983) Energy transfer in insects. Annu Rev Entomol 28:455–486CrossRefGoogle Scholar
  57. Zhou Y, Abram PK, Boivin G, Brodeur J (2014) Increasing host age does not have the expected negative effects on the fitness parameters of an egg parasitoid. Entomol Exp Appl 151:106–111CrossRefGoogle Scholar

Copyright information

© Sociedade Entomológica do Brasil 2019

Authors and Affiliations

  • A P Queiroz
    • 1
  • B M Favetti
    • 2
  • R Hayashida
    • 1
  • M L M Grande
    • 3
  • M M Neiva
    • 1
  • A R Panizzi
    • 4
  • A F Bueno
    • 5
    Email author
  1. 1.Univ Federal do ParanáCuritibaBrasil
  2. 2.Instituto Agronômico do Paraná (IAPAR)Londrina,Brasil
  3. 3.Univ Estadual de LondrinaLondrinaBrasil
  4. 4.Empresa Brasileira de Pesquisa Agropecuária – Embrapa TrigoPasso FundoBrasil
  5. 5.Empresa Brasileira de Pesquisa Agropecuária – Embrapa SojaLondrinaBrasil

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