Skip to main content
Log in

Development and parasitization of an aphid’s secondary parasitoid, Dendrocerus laticeps (Hymenoptera: Megaspilidae), on Aphidius colemani (Hymenoptera: Braconidae)

  • Original Research Paper
  • Published:
Applied Entomology and Zoology Aims and scope Submit manuscript

Abstract

Banker-plant systems using Aphidius species have been employed to control pest aphids in greenhouses growing eggplant and sweet pepper in Japan. However, a strong negative correlation between the occurrence of secondary parasitoids and aphid-control success by this system was reported by Nagasaka et al. (2010). To control secondary parasitoid populations, detailed knowledge of their ecological characteristics is needed. In this paper, the development and parasitization ability of Dendrocerus laticeps (Hedicke) (Hymenoptera: Megaspilidae), a major secondary ectoparasitoid of Aphidius species in Japan, were examined under 25 °C laboratory conditions. The maximum female longevity was about 11 days when honeydew was available. Parasitization occurred only on mummified aphids, and the age of mummified aphids did not influence the ecological value of offspring. The maximum parasitization ability was 18.9 hosts/day estimated by Holling’s disc equation. Possible lifetime fecundity was 100.35. The intrinsic rate of natural increase estimated by the bootstrap method ranged from 0.211 to 0.321, depending on the assumptions made about larval mortality. The countermeasures for avoiding the negative impacts of D. laticeps in a banker-plant system include the development of a refuge for mummified aphids and increasing the temperature around the banker plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abe J, Mitsunaga T, Kumakura H, Yano E (2011) Comparative studies on development and reproduction of four cereal aphid species reared on sorghum or barley to evaluate as alternative prey for banker plant system. Jpn J Appl Entomol Zool 55:227–239 (in Japanese with English summary)

    Article  Google Scholar 

  • Agrawal AA, Lau JA, Hambäck PA (2006) Community heterogeneity and the evolution of interactions between plants and insect herbivores. Q Rev Biol 81:349–376

    Article  PubMed  Google Scholar 

  • Barrett BA, Brunner JF (1990) Types of parasitoid-induced mortality, host stage preference, and sex ratios exhibited by Pnigalio flavipes (Hymenoptera: Eulophidae) using Phyllonorycter elmalla (Lepidoptera: Gracillariidae) as a host. Environ Entomol 19:803–807

    Google Scholar 

  • Buitenhuis R (2004) A comparative study of the life history and foraging behaviour of aphid hyperparasitoids. PhD thesis, Univ Laval, pp 172

  • Chow A, Mackauer M (1999) Host handling time and specificity of the hyperparasitoid wasp, Dendrocerus carpenteri (Curtis)(Hym., Megaspilidae): importance of host age and species. J Appl Entomol 123:83–91

    Article  Google Scholar 

  • Colley MR, Luna JM (2000) Relative attractiveness of potential beneficial insectary plants to aphidophagous hoverflies (Diptera: Syrphidae). Environ Entomol 29:1054–1059

    Article  Google Scholar 

  • Davis JA, Radcliffe EB, Ragsdale DW (2007) Resistance to green peach aphid, Myzus persicae (Sulzer), and potato aphid, Macrosiphum euphorbiae (Thomas), in potato cultivars. Am J Potato Res 84:259–269

    Article  Google Scholar 

  • DeBach P (1974) Biological control by natural enemies. Cambridge Univ Press, Cambridge, p 323

    Google Scholar 

  • Desneux N, Fauvergue X, Moncharmont FXD, Kerhoas L, Ballanger Y, Kaiser L (2005) Diaeretiella rapae limits Myzus persicae populations after application of deltamethrin in oilseed rape. J Econ Entomol 98:9–17

    Article  PubMed  Google Scholar 

  • Eastop VF (1977) Worldwide importance of aphids as virus vectors. In: Harris F, Maramorosch K (eds) Aphids as virus vectors. Academic, New York, pp 413–431

    Google Scholar 

  • Efton B (1982) The jackknife, the bootstrap and other resampling plans. Society for Industrial and Applied Mathematics, Philadelphia

    Google Scholar 

  • Elliot NC, French BW, Burd JD, Kindler SD, Reed DK (1994) Parasitism, adult emergence, sex ratio, and size of Aphidius colemani (Hymenoptera: Aphididae) on several aphid species. Great Lake Entomol 27:137–142

    Google Scholar 

  • Greathead D (1986) Parasitoids in classical biological control. In Waage J, Greathead D (eds) Insect parasitoids. 13th Symp Royal Entomol Soc London, Academic, London, 289–318

  • Hansen LS (1983) Introduction of Aphidoletes aphidimyza (Rond.)(Diptera: Cecidomyiidae) from an open rearing unit for the control of aphids in glasshouses. Bull IOBC/WPRS 6:146–150

    Google Scholar 

  • Höller C, Borgemeister C, Haardt H, Powell W (1993) The relationship between primary parasitoids and hyperparasitoids of cereal aphids: an analysis of field data. J Anim Ecol 62:12–21

    Article  Google Scholar 

  • Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398

    Article  Google Scholar 

  • Horn DJ (1989) Secondary parasitism and population dynamics of aphid parasitoid (Hymenoptera: Aphidiidae). J Kans Entomol Soc 62:203–210

    Google Scholar 

  • Jervis MA, Kidd NAC (1986) Host-feeding strategies in hymenopteran parasitoids. Biol Rev 61:395–434

    Article  Google Scholar 

  • Jervis MA, Kidd NAC, Heimpel GE (1996) Parasitoid adult feeding behaviour and biocontrol––a review. Biocontrol News Inf 17:11–22

    Google Scholar 

  • Luck R, Messenger PS, Barbieri JF (1981) The influence of hyperparasitism on the performance of biological control agents. In Rosen D, Berkeley CA (eds) The role of hyperparasitism in biological control: a symposium. Division of Agricultural Sciences, University of California, 34–42

  • Mackauer M, Völkl W (1993) Regulation of aphid populations by aphidiid wasps: does parasitoid foraging behaviour or hyperparasitism limit impact? Oecologia 94:339–350

    Article  Google Scholar 

  • May RM, Hassell MP (1981) The dynamics of multiparasitoid–host interactions. Am Nat 117:234–261

    Article  Google Scholar 

  • Meyer JS, Ingersoll CG, McDonald LL, Boyce MS (1986) Estimating uncertainty in population growth rates: jackknife and bootstrap techniques. Ecology 67:1156–1166

    Article  Google Scholar 

  • Mitsunaga T, Shimoda T, Yano E (2004) Influence of food supply on longevity and parasitization ability of a larval endoparasitoid, Cotesia plutellae (Hymenoptera: Braconidae). Appl Entomol Zool 39:691–697

    Article  Google Scholar 

  • Nagai K, Hikawa M (2012) Evaluation of Black-eyed Susan Rudbeckia hirta L. (Asterales: Asteraceae) as an insectary plant for a predacious natural enemy Orius sauteri (Poppius) (Heteroptera: Anthocoridae). Jpn J Appl Entomol Zool 56:57–64 (in Japanese with English summary)

    Article  Google Scholar 

  • Nagasaka K, Oya S (2003) A practical application of a banker plant system to aphid control in greenhouse. Plant Prot 57:505–509 (in Japanese)

    Google Scholar 

  • Nagasaka K, Takahasi N, Okabayashi T (2010) Impact of secondary parasitism on Aphidius colemani in the banker plant system on aphid control in commercial greenhouses in Kochi, Japan. Appl Entomol Zool 45:541–550

    Article  Google Scholar 

  • Ohta I, Ohtaishi M (2004) Fertility, longevity, and intrinsic rate of increase of Aphidius gifuensis Ashmead (Hymenoptera: Braconidae) on the green peach aphid, Myzus persicae (Sulzer)(Homoptera: Aphididae). Appl Entomol Zool 39:113–117

    Article  Google Scholar 

  • Pelletier Y, Pompon J, Dexter P, Quiring D (2010) Biological performance of Myzus persicae and Macrosiphum euphorbiae (Homoptera: Aphididae) on seven wild Solanum species. Ann Appl Biol 156:329–336

    Article  Google Scholar 

  • Santolamazza-Carbone S, Cordero-Rivera A (2003) Superparasitism and sex ratio adjustment in a wasp parasitoid: results at variance with local mate competition. Oecologia 136:365–373

    Article  PubMed  Google Scholar 

  • SAS Institute (2009) JMP, version 8.0.1, SAS Institute, Cary

  • Scholz D, Höller C (1992) Competition for hosts between two hyperparasitoids of aphids, Dendrocerus laticeps and Dendrocerus carpenteri (Hymenoptera: Megaspilidae): the benefit of interspecific host discrimination. J Ins Behav 5:289–300

    Article  Google Scholar 

  • Stapel JO, de Cortesero AM, Moraes CM, Tumlinson JH, Lewis WJ (1997) Extrafloral nectar, honeydew, and sucrose effects on searching behavior and efficiency of Microplitis croceipes (Hymenoptera: Braconidae) in cotton. Envir Entomol 26:617–623

    Google Scholar 

  • Sullivan DJ (1987) Insect hyperparasitism. Ann Rev Entomol 32:49–70

    Article  Google Scholar 

  • Tylianakis JM, Didham RK, Wratten SD (2004) Improved fitness of aphid parasitoids receiving resource subsidies. Ecology 85:658–666

    Article  Google Scholar 

  • van Lenteren JC, Woets J (1988) Biological and integrated pest control in greenhouses. Ann Rev Entomol 33:239–269

    Article  Google Scholar 

  • van Steenis MJ (1995) Evaluation and application of parasitoids of biological control of Aphis gossypii in glasshouse cucumber crops. PhD thesis. Wageningen Agricultural Univ, p 215

  • van Steenis MJ (2009) Intrinsic rate of increase of Aphidius colemani Vier. (Hym. Braconidae), a parasitoid of Aphis gossypii Glov. (Hom. Aphididae), at different temperatures. J Appl Entomol 116:192–198

    Article  Google Scholar 

  • Walker GP, Cameron PJ (1981) The biology of Dendrocerus carpenteri (Hymenoptera: Ceraphronidae), a parasite of Aphidius species, and field observations of Dendrocerus species as hyperparasites of Acyrthosiphon species. N Zeal J Zool 8:531–538

    Article  Google Scholar 

  • Wolfram Research (2004) Mathematica, version 5.1, Wolfram Research Inc., Champaign

  • Yano E (2006) Ecological considerations for biological control of aphids in protected culture. Popul Ecol 48:333–339

    Article  Google Scholar 

  • Zamani AA, Haghani M, Kheradmand K (2012) Effect of temperature on reproductive parameters of Aphidius colemani and Aphidius matricariae (Hymenoptera: Braconidae) on Aphis gossypii (Hemiptera: Aphididae) in laboratory conditions. J Crop Prot 1:35–40

    Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. Y. Suzuki for his useful comments. We thank Mr. H. Tanaka and Mrs. A. Iwasaki for rearing the insects and plants. We are also indebted to two anonymous reviewers for their critical reading of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takayuki Mitsunaga.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mitsunaga, T., Nagasaka, K. & Moriya, S. Development and parasitization of an aphid’s secondary parasitoid, Dendrocerus laticeps (Hymenoptera: Megaspilidae), on Aphidius colemani (Hymenoptera: Braconidae). Appl Entomol Zool 49, 511–518 (2014). https://doi.org/10.1007/s13355-014-0278-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13355-014-0278-7

Keywords

Navigation