Skip to main content
SpringerLink
Log in

Intraguild predation on the aphid parasitoid Aphelinus asychis by the ladybird Harmonia axyridis

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

We investigated intraguild predation (IGP) on an aphid parasitoid, Aphelinus asychis Walker (Hymenoptera: Aphelinidae), by the multicolored Asian ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), and used the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) as the prey/host in the laboratory. The ladybirds reared on artificial diet and on aphids consumed more aphids than mummies, while those reared on parasitized aphids consumed similar numbers of aphids and mummies. The ladybirds chose more mummies in treatments when mummies were more abundant, and more aphids when numbers of aphids and mummies were equal, or when aphids were more abundant. However, at all density treatments, rejection rates of mummies (36%) were much greater than of aphids (2%). H. axyridis prey on more aphids than A. asychis mummies, which enhances biological control by the two species. However, prior feeding experience affected subsequent choice, increasing the competition between natural enemies which would reduce their combined effectiveness for biological control.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arim M, Marquet PA (2004) Intraguild predation: a widespread interaction related to species biology. Ecol Lett 7:557–564

    Article  Google Scholar 

  • Bilu E, Coll M (2007) The importance of intraguild interactions to the combined effect of a parasitoid and a predator on aphid population suppression. BioControl 52:753–763

    Article  Google Scholar 

  • Bilu E, Coll M (2009) Parasitized aphids are inferior prey for a coccinellid predator: implications for intraguild predation. Environ Entomol 38:153–158

    Article  PubMed  Google Scholar 

  • Brodeur J, Rosenheim JA (2000) Intraguild interactions in aphid parasitoids. Entomol Exp Appl 97:93–108

    Article  Google Scholar 

  • Byeon YW, Tuda M, Takagi M, Kim JH, Kim YH (2009) Non-reproductive host killing caused by Aphelinus asychis (Hymenoptera: Aphelinidae), a parasitoid of cotton aphid, Aphis gossypii (Homoptera: Aphididae). J Fac Agric Kyushu Univ 54:369–372

    Google Scholar 

  • Byeon YW, Tuda M, Kim JH, Choi MY (2011) Functional responses of aphid parasitoids, Aphidius colemani (Hymenoptera: Braconidae) and Aphelinus asychis (Hymenoptera: Aphelinidae). Biocontrol Sci Technol 21:57–70

    Article  Google Scholar 

  • Chacón JM, Heimpel GE (2010) Density-dependent intraguild predation of an aphid parasitoid. Oecologia 164:213–220

    Article  PubMed  Google Scholar 

  • Choh Y, Ignacio M, Sabelis MW, Janssen A (2012) Predator-prey role reversals, juvenile experience and adult antipredator behavior. Sci Rep 2:728

    Article  PubMed  PubMed Central  Google Scholar 

  • Colfer RG, Rosenheim JA (2001) Predation on immature parasitoids and its impact on aphid suppression. Oecologia 126:292–304

    Article  Google Scholar 

  • Costamagna AC, Landis DA, Difonzo CD (2007) Suppression of soybean aphids by generalist predators results in a tropic cascade in soybean. Ecol Appl 17:441–451

    Article  PubMed  Google Scholar 

  • Denoth M, Frid L, Myers JH (2002) Multiple agents in biological control: improving the odds? Biol Control 24:20–30

    Article  Google Scholar 

  • Foray V, Pelisson PF, Bel-Venner MC, Desouhant E, Venner S, Menu F, Giron D, Rey B (2012) A handbook for uncovering the complete energetic budget in insects: the van Handel’s method (1985) revisited. Physiol Entomol 37:295–302

    Article  Google Scholar 

  • Frago E, Godfray HCJ (2014) Avoidance of intraguild predation leads to a long-term positive trait-mediated indirect effect in an insect community. Oecologia 174:943–952

    Article  PubMed  Google Scholar 

  • Gontijo LM, Beers EH, Snyder WE (2015) Complementary suppression of aphids by predators and parasitoids. Biol Control 90:83–91

    Article  Google Scholar 

  • Handel EV (1985) Rapid determination of glycogen and sugars in mosquitoes. J Am Mosq Control Assoc 1:299–301

    PubMed  Google Scholar 

  • Hartley CP (1922) Some bionomics of Alphelinus semiflavus (Howard). Ohio J Sci 22:209–235

    Google Scholar 

  • Koch RL (2003) The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J Insect Sci 3:32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu YH, Kang ZW, Guo Y, Zhu GS, Shah MMR, Song Y, Fan YL, Jing XF, Liu TX (2016) Nitrogen hurdle of host alternation for a polyphagous aphid and the associated changes of endosymbionts. Sci Rep 6:24781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDonald JH (2014) Handbook of biological statistics, 3rd edn. Sparky House Publishing, Baltimore

    Google Scholar 

  • Meisner M, Harmon JP, Harvey CT, Ives AR (2011) Intraguild predation on the parasitoid Aphidius ervi by the generalist predator Harmonia axyridis: the threat and its avoidance. Entomol Exp Appl 138:193–201

    Article  Google Scholar 

  • Moreno-Ripoll R, Gabarra R, Symondson WOC, King RA, Agustí N (2013) Do the interactions among natural enemies compromise the biological control of the whitefly Bemisia tabaci? J Pest Sci 87:133–141

    Article  Google Scholar 

  • Okuyama T (2009) Intraguild predation in biological control: consideration of multiple resource species. BioControl 54:3–7

    Article  Google Scholar 

  • Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN (2007) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl 53:147–168

    Article  Google Scholar 

  • Polis GA, Myers CA (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330

    Article  Google Scholar 

  • Sighinolfi L, Febvay G, Dindo ML, Rey M, Pageaux JF, Grenier S (2013) Biochemical content in fatty acids and biological parameters of Harmonia axyridis reared on artificial diet. Bull Insectol 66:283–290

    Google Scholar 

  • Sitvarin MI, Rypstra AL (2014) The importance of intraguild predation in predicting emergent multiple predator effects. Ecology 95:2936–2945

    Article  Google Scholar 

  • Snyder WE, Ives AR (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology 84:91–107

    Article  Google Scholar 

  • Snyder WE, Ballard SN, Yang S, Clevenger GM, Miller TD, Ahn JJ, Hatten TD, Berryman AA (2004) Complementary biocontrol of aphids by the ladybird beetle Harmonia axyridis and the parasitoid Aphelinus asychis on greenhouse roses. Biol Control 30:229–235

    Article  Google Scholar 

  • Takizawa T, Yasuda H, Agarwanla BK (2000) Effects of parasitized aphids (Homoptera: Aphididae) as food on larval performance of three predatory ladybeetles (Coleoptera: Coccinellidae). Appl Entomol Zool 35:467–472

    Article  Google Scholar 

  • Tatsumi E, Takada H (2005) Evaluation of Aphelinus asychis and A. albipodus (Hymenoptera: Aphelinidae) as biological control agents against three pest aphids. Appl Entomol Zool 40:379–385

    Article  Google Scholar 

  • Xue Y, Bahlai CA, Frewin A, McCreary CM, Des Marteaux LE, Schaafsma AW, Hallett RH (2012) Intraguild predation of the aphid parasitoid Aphelinus certus by Coccinella septempunctata and Harmonia axyridis. BioControl 57:627–634

    Article  Google Scholar 

  • Yang NW, Zang LS, Wang S, Guo JY, Xu HX, Zhang F, Wang FH (2014) Biological pest management by predators and parasitoids in the greenhouse vegetables in China. Biol Control 68:92–102

    Article  Google Scholar 

Download references

Acknowledgements

This work was partially supported by the National Basic Research Program of Ministry of Science and Technology, China (973 Programs, 2013CB127600), Natural Science Foundation of China (31471819 and 31272089), Special Fund for Agro-Scientific Research in the Public Interest (201103022), and China Agriculture Research System (CARS-25-B-06). We are grateful for the assistance of all staff and students in the Key Laboratory of Applied Entomology, Northwest A&F University at Yangling, Shaanxi, China.

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology for Arid Areas and Key Laboratory of IPM of Crop Pests on the Northwest Loess Plateaus of Ministry of Agriculture, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Wenyan Fu, Xinglin Yu, Nazeer Ahmed, Shize Zhang & Tongxian Liu

Authors
  1. Wenyan Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xinglin Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nazeer Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shize Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tongxian Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Shize Zhang or Tongxian Liu.

Additional information

Handling Editor: Patrick De Clercq

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fu, W., Yu, X., Ahmed, N. et al. Intraguild predation on the aphid parasitoid Aphelinus asychis by the ladybird Harmonia axyridis . BioControl 62, 61–70 (2017). https://doi.org/10.1007/s10526-016-9774-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-016-9774-8

Keywords

Search

Navigation