Skip to main content
Log in

The contribution of a beneficial insectary plant Scaevola aemula to survival and long-term establishment of flightless Harmonia axyridis in greenhouses

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The fairy fan flower, Scaevola aemula R. Br., is a primary candidate insectary plant for maintaining populations of generalist predators. We conducted release experiments in greenhouses of cultivated eggplants to evaluate the effects of intercropping S. aemula on the establishment of flightless Harmonia axyridis Pallas. Compared with a monoculture of eggplant, all release experiments showed that flightless H. axyridis remained in greater numbers in plots with S. aemula planted alongside eggplant. In the release experiment of flightless H. axyridis larvae, the incidence of aphids in the plot with transplanted S. aemula was suppressed compared with that in the release plot without transplanted S. aemula. In a laboratory experiment, the longevity of flightless H. axyridis adults on blossom stems of S. aemula was greater than when open flowers and buds were removed, suggesting that the insects fed on floral resources such as the pollen of S. aemula. Our findings showed that the floral resources of S. aemula can enhance aphid suppression by improving the establishment of flightless H. axyridis.

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

  • Adachi-Hagimori T, Shibao M, Tanaka H, Seko T, Miura K (2011) Control of Myzus persicae and Lipaphis erysimi (Hemiptera: Aphididae) by adults and larvae of a flightless strain of Harmonia axyridis (Coleoptera: Coccinellidae) on non-heading Brassica cultivars in the greenhouse. BioControl 56:207–213

    Article  Google Scholar 

  • Berkvens N, Bonte J, Berkvens D, Deforce K, Tirry L, De Clercq P (2008) Pollen as an alternative food for Harmonia axyridis. BioControl 53:201–210

    Article  Google Scholar 

  • Berndt LA, Wratten SD (2005) Effects of alyssum flowers on the longevity, fecundity, and sex ratio of the leafroller parasitoid Dolichogenidea tasmanica. Biol Control 32:65–69

    Article  Google Scholar 

  • Bhalla PL, Sweeney K (1998) Micropropagation of Scaevola –Australian native of ornamental horticulture. Aust J Exp Agric 38:399–401

    Article  Google Scholar 

  • Bonte M, Samih MA, De Clercq P (2010) Development and reproduction of Adalia bipunctata on factitious and artificial foods. BioControl 55:485–491

    Article  Google Scholar 

  • Brennan EB (2013) Agronomic aspects of strip intercropping lettuce with alyssum for biological control of aphids. Biol Control 65:302–311

    Article  Google Scholar 

  • Cohen AC, Smith LK (1998) A new concept in artificial diets for Chrysoperla rufilabris: the efficacy of solid diets. Biol Control 13:49–54

    Article  Google Scholar 

  • Collier T, van Steenwyk R (2004) A critical evaluation of augmentative biological control. Biol Control 31:245–256

    Article  Google Scholar 

  • Crowder DW (2007) Impact of release rates on the effectiveness of augmentative biological control agents. J Insect Sci 7:15

    Article  PubMed  PubMed Central  Google Scholar 

  • De Clercq P, Arijs Y, van Meir T, van Stappen G, Sorgeloos P, Dewettinck K, Rey M, Grenier S, Febvay G (2005a) Nutritional value of brine shrimp cysts as a factitious food for Orius laevigatus (Heteroptera: Anthocoridae). Biocontrol Sci Technol 15:467–479

    Article  Google Scholar 

  • De Clercq P, Bonte M, Van Speybroeck K, Bolckmans K, Deforce K (2005b) Development and reproduction of Adalia bipunctata (Coleoptera: Coccinellidae) on eggs of Ephestia kuehniella (Lepidoptera: Phycitidae) and pollen. Pest Manag Sci 61:1129–1132

    Article  PubMed  Google Scholar 

  • Dixon AFG (2000) Insect predator-prey dynamics: ladybird beetles and biological control. Cambridge University Press, Cambridge

    Google Scholar 

  • Dreistadt SH, Flint ML (1996) Melon aphid (Homoptera: Aphididae) control by inundative convergent lady beetle (Coleoptera: Coccinellidae) release on chrysanthemum. Environ Entomol 25:688–697

    Article  Google Scholar 

  • Eubanks MD, Denno RF (2000) Host plants mediate omnivore-herbivore interactions and influence prey suppression. Ecology 81:936–947

    Google Scholar 

  • Everitt BS, Hothorn T (2010) A handbook of statistical analyses using R, 2nd edn. CRC Press, Boca Raton

    Google Scholar 

  • Frank SD (2010) Biological control of arthropod pests using banker plant systems: past progress and future directions. Biol Control 52:8–16

    Article  Google Scholar 

  • Frazer BD (1988) Coccinellidae. In: Minks AK, Harrewijn P (eds) Aphids: their biology, natural enemies and control, vol 2B. Elsevier, Amsterdam, pp 231–247

    Google Scholar 

  • Goleva I, Zebitz CPW (2013) Suitability of different pollen as alternative food for the predatory mite Amblyseius swirskii (Acari, Phytoseiidae). Exp Appl Acarol 61:259–283

    Article  CAS  PubMed  Google Scholar 

  • Gontijo LM, Beers EH, Snyder WE (2013) Flowers promote aphid suppression in apple orchards. Biol Control 66:8–15

    Article  Google Scholar 

  • Heimpel GE, Asplen MK (2011) A ‘Goldilocks’ hypothesis for dispersal of biological control agents. BioControl 56:441–450

    Article  Google Scholar 

  • Hogg BN, Bugg RL, Daane KM (2011a) Attractiveness of common insectary and harvestable floral resources to beneficial insects. Biol Control 56:76–84

    Article  Google Scholar 

  • Hogg BN, Nelson EH, Mills NJ, Daane KM (2011b) Floral resources enhance aphid suppression by a hoverfly. Entomol Exp Appl 141:138–144

    Article  Google Scholar 

  • Hongo T, Obayashi N (1997) Use of diapause eggs of brine shrimp, Artemia salina (Linne) for artificial diet of coccinellid beetle, Harmonia axyridis (Pallas). Jpn J Appl Entomol Zool 41:101–105

    Article  Google Scholar 

  • Iguchi M, Fukushima F, Miura K (2012) Control of Aphis gossypii and Myzus persicae (Hemiptera: Aphididae) by a flightless strain of Harmonia axyridis (Coleoptera: Coccinellidae) on green pepper plants in open fields. Entomol Sci 15:127–132

    Article  Google Scholar 

  • Lommen STE, Holness TC, van Kuik AJ, de Jong PW, Brakefield PM (2013) Releases of a natural flightless strain of the ladybird beetle Adalia bipunctata reduce aphid-born honeydew beneath urban lime trees. BioControl 58:195–204

    Article  Google Scholar 

  • Lundgren JG (2009) Nutritional aspects of non-prey foods in the life histories of predaceous Coccinellidae. Biol Control 51:294–305

    Article  Google Scholar 

  • MAFF (2014) Development of flightless multicolored asian lady beetle (Harmonia axyridis) and its application technology. In: ten outstanding topics in agriculture, forestry and fisheries research, 2014. http://www.maff.go.jp/e/maffud/2014/no784.html. Accessed 25 Dec 2014

  • Marples NM, de Jong PW, Ottenheim MM, Verhoog MD, Brakefield PM (1993) The inheritance of a wingless character in the 2spot ladybird (Adalia bipunctata). Entomol Exp Appl 69:69–73

    Article  Google Scholar 

  • Nagamori S, Hikawa M, Sano T, Nagai K (2007) Arthropod species and their seasonal appearance on landscape plants. Bull Okayama Pref Agric Exp Sta 25:17–28

    Google Scholar 

  • Nagamori S, Hikawa M, Nagashima S, Kondo A, Sano T, Nagai K, Nakasuji F (2010) Screening of ground-cover plants for conservation of a predacious bugs, Orius spp., in a biological control program for vegetables. Bull Okayama Pref Agri 1:5–12

    Google Scholar 

  • Nakayama S, Seko T, Takatsuki J, Miura K, Miyatake T (2010) Walking activity of flightless Harmonia axyridis (Coleoptera: Coccinellidae) as a biological control agent. J Econ Entomol 103:1564–1568

    Article  PubMed  Google Scholar 

  • Ohta I, Takeda M (2014) Adult survival of Orius strigicollis (Poppius) on different flowering plants and its development and fecundity on buckwheat flowers. Ann Rept Kansai Pl Prot 56:1–5

    Article  Google Scholar 

  • Parolin P, Bresch C, Poncet C, Desneux N (2012) Functional characteristics of secondary plants for increased pest management. Int J Pest Manag 58:368–376

    Google Scholar 

  • Pinheiro LA, Torres L, Raimundo J, Santos SAP (2013) Effect of floral resources on longevity and nutrient levels of Episyrphus balteatus (Diptera: Syrphidae). Biol Control 67:178–185

    Article  Google Scholar 

  • Prasad RP, Snyder WE (2006) Polyphagy complicates conservation biological control that targets generalist predators. J Appl Ecol 43:343–352

    Article  Google Scholar 

  • Pumariño L, Alomar O (2012) The role of omnivory in the conservation of predators: Orius majusculus (Heteroptera: Anthocoridae) on sweet alyssum. Biol Control 62:24–28

    Article  Google Scholar 

  • Riddick EW, Wu Z, Rojas G (2014) Potential utilization of Artemia franciscana eggs as food or Coleomegilla maculata. BioControl 59:575–583

    Article  CAS  Google Scholar 

  • Seko T (2015) Augmentative release of flightless Harmonia axyridis in greenhouses with cultivated vegetables. JATAFF J 3:9–13

    Google Scholar 

  • Seko T, Yamashita K, Miura K (2008) Residence period of a flightless strain of the ladybird beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in open fields. Biol Control 47:194–198

    Article  Google Scholar 

  • Seko T, Miyatake T, Miura K (2012) Assessment of hybrid vigor between flightless lines to restore survival and reproductive characteristics in the ladybird beetle Harmonia axyridis. BioControl 57:85–93

    Article  Google Scholar 

  • Seko T, Sumi A, Nakano A, Kameshiro M, Kaneda T, Miura K (2014) Suppression of aphids by augmentative release of larvae of flightless Harmonia axyridis. J Appl Entomol 5:326–337

    Article  Google Scholar 

  • Spellman B, Brown MW, Mathews CR (2006) Effect of floral and extrafloral resources on predation of Aphis spiraecola by Harmonia axyridis on apple. BioControl 51:715–724

    Article  Google Scholar 

  • Starman TW, Williams MS (2000) Growth retardants affect growth and flowering of Scaevola. HortScience 35:36–38

    CAS  Google Scholar 

  • R Development Core Team (2011) In: R: a language and environment for statistical computing. R Foundation, Vienna. http://www.R-project.org

  • Tourniaire R, Ferran A, Gambier J, Giuge L, Bouffault F (1999) Locomotor behavior of flightless Harmonia axyridis Pallas (Col., Coccinellidae). J Insect Behav 12:545–558

    Article  Google Scholar 

  • Trevelyan R (1995) The feeding ecology of Stephen’s lory and nectar availability in its food plants. Biol J Linnean Soc 56:185–197

    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 Rijn PCJ, Tanigoshi LK (1999) The contribution of extrafloral nectar to survival and reproduction of the predatory mite Iphiseius degenerans on Ricinus communis. Exp Appl Acarol 23:281–296

    Article  Google Scholar 

  • Waite MO, Scott-Dupree CD, Brownbridge M, Buitenhuis R, Murphy G (2014) Evaluation of seven plant species/cultivars for their suitability as banker plants for Orius insidiosus (Say). BioControl 59:79–87

    Article  CAS  Google Scholar 

  • Yano E (2003) Natural enemies: ecology and biological control. Yokendo Ltd., Tokyo

    Google Scholar 

  • Zhang D, Moran RE, Stack LB (2004) Effect of phosphorus fertilization on growth and flowering of Scaevola aemula R. Br. ‘New Wonder’. HortScience 39:1728–1731

    Google Scholar 

Download references

Acknowledgements

We especially thank Y. Sato, M. Matsui and T. Oishi for technical support in the greenhouses at the NARO Western Region Agricultural Research Center, and Dr. K. Nagai for suggesting the release experiment at the Research Institute for Agriculture, Okayama Prefectural Technology Center for Agriculture, Forestry and Fisheries. This work was supported in part by Science and technology research promotion program for agriculture, forestry, fisheries and food industry (No. 28021C) from the Ministry of Agriculture, Forestry and Fisheries of Japan. Two anonymous reviewers and an editor provided helpful comments on an earlier version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tomokazu Seko.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

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

Seko, T., Abe, J., Miura, K. et al. The contribution of a beneficial insectary plant Scaevola aemula to survival and long-term establishment of flightless Harmonia axyridis in greenhouses. BioControl 62, 221–231 (2017). https://doi.org/10.1007/s10526-017-9790-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-017-9790-3

Keywords

Navigation