Skip to main content
Log in

Pesticide-mediated displacement of a phytoseiid predator, Neoseiulus womersleyi, by another phytoseiid predator, N. californicus (Acari: Phytoseiidae)

  • Published:
Experimental and Applied Acarology Aims and scope Submit manuscript

Abstract

Neoseiulus womersleyi and N. californicus are two predators that are frequently used to control spider mites in fruit-tree orchards. Neoseiulus womersleyi used to be the dominant predator species in Japan, but since the 1990s in central and southwestern Japan, N. californicus populations have been increasing and have displaced populations of N. womersleyi. We previously observed the same phenomenon under laboratory conditions when these species were released at a 1:1 ratio, and attributed the displacement to asymmetrical intraguild predation. However, the ratio in fruit-tree orchards could be different from 1:1. Therefore, we hypothesized that differential susceptibilities to pesticides might accelerate species displacement of N. womersleyi by N. californicus, even if the ratio between these two species was extremely skewed in favor of N. womersleyi and no species displacement occurred otherwise. We examined the effects of 21 pesticides on egg-to-adult and adult survivorship in N. womersleyi and N. californicus. Among these pesticides, two neonicotinoids (acetamiprid and imidacloprid) had much severer effects on N. womersleyi than on N. californicus and thus could possibly account for the species displacement. When the two species were released onto leaf arenas at an N. californicus: N. womersleyi ratio of 1:9 in the absence of insecticide, no displacement was observed. However, just after acetamiprid or imidacloprid application, the proportion of N. californicus increased, causing N. californicus to displace N. womersleyi. Our results indicate that displacement in predator complexes of fruit-tree orchards could be due to different degrees of pesticide susceptibility.

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

Similar content being viewed by others

References

  • Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    Article  CAS  Google Scholar 

  • Amano H (2001) Species structure and abundance of invertebrate natural enemies in sustainable agroecosystems. In: Shiomi M, Koizumi H (eds) Structure and function in agroecosystem design and management. CRC Press, New York, pp 167–182

    Google Scholar 

  • Amano H, Ishii Y, Kobori Y (2004) Pesticide susceptibility of two dominant phytoseiid mites, Neoseiulus californicus and N. womersleyi, in conventional Japanese fruit orchards (Gamasina: Phytoseiidae). J Acarol Soc Jpn 13:65–70

    Article  Google Scholar 

  • Beers EH, Schmidt RA (2014) Impacts of orchard pesticides on Galendromus occidentalis: lethal and sublethal effects. Crop Prot 56:16–24

    Article  CAS  Google Scholar 

  • Beers EH, Brunner JF, Willet MJ, Warner GM (eds) (1993) Orchard pest management: a resource book for the Pacific Northwest. Good Fruit Grower, Yakima, WA. http://jenny.tfrec.wsu.edu/opm/

  • Beers EH, Brunner JF, Dunley JE, Doerr M, Granger K (2005) Role of neonicotinyl insecticides in Washington apple integrated pest management. Part II. Nontarget effects on integrated mite control. J Insect Sci 5:16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Braks MAH, Honorio NA, Lounibos LP, Lourenco-de-Oliveira R, Juliano SA (2004) Interspecific competition between two invasive species of container mosquitoes, Aedes aegypti and Aedes albopictus (Diptera: Culicidae), in Brazil. Ann Entomol Soc Am 97:130–139

    Article  Google Scholar 

  • Brown JK, Frohlich DR, Rosell RC (1995) The sweetpotato or silverleaf whiteflies: biotypes of Bemisia tabaci or species complex? Annu Rev Entomol 40:511–534

    Article  CAS  Google Scholar 

  • Chu D, Wan FH, Zhang YJ, Brown JK (2010) Change in the biotype composition of Bemisia tabaci in Shandong Province of China from 2005 to 2008. Environ Entomol 39:1028–1036

    Article  PubMed  Google Scholar 

  • DeBach PE (1966) The competitive displacement and coexistence principles. Annu Rev Entomol 11:183–212

    Article  Google Scholar 

  • Dennehy T, Degain B, Harpold V, Zaborac M, Morin S et al (2010) Extraordinary resistance to insecticides reveals exotic Q Biotype of Bemisia tabaci in the New World. J Econ Entomol 103:2174–2176

    Article  CAS  PubMed  Google Scholar 

  • Fungicide Resistance Action Committee (FRAC) (2016) FRAC Code List ©*2016: fungicides sorted by mode of action. http://www.frac.info. Accessed 20 Feb 2016

  • Gao Y, Reitz SR, Wei Q, Yu W, Lei Z (2012) Insecticide-mediated apparent displacement between two invasive species of leafminer fly. PLoS ONE 7:e36622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gotoh T, Akizawa T, Watanabe M, Tsuchiya A, Shimazaki S (2005) Cold hardiness of Neoseiulus californicus and N. womersleyi (Acari: Phytoseiidae). J Acarol Soc Jpn 14:93–103

    Article  Google Scholar 

  • Gotoh T, Hanawa M, Shimazaki S, Yokoyama N, Fu C-Q, Sugawara R, Yano S (2014) Factors determining species displacement of related predatory mite species (Acari: Phytoseiidae). Exp Appl Acarol 63:205–215

    Article  PubMed  Google Scholar 

  • Gröning J, Lücke N, Finger A, Hochkirch A (2007) Reproductive interference in two ground-hopper species: testing hypotheses of coexistence in the field. Oikos 116:1449–1460

    Article  Google Scholar 

  • Hochkirch A, Gröning J, Bücker A (2007) Sympatry with the devil: reproductive interference could hamper species coexistence. J Anim Ecol 76:633–642

    Article  PubMed  Google Scholar 

  • Hogmire HW, Brown MW, Schmitt JJ, Winfield TM (1992) Population development and insecticide susceptibility of apple aphid and spirea aphid (Homoptera: Aphididae) on apple. J Entomol Sci 27:113–119

    Google Scholar 

  • Horowitz AR, Denholm I, Gorman K, Cenis JL, Kontsedalov S, Ishaaya I (2003) Biotype Q of Bemisia tabaci identified in Israel. Phytoparasitica 31:94–98

    Article  Google Scholar 

  • Horowitz AR, Kontsedalov S, Khasdan V, Ishaaya I (2005) Biotypes B and Q of Bemisia tabaci and their relevance to neonicotinoid and pyriproxyfen resistance. Arch Insect Biochem Physiol 58:216–225

    Article  CAS  PubMed  Google Scholar 

  • Insecticide Resistance Action Committee (IRAC) (2015) Mode of action classification 2015. Version 8. http://www.irac-online.org. Accessed 20 Feb 2016

  • Izawa H, Fuji K, Matoba T (2000) Control of multiple species of Lepidopterous insect pests using a mating disruptor and reduced pesticide applications in Japanese pear orchards. Jpn J Appl Entomol Zool 44:165–171. (in Japanese)

  • Ji J, Zhang Y-X, Wang J, Lin J-Z, Sun L, Chen X, Ito K, Saito Y (2015) Can the predatory mites Amblyseius swirskii and Amblyseius eharai reproduce by feeding solely upon conspecific or heterospecific eggs (Acari: Phytoseiidae)? Appl Entomol Zool 50:149–154

    Article  CAS  Google Scholar 

  • Kishimoto H (2002) Species composition and seasonal occurrence of spider mites (Acari: Tetranychidae) and their predators in Japanese pear orchards with different agrochemical spraying programs. Appl Entomol Zool 37:603–615

    Article  Google Scholar 

  • Lowery DT, Smirle MJ, Foottit RG, Beers EH (2006) Susceptibilities of apple aphid and spirea aphid collected from apple in the Pacific Northwest to selected insecticides. J Econ Entomol 99:1369–1374

    Article  CAS  PubMed  Google Scholar 

  • Luo C, Jones CM, Devone G, Zhang F, Denholm I, Gorman K (2010) Insecticide-resistance in Bemisia tabaci biotype-Q from China. Crop Prot 29:429–434

    Article  CAS  Google Scholar 

  • McMurtry JA, De Moraes GJ, Sourassou NF (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst Appl Acarol 18:297–320

    Article  Google Scholar 

  • Mochizuki M (1990) A strain of the predatory mite Amblyseius longispinosus (Evans) resistant to permethrin, developing in the tea plantation of Shizuoka Prefecture (Acarina: Phytoseiidae). Jpn J Appl Entomol Zool 34:171–174. (in Japanese)

  • Palevsky E, Gerson E, Zhang Z-Q (2013) Can exotic phytoseiids be considered ‘wanted invaders’ in perennial cropping systems? Exp Appl Acarol 59:11–26

    Article  PubMed  Google Scholar 

  • Parrella MP, Keil CB, Morse JG (1984) Insecticide resistance in Liriomyza trifolii. Calif Agric 38:22–23

    Google Scholar 

  • Rao Q, Xu YH, Luo C, Zhang HY, Jones CM, Devine GJ, Gorman K, Denholm I (2012) Characterisation of neonicotinoid and pymetrozine resistance in strains of Bemisia tabaci (Hemiptera: Aleyrodidae) from China. J Integ Agr 11:321–326

    Article  CAS  Google Scholar 

  • Reitz SR, Trumble JT (2002) Competitive displacement among insects and arachnids. Annu Rev Entomol 47:435–465

    Article  CAS  PubMed  Google Scholar 

  • Schausberger P (2003) Cannibalism among phytoseiid mites: a review. Exp Appl Acarol 29:173–191

    Article  PubMed  Google Scholar 

  • Schausberger P, Walzer A (2001) Combined versus single species release of predaceous mites: predator–predator interactions and pest suppression. Biol Control 20:269–278

    Article  Google Scholar 

  • Schmidt-Jeffris RA, Beers EH (2015) Comparative biology and pesticide susceptibility of Amblydromella caudiglans and Galendromus occidentalis as spider mite predators in apple orchards. Exp Appl Acarol 67:35–47

    Article  CAS  PubMed  Google Scholar 

  • Sun D-B, Liu Y-Q, Qin L, Xu J, Li F-F, Liu S-S (2013) Competitive displacement between two invasive whiteflies: insecticide application and host plant effects. Bull Entomol Res 103:344–353

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Osawa N, Nishida T (2012) Asymmetric reproductive interference between specialist and generalist predatory ladybirds. J Anim Ecol 81:1077–1085

    Article  Google Scholar 

  • Szczepaniec A, Creary SF, Laskowski KL, Nyrop JP, Raupp MJ (2011) Neonicotinoid insecticide imidacloprid causes outbreaks of spider mites on elm trees in urban landscapes. PLoS ONE 6:e20018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsueda H, Tsuchida K (2011) Reproductive differences between Q and B whiteflies, Bemisia tabaci, on three host plants and negative interactions in mixed cohorts. Entomol Exp Appl 141:197–207

    Article  Google Scholar 

  • Wakabayashi H (2000) Utilization of predacious phytoseiid mites in control of spider mites on fruit trees in Nagano prefecture. Jpn Agric Technol (Kongetsu-no-nogyo) 44(5):113–119 (in Japanese)

    Google Scholar 

  • Wang ZY, Yan HF, Yang YH, Wu YD (2010) Biotype and insecticide resistance status of the whitefly Bemisia tabaci from China. Pest Manag Sci 66:1360–1366

    Article  CAS  PubMed  Google Scholar 

  • Yuan LZ, Wang SL, Zhou JC, Du YZ, Zhang YJ, Wang JJ (2012) Status of insecticide resistance and associated mutations in Q-biotype of whitefly, Bemisia tabaci, from eastern China. Crop Prot 31:67–71

    Article  Google Scholar 

  • Zhang Y-X, Ji J, Lin J-Z, Chen X, Saito Y (2014) Female performance towards offspring under starved conditions in four phytoseiid species (Acari: Phytoseiidae). Exp Appl Acarol 65:29–41

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Koichi Goka (NIAES), Dr. Yasuki Kitashima (Ibaraki University) and Mr. Reo Sugawara (Ibaraki University) for their valuable suggestions on this study. We are also thankful to Dr. Hirotsuna Hoshi (Fukushima Agricultural Technology Center) for providing us with useful information.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tetsuo Gotoh.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ullah, M.S., Hanawa, M. & Gotoh, T. Pesticide-mediated displacement of a phytoseiid predator, Neoseiulus womersleyi, by another phytoseiid predator, N. californicus (Acari: Phytoseiidae). Exp Appl Acarol 69, 453–464 (2016). https://doi.org/10.1007/s10493-016-0053-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10493-016-0053-2

Keywords

Navigation