Skip to main content
Log in

Does pollen availability mitigate the impact of pesticides on generalist predatory mites?

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The effect of the provision of pollen on the impact of pesticides on the predatory mite Kampimodromus aberrans was assessed at individual and population levels. In the laboratory we evaluated the influence of pollen amount and pollen application frequency on lethal and sub-lethal effects of chlorpyrifos and spinosad. In a potted plant experiment, the effects of pesticides and pollen were assessed on predatory mite population abundance. In the laboratory, survival and fecundity of predatory mites were reduced by insecticides, and spinosad was more toxic than chlorpyrifos. In the same experiment, high pollen application frequency alleviated the sub-lethal effect induced by chlorpyrifos. On potted plants, pollen applications reduced the impact of chlorpyrifos on K. aberrans, whereas without pollen applications the impact of spinosad and chlorpyrifos on the predatory mite population was similar. Results obtained here highlight that the provision of fresh pollen is of particular importance for predatory mites when pesticides are applied.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adar E, Inbar M, Gal S, Doron N, Zhang ZQ, Palevsky E (2012) Plant-feeding and non-plant feeding phytoseiids: differences in behavior and cheliceral morphology. Exp Appl Acarol 58:341–357

    Article  PubMed  Google Scholar 

  • Addison JA, Hardman JM, Walde SJ (2000) Pollen availability for predaceous mites on apple: spatial and temporal heterogeneity. Exp Appl Acarol 24:1–18

    Article  PubMed  CAS  Google Scholar 

  • Aguilar-Fenollosa E, Ibanez-Gual MV, Pascual-Ruiz S, Hurtado M, Jacas JA (2011a) Effect of ground-cover management on spider mites and their phytoseiid natural enemies in clementine mandarin orchards (II): top-down regulation mechanisms. Biol Control 59:171–179

    Article  Google Scholar 

  • Aguilar-Fenollosa E, Pascual-Ruiz S, Hurtado MA, Jacas JA (2011b) Efficacy and economics of ground cover management as a conservation biological control strategy against Tetranychus urticae in clementine mandarin orchards. Crop Prot 30:1328–1333

    Article  Google Scholar 

  • Ahmad S, Pozzebon A, Duso C (2013) Augmentative releases of the predatory mite Kampimodromus aberrans in organic and conventional apple orchards. Crop Prot 52:47–56

    Article  Google Scholar 

  • Bakker FM, Jacas JA (1995) Pesticides and phytoseiid mites: strategies for risk assessment. Ecotox Environ Safe 32:58–67

    Article  CAS  Google Scholar 

  • Baldessari M, Angeli G, Girolami V, Cross J, Ioriatti C (2005) Effects of plant protection products on Kampimodromus aberrans (Oudemans): the dietary effect of airborne pollen. IOBC/WPRS Bull 28:151–155

    Google Scholar 

  • Bale JS, van Lenteren JC, Bigler F (2008) Biological control and sustainable food production. Philos Trans R Soc B-Biol Sci 363:761–776

    Article  CAS  Google Scholar 

  • Banken JAO, Stark JD (1991) Multiple routes of pesticide exposure and the risk of pesticides to biological controls: a study of neem and the sevenspotted lady beetle (Coleoptera: Coccinellidae). J Econ Entomol 91:1–6

    Google Scholar 

  • Begum M, Gurr GM, Wratten SD, Hedberg PR, Nicol HI (2006) Using selective food plants to maximize biological control of vineyard pests. J Appl Ecol 43:547–554

    Article  Google Scholar 

  • Bernard MB, Cole P, Kobelt A, Horne PA, Altmann J, Wratten SD, Yen AL (2010) Reducing the impact of pesticides on biological control in Australian vineyards: pesticide mortality and fecundity effects on an indicator species, the predatory mite Euseius victoriensis (Acari: Phytoseiidae). J Econ Entomol 103:2061–2071

    Article  PubMed  CAS  Google Scholar 

  • Bostanian NJ, Goulet H, O’Hara J, Masner L, Racette G (2004) Towards insecticide free apple orchards: flowering plants to attract beneficial arthropods. Biocontrol Sci Technol 14:25–37

    Article  Google Scholar 

  • Broufas GD, Pappas ML, Koveos DS (2007) Development, survival, and reproduction of the predatory mite Kampimodromus aberrans (Acari: Phytoseiidae) at different constant temperatures. Environ Entomol 36:657–665

    Article  PubMed  CAS  Google Scholar 

  • Candolfi MP, Bakker F, Canez V, Miles M, Neumann C, Pilling E, Primiani M, Romijn K, Schmuck R, Storck-Weyhermuller S, Ufer A, Waltersdorfer A (1999) Sensitivity of non-target arthropods to plant protection products: could Typhlodromus pyri and Aphidius spp be used as indicator species. Chemosphere 39:1357–1370

    Article  CAS  Google Scholar 

  • Candolfi M, Barrett K, Campbell P, Forster R, Grandy N, Huet M-C, Lewis G, Oomen P, Schmuck R, Vogt H (2000) Guidance document on regulatory testing procedures for pesticides with non-target arthropods ESCORT Workgroup, Wageningen, The Netherlands 2000. Society of Environmental Toxicology And Chemistry - Europe (SETAC)

  • Croft BA (1990) Arthropod biological control agents and pesticides. Wiley Interscience, New York, USA

  • Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    Article  PubMed  CAS  Google Scholar 

  • Duso C (1989) Role of Amblyseius aberrans (Oud), Typhlodromus pyri Scheuten and Amblyseius andersoni (Chant) in vineyards: I. The effects of single or mixed phytoseiid population releases on spider mite densities. J Appl Entomol 107:474–492

  • Duso C, Camporese P (1991) Developmental times and oviposition rates of predatory mites Typhlodormus pyri and Amblyseius andersoni (Acari, Phytoseiidae) reared on different foods. Exp Appl Acarol 13:117–128

    Article  Google Scholar 

  • Duso C, Malagnini V, Paganelli A, Aldegheri L, Bottini M, Otto S (2004) Pollen availability and abundance of predatory phytoseiid mites on natural and secondary hedgerows. BioControl 49:397–415

    Article  Google Scholar 

  • Duso C, Fanti M, Pozzebon A, Angeli G (2009) Is the predatory mite Kampimodromus aberrans a candidate for the control of phytophagous mites in European apple orchards? BioControl 54:369–382

    Article  Google Scholar 

  • Duso C, Castagnoli M, Simoni S, Angeli G (2010) The impact of eriophyoids on crops: recent issues on Aculus schlechtendali, Calepitrimerus vitis and Aculops lycopersici. Exp Appl Acarol 51:151–168

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Fernandez J, de LP, Hormaza JI, Boyero JR, Vela JM, Wong E, Trigo MM, Montserrat M (2009) Alternative food improves the combined effect of an omnivore and a predator on biological pest control a case study in avocado orchards. Bull Entomol Res 99:433–444

    Article  PubMed  CAS  Google Scholar 

  • Isaacs R, Tuell J, Fiedler A, Gardiner M, Landis D (2009) Maximizing arthropod-mediated ecosystem services in agricultural landscapes: the role of native plants. Front Ecol Environ 7:196–203

    Article  Google Scholar 

  • Jonsson M, Wratten SD, Landis DA, Gurr GM (2008) Recent advances in conservation biological control of arthropods by arthropods. Biol Control 45:172–175

    Article  Google Scholar 

  • Kasap I (2005) Life-history of the predaceous mite Kampimodromus aberrans (Oudemans) (Acarina: Phytoseiidae) on four different types of food. Biol Control 35:40–45

  • Kreiter S, Tixier MS, Croft BA, Auger P, Barret D (2002) Plants and leaf characteristics influencing the predaceous mite Kampimodromus aberrans (Acari : Phytoseiidae) in habitats surrounding vineyards. Environ Entomol 31:648–660

    Article  Google Scholar 

  • Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201

    Article  PubMed  CAS  Google Scholar 

  • Lee JC, Menalled FB, Landis DA (2001) Refuge habitats modify impact of insecticide disturbance on carabid beetle communities. J Appl Ecol 38:472–483

    Article  Google Scholar 

  • Lester PJ, Thistlewood HMA, Harmsen R (1998) The effects of refuge size and number on acarine predator-prey dynamics in a pesticide-disturbed apple orchard. J Appl Ecol 35:323–331

    Article  Google Scholar 

  • Littell RC, Henry PR, Ammerman CJ (1998) Statistical analysis of repeated measures data using SAS procedures. J Animal Sci 76:1216–1231

    CAS  Google Scholar 

  • Lorenzon M, Pozzebon A, Duso C (2012) Effects of potential food sources on biological and demographic parameters of the predatory mites Kampimodromus aberrans, Typhlodromus pyri and Amblyseius andersoni. Exp Appl Acarol 58:259–278

    Article  PubMed  Google Scholar 

  • Lundgren JG (2009) Relationships of natural enemies and non-prey foods. Springer, Dordrecht, The Netherlands

  • Malison M (1996) Influence of the measurement unit of populations in density dependent fecundity studies of the predatory mite Amblyseius aberrans (Oud) (Acarina, Phytoseiidae). J Appl Entomol-Zeitschr Angew Entomol 120:1–6

    Article  Google Scholar 

  • Maoz Y, Gal S, Argov Y, Coll M, Palevsky E (2011) Biocontrol of persea mite, Oligonychus perseae, with an exotic spider mite predator and an indigenous pollen feeder. Biol Control 59:147–157

  • McMurtry JA, Croft BA (1997) Life-styles of phytoseiid mites and their role in biological control. Annu Rev Entomol 42:291–321

    Article  PubMed  CAS  Google Scholar 

  • Montserrat M, Guzmán C, Sahún RM, Belda JE, Hormaza JI (2012) Pollen supply promotes, but high temperatures demote, predatory mite abundance in avocado orchards. Agric Ecosyst Environ 164:155–161

    Article  Google Scholar 

  • Nomikou M, Sabelis MW, Janssen A (2010) Pollen subsidies promote whitefly control through the numerical response of predatory mites. BioControl 55:253–260

    Article  Google Scholar 

  • Ozman-Sullivan SK (2006) Life history of Kampimodromus aberrans as a predator of phytoptus avellanae (Acari: Phytoseiidae, Phytoptidae). Exp Appl Acarol 38:15–23

  • Pozzebon A, Duso C (2008) Grape downy mildew Plasmopara viticola, an alternative food for generalist predatory mites occurring in vineyards. Biol Control 45:441–449

    Article  Google Scholar 

  • Pozzebon A, Duso C, Pavanetto E (2002) Side effects of some fungicides on phytoseiid mites (Acari, Phytoseiidae) in north-Italian vineyards. Anz Schädlingsk-J Pest Sci 75:132–136

    Article  Google Scholar 

  • Pozzebon A, Loeb GM, Duso C (2009) Grape powdery mildew as a food source for generalist predatory mites occurring in vineyards: effects on life-history traits. Ann Appl Biol 155:81–89

    Article  Google Scholar 

  • Pozzebon A, Borgo M, Duso C (2010) The effects of fungicides on non-target mites can be mediated by plant pathogens. Chemosphere 79:8–17

    Article  PubMed  CAS  Google Scholar 

  • Pozzebon A, Duso C, Tirello P, Ortiz PB (2011) Toxicity of thiamethoxam to Tetranychus urticae Koch and Phytoseiulus persimilis Athias-Henriot (Acari Tetranychidae, Phytoseiidae) through different routes of exposure. Pest Manag Sci 67:352–359

    Article  PubMed  CAS  Google Scholar 

  • Sabelis MW (1985) Predation on spider mites. In: Helle W, Sabelis MW (eds) Spider mites: their biology, natural enemies and control, world crop pests, vol 1B. Elsevier, Amsterdam, The Netherlands, pp 103–127

  • Schausberger P (1992a) Investigations on the influence of the predator population density on the rate of oviposition in Amblyseius finlandicus Oud. (Acari, Phytoseiidae). Anz. Schädlingsk Pflanzensch Umweltsch 65:36–39

    Article  Google Scholar 

  • Schausberger P (1992b) Vergleichende untersuchungen über den einfluss unterschiedlicher nahrung aud die präimaginalentwicklung und die reproduktion von Amblyseius aberrans oud und Amblyseius finlandicus oud (Acarina, Phytoseiidae). J Appl Entomol 113:476–486

    Article  Google Scholar 

  • Stark JD, Banks JE, Vargas R (2004) How risky is risk assessment: the role that life history strategies play in susceptibility of species to stress. Proc Natl Acad Sci USA 101:732–736

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Steinmann KP, Zhang MH, Grant JA (2011) Does use of pesticides known to harm natural enemies of spider mites (Acari: tetranychidae) result in increased number of miticide applications? an examination of California walnut orchards. J Econ Entomol 104:1496–1501

    Article  PubMed  Google Scholar 

  • Sterk G, Hassan SA, Baillod M, Bakker F, Bigler F, Blumel S, Bogenschutz H, Boller E, Bromand B, Brun J, Calis JNM, Coremans-Pelseneer J, Duso C, Garrido A, Grove A, Heimbach U, Hokkanen H, Jacas J, Lewis G, Moreth L, Polgar L, Roversti L, Samsoe-Peterson L, Sauphanor B, Schaub L, Staubli A, Tuset JJ, Vainio A, van de Veire M, Viggiani G, Vinuela E, Vogt H (1999) Results of the seventh joint pesticide testing programme carried out by the IOBC/WPRS-Working Group ‘Pesticides and Beneficial Organisms’. BioControl 44:99–117

  • Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594

    Article  PubMed  CAS  Google Scholar 

  • Thio BJR, Clark KK, Keller AA (2011) Magnetic pollen grains as sorbents for facile removal of organic pollutants in aqueous media. J Hazard Mater 194:53–61

    Article  PubMed  CAS  Google Scholar 

  • Thompson GD, Dutton R, Sparks TC (2000) Spinosad—a case study: an example from a natural products discovery programme. Pest Manag Sci 56:696–702

    Article  CAS  Google Scholar 

  • Tirello P, Pozzebon A, Duso C (2012) Resistance to chlorpyriphos in the predatory mite Kampimodromus aberrans. Exp Appl Acarol 56:1–8

    Article  PubMed  Google Scholar 

  • Tirello P, Pozzebon A, Duso C (2013) The effect of insecticides on the non-target predatory mite Kampimodromus aberrans: laboratory studies. Chemosphere 93:1139–1144

    Article  PubMed  CAS  Google Scholar 

  • Tixier MS, Kreiter S, Auger P (2002) Colonization of vineyards by Kampimodromus aberrans (Oudemans) (Acari Phytoseiidae): dispersal from surrounding plants as indicated by random amplified polymorphism DNA typing. Agric For Entomol 4:225–264

    Article  Google Scholar 

  • Tsolakis H, Ragusa E, Ragusa Di Chiara S (2000) Distribution of phytoseiid mites (Parasitiformes, Phytoseiidae) on hazelnut at two different altitudes in Sicily (Italy). Environ Entomol 29:1251–1257

    Article  Google Scholar 

  • van Rijn PCJ, Tanigoshi LK (1999a) Pollen as food for the predatory mites Iphiseius degenerans and Neoseiulus cucumeris (Acari: phytoseiidae): dietary range and life history. Exp Appl Acarol 23:785–802

  • van Rijn PCJ, Tanigoshi LK (1999b) 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 

  • van Rijn PCJ, van Houten YM, Sabelis MW (2002) How plants benefit from providing food to predators even when it is also edible to herbivores. Ecology 83:2664–2679

    Article  Google Scholar 

  • Vanbilsen D, Hoekstra FA (1993) Decreased membrane integrity in aging Typha latifolia L pollen-accumulation of lysolipids and free fatty-acids. Plant Physiol 101:675–682

    CAS  Google Scholar 

  • Villa S, Vighi M, Finizio A, Serini GB (2000) Risk assessment for honeybees from pesticide-exposed pollen. Ecotoxicology 9:287–297

    Article  CAS  Google Scholar 

  • Wäckers FL (2005) Suitability of (extra-) floral nectar, pollen, and honeydew as insect food sources. In: Wäckers FL, van Rijn PCJ, Bruin J (eds) Plant-provided food for carnivorous insects. Cambridge University Press, Cambridge, UK, pp 17–74

  • Wade MR, Zalucki MP, Wratten SD, Robinson KA (2008) Conservation biological control of arthropods using artificial food sprays: current status and future challenges. Biol Control 45:185–199

    Article  Google Scholar 

Download references

Acknowledgments

This study has been supported by PRIN projects and Treviso province. We thank Virna Klaric for the support in laboratory trials. We also thank V. Girolami, M. Baldessari, G. Angeli and V. Malagnini for insightful discussions in an early stage of the study. We thank Patrick De Clercq, Dirk Babendreier and two anonymous reviewers for comments that improved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alberto Pozzebon.

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

Pozzebon, A., Ahmad, S., Tirello, P. et al. Does pollen availability mitigate the impact of pesticides on generalist predatory mites?. BioControl 59, 585–596 (2014). https://doi.org/10.1007/s10526-014-9598-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-014-9598-3

Keywords

Navigation