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Efficacy of indigenous predatory mites (Acari: Phytoseiidae) against the citrus rust mite Phyllocoptruta oleivora (Acari: Eriophyidae): augmentation and conservation biological control in Israeli citrus orchards

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Abstract

The citrus rust mite (CRM), Phyllocoptruta oleivora (Acari: Eriophyidae) is a cosmopolitan key pest of citrus, inflicting severe economic damage if not controlled. In Israel, CRM damages all citrus cultivars. International regulation and increasing control failures of CRM led growers to seek sustainable biological control solutions such as acarine biological control agents. Laboratory studies conducted in Israel have indicated that the indigenous predator species Amblyseius swirskii, Iphiseius degenerans, Typhlodromus athiasae and Euseius scutalis (all Acari: Phytoseiidae) can potentially control CRM. Our general objective in the present study was to bridge the gap of knowledge between laboratory studies and the lack of control efficacy of these species in commercial orchards. Predator augmentation in the field showed that although predator populations increased immediately following releases they later decreased and did not affect CRM populations. When A. swirskii augmentation was combined with a series of maize pollen applications, A. swirskii populations were enhanced substantially and continuously but again CRM populations were not affected. Growth chamber studies with CRM-infested seedlings, with or without a maize pollen supplement, indicated that pollen provisioning led to population increase of E. scutalis and A. swirskii but only E. scutalis significantly lowered CRM populations. Control with E. scutalis was confirmed in the field on CRM infested seedlings with pollen provisioned by adjacent flowering Rhodes grass. While experiments in mature citrus orchard showed that pollen supplement usually increased predator populations they also indicated that other factors such as intraguild interactions and pesticide treatments should be taken into account when devising CRM biological control programs.

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References

  • Altieri MA (1999) The ecological role of biodiversity in agroecosystems. Agr Ecosyst Environ 74:19–31

    Article  Google Scholar 

  • Argov Y, Amitai S, Beattie GAC, Gerson U (2002) Rearing, release and establishment of imported predatory mites to control citrus rust mite in Israel. Biocontrol 47:399–409

    Article  Google Scholar 

  • Childers CC (1994) Biological control of phytophagous mites on Florida citrus utilizing predatory arthropods. Pest management in the subtopics, biological control: a Florida perspective, 1st edn. Intercept Ltd., Andover, pp 255–288

    Google Scholar 

  • Conover WJ, Iman RL (1981) Rank transformations as a bridge between parametric and nonparametric statistics. Am Stat 35:124–129

    Google Scholar 

  • EU (2009) Establishing a framework for community action to achieve the sustainable use of pesticides. Directive 2009/128/EC of the European Parliament of 21 October 2009. Official Journal of the European Union. Legislation 309:71–86

    Google Scholar 

  • Gan-Mor S, Bechar A, Ronen B, Eisikowitch D, Vaknin Y (2003) Electrostatic pollen applicator development and tests for almond, kiwi, date and pistachio: an overview. Appl Eng Agric 19:119–124

    Google Scholar 

  • Gerson U (2003) Acarine pests of citrus: overview and non-chemical control. Syst Appl Acarol 8:3–12

    Google Scholar 

  • Gerson U, Vacante V (2011) Acari. In: Vacante V, Gerson U (eds) Integrated control of citrus pests in the mediterranean region. Bentham Science Publishers, pp 88–108

  • Gerson U, Smiley RL, Ochoa R (2003) Mites (acari) for pest control. Blackwell Science, Oxford

    Book  Google Scholar 

  • González-Fernández JJ, De la Peña F, 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  Google Scholar 

  • Grafton CE, Ouyang Y, Bugg RL (1999) Leguminous cover crops to enhance population development of Euseius tularensis (Acari: Phytoseiidae) in citrus. Biol Control 16:73–80

    Article  Google Scholar 

  • Hoddle MS, Aponte O, Kerguelen V, Heraty J (1999) Biological control of Oligonychus perseae (Acari: Tetranychidae) on avocado: I. Evaluating release timings, recovery and efficacy of six commercially available phytoseiids. Inter J Acarol 25:211–219

    Article  Google Scholar 

  • Hoddle MS, Robinson L, Virzi J (2000) Biological control of Oligonychus perseae (Acari: Tetranychidae) on avocado: III. Evaluating the efficacy of varying release rates and release frequency of Neoseiulus californicus (Acari: Phytoseiidae). Inter J Acarol 26:203–214

    Article  Google Scholar 

  • Israel Meteorological Service (2014) Long term climate information. Israel Ministry of Transport. http://www.ims.gov.il/IMSEng/CLIMATE/LongTermInfo/. Accessed 3/2/2014

  • JMP® (2007) Version 7, SAS Institute Inc. Cary, NC, 1989–2007

  • Jung CL, Croft BA (2001) Ambulatory and aerial dispersal among specialist and generalist predatory mites (Acari:Phytoseiidae). Environ Entomol 30:1112–1118

    Article  Google Scholar 

  • Kerguelen V, Hoddle MS (1999) Biological control of Oligonychus perseae (Acari: Tetranychidae) on avocado: II. Evaluating the efficacy of Galendromus helveolus and Neoseiulus californicus (Acari: Phytoseiidae). Inter J Acarol 25:221–229

    Article  Google Scholar 

  • Koji S, Khan ZR, Midega CAO (2007) Field boundaries of Panicum maximum as a reservoir for predators and a sink for Chilo partellus. J Appl Entomol 131:186–196

    Article  Google Scholar 

  • Mailloux J, Le Bellec F, Kreiter S, Tixier MS, Dubois P (2010) Influence of ground cover management on diversity and density of phytoseiid mites (Acari: Phytoseiidae) in Guadeloupean citrus orchards. Exp Appl Acarol 52:275–290

    Article  PubMed  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

    Article  Google Scholar 

  • McMurtry JA, Scriven GT (1966) The influence of pollen and prey density on the number of prey consumed by Amblyseius hibisci (Acarina: Phytoseiidae). Ann Entomol Soc Am 59:147–149

    Google Scholar 

  • Messelink GJ, Van Maanen R, Van Holstein-Saj R, Sabelis MW, Janssen A (2010) Pest species diversity enhances control of spider mites and whiteflies by a generalist phytoseiid predator. Biocontrol 55:387–398

    Article  Google Scholar 

  • Momen F, Abdel-Khalek A (2009) Cannibalism and intraguild predation in the phytoseiid mites Typhlodromips swirskii, Euseius scutalis and Typhlodromus athiasae (Acari: Phytoseiidae). Acarina 17:223–229

    Google Scholar 

  • Nomikou M, Janssen A, Schraag R, Sabelis MW (2002) Phytoseiid predators suppress populations of Bemisia tabaci on cucumber plants with alternative food. Exp Appl Acarol 27:57–68

    Article  PubMed  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 

  • Palevsky E, Argov Y, Ben David T, Gerson U (2003) Identification and evaluation of potential predators of citrus rust mite. Syst Appl Acarol 8:39–48

    Google Scholar 

  • Park HH, Shipp L, Buitenhuis R, Ahn JJ (2011) Life history parameters of a commercially available Amblyseius swirskii (Acari: Phytoseiidae) fed on cattail (Typha latifolia) pollen and tomato russet mite (Aculops lycopersici). J Asia-Pacific Entomol 14:497–501

    Article  Google Scholar 

  • Porath A, Swirski E (1965) A survey of phytoseiid mites (Acarina: Phytoseiidae) on citrus, with a description of one new species. Israel J Agric Res 15:87–100

    Google Scholar 

  • Raworth DA, Fauvel G, Auger P (1994) Location, reproduction and movement of Nesoseiulus californicus (Acari: Phytoseiidae) during the autumn, winter and spring in orchards in the south of France. Exp Appl Acarol 18:593–602

    Article  Google Scholar 

  • Reddi CS, Reddi NS (1986) Pollen production in some anemophilous angiosperms. Grana 25:55–61

    Article  Google Scholar 

  • Rubin A (1969) Observations on the biology of the Israeli predacious mite, Iphiseius degenerans Berlese in the laboratory, comparing feeding habits in the citrus orchard and on castor bean. Proc Pacific Branch Ent Soc Am 53:29–30

    Google Scholar 

  • Smith D, Papacek DF (1991) Studies of the predatory mite Amblyseius victoriensis (Acarina: Phytoseiidae) in citrus orchards in south-east Queensland: control of Tegolophus australis and Phyllocoptruta oleivora (Acarina: Eriophyidae), effect of pesticides, alternative host plants and augmentative release. Exp Appl Acarol 12:195–217

    Article  CAS  Google Scholar 

  • Swirski E (1977) Integrated control of mites in Israel. Int Cong Cit 2:477–480

    Google Scholar 

  • Swirski E, Amitai S, Dorzia N (1967a) Laboratory studies on the feeding, development and oviposition of the predaceous mite Typhlodromus athiasae P. and S. (Acarina: Phytoseiidae) on various kinds of food substances. Israel J Agric Res 17:213–218

    Google Scholar 

  • Swirski E, Amitai S, Dorzia N (1967b) Laboratory studies on the feeding, development and reproduction of the predaceous mites Amblyseius rubini Swirski and Amitai and Amblyseius swirski Athias (Acarina: Phytoseiidae) on various kinds of food substances. Israel J Agric Res 17:101–119

    Google Scholar 

  • van Rijn PCJ, Tanigoshi LK (1999a) 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, Tanigoshi LK (1999b) 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

    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 

  • Walklate PJ (1992) A simulation study of pesticide drift from an air-assisted orchard sprayer. Agric Eng Res 51:263–283

    Article  Google Scholar 

  • Yothers WW, Mason AC (1938) The citrus rust mite and its control. US Dep Agric Tech Bull 176:1–16

    Google Scholar 

Download references

Acknowledgments

We extend our gratitude to the growers of (from South to North) Shibolim, Yesodot, Hadera, Gan Shmuel, Beit She’arim and Beit Ha’emek for their cooperation. We thank Jonathan Abrahams, Shmuel Gross and Benny Ronen for their technical support. We would like to thank Bio-Bee, Israel, and especially Shimon Steinberg, Yehoshua Kaminsky and Arnon Alouche for their cooperation, collaboration and for supplying some of the materials and mites needed for this study. We express our gratitude to Dr. Hillary Voet for her statistical guidance. This work was supported by the Israeli Plant Production and Marketing Board and the Chief Scientist of the Israeli Ministry of Agriculture, research projects 864-0045-08 and 131-1093-03. This manuscript is a contribution of the Institute of Plant Protection, Volcani Center, ARO, Israel.

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Correspondence to Eric Palevsky.

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Maoz, Y., Gal, S., Argov, Y. et al. Efficacy of indigenous predatory mites (Acari: Phytoseiidae) against the citrus rust mite Phyllocoptruta oleivora (Acari: Eriophyidae): augmentation and conservation biological control in Israeli citrus orchards. Exp Appl Acarol 63, 295–312 (2014). https://doi.org/10.1007/s10493-014-9786-y

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