Improving the compatibility of pesticides and predatory mites: recent findings on physiological and ecological selectivity

https://doi.org/10.1016/j.cois.2020.03.005Get rights and content

Highlights

  • • New approaches have been proposed in the evaluation of pesticide selectivity toward natural enemies, in particular predatory mites.

  • • Predatory mites (i.e. phytoseiids) can become resistant to pesticides by mainly detoxification but also target-site mutations.

  • • Some recently developed acaricides show a natural differential affinity for the target-site between spider mites and phytoseiids.

  • • Pesticide-free refuges and pesticide-treated nets increase the compatibility of pesticides with phytoseiids.

  • • Providing alternative foods can reduce the impact of pesticides on phytoseiids.

Integrated pest management relies upon the application of selective pesticides that do not hinder biological control. Phytoseiid mites represent an interesting case-study: they are amongst the most frequently used biological control agents and often are less affected by pesticides than their prey by natural tolerance or by developing resistance. The selectivity of a pesticide is determined by physiological processes that include metabolism, transport, and the affinity to the target-site. Genomic and transcriptomic studies start to elucidate the genetic and molecular mechanisms of differential toxicity in some phytoseiid species, such as a mutation in the sodium channel conferring pyrethroid resistance. Ecological selectivity is achieved by smart applications of pesticides and management practices that influence the persistence of phytoseiid mites on plants. Although modern pesticides often show lower acute toxicity, there is a need for robust assays and procedures that quantify lethal and sublethal effects, through different routes and times of exposure.

Introduction

The compatibility between pesticides and biological control agents (BCA) is a major concern in agriculture, particularly in perennial crop systems where pest management programs can change rapidly, causing concerns for Integrated Pest Management (IPM) practitioners. In an attempt to reduce the impact on human health and the environment, broad-spectrum pesticides have been widely replaced by reduced-risk pesticides in many regions worldwide. This innovation has led to an overall positive effect on IPM and conservation biological control [1, 2, 3]. However, even if the evolution of more selectivity is evident in modern crop protection chemistry, some of the reduced-risk insecticides are still harmful to BCA [4, 5, 6]. Also, in organic crop systems, the selectivity of some natural pesticides proved to be lower than anticipated [7,8].

The aim to drastically reduce pesticide use is a priority in several countries, but many factors may impede achieving this objective. For example, recent issues with invasive pests such as the brown marmorated stink bug Halyomorpha halys in America and Europe promoted insecticide use, disrupting IPM in fruit orchards [9]. Secondly, alternatives to fungicides, such as bio-pesticides are promising [10], but their implementation remains limited, and extensive use of non-selective fungicides negatively affects BCA [1,11]. Very little is known whether other plant protection products (e.g. herbicides) may influence BCA [12].

Mesostigmatid predators (Acari Mesostigmata) are common in agricultural systems where they regulate population densities of arthropod and nematode pests. There is worldwide interest in the ecosystem services they provide, and the identification of new biological control agents (BCA), and their use as alternatives to pesticides is still a hot topic [13]. The family Phytoseiidae is the most studied within the Mesostigmata (89% of papers using the keyword ‘predatory mites’ in Scopus, URL: https://www.scopus.com) and several phytoseiid species are key-predators of spider mites, thrips, and whiteflies. Studies on phytoseiid biology, ecology, and behavior continue to increase in number. However, how pesticides affect phytoseiid persistence in crop systems and their efficiency to control pests remains poorly investigated.

Interestingly, several phytoseiid species became indicator species in ecotoxicological studies for regulatory purposes [14], but there is no agreement on how best to assess and evaluate pesticide effects on phytoseiids. Here, current trends in the evaluation of pesticide effects on phytoseiids are analyzed, together with factors determining the compatibility between pesticides and phytoseiids, focusing on ecological and physiological selectivity.

Section snippets

How to test pesticide effects on phytoseiids?

When evaluating the selectivity of pesticides on phytoseiids, laboratory tests are most often chosen due to the uncertainty of biotic and abiotic factors acting in the open field [15,16]. However, laboratory procedures do not reproduce the effects of the repeated application of pesticides in a growing season, which commonly occurs with many products (e.g. fungicides). Field tests are considered more realistic for a variety of reasons, that is,: non-perfect coverage (and the presence of

Physiological selectivity

Upon contact, the toxicity of a pesticide to phytoseiids is determined by critical physiological processes, including penetration, activation, metabolism, transport, excretion, and finally affinity for the target-site. These are usually referred to as toxicokinetic and toxicodynamic mechanisms [32] that can determine selectivity.

The metabolization of insecticides and acaricides is not only important as a major detoxification route, but it is also vital for the activation of pro-insecticides

Ecological selectivity and management practices that enhance compatibility

Biological control tactics that are based on ecological selectivity might be exploited to improve the use of compounds that are not physiologically selective but crucial in plant protection. Ecological selectivity can be achieved by limiting the exposure of a BCA to pesticides in time and space [20]. The temporal separation is a primary aspect, and laboratory evaluations have considered the effects of exposure to aged residues under realistic conditions [50,51]. Also, spatial separation between

Conclusions and prospects

The use of pesticides has changed and continues to change today, as products currently applied in various regions in the world often have a lower acute toxicity and improved selectivity compared to those applied in the past. Characterizing the variety of sublethal side-effects makes it possible to delineate the ecotoxicological profile of a pesticide, but this remains challenging. Repellency or reduced prey consumption can be an explanation for the poor correspondence between predator densities

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank two anonymous reviewers and Dr. Sabina Bajda-Wybouw for constructive comments on earlier version of this manuscript. This work was partially funded by DAFNAE University of PadovaBIRD167802, BIRD192381 and DOR to C.D. and A.P. TVL received support from Eranet C-IPM via the Research Foundation Flanders (FWO) (DefDef, G0H4917N) and the Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program [grant 772026-POLYADAPT and 773902-SuperPests].

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