We present a synthetic review and expert consultation that assesses the actual risks posed by arthropod pests in four major crops, identifies targets for integrated pest management (IPM) in terms of cultivated land needing pest control and gauges the implementation “readiness” of non-chemical alternatives. Our assessment focuses on the world’s primary target pests for neonicotinoid-based management: western corn rootworm (WCR, Diabrotica virgifera virgifera) in maize; wireworms (Agriotes spp.) in maize and winter wheat; bird cherry-oat aphid (Rhopalosiphum padi) in winter wheat; brown planthopper (BPH, Nilaparvata lugens) in rice; cotton aphid (Aphis gossypii) and silver-leaf whitefly (SLW, Bemisia tabaci) in cotton. First, we queried scientific literature databases and consulted experts from different countries in Europe, North America, and Asia about available IPM tools for each crop-pest system. Next, using an online survey, we quantitatively assessed the economic relevance of target pests by compiling country-level records of crop damage, yield impacts, extent of insecticide usage, and “readiness” status of various pest management alternatives (i.e., research, plot-scale validation, grower-uptake). Biological control received considerable scientific attention, while agronomic strategies (e.g., crop rotation), insurance schemes, decision support systems (DSS), and innovative pesticide application modes were listed as key alternatives. Our study identifies opportunities to advance applied research, IPM technology validation, and grower education to halt or drastically reduce our over-reliance on systemic insecticides globally.
Neonicotinoid insecticides are extensively used against multiple herbivorous insects in annual crops across the globe (Furlan and Kreutzweiser 2015; Simon-Delso et al. 2015). Their in-field application is primarily preventative and unguided, thus conflicting with globally accepted principles of integrated pest management (IPM) (Furlan et al. 2017a; Kogan 1998; Pedigo and Rice 2014; Barzman et al. 2015). Scant information is available on the actual benefits of these products in terms of crop performance, economic yield or farm-level profit, and the few existing peer-reviewed studies demonstrate how yield benefits of, e.g., neonicotinoid seed coatings are routinely negligible (Bredeson and Lundgren 2015b; Furlan and Kreutzweiser 2015; Bredeson and Lundgren 2015a; Matyjaszczyk et al. 2015; Milosavljević et al. 2019; Furlan et al. 2018). Globally, efforts are being made to reduce farmer reliance on and overuse of chemical pesticides—including applied research, farm-level validation and communication of alternative pest management options (Horgan 2017). For example, in the European Union (EU), Commission Directive 2009/128/EC enables vigilance over the sustainable use of chemically synthesized pesticides, secures a continuing reliance upon IPM, and provides the legal framework to pursue a lasting, far-reaching reduction in the prophylactic usage of systemic insecticides (Furlan et al. 2018). Despite this increased attention, global insecticide use has increased dramatically in recent decades and farmers in multiple countries now favor prophylactic pest management approaches over IPM (Horgan 2017).
Worldwide, neonicotinoids are used to control a wide range of herbivorous insects in broad-acre crops, such as maize (globally cultivated on 171 M ha), wheat (220 M ha), rice (paddy; 162 M ha) and cotton (approximately 33 M ha). As the world’s most widely used insecticides, neonicotinoids currently represent 25% of the global insecticide market (Hladik et al. 2018). One of the key concerns regarding neonicotinoids is their routine, prophylactic use as “convenience” pesticides, i.e., seed coatings, stem dips or drench applications (Mourtzinis et al. 2019). While seed coatings indeed lessen the amount of overspray and drift, the products readily leach into the soil and water phase and are widely detected in the broader farming environment (i.e., surface waters, plant pollen, nectar, and other exudates) (Bonmatin et al. 2015; Alford and Krupke 2019). Furthermore, the consumption of active substance per hectare is several times higher for seed treatment than for (targeted) foliar applications (Matyjaszczyk 2017). Lastly, their “blanket” application at the time of planting (or crop seeding) interferes with the action of natural enemies and thus compromises natural, cost-free biological control (Seagraves and Lundgren 2012; Douglas and Tooker 2016). As such, neonicotinoid insecticides contribute to biodiversity loss, impact environmental health, and undermine ecological resilience of farmland ecosystems (Eng et al. 2019; Humann-Guilleminot et al. 2019a; Sánchez-Bayo and Wyckhuys 2019).
Farmers’ dependency on neonicotinoid insecticides is of global concern and has continued unabated in the United States (US) for over two decades (Jeschke et al. 2011; Simon-Delso et al. 2015; Douglas and Tooker 2015; Hladik et al. 2018). Following the first registration of imidacloprid in 1991, six other active ingredients were released on the US market (Bass et al. 2015). In the mid-2000s, active marketing of insecticide-coated seeds, mounting insecticide resistance issues, and public concern over high mammalian toxicity of older products led to a surge in neonicotinoid usage over extensive geographical areas, e.g., US Midwest (Meehan and Gratton 2016). By 2014, 1.16 million kg/year of thiametoxam was applied to US corn, soybean, wheat, and cotton (NAWQA 2014). At present, neonicotinoid seed coatings are used in virtually 100% of the conventional maize planted in the US and canola in Canada. Seed coatings are equally used in other crops (i.e., soybean, oilseed rape, cereals, rice, cotton, sunflower) in the USA and across the globe (Hladik et al. 2018; Douglas and Tooker 2015; Esser et al. 2015).
In the EU, the first neonicotinoid (imidacloprid) was registered in the mid 1990s. Few years after neonicotinoids approval, bee health problems and other non-target impacts have surfaced (Pistorius et al. 2009, Doucet-Personeni et al. 2003; Henry et al. 2012; Whitehorn et al. 2012; Alix and Mercier 2009; Bortolotti et al. 2009; Burgio et al. 2012). Subsequently, in some EU member states, the use of particular active ingredients was suspended on certain crops in pollinator habitats, e.g., on sunflower and oilseed rape in France (Maxim and van der Sluijs 2013), or on maize in Italy (Bortolotti et al. 2009). In Italy, after this precautionary suspension, the number of bee mortality events linked to maize cultivation drastically declined while maize yield levels remained unchanged (Sgolastra et al. 2017). Yet, neonicotinoids were deemed to be “essential” components to EU farming, and their continent-wide suspension was anticipated to cause unacceptable production losses and (socio-)economic upheaval (Noleppa and Hahn 2013). The ensuing debate juxtaposed these presumed (socio-)economic impacts against an increase in primary productivity and farm profitability related to reconstituted pollination and other biodiversity-based ecosystem services (Garibaldi et al. 2014), while scientific information did not report any benefits of neonicotinoids on crop yields (Seltenrich 2017), quality of harvested produce, or farm-level profitability (LaCanne and Lundgren 2018). Parallel to the accumulating scientific evidence of their deleterious effects on human health (Seltenrich 2017) and biodiversity, including vertebrate and invertebrate wildlife (Chagnon et al. 2015; Pisa et al. 2015; Gibbons et al. 2015; Humann-Guilleminot et al. 2019b; Pisa et al. 2017; Sánchez-Bayo et al. 2016; Lundin et al. 2015; Tosi et al. 2017; Taliansky-Chamudis et al. 2017; Pecenka and Lundgren 2015; Douglas et al. 2015), there was a disclosure of scientific arguments and field observations (Blacquière et al. 2012; Carreck and Ratnieks 2014; Cresswell et al. 2012). From 2012 onward, the European Food Safety Authority (EFSA) suggested to suspend certain uses of active ingredients, and by March 2017, the European Commission had proposed a ban of all outdoor usage of three neonicotinoid pesticides (i.e., imidacloprid, clothianidin, and thiamethoxam). However, crops that are considered “non-attractive” to honeybees, e.g., cereals, sugar beet, occupy the largest surface of arable land in Europe (approx. 60%, Eurostat 2017), still receive considerable rates of neonicotinoid application (Simon-Delso et al. 2015), and current application schemes equally pose risk to non-target organisms, including natural enemies and pollinators (Calvo-Agudo et al. 2019). Certainly, as neonicotinoids affect all ecosystem components, a sole focus on (domesticated) honeybees is insufficient (Pisa et al. 2017).
Multiple efforts have also been made in North-America to counteract the above trends: the United States Environmental Protection Agency (USEPA) recently re-evaluated the registration of neonicotinoids, especially in relation to pollinators (USEPA 2014); the Government of Ontario (Canada) pursued an 80% cut in the use of neonicotinoid-treated maize and soybean seed by 2017 (Gov. of Ontario 2015). In 2011, imidacloprid was voluntarily withdrawn from use on bee-pollinated almonds in California, while other products are on the Pesticide Action Network (PAN) International’s list of highly hazardous pesticides (2010) for global phase-out, because of their toxicity to bees or potential role as carcinogens (i.e., thiacloprid). In China, one of the world’s key suppliers of neonicotinoid insecticides, domestic use is considerable, especially in the country’s 30 million hectare rice crop (Shao et al. 2013). Presently, six types of neonicotinoid are registered for domestic use. Whereas imidacloprid, acetamiprid, nitenpyram, and thiacloprid are developed by companies outside China, paichongding and imidaclothiz are newly developed compounds with independent intellectual property rights.
In maize (Zea mays (L.)), two key pests are targeted with neonicotinoids: (1) the western corn rootworm (WCR), Diabrotica virgifera ssp. virgifera LeConte (Coleoptera: Chrysomelidae) and (2) a complex of wireworm species (Agriotes spp. Coleoptera: Elateridae). For D. virgifera control, farmers typically apply granular soil insecticides or insecticide-coated seeds against the larvae and foliar insecticides against the adults (Ward et al. 2004). The combined cost of soil insecticides and aerial sprays, plus the yearly pest-inflicted crop losses, approached US$1 billion annually in the 1980s (Metcalf 1986). Following its 1990s detection and spread in Europe, the damage potential of D. virgifera—in the absence of control—was estimated at 472 million Euro annually (Wesseler and Fall 2010). Wireworms (Agriotes brevis Candeze, A. sordidus Illiger, and A. ustulatus Schäller) are of primary concern in Central and Southern Europe, with underground larval feeding resulting in root damage in maize and other cereal crops (Furlan 1996, 2004; Furlan 2014; Furlan and Tóth 2007). At present, soil insecticides are the preferred mode of wireworm control, impeding a further deployment of IPM strategies (Furlan 2005; Furlan and Kreutzweiser 2015). The bird cherry-oat aphid Rhopalosiphum padi (Linnaeus) causes direct feeding damage on cereals, transmits plant pathogens (e.g., barley yellow dwarf virus) and interferes with photosynthesis through its extensive production of honeydew (Dedryver et al. 2010; Mann et al. 1997; Finlay and Luck 2011; Harrington et al. 2007). Since the late 1980s, R. padi control has primarily been based on seed treatments and insecticide sprays, raising environmental concerns (Bredeson et al. 2015; Dedryver et al. 2010). In rice, the brown planthopper (BPH) Nilaparvata lugens (Stål) can cause up to 70% yield losses through direct feeding and virus transmission—with aggregate economic losses estimated at $20–100 million/year for India, Indonesia, Philippines, Japan and Taiwan (Heinrichs and Mochida 1984; Bateman 2016). Considered a “Green Revolution” pest, rice planthoppers first gained prominence in tropical Asia during the 1960s and 1970s when high-yielding rice varieties were actively promoted together with synthetic pesticides (Bottrell and Schoenly 2012; Escalada and Heong 2004). Brown planthopper outbreaks are due to the insecticide-induced mortality of natural enemies and an ensuing loss of regulating ecosystem services (Horgan and Crisol 2013; Bottrell and Schoenly 2012; Horgan 2018; Spangenberg et al. 2015) plus the widespread development of brown planthopper resistance to insecticides, including neonicotinids (Zhang et al. 2016; Min et al. 2014; Basanth et al. 2013; Puinean et al. 2010; Hadi et al. 2015; Matsumura et al. 2008) and insecticide-induced hormesis in which insecticide treatments enhance brown planthopper survival, development and reproduction (Yin et al. 2014; Nanthakumar et al. 2012; Horgan 2018; Zhu et al. 2004; Azzam et al. 2009; Azzam et al. 2011). Though brown planthopper-resistant rice varieties have been developed, widespread adaptation to resistance genes has compromised their effectiveness and insecticide applications thus remain the mainstay of Asian rice farmers (Spangenberg et al. 2015; Horgan 2018). In cotton, the cotton aphid, Aphis gossypii Glover and the silverleaf whitefly, Bemisia tabaci Gennadius inflict crop damage through direct feeding, virus vectoring and the extensive secretion of honeydew (Lu et al. 2012; Dedryver et al. 2010). The heightened adoption of Bacillus thuringiensis (Bt) transgenic cotton—for lepidopteran pest control—has led to increases in sap-feeder populations such as B. tabaci or A. gossypii (Lu et al. 2012). Though genetically engineered crops are well-suited to support biological control (Romeis et al. 2018), the increased infestation pressure of these sap-feeders has instead triggered the use of systemic insecticides (Deguine et al. 2008). Furthermore, rapidly evolved resistance to neonicotinoids has been recorded, e.g., in Australia (Herron and Wilson 2011), West Africa (Houndété et al. 2010), and Asia (Koo et al. 2014; Matsuura and Nakamura 2014; Ahmad and Arif 2008) with a resulting intensification of pesticide use and accompanying harmful impacts on resident natural enemy communities (Gerling and Naranjo 1998; Naveed et al. 2008; Yao et al. 2015; Sohrabi et al. 2012).
Aside from neonicotinoid insecticides, numerous management techniques have been investigated for the above crop × pest complexes; many with highly favorable environmental, human health, and socio-economic profiles. Nature-based innovations (e.g., biological control) can be deployed in open-field and protected cultivation, have proven advantages over insecticides (Bommarco et al. 2011; Naranjo et al. 2015; Shields et al. 2019) and favorable food safety profiles (Bale et al. 2008), yet are faced with globally lagging rates of grower adoption and deficient stakeholder awareness (Shields et al. 2019; van Lenteren 2012; Wyckhuys et al. 2018; Wyckhuys et al. 2019c; Barratt et al. 2018). Other approaches such as pest insurance schemes (Quiggin et al. 1993; Miranda and Vedenov 2001), ecological engineering (e.g., (Gurr et al. 2016), pesticide taxes coupled with enhanced grower education (Praneetvatakul et al. 2013), regenerative farming (LaCanne and Lundgren 2018), customized decision-support tools, cultural control, and other IPM options have equally been examined. Many of these practices constitute part of an agricultural systems “redesign”—a necessary component for transformative change in the world’s agriculture sector, and a core component of sustainable intensification (Pretty et al. 2018). For certain technologies, considerable progress has been made on the research front, yet advances in (on-farm, participatory) technology validation, farmer extension or wide-ranging diffusion have been limited. Some technologies have been readily adopted, validated, and adapted by individual growers or (small- to mid-size) farmer nuclei in certain countries, and these successes now wait to be communicated, up-scaled and transferred to other areas (Westphal et al. 2015; Gurr et al. 2016).
The present paper is the continuation of the Worldwide Integrated Assessment (WIA) on systemic insecticides published in 2015 which included alternative aspects (Furlan and Kreutzweiser 2015), and then of the WIA update published in 2018 which also included a chapter on alternatives (Furlan et al. 2018). Here, we provide a systematic assessment of alternatives to neonicotinoids for the management of key arthropod pests in four arable crops of global relevance (i.e., maize, cotton, rice, and winter wheat). More specifically, we draw upon (i) a review of scientific literature, (ii) an expert consultation involving 16 scientists and crop protection professionals from multiple countries on a crop-specific and geographically explicit “readiness” assessment of pest management alternatives, and (iii) a risk assessment of pest outbreaks, as conducted through online survey tools. Our systematic assessment of the state of development (i.e., research, plot-scale validation, grower-uptake) for a select set of technologies constitutes a valuable resource for scientists, pest management professionals, extension officers, agro-enterprises, and individual farmers. Our work also informs policy dialogue and can create global traction for the “redesign” of farming systems founded upon agro-ecology, ecologically centered IPM, and arthropod biological control.
Materials and methods
Two scientific literature databases (i.e., Springerlink and Sciencedirect) were queried using keyword combinations specific to the different crop × pest systems: “Diabrotica AND control AND maize” and “Agriotes AND control AND maize,” etc. Searches were limited to articles published in English from January 1999 until March 2017. All publication abstracts were screened, and literature references were selected based on their relevance for crop protection in the seven target crop × pest systems, i.e., Diabrotica × corn, Nilaparvata × rice, Agriotes × maize, Agriotes × wheat, Rhopalosiphum padi × wheat, Aphis gossypii × cotton, Bemisia tabaci × cotton.
Our initial dataset was composed of 266 relevant literature references, of which 216 covered technologies that were deemed to be effective—as expressed by the papers’ authors. A particular pest management technology was considered effective if a statistically significant level of control of the target pest was reported. In case one single scientific study comprised multiple effective (and non-effective) tools, these were listed as separate lines in the dataset. From the collated set of references, we extracted those that specifically addressed the evaluation of non-chemical crop protection alternatives, and organized these into six main categories depending upon the primary type of pest management tactic: (1) biological control, (2) cultural (e.g., sanitation, crop rotation, nutrition or water management) or mechanical control, (3) innovative pesticides and application regimes (e.g. attractants, reduced product doses, anti-resistance strategies), (4) host plant resistance, (5) decision-support tools (e.g., monitoring schemes, predictive models, early-warning systems), and (6) other tools such as farming systems adaptations, multi-faceted IPM packages, and others. As the same technology was regularly covered in multiple articles, we consolidated literature records for the expert evaluation: a total of 17 different tools for western corn rootworm, 26 for bird cherry-oat aphid, 25 for wireworms, and 23 for brown planthopper were included in the questionnaire and evaluated by experts. Furthermore, for studies that were exclusively based on field data, we mapped the availability of different technologies within particular geographical areas. Overall, Africa was underrepresented in the dataset.
Expert evaluation of the alternative tools
Literature references were compiled and tabulated per crop × pest system, and subsequently shared by email with expert scientists and pest management professionals for further commenting and updating. Experts could rank the “readiness” of each management alternative using the following criteria: RESEARCH = at research stage; READY = available for immediate implementation, though not yet adopted by local growers; PRACTICED = adopted and used by (nuclei of) growers in a particular country or region. Furthermore, experts were requested to indicate their perceived importance of two potential “roadblocks” or constraints to broader technology diffusion and uptake, i.e., ENVI = technology is considered ineffective under local environmental conditions; ECONOM = current technology is deemed to be too expensive or not economically viable, thus limiting wider adoption.
Online survey for pest risk assessment
An online survey was made available through a dedicated cloud-based platform (i.e., SurveyMonkey) and shared with the above mentioned global experts. Through this survey tool, experts were able to rank the perceived importance of a given insect herbivore (in a particular crop) and share information on its infestation pressure as related to (locally established) economic thresholds, or other metrics reflective of its economic relevance. Also, through the online survey, data were gathered on the relative extent of neonicotinoid use (i.e., % growers, treated area) and pest management alternatives.
For either evaluation method, feedback was obtained from a total of 16 scientific experts and crop protection professionals, from China, Croatia, Germany, Hungary, Indonesia, Italy, Philippines, Poland, Slovenia, Spain, USA, and Vietnam. Experts provided additional papers, non-peer-reviewed documents and reports, and other information to update our database of pest management alternatives. As no feedback was received for cotton pests, no assessments could be carried out for A. gossypii and B. tabaci, so cotton was excluded from the further evaluation. No responses were received from scientists in Africa, Latin America and the Caribbean, or in Central Asia.
Given that the collected data are descriptive, results were tabulated to provide a full overview of the evaluated alternatives. Results from the expert evaluation (average number of tools ranked per category) were visualized using polar bars, while the geographical coverage of field-tested alternatives is shown in maps. Lastly, bar charts show the results of the pest risk assessment—as obtained through the online survey.
Literature review and expert evaluation of alternative tools
Most literature references were found for B. tabaci, while the lowest number of references was recorded for A. gossypii and D. virgifera (Table 1). Biological control featured prominently as management alternative for all crop × pest systems, ranging from few effective technologies for N. lugens to more than half of the alternative management tools for B. tabaci (Table 1). Only half of the effective management tools were based on field data, most of which were from Europe for wireworms in maize and winter wheat, from Asia on N. lugens in rice, and from Asia and North-America on B. tabaci in cotton. In the following sections, we describe findings for the most effective management alternatives.
Approximately half of the tools were only reported to be at a research stage. Biological control was extensively documented in literature records, yet the majority of those were evaluated to be only at a research stage. The highest percent of tools in practice were found for bird cherry-oat aphid control, and primarily included CBC (Conservation Biological Control) through landscape and habitat-level management (Fig. 1). For brown plant hopper control in rice, mostly cultural and mechanical control technologies were put in practice by growers, however only in a geographically limited area (i.e., parts of Vietnam and Indonesia). For wireworm control, cultivation practices and DSS were most practiced. Western corn rootworm control was built around three main pillars: DSS, host plant resistance and cultural practices (i.e., crop rotation). The online survey further revealed low perceived risk of western corn rootworm in maize, aphids in winter wheat and wireworms in maize and in winter wheat (Fig. 2), thus creating room for field-level evaluation and grower adoption of non-chemical alternatives (Fig. 3). For western corn rootworm and wireworms, several countries reported 75–100% adoption levels of neonicotinoids in their respective maize and wheat crops (Fig. 3). Though brown planthopper poses low to intermediate risks in rice (i.e., 25–50%), rice fields are routinely treated with neonicotinoids (Figs. 2 and 3). Below we discuss the main alternatives to neonicotinoids in further detail.
For bird cherry-oat aphid control in winter wheat, nine different CBC tools were reportedly practiced in Italy, Hungary, Spain and USA (Tables 2 and 3). In winter wheat, aphid biological control was primarily at the research stage, and few countries mentioned economic or environmental roadblocks for subsequent grower adoption. For wireworm control in maize and winter wheat, biological control is primarily at the research stage and only two technologies—using entomopathogenic fungi—are being practiced in Germany and the USA (Tables 5 and 6). Most countries reported the existence of environmental and economic roadblocks for the field-level use of biopesticides and nematodes, while landscape and habitat management tools were considered “ready for implementation” in Slovenia and Hungary. Few countries indicated studies at research stage, and only nematodes might be ready for use in Germany. For western corn rootworm management in maize, no biological control technologies are being implemented yet—possibly due to locally perceived economic and environmental barriers, or technology related issues (Table 7).
For brown planthopper control, several biological control tools have been described in the literature. Yet, only one landscape management tool was practiced in Indonesia, most options are ready for implementation in Vietnam, and remain at the research stage in Papua New Guinea (Table 8). CBC—particularly the use of flower strips to enhance in-field populations of parasitoids—has been implemented in southern Vietnam, and has been extensively researched at experimental stations in Thailand, China and the Philippines and in farmers’ fields in China. In Vietnam, its farm-level adoption may potentially accelerate.
Under field conditions, micro-organisms and biopesticides are perceived to have more potential for use than macro-organisms because they are easier to store and transport, and can be bulked up under laboratory conditions. Nematodes have been used to control soil pests such as WCR in maize under laboratory and field conditions (Kurtz et al. 2008; Toepfer et al. 2010) and wireworms under laboratory conditions (Ansari et al. 2009). In arable crops, the following species of entomopathogenic fungi have been tested: Beauveria bassiana, Metarhizium spp. and Lecanicillium lecanii (Verticillium) (Kabaluk 2014; Kim and Kim 2008; Ritter and Richter 2013; Ansari et al. 2009). Fungal applications may be combined with augmentative releases of predators (i.e. Orius laevigatus (Down et al. 2009)) or parasitoids (Lazreg et al. 2009), and several of these organisms can contribute significantly to B. tabaci control (Antony et al. 2004; Bellamy et al. 2004; Hoelmer 2007; Viscarret and López 2004; Yang and Wan 2011).
Certain plant-produced compounds can prolong the shelf-life of beneficial entomopathogenic nematodes in Diabrotica management (Jaffuel et al. 2015). Other compounds have repellent or insecticidal effects, and their extracts can be used as biopesticides. Several biopesticides are also fully compatible with natural biological control, e.g., extracts of Ruta chalepensis, Peganum harmala and Alkanna strigosa inflict levels of B. tabaci mortality similar to imidacloprid without negatively affecting its parasitoid Eretmocerus mundus (Al-Mazra’awi et al. 2009).
Naturally occurring arthropod predators and parasitoids play a central role in regulating pest populations in arable crops, and their active in-field conservation can constitute a desirable, cost-effective means of pest control (e.g., (Landis et al. 2000, Naranjo et al. 2015, Shields et al. 2019, Veres et al. 2013). Predaceous spiders consume large numbers of aphids and B. tabaci (Choate and Lundgren 2015; Kuusk et al. 2008) and conservation measures can lower pest population numbers, associated feeding damage and pest-inflicted yield losses—especially in systems where there is little concern about insect-mediated virus transmission (Naranjo 2001). CBC schemes involve a deliberate suspension (or drastic reduction) of pesticide applications, and the deployment or preservation of in-field shelters, nectar, alternative prey/host items, and pollen to support resident natural enemy communities (so-called SNAP; (Gurr et al. 2017)). Many of these interventions can be laborious and involve added costs, but the returns on investment can be high and should appeal to growers (Naranjo et al. 2015). Ample CBC research has been conducted for several of the target pests, and this increased research attention is warranted. The spatio-temporal availability of certain crop and non-crop habitats can impact field populations of pests and improve their associated natural enemies (Veres et al. 2012; Burgio et al. 2006), although landscape-level impacts can be inconsistent and sometimes difficult to predict (Karp et al. 2018). Hence, interventions have to be carefully chosen and science based to enhance (or sustain) natural enemy populations while counteracting pest attack. For example, certain host plants that are beneficial for natural enemies—e.g., ragweed for B. tabaci—can also serve as alternative hosts that favor pest immigration (Naveed et al. 2007; Zhang et al. 2014).
The manipulation of rhizosphere interactions and associated plant defenses can be a lucrative option to further enhance CBC, specifically against soil-dwelling pests (such as wireworms). The stimulation of plant defenses, e.g., by integrating plant mutualists into the standing crop (i.e., beneficial microbes, fungi or entomopathogenic nematodes), by directly manipulating soil organic matter, edaphic fauna and soil fertility or by—indirectly—altering crop rotation sequences can provide important feedback mechanisms that boost pest control or enhance natural enemy abundance (Johnson et al. 2016; Wyckhuys et al. 2017). Resistance priming—through silicon amendments, or EPNs—also offers opportunities for management of sap-feeding pests such as BPH and B. tabaci (An et al. 2016; Yang et al. 2017). CBC can equally involve the promotion of entomophthoralean fungi, i.e. by enhancing fungal infection of R. padi through feeding on its winter host bird cherry (Nielsen and Steenberg 2004) as well as endophytic entomopathogens on A. gossypii (Gurulingappa et al. 2010). Besides invertebrates, vertebrates can assume an important role in the biological control of several of the target pests. Frogs, fish and ducks can consume large numbers of rice pests, including planthoppers (Khatiwada et al. 2016; Zou et al. 2017; Sheng-miao et al. 2004); for WCR and wireworms, birds act as key predators and can suppress field populations (Bollinger and Caslick 1985; Sheng-miao et al. 2004) and rodents possibly engage in larval predation (Tschumi et al. 2018). A phase-out of neonicotinoid use is key to safeguard and fully exploit these vertebrate-mediated pest control services (e.g., (Humann-Guilleminot et al. 2019b). For example, Gurr et al. (2016) have indicated that pest suppression in ecologically engineered rice fields in China was greatest where farmers suspended the use of chemical insecticides. Different trophic levels can also play a role, with aphid suppression related to Collembola-mediated changes in nitrogen resource allocation and wheat crop growth (Schütz et al. 2008).
CBC carries ample potential in the management of target pests in our four focal arable crops. However, the success of CBC will be related to the effective communication to growers of ecological concepts and encouragement of adoption through participatory research or because of recognized economic advantages from crop diversification (e.g., producing sesame on rice bunds). Such features have encouraged the rapid adoption of ecological engineering for planthopper management in Asia (Westphal et al. 2015; Gurr et al. 2016; Horgan et al. 2016). However, for many crop × pest systems, comprehensive evaluations of natural enemy impacts on pest populations have not been carried out and key information is thus absent to guide the development of habitat manipulation schemes.
The scientifically guided introduction of specialist natural enemies for control of invasive pests is a powerful and self-propelling method of biological control (Wyckhuys et al. 2019b) that carries potential for the management of several target pests. For A. gossypii, introductions have been made of several natural enemies—including aphidiine and aphelinid wasps, and syrphid flies—in the Pacific islands (Waterhouse 1998). Opportunities may also exist to employ non-native natural enemies for the control of WCR in its invaded range in Europe (Kuhlmann and van der Burgt 1998; Toepfer et al. 2009).
Cultural or mechanical control
Crop husbandry or cultural practices such as crop rotation, or adapted fertilisation and water management, have received ample attention for the control of silverleaf whitefly in cotton, wireworms in maize and winter wheat, and brown planthopper in rice (Table 1). Experts signaled that various cultural practices are used against brown planthopper, western corn rootworm, and wireworm in the above crops (Fig. 1). For wireworm, crop rotation measures are either “in practice” or “ready for implementation” in all countries, except for USA (Table 5). Soil fertility management was in practice—with certain environmental constraints—in Germany, and ready to use in Italy. Tillage is commonly practiced in Hungary and in Spain, and ready for implementation in Slovenia, while its effects are still being researched in Germany, Italy and the USA (Esser et al. 2015). For brown planthopper in rice, plant nutrition and water management are either put in practice or ready for implementation, in Vietnam and Papua New Guinea (Table 8). This includes the reduction of nitrogen application rates as part of Vietnam’s “three reductions—three gains” (3R3G) campaign (Horgan 2018). In Indonesia, local government authorities can delay farmer access to irrigation water to enforce fallow periods and abate severe brown planthopper outbreaks (Horgan & Stuart, personal observation). For aphids in wheat and western corn rootworm in maize, few agronomic tools were recorded (Tables 2 and 7), however crop rotation is widely practiced for western corn rootworm control (Fig. 1). Nutrition management is in practice in Hungary and ready for implementation in Spain for aphid control (Table 2). Meadow plowing timing, just before maize seeding, is an effective tactic to prevent wireworm damage to maize (Furlan et al. 2020). Crop rotation can assist with pest control in multiple ways, e.g., by providing a habitat in which pest species are unable to successfully complete their lifecycle (e.g., by replacing host plants with non-hosts, or by creating conditions that disproportionately favor a pest’s natural enemies). Diversification measures can equally be implemented within a given crop, by concurrently establishing a companion crop through intercropping, strip-cropping or relay cropping. These kinds of system-level adaptations have been tested for all target pests.
Though regularly overlooked by pest management professionals, plant nutrition, and water management can be important levers within system-level IPM strategies, and this has received some attention for all pests except WCR. For aphids, BPH and SLW, ecological fitness significantly increased with enhanced levels of nitrogen fertilization of the host crop (Aqueel and Leather 2011; Lu et al. 2004; Crafts-Brandner 2002; Bi et al. 2003). On the contrary, for BPH, additions of potassium and silicon can increase resistance of rice plants and thus lower pest-inflicted production losses (Rashid et al. 2016; Liu et al. 2013; He et al. 2015). Balanced fertilization schemes and the incorporation of organic matter in paddy rice systems can further enhance the build-up of natural enemy populations and boost pest control (Settle et al. 1996).
Innovative pesticides and application regimes
Novel insecticides or innovative application methods are available for most target pests, and > 50% records report their in-field evaluation (Table 1), primarily in Asia and North America. For bird cherry-oat aphid, innovative insecticides were not deemed relevant (Table 4). For wireworm, attract and kill, mass trapping, or physical barriers were reported, yet environmental or economic roadblocks to their implementation were regularly mentioned (Table 6). Innovative chemical-based approaches for western corn rootworm control in maize (attract and kill, mating disruption, protein biopesticide) and for brown planthopper in rice (reduced dose, innovative insecticides, anti-resistance strategies) were only at the research stage and are considered in few countries (Tables 7 and 9).
Attract and kill strategies are the most commonly reported alternative pest control method, and attractants are regularly combined with insecticides or with entomopathogenic fungi (Vernon et al. 2016; Brandl et al. 2017). Besides attract and kill measures, non-systemic insecticides, synergists, surfactants, anti-resistance strategies and reduced dose applications are all described. For certain pesticidal products, targeted and well-timed foliar sprays can present significant advantages over unguided “blanket” drench applications or IPM-incompatible seed dressings (Kumar et al. 2012). Insecticide resistance development can also be reversed by entirely suspending insecticide use over specific time periods (Yang et al. 2014).
Decision support systems
Decision support systems (DSS), including monitoring systems, action thresholds and predictive population models, are important pillars of IPM in all pest × crop systems. For western corn rootworm and wireworms, DSS are commonly put in practice (Fig. 1), with monitoring tools and predictive models used for wireworm control in the USA, Germany, Italy, Slovenia, and Hungary (Table 6). Similarly, for western corn rootworm, pheromone traps and yellow sticky cards are used for monitoring in nearly all countries though models are used to a lesser degree than for wireworms (Table 7). For bird cherry-oat aphid, forecasting models—based upon sowing time—are either in practice or “implementation ready” in Hungary, USA, Italy, and Spain (Table 3 and 4). For brown planthopper, intervention thresholds and population models are only occasionally put in practice—despite the prime importance of this pest in Asia’s rice crop (Table 9). Networks of light traps have been established in several Asian countries including China, Japan, Korea, and Indonesia (Horgan, personal observation); however, though these traps have helped characterize brown planthopper migration and assess the effect of meteorological parameters on migration patterns, they are not routinely used as early warning systems. In Vietnam, simple light traps have been employed at local scales to determine peak brown planthopper populations after which farmers can plant their rice crops (escape strategy: (Horgan 2018). Most of DSS tools or pheromone lures are not adapted to field conditions (40%), and the bulk of field-level records originate from Europe (40%, Table 1).
The overall aim of DSS development is to predict a pest’s population dynamics and to identify suitable intervention strategies (and their timing) based upon existing economic threshold levels. Modeling rhizosphere interactions can also help to assess the risk of soil pest attack (Johnson et al. 2016). For wireworms, a range of abiotic factors (e.g., altitude, precipitation, temperature, pH, organic matter content) can be incorporated as predictive variables (Jung et al. 2014; Staudacher et al. 2013; Hermann et al. 2013; Furlan et al. 2017a, 2017b). For aphid pests, abiotic factors, presence, and abundance of natural enemies and aphid identification modules are built into DSS models such as GETLAUS, CEAS, and APHIDSim (Gosselke et al. 2001; Piyaratne et al. 2013; Rossing et al. 1994; Gonzalez-Andujar et al. 1993; Kwon and Kim 2017). Aside from theoretical models (Wu et al. 2014; Fabre et al. 2010; Ma et al. 2001; Xian et al. 2007; Giarola et al. 2006), spatially explicit models can account for landscape composition and configuration, or for other factors such as wind speed and wind direction (Parry et al. 2006). Thresholds have been defined for wireworms (Furlan 2014), brown planthopper (Zheng et al. 2007) and for different cotton pests, including A. gossypii (Silvie et al. 2013; Sequeira and Naranjo 2008). Data input for DSS are regularly collected through field-level monitoring: WCR and wireworms can be monitored using sticky traps, pheromone traps or bait traps (Sufyan et al. 2011; Vuts et al. 2014; Benefer et al. 2012; Parker 1994, 1996; van Herk and Vernon 2013; Tóth et al. 2002; Tóth et al. 2007; Vuts et al. 2012; Tóth 2013; Tóth et al. 2015; Furlan et al. 2017a, 2017b; Bažok et al. 2011; Kos et al. 2014). In Northern Italy (Emilia-Romagna region) a monitoring net for two wireworm species has been employed in 2017 and 2018 using about 1100 pheromone traps per year, providing provisional threshold to alert farmers on infestation risk. For other pests, yellow pan trapping, sweep-net sampling or other kind of population assessments can be used.
Although the principles of IPM are universally applicable, certain environmental and socio-economic factors can hamper IPM adoption (Vasileiadis et al. 2011). IPM entails the exhaustive use of non-insecticidal approaches (i.e., cultural, mechanical, phytosanitary practices) to prevent herbivores from reaching damaging population densities, draws on biological control as both a preventative and curative tactic, pursues the integrated use of mutually compatible technologies, and treats synthetic pesticides as a measure of “last resort” (Pedigo 1989). Prophylactic applications of systemic insecticides—e.g., as seed dressings or dips at the onset of the cropping season—are in direct conflict with this IPM concept, and have no room in IPM-managed systems. For bird cherry-oat aphid, the following measures do fit under the IPM umbrella: biological control, targeted chemical control—preferably with compatible products—as guided by decision rules and threshold levels, plant resistance and certain farming practices such as delayed sawing or nutrition management (Dedryver et al. 2010). For A. gossypii, mandatory dates for planting and harvest, post-harvest sanitation, and establishment of host-free periods along with—minimal—tactical use of insecticides can aid the recovery of cotton agro-ecosystems and concurrently lower pest pressure (Ellsworth and Martinez-Carrillo 2001; Naranjo 2001). Also, the establishment of groundcover, intercropping or trap crops help conserve resident natural enemy communities and prevent build-up of pest populations (Deguine et al. 2008). For B. tabaci, the IPM “pyramid” is composed of three main components: regular pest sampling, preventative measures, and a minimal, scientifically guided use of insecticides—prioritizing compatible insect growth regulators, IGRs (Ellsworth and Martinez-Carrillo 2001). Though genetically engineered crops are compatible with biological control (Romeis et al. 2018), large-scale, genetically uniform plantings of GM cotton can disproportionately favor whitefly pests. In those systems, measures can still be adopted to conserve arthropod natural enemies (Deguine et al. 2008). For aphid control, integrated weed and insect management strategies can reduce application costs without sacrificing the efficacy of either strategy, though full advantage needs to be taken of non-chemical measures (Ma et al. 2016). In rice systems, non-chemical technologies are well-advanced for insect pest management (Hong-xing et al. 2017). For rice brown planthopper, in addition to host plant resistance, adequate nutrient or irrigation management and conservation biological control (e.g.,(Gurr et al. 2016, Hemerik et al. 2018), particular fungicides interfere with pest development and can be included in IPM packages (Nanthakumar et al. 2012; Shentu et al. 2016). For each of the above pests, IPM packages are at different stages of development—ranging from scientific evaluation, farm-level validation and adaptation, to grower adoption. In Europe, complete and economically viable IPM packages are available for the management of wireworms and western corn rootworm in maize.
Risk assessment and IPM “readiness” for selected crop × pest systems
Overall, pest risk levels were rated low to medium (i.e., brown planthopper) for all target pests, independent of the use of neonicotinoids (Fig. 2). Soil/seed treatments and foliar use of neonicotinoids varied among crop × pest systems and regions (Fig. 2), with nearly 100% of rice fields routinely treated against brown planthopper. Even so, 25–75% of those fields could be managed with alternative tools. Extent of field application with neonicotinoids was lowest for winter wheat (i.e., to control R. padi), and this likely can be entirely replaced with alternative tools (Fig. 3). In the following section, results from the expert evaluation and associated risk assessment are presented according to pest species.
Bird cherry-oat aphid in winter wheat
Overall, pest status—and economic importance—of R. padi in European winter wheat is low to very low (0–25%) (Table 10, Fig. 2), largely because of a complex of effective resident natural enemies that colonize fields at the onset of the cropping season. In Slovenia, pyrethroid applications against the cereal leaf beetle Oulema melanopus (L.) can indirectly control R. padi. The pest is of local concern in certain areas, where foliar sprays are used for its control. In none of the European countries, experts voiced a need to use neonicotinoids as either seed or foliar applications (Table 10, Fig. 2). Yet, the current extent of reliance upon these products varied greatly between countries. In Spain, growers tend to resort to neonicotinoids to prevent barley yellow dwarf virus (BYDV) infection, though this is not regularly warranted: most Spanish farmers alter the sowing date to reduce aphid infestation and thus minimize the risk of virus attack. In Italy, 50-75% of fields rely upon CBC, and aphid infestations on organic farms are significantly lower than in those practicing IPM. In Slovenia, 25–50% of fields are managed through alternative tools—including those that rely upon IPM to manage O. melanopus. On the other hand, in the Western USA, 25–50% of wheat fields are planted with neonicotinoid-coated seeds, though the economic rationale for this high level of usage may be entirely lacking. Overall, biological control (including CBC), landscape-level management, farming systems adaptation (i.e., crop rotation, cultural practices), DSS, host plant resistance, and innovative pesticide application are available R. padi management tactics yet are not widely known or exist solely at the research stage. Most alternatives are either practiced or ready for implementation in Italy, Hungary, and Spain: CBC and landscape-level interventions are in practice in Italy and Spain. Locally, diverse and abundant arthropod natural enemies and entomopathogenic fungi exist in or near wheat fields and contribute to aphid biological control. In the Carpathian Basin, farmers recognize that an optimized plant density and nitrogen supply are cost-effective measures for R. padi control. Also, intercropping with oilseed rape, garlic or less susceptible varieties are interesting alternatives that are ready for implementation. In the Western USA, growers do alter sowing dates, while nutrition management tactics are still at the research stage. DSS such as the Cereal Aphid Expert System (CAES) are practiced in Italy and ready for deployment in Spain. Lastly, organic farming and full-fledged IPM packages are practiced in Italy and Slovenia.
None of the experts evaluated bird cherry-oat aphid as a high-risk pest (Table 10, Fig. 2), possibly due to the low degree of usage of non-selective insecticides, an enhanced adoption of field-level diversification tactics, and a resulting increased impact of locally occurring natural enemies. In Europe, CBC can be the primary alternative to neonicotinoids, while nutrition management, host plant resistance and DSS carry ample potential for further development, fine-tuning, and promotion (Gosselke et al. 2001; Gonzalez-Andujar et al. 1993; Day et al. 2015). In the USA, R. padi was equally perceived to be a low-risk pest, yet 25–50% of current winter wheat acreage is annually sown with neonicotinoid-coated seeds. For a low-risk pest, such high levels of neonicotinoid use seem unwarranted.
Wireworm in maize and winter wheat
Wireworms were historically regarded as limiting pests of several cultivated crops in Europe. However, our expert assessment reveals that the perceived risk of wireworms is generally low, except for Croatia (25–50%) and the western USA (25–50%). A long-term risk assessment is available for wireworm in Europe. Furlan et al. (2017a) showed how certain parameters (e.g. grassland in rotation or in the vicinity of the field) greatly increase the risk of crop damage from wireworms in maize. The probability of economic damage was less than 4% (as studied over a 29-year period) in Italy, and these patterns equally hold for other EU countries. Overall, plant damage was low or even negligible in most cases (> 90% had less than 5% wireworm plant damage). In (few) cases with > 15% plant damage, maize yield did not differ between untreated plots and those were soil insecticide was used. The decision to treat crops with soil insecticides (including neonicotinoid seed coating) is based exclusively on wireworm risk assessment, considering that no chemical treatments at maize sowing are needed to control black cutworm, western corn rootworm, and other minor soil pests (Kaster and Showers 1984; Furlan and Kreutzweiser 2015). Some local exceptions may occur to address e.g. Tanymecus dilaticollis Gyll. damage in some areas of Romania (Saringer and Takács 1994); thus local adaptations of IPM strategies need to be considered. Even in areas where wireworms are ranked as a key pest, their impact on crop yields tends to be low and possibly of minor economic importance (Table 10, Fig. 2), except for Pennsylvania (USA), where wireworm damage—though often confined to certain areas of a field—can cause stand losses up to 75–80%. Wireworm damage is patchily distributed, usually remains undetected and infrequently exceeds 15% of a standing crop. It can be severe in some cases—reaching high infestation levels. In Europe, no soil insecticides are used in winter wheat and no significant wireworm damage is recorded, though maize fields are regularly treated with soil insecticides, including neonicotinoids (Table 10, Fig. 2). In the Western USA however, virtually 100% of maize and wheat fields are treated with neonicotinoid soil-insecticides. As resident wireworm populations are likely to be of minor economic importance, there is ample room for implementation of non-chemical alternatives (Table 10, Fig. 2). For example, incorporating barley and oats into crop rotations can reduce wireworm attack (Milosavljević et al. 2019). In the US Midwest, near-universal applications of soil insecticides are directed against western corn rootworm, while negligible wireworm damage is recorded in untreated plots. In Europe, wireworm management differs greatly between countries and production areas. In Slovenia, 40–65% of maize growers use soil insecticides or seed treatments, and similar patterns are reported for Italy. Although no specific measures are used against wireworms, crop rotation, tillage, non-neonicotinoid insecticides and the planting of biocidal plants are widely practiced by local growers. Slovenian livestock producers are affected by wireworms when including meadows in rotation schemes and regularly revert to neonicotinoids. Yet, most producers do not conduct pest monitoring, and thus remain uniformed whether local wireworm populations exceed economic thresholds and cause economically significant losses. In Spain, insecticidal soil treatments are regularly used in a prophylactic manner and may be largely superfluous.
Our expert evaluation revealed how numerous tools are either practiced or “implementation ready” (Tables 5 and 6). Biological control, e.g., entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae, are used in Germany and ready for use in Italy and Slovenia. In Hungary, environmental conditions (i.e., drought) may limit the use of nematodes but could favor field application of Metarhizium spp. In the USA, biological control options are mainly at a research stage. Crop rotation is commonly practiced in all countries. In Hungary, the use of Phacelia tanacetifolia as green manure causes high levels of pest mortality, while the repellent effect of CaCN2 is recognized in Italy, but not yet practiced. In Germany, the latter alternative is practiced, but does require a careful timing of application. Lastly, tillage is widely adopted as a management strategy in Hungary and Spain.
Monitoring tools and DSS in general are practiced in the USA but only used to a limited extent in Europe (e.g., Hungary, Slovenia). In Italy’s Emilia-Romagna region, a monitoring network with pheromone traps has been deployed to forecast area-wide risk of wireworm attack: when a 700–1000 captures/trap threshold is reached for particular wireworm species, larval sampling is suggested to further guide management actions. Also, once the above threshold is exceeded, the use of soil treatments is restricted to max. 50% of field area. In Germany, simple traps are used and abiotic risk factors are taken into account for wireworm management. Attract and kill and alternative insecticides are either unknown or not applicable for most of the countries given existing restrictions on the use of fipronil, bifenthrin and lindane. In Germany, attract and kill is used with a different product (ATTRACAP), while chlorpyrifos is used in Spain for soil treatment—though concerns exist over its potential environmental impacts.
Western corn rootworm in maize
Overall, the risk of western corn rootworm damage was rated low (except Slovenia). However, western corn rootworm risk is inflated in systems with continuous mono-culture planting, as compared to those where crop rotation is used. Especially dairy farmers appear to be reluctant to adopt crop rotation given their often-exclusive reliance upon maize as animal feed, and regularly suffer western corn rootworm damage of up to 50%. Yet, there are ample rotation options that can improve both milk quality and farm profit (Furlan et al. 2018). Across Europe, neonicotinoids are used in less than 25% of maize area (Table 10, Fig. 2). In contrast, in the USA, most maize fields are treated with soil-applied neonicotinoids (Table 10, Fig. 2) and 25–50% of untreated fields are effectively managed with alternative tools. Hence, there is ample potential for these tools to be used over substantially greater areas.
Most alternatives are exclusively at the research stage or not widely known (Table 7), except for crop rotation and pheromone trapping for monitoring purposes. In Hungary, models to guide crop rotation are used. In the USA, Diabrotica-resistant GM corn hybrids are used along with planting refuges. Lastly, nematode biological control is ready for use in Germany and GM tactics wait to be deployed in Hungary. Our expert evaluation yielded few western corn rootworm management tools. In Slovenia, DSS are available that use degree-day models to predict adult emergence while pheromone-based mating disruption and nematode application is at the research stage. In Germany, laboratory research is ongoing to refine attract and kill using CO2-release capsules and Metarhizium fungi. Experts regularly list environmental and economic impediments to the further adoption and up-scaling of biological control.
Despite low rate of seed or soil treatments (except for Slovenia), the perceived western corn rootworm risk across Europe is still low. In the USA, there is ample potential to reduce reliance upon neonicotinoids, as numerous alternatives are already in practice: crop rotation, Bt corn, monitoring traps, refuges along with Diabrotica-resistant hybrids. The main driver of western corn rootworm attacks is continuous corn planting, and system-level changes—e.g., adoption of crop rotation—can thus drastically lower pest issues. Biological control with Bt, nematodes, or entomopathogenic fungi and biopesticides is equally effective: Azadirachta indica A. Juss. (L.) fruit and leaves have insecticidal effects, while Gliricidia sepium and turmeric act as repellents. Attract and kill options can either use natural attractants (e.g., powdered roots of buffalo gourd, corn seedling volatiles, CO2, extracts of germinating corn) or synthetic volatiles to attract larvae. Lastly, pheromone-based monitoring can feed DSS and guide farmers’ management decisions. In conclusion, multiple alternatives and IPM technology packages are well-tailored to maize production systems globally, and can simultaneously resolve wireworm and western corn rootworm issues. European maize and wheat has historically been grown in a profitable fashion without any chemical insecticides. If today’s growers can steer clear of continuous maize cropping, they can side-step wireworm issues and avoid financial expenditures for insecticide usage.
Brown planthopper in rice
Largely considered a minor rice pest until the mid-1960s, Nilaparvata lugens has assumed the status of destructive pest due to “green revolution” style crop intensification (Pathak and Dhaliwal 1981; Heinrichs and Mochida 1984). Though sharp reductions in pesticide use restored natural enemy communities and resolved N. lugens pest issues during the 1980s and 1990s, (neonicotinoid) insecticides are once again increasingly used, leading to major insecticide resistance issues and triggering N. lugens outbreaks over extensive areas in tropical Asia (Bottrell and Schoenly 2012). In general, N. lugens outbreaks are indicative of crop mismanagement, insecticide abuse and unsustainable rice intensification (Sogawa et al. 2009). In only a few areas, the risk of N. lugens is considered zero e.g., in a high percentage of fields in southern Vietnam. Adoption levels of alternatives greatly vary between sites and individual countries.
Overall, the pest status of brown planthopper was considered medium (25–50%), and its economic damage was rated as low to medium by experts. Yet, neonicotinoid granules are used on 50–75% of the rice area in Vietnam’s Mekong Delta and on 25–50% fields in northern parts of this country (Table 10, Fig. 2). In China, no granular neonicotinoids are used, and 50–75% of untreated fields are managed using alternatives (Table 10). However, both Chinese and northern Vietnamese rice growers adopt foliar sprays of neonicotinoids in 75–100% of fields—though alternatives could readily be used over much of this area (Fig. 2). The high use of insecticide in northern Vietnam and China is associated with high adoption of hybrid rice varieties (> 70% of rice production area), many of which are hyper-susceptible to the white planthopper, Sogatella furcifera, and susceptible to brown planthopper (Horgan and Crisol 2013). In recent years, much research attention has been placed on developing improved hybrid varieties with resistance to both planthopper species (Horgan 2018). In southern Vietnam, large numbers of fields are treated with alternatives as promoted through national programs such as Three Reductions Three Gains (3R3G—reduce seeds, fertilizer, pesticides and gain yield, crop output, and net income) or the “1 Must Do 5 Reductions” (1M5R), which entails using certified seed while pursuing reductions in seed, fertilizer, chemical pesticide inputs, water use, and post-harvest losses.
Alternative tools are practiced in several key rice-producing regions: fertility management (i.e., silicon addition, balanced nitrogen inputs) and resistant varieties are adopted in Vietnam and Indonesia. On the other hand, adapted potassium fertilization is ready for implementation in some countries. Also, IPM packages consisting of appropriate water management (i.e., avoidance of water-stress), insecticide reduction and host plant resistance are adopted in Vietnam. In both Vietnam and Indonesia, the planting of varieties with brown planthopper resistance genes has been hindered by the widespread and rapid adaptation of planthoppers to resistant varieties; however, some success was achieved in Indonesia with the local variety Inapari 13. Landscape-level diversification is practiced in Indonesia and in southern Vietnam, and is ready for implementation in the Philippines. However, although the effects of diversification on planthoppers have been relatively well studied, their impact on multi-species pest complexes has been difficult to anticipate and diversification recommendations thus need to be fine-tuned and locally adapted. Numerous additional tools were considered to be “implementation ready”: biopesticides for example are ready to use in Vietnam. In the Philippines, many alternatives have received research attention, but their practical application (or field-level evaluation and adaptation) is lagging.
Experiences in southern Vietnam and in Indonesia show that holistic, systems-level interventions that combine good agronomy (including the incorporation of organic matter and animal manure), synchronous planting, host plant resistance, and biological control (e.g., 3R3G, 1M5R, or the application of plant growth promoting rhizobacteria), could successfully lower—or even completely eliminate—synthetic insecticides. These kinds of approaches urgently wait to be transferred to other areas and adapted to meet local growers’ needs, conditions, and farming contexts.
This study offers a synthetic review of the extent of usage of neonicotinoid insecticides in four globally important arable cropping systems (i.e., wheat, maize, rice, and cotton), and provides a systematic listing of non-chemical alternatives to replace these products in each system. Our work shows that neonicotinoid use is highest in rice against brown planthopper and in maize against soil-borne pests, and lowest in winter wheat against bird cherry-oat aphid and wireworms though only based on European data. For each of the crop × pest systems, myriad well-tested, cost-effective alternatives are available to swiftly transition away from neonicotinoids. As insect herbivores generally pose low risk in European cereal systems, we do not anticipate notable increases in crop damage (or declines in farm-level revenue) following the continent-wide ban on various popular neonicotinoids. Instead, current EU-wide restrictions on the use of imidacloprid, clothianidin, and thiamethoxam will help restore on-farm biodiversity, strengthen ecosystem services, and enhance in-field biological control. Furthermore, multiple alternatives are available at differing stages of readiness, several of which have been validated, adapted, and successfully used by farmers. Alternatives are locally adopted by non-negligible numbers of farmers in winter wheat to control bird cherry-oat aphid (in Hungary and in Spain), yet farmers wait to adopt alternatives for wireworm management in most countries (Italy, Croatia, Germany, USA). Similar to cereal-based systems, numerous IPM alternatives are available and validated for maize systems, but their farm-level adaptation has not yet fully been realized, especially outside Europe. This may be explained by the higher gross margin of maize compared to cereals, or to the different land-use patterns and agro-landscape structure in Europe as compared to the rest of the word. Overall, we can confidently say that farmers who adopt non-chemical alternatives in small cereals and maize systems are likely to increase profitability of their operations, protect the environment while securing a steady output of safe, nutrient-rich farm produce.
For each of the target pests, despite the current over-reliance on neonicotinoids, promising trends can be observed in all arable crop systems. In the USA and Spain, current coverage of neonicotinoid-treated cereal crops is very high, and there may be considerable potential for reduction. For maize and winter wheat, IPM packages and “regenerative” farming schemes have been devised and field-tested, under which crop yields are sustained and farm profit can even be doubled (e.g., (LaCanne and Lundgren 2018)). For A. gossypii and B. tabaci, though alternatives are well-described in the literature, research findings urgently need to be translated into practice. In certain systems, e.g., Arizona cotton, IPM packages consisting of altered planting dates, sanitary measures, and host-free periods permit a drastic reduction in insecticide use while maximizing field-level abundance and pest suppression potential of natural enemies (e.g., Ellsworth and Martinez-Carrillo (2001); Naranjo (2001)), and these experiences can readily be transferred to other production regions, e.g., in China, Pakistan, Egypt, or West Africa. Also, the well-developed biological control programs for pests such as Bemisia tabaci in greenhouse settings can help feed the design of CBC schemes (and possibly augmentative biological control interventions) in open-field crops. Our survey reveals comparatively high levels of neonicotinoid use in rice production, and low degrees of adoption of alternatives (except for areas in Vietnam, where rice growers have embraced 3R3G or 1M5R). More research is needed to develop full-fledged IPM packages that need to be validated by farmer groups. For brown planthopper in rice, one can now build upon initial successes with these 3R3G or 1M5R, and pursue a further incorporation of semio-chemicals, ecological engineering tactics and agronomic measures to achieve further reductions in insecticide use; however, past successes have been achieved through dedicated attention and due investment in communication strategies and campaign-type implementation. Evidence suggests that once funding for such communication campaigns declines or the campaigns otherwise cease, insecticide use will likely increase (Horgan 2018).
For all crops, organic farming practices can equally restore or bolster ecosystem services such as biological control and help suppress pest populations, though their efficacy is likely pest-dependent (Muneret et al. 2018). In rice, participatory farmer training programs—eventually complemented with mass-media communication campaigns (including farmer-to-farmer video)—can help validate and adapt non-chemical alternatives to local farming contexts and rice production typologies (e.g., upland, low-land paddy). To facilitate these transitions, we introduce some guiding concepts and illuminate examples of successful agricultural extension (and transformation) programs in the section below.
From theory to practice: facilitating the diffusion of alternatives
Our work reveals how several nuclei of farmers worldwide have successfully transitioned away from neonicotinoid insecticides, and instead employ non-chemical management alternatives. Opportunities exist to accelerate this process, engage more growers in regenerative styles of farming and ultimately reach a “tipping point” towards ecological intensification (e.g. (Tittonell 2014, Bommarco et al. 2013, Pretty et al. 2018). In order to enable this transition, a sound understanding is required of the various factors that shape farmers’ technology adoption and the relative contribution of, e.g., cultural, social, economic, climatic, agronomic and in-field ecological processes. Farmer decision-making is complex, and a “systems-level” perspective is essential to fully appreciate why growers in particular localities refrain from using, e.g., biological control while continuing to rely upon (insecticide-based) approaches despite their—often—questionable efficacy, cost-effectiveness, and environmental profile. To successfully upscale alternatives, a focus on “innovation systems” instead of technical particularities of individual technologies is required (Schut et al. 2014), and an integration of individual practices under an IPM umbrella is a must (Stenberg 2017). Using Rogers’ (1962) “Diffusion of innovations” framework, Wyckhuys et al. (2018) identified five key “roadblocks” for a broader adoption of biological control. We adopt this same framework to examine current adoption patterns of neonicotinoid alternatives, and list concrete opportunities to remediate certain “roadblocks” for individual farming contexts and crop × pest systems.
Availability of sufficient knowledge on neonicotinoid alternatives
Diagnosing the “readiness” status of alternative technologies in 7 pest × crop complexes, our works reveals an immense disparity in the local availability of alternatives (and supporting ecological knowledge) between cropping systems, IPM categories and geographies. For example, while 7 different management alternatives are “under research” for brown planthopper in Papua New Guinea, there is only one biological control option “ready for implementation” and none in practice. Earlier work has revealed an overall absence of CBC options for several of the world’s crops and accentuated how multiple insecticide-importing nations have limited or no alternative technologies on offer (Wyckhuys et al. 2013), with only a few commercially available natural enemies in the tropics (van Lenteren 2012). As local absence of alternatives effectively impedes their field-level adoption, our work calls for an acceleration of applied research in rice and for a (farm-level, participatory) technology validation in rice and maize. As a next step, locally validated technologies can be shared with farmers and the general public through, e.g., (mass-media) extension campaigns, “innovation” platforms for knowledge co-creation and sharing, farmer-to-farmer video channels, or online public media (Van Mele et al. 2009; Pretty et al. 2018; Wyckhuys et al. 2019c).
Divergent interests and priorities of farmers
In their daily chores, farmers have to find a delicate balancing act, diverting their attention, time and (often scarce) resources to address multiple concerns. Unpredictable weather patterns, inadequate plant nutrition, crop failure, shifts in availability (or pricing) of inputs and supplies, and fluctuations in demand for harvested produce are all issues on farmers’ minds, and shape farming decisions. Insect pests indeed can constrain crop production and have been shown to reduce yields by 10–16% worldwide (Oerke 2006), and farmers thus rightly worry about an eventual occurrence of pest outbreaks. Also, given their busy schedules, risk-averse farmers with sufficient financial resources regularly favor practices that circumvent laborious monitoring and require little thought (e.g., calendar-based sprays or “convenience” application modes), so-called “lazy-man tactics” (i.e., insecticide seed coating) and other preventative measures. Also, farmers’ actions are often guided by their beliefs and perceptions—instead of by actual pest numbers, pest-induced crop loss or the real financial implications of taking pest control action (Heong et al. 2002; Mourtzinis et al. 2019). Given that our expert panel ranked all target pests as “low- to intermediate-risk” and that many pest problems are secondary (i.e., triggered by farmers’ own insecticide use), it is clear that those perceptions—and associated actions—are radically misguided. For example, in cotton production in the San Joaquin Valley (California), farmers who opt for “preventative” early-season insecticide sprays suffered from secondary pest problems and spent an additional $15/ha to resolve those, once again with synthetic insecticides (Gross and Rosenheim 2011). In Nicaraguan cabbage production, farmers who refrained from insecticide use ran substantially higher profits than those who did not (Bommarco et al. 2011); similar findings have been made for Philippine and Indonesian rice systems. Well-conceptualized and concerted efforts to rectify farmers’ perceptions (and related risk-averse behavior) can thus prevent induced pest issues while greatly benefiting farmers’ pockets.
Weak (agro-ecological) knowledge base
When interviewing farmers in the 1990s, anthropologists were regularly told “nothing kills insects, except for insecticides” (Wyckhuys et al. 2019a, 2019c). Though one might expect shallow ecological knowledge among illiterate, unschooled or resource-poor growers in the developing world, similar patterns—rather surprisingly—have been recorded among contemporary farmers in Western Europe (Zhang et al. 2018). Aside for honeybee pollinators and ladybugs, human beings somehow face supreme difficulties to recognize or enumerate beneficial invertebrates irrespective of their multi-billion dollar contribution to pest management (Losey and Vaughan 2006). For example, overall knowledge of insects among USA college students is restricted to a mere 13 species (Bixler 2017). Switzerland and Japan—countries that top the ranks globally in terms of general education—reported similar patterns (Breuer et al. 2015; Hosaka et al. 2017). In Canada, a national phone survey recorded a positive attitude towards biological control, but also commended intensifying tailored outreach and education (McNeil et al. 2010). In addition to a general disinterest or even fear towards invertebrate natural enemies (including spiders), locally held beliefs can preclude the on-farm trialing and adoption of non-pesticidal alternatives such as biological control (e.g., (Winarto 2004)). Many of the alternatives outlined in this paper are knowledge-intensive, i.e., require a fair degree of specialized (agro-ecological) knowledge on behalf of farmers to secure their successful on-farm adoption. Scientists often assume that farmers do possess the necessary knowledge base to successfully implement IPM; yet this assumption is false. In fact, the vast majority of farmers (and the general public) has no understanding whatsoever of insect-killing fungi or viruses, minute endo-parasitoids or predatory mites (Wyckhuys et al. 2019a). Hence, thoughtfully crafted communication initiatives are required to build or strengthen farmers’ ecological knowledge, provide workable alternatives and steer their decision-making away from costly and environmentally damaging insecticides.
Perceived attributes of alternatives
Several elements inherent to pest management—and perceived by individual farmers in different ways—can either accelerate or impede the uptake and subsequent diffusion of non-chemical alternatives. Five technology attributes in particular constrain the adoption of alternatives such as biological control (Wyckhuys et al. 2019c; Wyckhuys et al. 2018): (i) relative advantage, (ii) compatibility, (iii) complexity, (iv) traceability, and (v) observability. More specifically, (i) USA walnut and pear growers praise the low (financial, human health) cost and environmentally friendly profile of biological control, though often question its advantage in terms of effectiveness (Goldberger and Lehrer 2016). Despite major geographical and temporal variability in cost-effectiveness and yield benefit (Tooker et al. 2017) and inconsistent benefits for farm-level profitability (LaCanne and Lundgren 2018)), neonicotinoids seemingly have other comparative advantages that explain their present-day use on tens of millions of hectares worldwide. (ii) As the efficacy of biological control is often context-dependent, complementary on-farm and landscape-level CBC actions can be taken to bolster its success rates (Shields et al. 2019). Also, certain alternatives are not compatible with (conventional) farm management schemes, e.g., when there is zero weed tolerance on large-scale “manicured” farms (Marshall et al. 2003) or when unguided insecticide applications remain in use (e.g., (Fogel et al. 2013). (iii) A third possible impediment is the (perceived) complexity of alternatives such as CBC floral strips (Gurr et al. 2016), beetle banks or DSS, as compared to neonicotinoid seed coatings—which are readily applied at the time of seed drilling. Certain technologies—such as the non-use of insecticides (Goldberger and Lehrer 2016)—are far less complex, and could yield satisfactory results when coupled with supporting CBC measures and promoted through thoughtful, targeted messaging. (iv) Neonicotinoid-based technologies regularly score high in terms of trialability, as it is easier for a farmer to test the efficacy of seed coatings in a field corner than to effectively trial, e.g., habitat management interventions. In Asia’s rice-growing areas, insecticides are sold “over the counter” in small sachets—similar to fast-moving consumer goods such as candy bars, soap or shampoo, thus further encouraging their trial-adoption. To encourage farmers with the trialing of alternative technologies, one-time economic incentives could be considered (e.g., (Cullen et al. 2008). (v) Observability is a major impediment for technologies that rely upon the use of, e.g., small-sized predatory mites or endophagous parasitoids. On the other hand, farmers—across the globe—take joy in observing the “knock-down” effect of certain insecticides and are often satisfied when there is a total absence of insects—irrespective of them being pests or natural enemies—in crops established with neonicotinoid-coated seed. Hence, when developing and up-scaling non-chemical alternatives, it is important to thoroughly examine the above technology attributes (and the associated decision-making processes).
Perceived type of innovation-decision
Three types of innovation-decision (Rogers 1962), can be distinguished: (i) optional, (ii) collective, and (iii) authority innovation-decisions. All three types are relevant when promoting neonicotinoid alternatives and carry variable potential under different geographical, crop × pest or socio-cultural contexts. A fair share of management decisions in European or USA agriculture are directly made by individual farmers. This may be different for contract farming, where there might be both lucrative opportunities (Sullivan et al. 1999); for Guatemalan snow pea) and important roadblocks (Grossman 1999); for conventional plantation-style banana) to further ecologically centered IPM. The role of collective decision-making processes can best be exemplified by the voluntary enrollment in mutual funds and pest-insurance schemes by entire groups of Italian maize growers, collective efforts to pursue agricultural systems “redesign” (Pretty et al. 2018), or farmers’ organized supply of “quality produce” to supermarkets, e.g., in Vietnam (Moustier et al. 2010). The UN-sponsored “area-wide pest management (AW-IPM)” approach (Vreysen et al. 2007) possibly could be used as an operational framework to phase out neonicotinoid insecticides over large areas and collectively move toward implementation of alternatives. Under such schemes, authority decisions can equally help propel alternatives, as exemplified by Cuba’s 1990s conversion of a staggering 1 million ha to biological control under well-coordinated, state-sponsored programs (Nicholls et al. 2002). Several of the above modus operandi carry potential to deliver pest management alternatives for the arable crops covered in this paper and can help ensure lasting (if not transformative) change at scale.
Our work reiterates how (neonicotinoid) insecticides are not necessarily employed to resolve economically important pest issues, but instead often constitute superfluous cost components in farming operations. Their unguided use can further trigger pest resurgence, degrade ecological resilience of agro-ecosystems and compromise long-term farm profitability. Also, their prophylactic application (e.g., as seed coatings or stem dips) is in direct conflict with globally valid IPM concepts and contributes to biodiversity loss. Our expert panel and scientific literature review reveal how (a) in most systems, pest populations rarely exceed economic threshold levels and the recurrent broad-scale (often prophylactic) use of these products is unjustified; (b) effective IPM procedures and tools are available to immediately reduce or suspend (neonicotinoid) insecticide use; and (c) that such insecticide phase-out can help improve or sustain farm-level revenue streams. Our study identifies several effective alternatives to (neonicotinoid) insecticide use in most important arable crops in the world; some of these alternatives are ready to be used for all the crop × pest combinations. The first and most powerful alternative is just the concrete implementation of the IPM principles: low cost pest risk assessment with complementary limited in field evaluation to identify fields that do not require pest control. For most crop × pest combinations, practical methods are available to identify fields where pest control is needed. Their field-level implementation can be facilitated by establishing an effective independent advisory system and by providing insurance tools that make farmers comfortable with IPM implementation. As to Diabrotica, rotation proved to be the most effective and sustainable alternative. Rotation schemes may be flexible: maize may be rotated at varying frequencies (even after several years), only when monitoring reveals that WCR population levels are increasing, as demonstrated in practice by Furlan et al. 2018. For most crop × pest combinations, landscape management increasing biodiversity proves to be a sound as it can bolster biological control. In rice, pest-resistant varieties can mitigate insecticide use against Nilaparvata lugens.
To facilitate the broad diffusion and farm-level implementation of IPM alternatives, it is necessary to pursue the following five steps: (1) effectively communicate low-cost, labor-saving IPM alternatives among a broad range of stakeholders, including farmers, to trigger farmer experimentation, induce innovation and stimulate technology diffusion (Furlan et al. 2017b); (2) set precise and verifiable targets for IPM implementation for each crop × pest system in the different geographies (e.g., annually diminishing maximum % of insecticide-treated cultivated land); (3) create or re-constitute an independent advisory system that provides objective guidance and scientifically underpinned information on local availability and efficacy of (non-chemical) alternatives; (4) support insurance approaches—e.g., mutual funds—to account for eventual agro-ecological upsets and uncertainties involved in IPM implementation; (5) carry out comprehensive, unbiased risk assessment and development of plant health strategies for those crop × pest systems that currently lack solid and effective IPM packages. By judiciously following these steps, deploying supportive policies and enabling an effective implementation of ecologically centered IPM, neonicotinoid insecticide use can be scaled down swiftly and substantially. Doing so will carry considerable benefits for the environment, farmers and society at large.
Ahmad M, Arif MI (2008) Susceptibility of Pakistani populations of cotton aphid Aphis gossypii (Homoptera: Aphididae) to endosulfan, organophosphorus and carbamate insecticides. Crop Prot 27(3):523–531. https://doi.org/10.1016/j.cropro.2007.08.006
Alford AM, Krupke CH (2019) Movement of the neonicotinoid seed treatment clothianidin into groundwater, aquatic plants, and insect herbivores. Environ Sci Technol 53(24):14368–14376. https://doi.org/10.1021/acs.est.9b05025
Alix VC, Mercier T (2009) Risks to bees from dusts emitted at sowing of coated seeds: concerns, risk assessment and risk management. Julius-Kühn Archive
Al-mazra’awi MS, Ateyyat M (2009) Insecticidal and repellent activities of medicinal plant extracts against the sweet potato whitefly, Bemisia tabaci (Hom.: Aleyrodidae) and its parasitoid Eretmocerus mundus (Hym.: Aphelinidae). J Pest Sci 82(2):149–154
An R, Orellana D, Phelan LP, Cañas L, Grewal PS (2016) Entomopathogenic nematodes induce systemic resistance in tomato against Spodoptera exigua, Bemisia tabaci and Pseudomonas syringae. Biol Control 93:24–29. https://doi.org/10.1016/j.biocontrol.2015.11.001
Ansari MA, Evans M, Butt TM (2009) Identification of pathogenic strains of entomopathogenic nematodes and fungi for wireworm control. Crop Prot 28(3):269–272. https://doi.org/10.1016/j.cropro.2008.11.003
Antony B, Palaniswami MS, Kirk AA, Henneberry TJ (2004) Development of Encarsia bimaculata (Heraty and Polaszek) (Hymenoptera: Aphelinidae) in Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) nymphs. Biol Control 30(3):546–555. https://doi.org/10.1016/j.biocontrol.2004.01.018
Aqueel MA, Leather SR (2011) Effect of nitrogen fertilizer on the growth and survival of Rhopalosiphum padi (L.) and Sitobion avenae (F.) (Homoptera: Aphididae) on different wheat cultivars. Crop Prot 30(2):216–221. https://doi.org/10.1016/j.cropro.2010.09.013
Azzam S, Wang F, Wu J-C, Shen J, Wang L-P, Yang G-Q, Guo Y-R (2009) Comparisons of stimulatory effects of a series of concentrations of four insecticides on reproduction in the rice brown planthopper Nilaparvata lugens Stål (Homoptera: Delphacidae). Int J Pest Manag 55(4):347–358. https://doi.org/10.1080/09670870902934872
Azzam S, Yang F, Wu J-C, Geng J, Yang G-Q (2011) Imidacloprid-induced transference effect on some elements in rice plants and the brown planthopper Nilaparvata lugens (Hemiptera: Delphacidae). Insect Sci 18(3):289–297. https://doi.org/10.1111/j.1744-7917.2010.01352.x
Bale JS, van Lenteren JC, Bigler F (2008) Biological control and sustainable food production. Philos Trans R Soc Lond Ser B Biol Sci 363(1492):761–776. https://doi.org/10.1098/rstb.2007.2182
Barratt BIP, Moran VC, Bigler F, van Lenteren JC (2018) The status of biological control and recommendations for improving uptake for the future. BioControl 63(1):155–167. https://doi.org/10.1007/s10526-017-9831-y
Barzman M, Paolo B, Nicholas A, Birch E, Boonekamp P, Dachbrodt-Saaydeh S, Graf B, Hommel B, Jensen JE, Kiss J, Kudsk P, Lamichhane JR, Messéan A, Moonen A-C, Ratnadass A, Ricci P, Sarah J-L, Sattin M (2015) Eight principles of integrated pest management. Agron Sustain Dev 35(4):1199–1215. https://doi.org/10.1007/s13593-015-0327-9
Basanth YS, Sannaveerappanavar VT, Sidde Gowda DK (2013) susceptibility of different populations of Nilaparvata lugens from major rice growing areas of Karnataka, India to Different Groups of Insecticides. Rice Sci 20(5):371–378. https://doi.org/10.1016/S1672-6308(13)60147-X
Bass C, Denholm I, Williamson MS, Nauen R (2015) The global status of insect resistance to neonicotinoid insecticides. Pestic Biochem Physiol 121:78–87. https://doi.org/10.1016/j.pestbp.2015.04.004
Bateman R (2016) The Role of Pesticides in SE Asian Rice IPM: a view from the Mekong Delta. Outlooks Pest Manag 27(2):53–60. https://doi.org/10.1564/v27_apr_02
Bažok R, Sivčev I, Kos T, Barčić JI, Kiss J, Jankovič S (2011) Pherocon AM trapping and the “whole plant count” method—a comparison of two sampling techniques to estimate the WCR adult densities in Central Europe. Cereal Res Commun 39(2):298–305 https://www.bib.irb.hr/444719?〈=ENLiving&rad = 444719
Bellamy DE, Asplen MK, Byrne DN (2004) Impact of Eretmocerus eremicus (Hymenoptera: Aphelinidae) on open-field Bemisia tabaci (Hemiptera: Aleyrodidae) populations. Biol Control 29(2):227–234. https://doi.org/10.1016/S1049-9644(03)00150-6
Benefer CM, Knight ME, Ellis JS, Hicks H, Blackshaw RP (2012) Understanding the relationship between adult and larval Agriotes distributions: The effect of sampling method, species identification and abiotic variables. Appl Soil Ecol 53:39–48. https://doi.org/10.1016/j.apsoil.2011.11.004
Bi JL, Toscano NC, Madore MA (2003) Effect of urea fertilizer application on soluble protein and free amino acid content of cotton petioles in relation to silverleaf whitefly (Bemisia argentifolii) populations. J Chem Ecol 29(3):747–761. https://doi.org/10.1023/a:1022880905834
Bixler RD (2017) Beautiful bugs, bothersome bugs, and FUN bugs: examining human interactions with insects and other arthropods AU - Shipley, Nathan J. Anthrozoös 30(3):357–372. https://doi.org/10.1080/08927936.2017.1335083
Blacquière T, Smagghe G, van Gestel CAM, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21(4):973–992. https://doi.org/10.1007/s10646-012-0863-x
Bollinger EK, Caslick JW (1985) Northern corn rootworm beetle densities near a red-winged blackbird roost. Can J Zool 63(3):502–505. https://doi.org/10.1139/z85-073
Bommarco R, Miranda F, Bylund H, Björkman C (2011) Insecticides suppress natural enemies and increase pest damage in cabbage. J Econ Entomol 104(3):782–791. https://doi.org/10.1603/EC10444
Bommarco R, Kleijn D, Potts SG (2013) Ecological intensification: harnessing ecosystem services for food security. Trends Ecol Evol 28(4):230–238. https://doi.org/10.1016/j.tree.2012.10.012
Bonmatin JM, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke C, Liess M, Long E, Marzaro M, Mitchell EA, Noome DA, Simon-Delso N, Tapparo A (2015) Environmental fate and exposure; neonicotinoids and fipronil. Environ Sci Pollut Res Int 22(1):35–67. https://doi.org/10.1007/s11356-014-3332-7
Bortolotti L, Sabatini AG, Mutinelli F, Astuti M, Lavazza A, Piro R, Tesoriero D, Medrzycki P, Sgolastra F, Porrini C (2009) Spring honey bee losses in Italy, pp 148–152 https://www.cabdirect.org/cabdirect/abstract/20113401186
Bottrell DG, Schoenly KG (2012) Resurrecting the ghost of green revolutions past: the brown planthopper as a recurring threat to high-yielding rice production in tropical Asia. J Asia Pac Entomol 15(1):122–140. https://doi.org/10.1016/j.aspen.2011.09.004
Brandl MA, Schumann M, Przyklenk M, Patel A, Vidal S (2017) Wireworm damage reduction in potatoes with an attract-and-kill strategy using Metarhizium brunneum. J Pest Sci 90(2):479–493. https://doi.org/10.1007/s10340-016-0824-x
Bredeson MM, Lundgren JG (2015a) A survey of the foliar and soil arthropod communities in sunflower (Helianthus annuus) fields of central and eastern South Dakota. J Kansas Entomol Soc 88(3):305–315. https://doi.org/10.2317/0022-8567-88.3.305
Bredeson MM, Lundgren JG (2015b) Thiamethoxam seed treatments have no impact on pest numbers or yield in cultivated sunflowers. J Econ Entomol 108(6):2665–2671. https://doi.org/10.1093/jee/tov249
Bredeson MM, Reese RN, Lundgren JG (2015) The effects of insecticide dose and herbivore density on tri-trophic effects of thiamethoxam in a system involving wheat, aphids, and ladybeetles. Crop Prot 69:70–76. https://doi.org/10.1016/j.cropro.2014.12.010
Breuer GB, Schlegel J, Kauf P, Rupf R (2015) The Importance of Being Colorful and Able to Fly: Interpretation and implications of childrenʼs statements on selected insects and other invertebrates. Int J Sci Educ 37(16):2664–2687. https://doi.org/10.1080/09500693.2015.1099171
Burgio G, Ferrari R, Boriani L, Pozzati M, van Lenteren J (2006) The role of ecological infrastructures on Coccinellidae (Coleoptera) and other predators in weedy field margins within northern Italy agroecosystems. Bull Insectol 59 http://www.bulletinofinsectology.org/pdfarticles/vol59-2006-059-067burgio.pdf
Burgio G, Ragaglini G, Petacchi R, Ferrari R, Pozzati M, Furlan L (2012) Optimization of Agriotes sordidus monitoring in northern Italy rural landscape, using a spatial approach. Bull Insectol 65(1):123–131. http://www.bulletinofinsectology.org/pdfarticles/vol65-2012-123-131burgio.pdf
Calvo-Agudo M, Gonzalez-Cabrera J, Pico Y, Calatayud-Vernich P, Urbaneja A, Dicke M, Tena A (2019) Neonicotinoids in excretion product of phloem-feeding insects kill beneficial insects. Proc Natl Acad Sci U S A 116(34):16817–16822. https://doi.org/10.1073/pnas.1904298116
Carreck NL, Ratnieks FLW (2014) The dose makes the poison: have “field realistic” rates of exposure of bees to neonicotinoid insecticides been overestimated in laboratory studies? J Apic Res 53(5):607–614. https://doi.org/10.3896/IBRA.1.53.5.08
Chagnon M, Kreutzweiser D, Mitchell EAD, Morrissey CA, Noome DA, Van der Sluijs JP (2015) Risks of large-scale use of systemic insecticides to ecosystem functioning and services. Environ Sci Pollut Res 22(1):119–134. https://doi.org/10.1007/s11356-014-3277-x
Choate BA, Lundgren JG (2015) Invertebrate communities in spring wheat and the identification of cereal aphid predators through molecular gut content analysis. Crop Prot 77:110–118. https://doi.org/10.1016/j.cropro.2015.07.021
Crafts-Brandner SJ (2002) Plant nitrogen status rapidly alters amino acid metabolism and excretion in Bemisia tabaci. J Insect Physiol 48(1):33–41. https://doi.org/10.1016/S0022-1910(01)00140-8
Cresswell JE, Desneux N, van Engelsdorp D (2012) Dietary traces of neonicotinoid pesticides as a cause of population declines in honey bees: an evaluation by Hillʼs epidemiological criteria. Pest Manag Sci 68(6):819–827. https://doi.org/10.1002/ps.3290
Cullen R, Warner KD, Jonsson M, Wratten SD (2008) Economics and adoption of conservation biological control:272–280. https://doi.org/10.1016/j.biocontrol.2008.01.016
Day RL, Hickman JM, Sprague RI, Wratten SD (2015) Predatory hoverflies increase oviposition in response to colour stimuli offering no reward: Implications for biological control. Basic Appl Ecol 16(6):544–552. https://doi.org/10.1016/j.baae.2015.05.004
Dedryver C-A, Le Ralec A, Fabre F (2010) The conflicting relationships between aphids and men: a review of aphid damage and control strategies. C R Biol 333(6):539–553. https://doi.org/10.1016/j.crvi.2010.03.009
Deguine J-P, Ferron P, Russell D (2008) Sustainable pest management for cotton production. A review. Agron Sustain Dev 28(1):113–137. https://doi.org/10.1051/agro:2007042
Doucet-Personeni C, Halm MP, Touffet F, Rortais A, and Arnold G (2003) Imidaclopride utilisé en enrobage de semences (Gaucho®) et troubles des abeilles. Comité Scientifique et Technique de l'Etude Multifactorielle des Troubles des Abeilles (CST). https://controverses.sciences-po.fr/archive/pesticides/rapportfin.pdf
Douglas MR, Tooker JF (2015) Large-scale deployment of seed treatments has driven rapid increase in use of neonicotinoid insecticides and preemptive pest management in U.S. field crops. Environ Sci Technol 49(8):5088–5097. https://doi.org/10.1021/es506141g
Douglas MR, Tooker JF (2016) Meta-analysis reveals that seed-applied neonicotinoids and pyrethroids have similar negative effects on abundance of arthropod natural enemies. PeerJ 4:e2776. https://doi.org/10.7717/peerj.2776
Douglas MR, Rohr JR, Tooker JF (2015) EDITOR'S CHOICE: Neonicotinoid insecticide travels through a soil food chain, disrupting biological control of non-target pests and decreasing soya bean yield. J Appl Ecol 52(1):250–260. https://doi.org/10.1111/1365-2664.12372
Down RE, Cuthbertson AGS, Mathers JJ, Walters KFA (2009) Dissemination of the entomopathogenic fungi, Lecanicillium longisporum and L. muscarium, by the predatory bug, Orius laevigatus, to provide concurrent control of Myzus persicae, Frankliniella occidentalis and Bemisia tabaci. Biol Control 50(2):172–178. https://doi.org/10.1016/j.biocontrol.2009.03.010
Ellsworth PC, Martinez-Carrillo JL (2001) IPM for Bemisia tabaci: a case study from North America. Crop Prot 20(9):853–869. https://doi.org/10.1016/S0261-2194(01)00116-8
Eng ML, Stutchbury BJM, Morrissey CA (2019) A neonicotinoid insecticide reduces fueling and delays migration in songbirds. Science 365(6458):1177–1180. https://doi.org/10.1126/science.aaw9419
Escalada MM, Heong KL (2004) A participatory exercise for modifying rice farmers’ beliefs and practices in stem borer loss assessment. Crop Prot 23(1):11–17. https://doi.org/10.1016/S0261-2194(03)00161-3
Esser AD, Milosavljević I, Crowder DW (2015) Effects of neonicotinoids and crop rotation for managing wireworms in wheat crops. J Econ Entomol 108(4):1786–1794. https://doi.org/10.1093/jee/tov160
Fabre F, Dedryver C-A, Plantegenest M, Hullé M, Rivot E (2010) Hierarchical Bayesian modelling of plant colonisation by winged aphids: inferring dispersal processes by linking aerial and field count data. Ecol Model 221(15):1770–1778. https://doi.org/10.1016/j.ecolmodel.2010.04.006
Finlay KJ, Luck JE (2011) Response of the bird cherry-oat aphid (Rhopalosiphum padi) to climate change in relation to its pest status, vectoring potential and function in a crop–vector–virus pathosystem. Agric Ecosyst Environ 144(1):405–421. https://doi.org/10.1016/j.agee.2011.08.011
Fogel MN, Schneider MI, Desneux N, Gonzalez B, Ronco AE (2013) Impact of the neonicotinoid acetamiprid on immature stages of the predator Eriopis connexa (Coleoptera: Coccinellidae). Ecotoxicology 22(6):1063–1071. https://doi.org/10.1007/s10646-013-1094-5
Furlan L (1996) The biology of Agriotes ustulatus Schäller (Col., Elateridae). I. Adults and oviposition. J Appl Entomol 120(1-5):269–274. https://doi.org/10.1111/j.1439-0418.1996.tb01605.x
Furlan L (2004) The biology of Agriotes sordidus Illiger (Col., Elateridae). J Appl Entomol 128(9-10):696–706. https://doi.org/10.1111/j.1439-0418.2004.00914.x
Furlan (2005) An IPM approach targeted against wireworms: what has been done and what still has to be done. IOBC/WPRS Bull 28(2):91–100 10.1.1.427.501
Furlan L (2014) IPM thresholds for Agriotes wireworm species in maize in Southern Europe. J Pest Sci 87(4):609–617. https://doi.org/10.1007/s10340-014-0583-5
Furlan L, Kreutzweiser D (2015) Alternatives to neonicotinoid insecticides for pest control: case studies in agriculture and forestry. Environ Sci Pollut Res 22(1):135–147. https://doi.org/10.1007/s11356-014-3628-7
Furlan L, Tóth M (2007) Occurrence of click beetle pest spp.(Coleoptera, Elateridae) in Europe as detected by pheromone traps: survey results of 1998-2006. IOBC WPRS Bull 30(7):19 http://csalomontraps.com/7publications/clickbeetles7.pdf
Furlan L, Contiero B, Chiarini F, Colauzzi M, Sartori E, Benvegnù I, Fracasso F, Giandon P (2017a) Risk assessment of maize damage by wireworms (Coleoptera: Elateridae) as the first step in implementing IPM and in reducing the environmental impact of soil insecticides. Environ Sci Pollut Res 24(1):236–251. https://doi.org/10.1007/s11356-016-7692-z
Furlan L, Vasileiadis VP, Chiarini F, Huiting H, Leskovšek R, Razinger J, Holb IJ, Sartori E, Urek G, Verschwele A, Benvegnù I, Sattin M (2017b) Risk assessment of soil-pest damage to grain maize in Europe within the framework of Integrated Pest Management. Crop Prot 97:52–59. https://doi.org/10.1016/j.cropro.2016.11.029
Furlan L, Pozzebon A, Duso C, Simon-Delso N, Sánchez-Bayo F, Marchand PA, Codato F, van Lexmond MB, Bonmatin J-M (2018) An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 3: alternatives to systemic insecticides. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-017-1052-5
Furlan L, Benvegnù I, Chiarini F, Loddo D, Morari F (2020) Meadow-ploughing timing as an integrated pest management tactic to prevent soil-pest damage to maize. Eur J Agron 112:125950. https://doi.org/10.1016/j.eja.2019.125950
Garibaldi LA, Carvalheiro LG, Leonhardt SD, Aizen MA, Blaauw BR, Isaacs R, Kuhlmann M, Kleijn D, Klein AM, Kremen C, Morandin L, Scheper J, Winfree R (2014) From research to action: enhancing crop yield through wild pollinators. Front Ecol Environ 12(8):439–447. https://doi.org/10.1890/130330
Gerling D, Naranjo SE (1998) The Effect of insecticide treatments in cotton fields on the levels of parasitism of Bemisia tabaci (Gennadius) sl. Biol Control 12(1):33–41. https://doi.org/10.1006/bcon.1998.0613
Giarola LTP, Martins SGF, Toledo Costa MCP (2006) Computer simulation of Aphis gossypii insects using Penna aging model. Phys A Stat Mech Appl 368(1):147–154. https://doi.org/10.1016/j.physa.2005.11.057
Gibbons D, Morrissey C, Mineau P (2015) A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife. Environ Sci Pollut Res 22(1):103–118. https://doi.org/10.1007/s11356-014-3180-5
Goldberger JR, Lehrer N (2016) Biological control adoption in western U.S. orchard systems: results from grower surveys. Biol Control 102(C):101–111. https://doi.org/10.1016/j.biocontrol.2015.09.004
Gonzalez-Andujar JL, Garcia-de Ceca JL, Fereres A (1993) Cereal aphids expert system (CAES): identification and decision making. Comput Electron Agric 8(4):293–300. https://doi.org/10.1016/0168-1699(93)90017-U
Gosselke U, Triltsch H, Roßberg D, Freier B (2001) GETLAUS01—the latest version of a model for simulating aphid population dynamics in dependence on antagonists in wheat. Ecol Model 145(2):143–157. https://doi.org/10.1016/S0304-3800(01)00386-6
Gross K, Rosenheim JA (2011) Quantifying secondary pest outbreaks in cotton and their monetary cost with causal-inference statistics. Ecol Appl 21(7):2770–2780. https://doi.org/10.1890/11-0118.1
Grossman LS (1999) The Political ecology of bananas : contract farming, peasants, and agrarian change in the Eastern Caribbean / L.S. Grossman. Vol. 55
Gurr GM, Lu Z, Zheng X, Xu H, Zhu P, Chen G, Yao X, Cheng J, Zhu Z, Catindig JL, Villareal S, Van Chien H, Cuong Le Q, Channoo C, Chengwattana N, Lan LP, Hai Le H, Chaiwong J, Nicol HI, Perovic DJ, Wratten SD, Heong KL (2016) Multi-country evidence that crop diversification promotes ecological intensification of agriculture. Nat Plants 2:16014 England
Gurr GM, Wratten SD, Landis DA, You M (2017) Habitat management to suppress pest populations: progress and prospects. Annu Rev Entomol 62:91–109. https://doi.org/10.1146/annurev-ento-031616-035050
Gurulingappa P, Sword GA, Murdoch G, McGee PA (2010) Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. Biol Control 55(1):34–41. https://doi.org/10.1016/j.biocontrol.2010.06.011
Hadi BAR, Garcia CPF, Heong KL (2015) Susceptibility of Nilaparvata lugens (Hemipteran: Delphacidae) populations in the Philippines to insecticides. Crop Prot 76:100–102. https://doi.org/10.1016/j.cropro.2015.07.002
Harrington RC, Suzanne J, Welham SJ, Verrier PJ, Denholm CH, Hullé M, Maurice D, Rounsevell MD, Cocu N, European Union Examine Consortium (2007) Environmental change and the phenology of European aphids. Glob Chang Biol 13(8):1550–1564. https://doi.org/10.1111/j.1365-2486.2007.01394.x
He W, Yang M, Li Z, Qiu J, Liu F, Xiaosheng Q, Qiu Y, Li R (2015) High levels of silicon provided as a nutrient in hydroponic culture enhances rice plant resistance to brown planthopper. Crop Prot 67:20–25. https://doi.org/10.1016/j.cropro.2014.09.013
Heinrichs, Mochida (1984) From secondary to major pest status: the case of insecticide-induced rice brown planthopper, Nilaparvata lugens, resurgence. Prot Ecol 1:201–218
Hemerik L, Bianchi F, van de Wiel I, Fu D, Zou Y, Xiao H, van der Werf W (2018) Survival analysis of brown plant hoppers (Nilaparvata lugens) in rice using video recordings of predation events. Biol Control 127:155–161. https://doi.org/10.1016/j.biocontrol.2018.08.023
Henry M, Béguin M, Requier F, Rollin O, Odoux J-F, Aupinel P, Aptel J, Tchamitchian S, Decourtye A (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336(6079):348–350. https://doi.org/10.1126/science.1215039
Heong KL, Escalada MM, Sengsoulivong V, Schiller J (2002) Insect management beliefs and practices of rice farmers in Laos. Agric Ecosyst Environ 92(2):137–145. https://doi.org/10.1016/S0167-8809(01)00304-8
Hermann A, Brunner N, Hann P, Wrbka T, Kromp B (2013) Correlations between wireworm damages in potato fields and landscape structure at different scales. J Pest Sci 86(1):41–51. https://doi.org/10.1007/s10340-012-0444-z
Herron GA, Wilson LJ (2011) Neonicotinoid resistance in Aphis gossypii Glover (Aphididae: Hemiptera) from Australian cotton. Aust J Entomol 50(1):93–98. https://doi.org/10.1111/j.1440-6055.2010.00788.x
Hladik ML, Main AR, Goulson D (2018) Environmental risks and challenges associated with neonicotinoid insecticides. Environ Sci Technol 52(6):3329–3335. https://doi.org/10.1021/acs.est.7b06388
Hoelmer KA (2007) Field cage evaluation of introduced Eretmocerus species (Hymenoptera: Aphelinidae) against Bemisia tabaci strain B (Homoptera: Aleyrodidae) on cantaloupe. Biol Control 43(2):156–162. https://doi.org/10.1016/j.biocontrol.2007.07.010
Hong-xing X, Yang Y-j, Lu Y-h, Zheng X-s, Jun-ce T, Feng-xiang L, Qiang F, Lu Z-x (2017) Sustainable management of rice insect pests by non-chemical-insecticide technologies in China. Rice Sci 24(2):61–72. https://doi.org/10.1016/j.rsci.2017.01.001
Horgan F (2017) Integrated pest management for sustainable rice cultivation: a holistic approach.
Horgan FG (2018) Integrating gene deployment and crop management for improved rice resistance to Asian planthoppers. Crop Prot 110:21–33. https://doi.org/10.1016/j.cropro.2018.03.013
Horgan FG, Crisol E (2013) Hybrid rice and insect herbivores in Asia. Entomol Exp Appl 148(1):1–19. https://doi.org/10.1111/eea.12080
Horgan FG, Ramal AF, Bernal CC, Villegas JM, Stuart AM, Almazan MLP (2016) Applying ecological engineering for sustainable and resilient rice production systems. Procedia Food Sci 6:7–15. https://doi.org/10.1016/j.profoo.2016.02.002
Hosaka T, Sugimoto K, Numata S (2017) Childhood experience of nature influences the willingness to coexist with biodiversity in cities. Palgrave Commun 3:17071. https://doi.org/10.1057/palcomms.2017.71
Houndété TA, Kétoh GK, Hema OSA, Brévault T, Glitho IA, Martin T (2010) Insecticide resistance in field populations of Bemisia tabaci (Hemiptera: Aleyrodidae) in West Africa. Pest Manag Sci 66(11):1181–1185. https://doi.org/10.1002/ps.2008
Humann-Guilleminot S, Binkowski ŁJ, Jenni L, Hilke G, Glauser G, Helfenstein F (2019a) A nation-wide survey of neonicotinoid insecticides in agricultural land with implications for agri-environment schemes. J Appl Ecol 56(7):1502–1514. https://doi.org/10.1111/1365-2664.13392
Humann-Guilleminot S, Clément S, Desprat J, Binkowski ŁJ, Glauser G, Helfenstein F (2019b) A large-scale survey of house sparrows feathers reveals ubiquitous presence of neonicotinoids in farmlands. Sci Total Environ 660:1091–1097. https://doi.org/10.1016/j.scitotenv.2019.01.068
Jaffuel G, Hiltpold I, Turlings TCJ (2015) Highly Potent Extracts from Pea (Pisum sativum) and Maize (Zea mays) Roots can be used to induce quiescence in entomopathogenic nematodes. J Chem Ecol 41(9):793–800. https://doi.org/10.1007/s10886-015-0623-5
Jeschke P, Nauen R, Schindler M, Elbert A (2011) Overview of the status and global strategy for neonicotinoids. J Agric Food Chem 59(7):2897–2908. https://doi.org/10.1021/jf101303g
Johnson SN, Benefer CM, Frew A, Griffiths BS, Hartley SE, Karley AJ, Rasmann S, Schumann M, Sonnemann I, Robert CAM (2016) New frontiers in belowground ecology for plant protection from root-feeding insects. Appl Soil Ecol 108:96–107. https://doi.org/10.1016/j.apsoil.2016.07.017
Jung J, Racca P, Schmitt J, Kleinhenz B (2014) SIMAGRIO-W: Development of a prediction model for wireworms in relation to soil moisture, temperature and type. J Appl Entomol 138(3):183–194. https://doi.org/10.1111/jen.12021
Kabaluk T (2014) Targeting the click beetle Agriotes obscurus with entomopathogens as a concept for wireworm biocontrol. BioControl 59(5):607–616. https://doi.org/10.1007/s10526-014-9603-x
Karp DS, Chaplin-Kramer R, Meehan TD, Martin EA, DeClerck F, Grab H, Gratton C, Hunt L, Larsen AE, Martinez-Salinas A, O'Rourke ME, Rusch A, Poveda K, Jonsson M, Rosenheim JA, Schellhorn NA, Tscharntke T, Wratten SD, Zhang W, Iverson AL, Adler LS, Albrecht M, Alignier A, Angelella GM, Zubair Anjum M, Avelino J, Batary P, Baveco JM, Fjja B, Birkhofer K, Bohnenblust EW, Bommarco R, Brewer MJ, Caballero-Lopez B, Carriere Y, Carvalheiro LG, Cayuela L, Centrella M, Cetkovic A, Henri DC, Chabert A, Costamagna AC, De la Mora A, de Kraker J, Desneux N, Diehl E, Diekotter T, Dormann CF, Eckberg JO, Entling MH, Fiedler D, Franck P, Frank van Veen FJ, Frank T, Gagic V, Garratt MPD, Getachew A, Gonthier DJ, Goodell PB, Graziosi I, Groves RL, Gurr GM, Hajian-Forooshani Z, Heimpel GE, Herrmann JD, Huseth AS, Inclan DJ, Ingrao AJ, Iv P, Jacot K, Johnson GA, Jones L, Kaiser M, Kaser JM, Keasar T, Kim TN, Kishinevsky M, Landis DA, Lavandero B, Lavigne C, Le Ralec A, Lemessa D, Letourneau DK, Liere H, Lu Y, Lubin Y, Luttermoser T, Maas B, Mace K, Madeira F, Mader V, Cortesero AM, Marini L, Martinez E, Martinson HM, Menozzi P, Mitchell MGE, Miyashita T, Molina GAR, Molina-Montenegro MA, O'Neal ME, Opatovsky I, Ortiz-Martinez S, Nash M, Ostman O, Ouin A, Pak D, Paredes D, Parsa S, Parry H, Perez-Alvarez R, Perovic DJ, Peterson JA, Petit S, Philpott SM, Plantegenest M, Plecas M, Pluess T, Pons X, Potts SG, Pywell RF, Ragsdale DW, Rand TA, Raymond L, Ricci B, Sargent C, Sarthou JP, Saulais J, Schackermann J, Schmidt NP, Schneider G, Schuepp C, Sivakoff FS, Smith HG, Stack Whitney K, Stutz S, Szendrei Z, Takada MB, Taki H, Tamburini G, Thomson LJ, Tricault Y, Tsafack N, Tschumi M, Valantin-Morison M, Van Trinh M, van der Werf W, Vierling KT, Werling BP, Wickens JB, Wickens VJ, Woodcock BA, Wyckhuys K, Xiao H, Yasuda M, Yoshioka A, Zou Y (2018) Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. Proc Natl Acad Sci U S A 115(33):E7863–e7870. https://doi.org/10.1073/pnas.1800042115
Kaster V, and Showers JW (1984) Modeling black cutworm (Lepidoptera: Noctuidae) field development in Iowa. Vol 13
Khatiwada JR, Ghimire S, Khatiwada SP, Paudel B, Bischof R, Jiang J, Haugaasen T (2016) Frogs as potential biological control agents in the rice fields of Chitwan, Nepal. Agric Ecosyst Environ 230:307–314. https://doi.org/10.1016/j.agee.2016.06.025
Kim JJ, Kim KC (2008) Selection of a highly virulent isolate of Lecanicillium attenuatum against cotton aphid. J Asia Pac Entomol 11(1):1–4. https://doi.org/10.1016/j.aspen.2008.02.001
Kogan M (1998) Integrated pest management: historical perspectives and contemporary developments. Annu Rev Entomol 43(1):243–270. https://doi.org/10.1146/annurev.ento.43.1.243
Koo H-N, An J-J, Park S-E, Kim J-I, Kim G-H (2014) Regional susceptibilities to 12 insecticides of melon and cotton aphid, Aphis gossypii (Hemiptera: Aphididae) and a point mutation associated with imidacloprid resistance. Crop Prot 55:91–97. https://doi.org/10.1016/j.cropro.2013.09.010
Kos T, Bažok R, Gunjača J, Igrc Barčić J (2014) Western corn rootworm adult captures as a tool for the larval damage prediction in continuous maize. J Appl Entomol 138(3):173–182. https://doi.org/10.1111/jen.12010
Kuhlmann U, van der Burgt WACM (1998) Possibilities for biological control of the western corn rootworm, Diabrotica virgifera virgifera LeConte, in Central Europe. Biocontrol News Inf 19(2):59–68 https://www.cabi.org/isc/abstract/19981107724
Kumar R, Kranthi S, Nitharwal M, Jat SL, Monga D (2012) Influence of pesticides and application methods on pest and predatory arthropods associated with cotton. Phytoparasitica 40(5):417–424. https://doi.org/10.1007/s12600-012-0241-5
Kurtz B, Hiltpold I, Turlings TCJ, Kuhlmann U, Toepfer S (2008) Comparative susceptibility of larval instars and pupae of the western corn rootworm to infection by three entomopathogenic nematodes. BioControl 54(2):255–262. https://doi.org/10.1007/s10526-008-9156-y
Kuusk AK, Cassel-Lundhagen A, Kvarnheden A, Ekbom B (2008) Tracking aphid predation by lycosid spiders in spring-sown cereals using PCR-based gut-content analysis. Basic Appl Ecol 9(6):718–725. https://doi.org/10.1016/j.baae.2007.08.012
Kwon SH, Kim D-S (2017) Effects of temperature and photoperiod on the production of sexual morphs of Aphis gossypii (Hemiptera: Aphididae) in Jeju, Korea. J Asia Pac Entomol 20(1):53–56. https://doi.org/10.1016/j.aspen.2016.11.006
LaCanne CE, Lundgren JG (2018) Regenerative agriculture: merging farming and natural resource conservation profitably. PeerJ 6:e4428. https://doi.org/10.7717/peerj.4428
Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201. https://doi.org/10.1146/annurev.ento.45.1.175
Lazreg F, Huang Z, Ali S, Ren S (2009) Effect of Lecanicillium muscarium on Eretmocerus sp. nr. furuhashii (Hymenoptera: Aphelinidae), a parasitoid of Bemisia tabaci (Hemiptera: Aleyrodidae). J Pest Sci 82(1):27–32. https://doi.org/10.1007/s10340-008-0215-z
Liu J-L, Zhang H-M, Chen X, Yang X, Jin-Cai W (2013) Effects of rice potassium level on the fecundity and expression of the vitellogenin gene of Nilaparvata lugens (Stål) (Hemiptera: Delphacidae). J Asia Pac Entomol 16(4):411–414. https://doi.org/10.1016/j.aspen.2013.06.001
Losey JE, Vaughan M (2006) The Economic Value of ecological services provided by insects. BioScience 56(4):311–323. https://doi.org/10.1641/0006-3568(2006)56[311:tevoes]2.0.co;2
Lu Z-X, Heong K-L, Yu X-P, Cui H (2004) Effects of plant nitrogen on ecological fitness of the brown planthopper, Nilaparvata lugens Stal. in rice. J Asia Pac Entomol 7(1):97–104. https://doi.org/10.1016/S1226-8615(08)60204-6
Lu Y, Wu K, Jiang Y, Guo Y, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487(7407):362–365. https://doi.org/10.1038/nature11153
Lundin O, Rundlöf M, Smith HG, Fries I, Bommarco R (2015) Neonicotinoid insecticides and their impacts on bees: a systematic review of research approaches and identification of knowledge gaps. PLoS One 10(8):e0136928. https://doi.org/10.1371/journal.pone.0136928
Ma F, Ding Z, Cheng X (2001) Chaos and predictable time-scale of the brown planthopper Nilaparvata Lugens (Stål) occurrence system. J Asia Pac Entomol 4(1):67–74. https://doi.org/10.1016/S1226-8615(08)60106-5
Ma X-y, Wu H-w, Jiang W-l, Ma Y-j, Ma Y (2016) Weed and insect control affected by mixing insecticides with glyphosate in cotton. J Integr Agric 15(2):373–380. https://doi.org/10.1016/S2095-3119(15)61188-1
Mann JA, Harrington R, Carter N, Plumb RT (1997) Control of aphids and barley yellow dwarf virus in spring-sown cereals. Crop Prot 16(1):81–87. https://doi.org/10.1016/S0261-2194(96)00068-3
Marshall EJP, Brown VK, Boatman ND, Lutman PJW, Squire GR, Ward LK (2003) The role of weeds in supporting biological diversity within crop fields*. Weed Res 43(2):77–89. https://doi.org/10.1046/j.1365-3180.2003.00326.x
Matsumura M, Takeuchi H, Satoh M, Sanada-Morimura S, Otuka A, Watanabe T, Van Thanh D (2008) Species-specific insecticide resistance to imidacloprid and fipronil in the rice planthoppers Nilaparvata lugens and Sogatella furcifera in East and South-east Asia. Pest Manag Sci 64(11):1115–1121. https://doi.org/10.1002/ps.1641
Matsuura A, Nakamura M (2014) Development of neonicotinoid resistance in the cotton aphid Aphis gossypii (Hemiptera: Aphididae) in Japan. Appl Entomol Zool 49(4):535–540. https://doi.org/10.1007/s13355-014-0289-4
Matyjaszczyk E (2017) Comparison between seed and foliar treatment as a tool in integrated pest management. J Agric Food Chem 65(30):6081–6086. https://doi.org/10.1021/acs.jafc.7b01095
Matyjaszczyk E, Sobczak J, Szulc M (2015) Is the possibility of replacing seed dressings containing neonicotinoids with other means of protection viable in major Polish agricultural crops? J Plant Prot Res 55(4). https://doi.org/10.1515/jppr-2015-0056
Maxim L, van der Sluijs J (2013) Seed-dressing systemic insecticides and honeybees. in late lessons from early warnings: science, precaution, innovation. European Environment Agency (EEA), Copenhagen
McNeil JN, Cotnoir PA, Leroux T, Laprade R, Schwartz JL (2010) A Canadian national survey on the public perception of biological control. BioControl 55(4):445–454. https://doi.org/10.1007/s10526-010-9273-2
Meehan TD, Gratton C (2016) A landscape view of agricultural insecticide use across the conterminous US from 1997 through 2012. PLoS One 11(11):e0166724–e0166724. https://doi.org/10.1371/journal.pone.0166724
Metcalf RL (1986) Methods for the study of pest Diabrotica. In: Krysan J, Miller T (eds) Foreword. Spingerl-Verlag, New York, pp 1–23 https://link.springer.com/content/pdf/bfm%3A978-1-4612-4868-2%2F1.pdf
Milosavljević I, Esser AD, Murphy KM, Crowder DW (2019) Effects of imidacloprid seed treatments on crop yields and economic returns of cereal crops. Crop Prot 119:166–171. https://doi.org/10.1016/j.cropro.2019.01.027
Min S, Lee SW, Choi B-R, Lee SH, Kwon DH (2014) Insecticide resistance monitoring and correlation analysis to select appropriate insecticides against Nilaparvata lugens (Stål), a migratory pest in Korea. J Asia Pac Entomol 17(4):711–716. https://doi.org/10.1016/j.aspen.2014.07.005
Miranda M, Vedenov DV (2001) Innovations in agricultural and natural disaster insurance. Am J Agric Econ 83(3):650–655. https://doi.org/10.1111/0002-9092.00185
Mourtzinis S, Krupke CH, Esker PD, Varenhorst A, Arneson NJ, Bradley CA, Byrne AM, Chilvers MI, Giesler LJ, Herbert A, Kandel YR, Kazula MJ, Hunt C, Lindsey LE, Malone S, Mueller DS, Naeve S, Nafziger E, Reisig DD, Ross WJ, Rossman DR, Taylor S, Conley SP (2019) Neonicotinoid seed treatments of soybean provide negligible benefits to US farmers. Sci Rep 9(1):11207. https://doi.org/10.1038/s41598-019-47442-8
Moustier P, Tam PTG, Anh DT, Binh VT, Loc NTT (2010) The role of farmer organizations in supplying supermarkets with quality food in Vietnam. Food Policy 35(1):69–78. https://doi.org/10.1016/j.foodpol.2009.08.003
Muneret L, Mitchell M, Seufert V, Aviron S, Djoudi EA, Petillon J, Plantegenest M, Thiery D, Rusch A (2018) Evidence that organic farming promotes pest control. Nat Sustain 1(7):361–368. https://doi.org/10.1038/s41893-018-0102-4
Nanthakumar M, Jhansi Lakshmi V, Shashi Bhushan V, Balachandran SM, Mohan M (2012) Decrease of rice plant resistance and induction of hormesis and carboxylesterase titre in brown planthopper, Nilaparvata lugens (Stål) by xenobiotics. Pestic Biochem Physiol 102(2):146–152. https://doi.org/10.1016/j.pestbp.2011.12.006
Naranjo SE (2001) Conservation and evaluation of natural enemies in IPM systems for Bemisia tabaci. Crop Prot 20(9):835–852. https://doi.org/10.1016/S0261-2194(01)00115-6
Naranjo SE, Ellsworth PC, Frisvold GB (2015) Economic value of biological control in integrated pest management of managed plant systems. Annu Rev Entomol 60:621–645. https://doi.org/10.1146/annurev-ento-010814-021005
Naveed M, Salam A, Saleem MA (2007) Contribution of cultivated crops, vegetables, weeds and ornamental plants in harboring of Bemisia tabaci (Homoptera: Aleyrodidae) and associated parasitoids (Hymenoptera: Aphelinidae) in cotton agroecosystem in Pakistan. J Pest Sci 80(4):191–197. https://doi.org/10.1007/s10340-007-0171-z
Naveed M, Salam A, Saleem MA, Sayyed AH (2008) Effect of foliar applications of some insecticides onBemisia tabaci, predators and parasitoids: Implications in its management in Pakistan. Phytoparasitica 36(4):377–387. https://doi.org/10.1007/bf02980817
Nicholls CI, Pérez N, Vasquez L, Altieri MA (2002) The Development and status of biologically based integrated pest management in Cuba. Integr Pest Manag Rev 7(1):1–16. https://doi.org/10.1023/a:1025728320114
Nielsen C, Steenberg T (2004) Entomophthoralean fungi infecting the bird cherry-oat aphid, Rhopalosiphum padi, feeding on its winter host bird cherry, Prunus padus. J Invertebr Pathol 87(1):70–73. https://doi.org/10.1016/j.jip.2004.05.003
Noleppa S, Hahn T (2013) The value of neonicotinoid seed treatment in the European Union: a socioeconomic, technological and environmental review. In Humboldt Forum for Food and Agriculture (HFFA)
Oerke EC (2006) Crop losses to pests. J Agric Sci 144(1):31–43. https://doi.org/10.1017/S0021859605005708
Parker WE (1994) Evaluation of the use of food baits for detecting wireworms (Agriotes spp., Coleoptera: Elateridae) in fields intended for arable crop production. Crop Prot 13(4):271–276. https://doi.org/10.1016/0261-2194(94)90014-0
Parker WE (1996) The development of baiting techniques to detect wireworms (Agriotes spp., Coleoptera: Elateridae) in the field, and the relationship between bait-trap catches and wireworm damage to potato. Crop Prot 15(6):521–527. https://doi.org/10.1016/0261-2194(96)00020-8
Parry HR, Evans AJ, Morgan D (2006) Aphid population response to agricultural landscape change: a spatially explicit, individual-based model. Ecol Model 199(4):451–463. https://doi.org/10.1016/j.ecolmodel.2006.01.006
Pathak and Dhaliwal (1981) Trends and strategies for rice insect problems is tropical Asia. IRRIResearch paper series 64 (1981 July)
Pecenka JR, Lundgren JG (2015) Non-target effects of clothianidin on monarch butterflies. Naturwissenschaften 102(3-4):19. https://doi.org/10.1007/s00114-015-1270-y
Pedigo LP (1989) Entomology and pest management. Macmillan Publishing Company, New York
Pedigo LP, Rice ME (2014) Entomology and pest management. Waveland Press
Pisa LW, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Downs CA, Goulson D, Kreutzweiser DP, Krupke C, Liess M, McField M, Morrissey CA, Noome DA, Settele J, Simon-Delso N, Stark JD, Van der Sluijs JP, Van Dyck H, Wiemers M (2015) Effects of neonicotinoids and fipronil on non-target invertebrates. Environ Sci Pollut Res 22(1):68–102. https://doi.org/10.1007/s11356-014-3471-x
Pisa L, Goulson D, Yang EC, Gibbons D, Sanchez-Bayo F, Mitchell E, Aebi A, van der Sluijs J, MacQuarrie CJK, Giorio C, Long EY, McField M, Bijleveld van Lexmond M, Bonmatin JM (2017) An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: impacts on organisms and ecosystems. Environ Sci Pollut Res Int. https://doi.org/10.1007/s11356-017-0341-3
Pistorius J, Bischoff G, Heimbach U (2009) Bee poisoning by abrasion of active substances from seed treatment of maize during seeding in spring 2008. J Kult 61(1):9–14 http://www.journal-kulturpflanzen.de
Piyaratne MKDK, Zhao H, Meng Q (2013) APHIDSim: A population dynamics model for wheat aphids based on swallowtail catastrophe theory. Ecol Model 253:9–16. https://doi.org/10.1016/j.ecolmodel.2012.12.032
Praneetvatakul S, Schreinemachers P, Pananurak P, Tipraqsa P (2013) Pesticides, external costs and policy options for Thai agriculture. Environ Sci Pol 27:103–113. https://doi.org/10.1016/j.envsci.2012.10.019
Pretty J, Benton TG, Bharucha ZP, Dicks LV, Flora CB, Charles H, Godfray J, Goulson D, Hartley SE, Lampkin N, Morris C, Gary P, Vara Prasad PV, Reganold J, Rockstrom J, Smith P, Thorne P, Wratten S (2018) Global assessment of agricultural system redesign for sustainable intensification. Nat Sustain 1(8):441–446. https://doi.org/10.1038/s41893-018-0114-0
Puinean AM, Denholm I, Millar NS, Nauen R, Williamson MS (2010) Characterisation of imidacloprid resistance mechanisms in the brown planthopper, Nilaparvata lugens Stål (Hemiptera: Delphacidae). Pestic Biochem Physiol 97(2):129–132. https://doi.org/10.1016/j.pestbp.2009.06.008
Quiggin JC, Karagiannis G, Stanton J (1993) Crop insurance and crop production: an empirical study of moral hazard and adverse selection. Aust J Agric Econ 37(2):95–113. https://doi.org/10.1111/j.1467-8489.1993.tb00531.x
Rashid MM, Jahan M, Islam KS (2016) Impact of nitrogen, phosphorus and potassium on brown planthopper and tolerance of its host rice plants. Rice Sci 23(3):119–131. https://doi.org/10.1016/j.rsci.2016.04.001
Ritter C, Richter E (2013) Control methods and monitoring of Agriotes wireworms (Coleoptera: Elateridae). J Plant Dis Prot 120(1):4–15. https://doi.org/10.1007/bf03356448
Rogers EM (1962) Diffusion of innovations. Free Press of Glencoe, New York
Romeis J, Naranjo SE, Meissle M, Shelton AM (2018) Genetically engineered crops help support conservation biological control. Biol Control 130:136–154. https://doi.org/10.1016/j.biocontrol.2018.10.001
Rossing WAH, Daamen RA, Hendrix EMT (1994) Framework to support decisions on chemical pest control under uncertainty, applied to aphids and brown rust in winter wheat. Crop Prot 13(1):25–34. https://doi.org/10.1016/0261-2194(94)90132-5
Sánchez-Bayo F, Wyckhuys KAG (2019) Worldwide decline of the entomofauna: a review of its drivers. Biol Conserv 232:8–27. https://doi.org/10.1016/j.biocon.2019.01.020
Sánchez-Bayo F, Goka K, Hayasaka D (2016) Contamination of the aquatic environment with neonicotinoids and its implication for ecosystems. Front Environ Sci 4(71). https://doi.org/10.3389/fenvs.2016.00071
Saringer G, Takács A (1994) Biology and control of Tanymecus dilaticollis Gyll.(Col., Curculionidae). Acta Phytopathol Entomol Hung 29:173–173 https://akjournals.com/view/journals/038/038-overview.xml
Schut M, Rodenburg J, Klerkx L, van Ast A, Bastiaans L (2014) Systems approaches to innovation in crop protection. A systematic literature review. Crop Prot 56:98–108. https://doi.org/10.1016/j.cropro.2013.11.017
Schütz K, Bonkowski M, Scheu S (2008) Effects of Collembola and fertilizers on plant performance (Triticum aestivum) and aphid reproduction (Rhopalosiphum padi). Basic Appl Ecol 9(2):182–188. https://doi.org/10.1016/j.baae.2006.07.003
Seagraves M, Lundgren J (2012) Effects of neonicitinoid seed treatments on soybean aphid and its natural enemies. J Pest Sci 85:125–132. https://doi.org/10.1007/s10340-011-0374-1
Seltenrich N (2017) Catching up with popular pesticides: more human health studies are needed on neonicotinoids. Environ Health Perspect 125(2):A41–A42. https://doi.org/10.1289/ehp.125-A41
Sequeira RV, Naranjo SE (2008) Sampling and management of Bemisia tabaci (Genn.) biotype B in Australian cotton. Crop Prot 27(9):1262–1268. https://doi.org/10.1016/j.cropro.2008.04.002
Settle WH, Ariawan H, Astuti ET, Cahyana W, Hakim AL, Hindayana D, Lestari AS (1996) Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77(7):1975–1988. https://doi.org/10.2307/2265694
Sgolastra F, Porrini C, Maini S, Bortolotti L, Medrzycki P, Mutinelli F, Lodesani M (2017) Healthy honey bees and sustainable maize production: why not. Bull Insectol 70(1):156–160 https://www.buzzaboutbees.net/support-files/neonicsandmaizeitalystudy.pdf
Shao X, Liu Z, Xu X, Li Z, Qian X (2013) Overall status of neonicotinoid insecticides in China: production, application and innovation. J Pestic Sci 38(1):1–9. https://doi.org/10.1584/jpestics.D12-037
Sheng-miao YU, Qian-yu JIN, You-nan OUYANG, De-hai XU (2004) Efficiency of controlling weeds, insect pests and diseases by raising ducks in the paddy fields. Chin J Biol Control 20(2):99–102 http://www.zgswfz.com.cn/CN/abstract/article_325.shtml
Shentu X-P, Li D-T, Xu J-F, Liang S, Xiao-Ping Y (2016) Effects of fungicides on the yeast-like symbiotes and their host, Nilaparvata lugens Stål (Hemiptera: Delphacidae). Pestic Biochem Physiol 128:16–21. https://doi.org/10.1016/j.pestbp.2015.10.010
Shields MW, Johnson AC, Pandey S, Cullen R, González-Chang M, Wratten SD, Gurr GM (2019) History, current situation and challenges for conservation biological control. Biol Control 131:25–35. https://doi.org/10.1016/j.biocontrol.2018.12.010
Silvie PJ, Renou A, Vodounnon S, Bonni G, Adegnika MO, Héma O, Prudent P, Sorèze J, Ochou GO, Togola M, Badiane D, Ndour A, Akantetou PK, Ayeva B, Brévault T (2013) Threshold-based interventions for cotton pest control in West Africa: What's up 10 years later? Crop Prot 43:157–165. https://doi.org/10.1016/j.cropro.2012.09.006
Simon-Delso N, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Chagnon M, Downs C, Furlan L, Gibbons DW, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke CH, Liess M, Long E, McField M, Mineau P, Mitchell EAD, Morrissey CA, Noome DA, Pisa L, Settele J, Stark JD, Tapparo A, Van Dyck H, Van Praagh J, Van der Sluijs JP, Whitehorn PR, Wiemers M (2015) Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ Sci Pollut Res 22(1):5–34. https://doi.org/10.1007/s11356-014-3470-y
Sogawa K, Liu G, Qiang Q (2009) Prevalence of whitebacked planthoppers in Chinese hybrid rice and whitebacked planthopper resistance in Chinese japonica rice. In: Heong KL, Hardy B (eds) Planthoppers: new threats to the sustainability of intensive rice production systems in Asia. International Rice Research Institute, Manila
Sohrabi F, Shishehbor P, Saber M, Mosaddegh MS (2012) Lethal and sublethal effects of buprofezin and imidacloprid on the whitefly parasitoid Encarsia inaron (Hymenoptera: Aphelinidae). Crop Prot 32:83–89. https://doi.org/10.1016/j.cropro.2011.10.005
Spangenberg JH, Douguet JM, Settele J, Heong KL (2015) Escaping the lock-in of continuous insecticide spraying in rice: developing an integrated ecological and socio-political DPSIR analysis. Ecol Model 295:188–195. https://doi.org/10.1016/j.ecolmodel.2014.05.010
Staudacher K, Schallhart N, Pitterl P, Wallinger C, Brunner N, Landl M, Kromp B, Glauninger J, Traugott M (2013) Occurrence of Agriotes wireworms in Austrian agricultural land. J Pest Sci 86(1):33–39. https://doi.org/10.1007/s10340-011-0393-y
Stenberg JA (2017) A conceptual framework for integrated pest management. Trends Plant Sci 22(9):759–769. https://doi.org/10.1016/j.tplants.2017.06.010
Sufyan M, Neuhoff D, Furlan L (2011) Assessment of the range of attraction of pheromone traps to Agriotes lineatus and Agriotes obscurus. Agric For Entomol 13(3):313–319. https://doi.org/10.1111/j.1461-9563.2011.00529.x
Sullivan GH, Sánchez G, Weller SC, Edwards CR (1999) Sustainable development in Central Americaʼs non-traditional export crops sector through adoption of integrated pest management practices: Guatemalan case study. Sustain Dev Int 1:123–126 https://p2infohouse.org/ref/22/21996.pdf
Taliansky-Chamudis A, Gomez-Ramirez P, Leon-Ortega M, Garcia-Fernandez AJ (2017) Validation of a QuECheRS method for analysis of neonicotinoids in small volumes of blood and assessment of exposure in Eurasian eagle owl (Bubo bubo) nestlings. Sci Total Environ 595:93–100. https://doi.org/10.1016/j.scitotenv.2017.03.246
Tittonell PA (2014) Ecological intensification of agriculture - sustainable by nature. Curr Opin Environ Sustain 8:53–61. https://doi.org/10.1016/j.cosust.2014.08.006
Toepfer S, Haye T, Erlandson M, Goettel M, Lundgren JG, Kleespies RG, Weber DC, Cabrera Walsh G, Peters A, Ehlers RU, Strasser H, Moore D, Keller S, Vidal S, Kuhlmann U (2009) A review of the natural enemies of beetles in the subtribe Diabroticina (Coleoptera: Chrysomelidae): implications for sustainable pest management. Biocontrol Sci Tech 19(1):1–65. https://doi.org/10.1080/09583150802524727
Toepfer S, Kurtz B, Kuhlmann U (2010) Influence of soil on the efficacy of entomopathogenic nematodes in reducing Diabrotica virgifera virgifera in maize. J Pest Sci 83(3):257–264. https://doi.org/10.1007/s10340-010-0293-6
Tooker JF, Douglas MR, Krupke CH (2017) Neonicotinoid seed treatments: limitations and compatibility with integrated pest management. Agric Environ Lett 2. https://doi.org/10.2134/ael2017.08.0026
Tosi S, Burgio G, Nieh JC (2017) Common neonicotinoid pesticide, thiamethoxam, impairs honey bee flight ability. Sci Rep 7(1):1201. https://doi.org/10.1038/s41598-017-01361-8
Tóth M (2013) Pheromones and attractants of click beetles: an overview. J Pest Sci 86(1):3–17. https://doi.org/10.1007/s10340-012-0429-y
Tóth M, Furlan L, Yatsynin VG, Ujváry I, Szarukán I, Imrei Z, Subchev M, Tolasch T, Francke W (2002) Identification of sex pheromone composition of click beetle Agriotes brevis Candeze. J Chem Ecol 28(8):1641–1652. https://doi.org/10.1023/a:1019984714858
Tóth M, Furlan L, Xavier A, Vuts J, Toshova T, Subchev M, Szarukán I, Yatsynin V (2007) New sex attractant composition for the click beetle Agriotes proximus: similarity to the Pheromone of Agriotes lineatus. J Chem Ecol 34(1):107–111. https://doi.org/10.1007/s10886-007-9398-7
Tóth M, Furlan L, Vuts J, Szarukán I, Ujváry I, Yatsynin VG, Tolasch T, Francke W (2015) Geranyl hexanoate, the female-produced pheromone of Agriotes sordidus Illiger (Coleoptera: Elateridae) and its activity on both sexes. Chemoecology 25(1):1–10. https://doi.org/10.1007/s00049-014-0170-5
Tschumi M, Ekroos J, Hjort C, Smith HG, Birkhofer K (2018) Rodents, not birds, dominate predation-related ecosystem services and disservices in vertebrate communities of agricultural landscapes. Oecologia 188(3):863–873. https://doi.org/10.1007/s00442-018-4242-z
van Herk WG, Vernon RS (2013) Wireworm damage to wheat seedlings: effect of temperature and wireworm state. J Pest Sci 86(1):63–75. https://doi.org/10.1007/s10340-012-0461-y
van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57(1):1–20. https://doi.org/10.1007/s10526-011-9395-1
Van Mele P, Vodouhe SD, Wanvoeke J (2009) The power of video to trigger innovation: rice processing in central Benin AU - Zossou, Espérance. Int J Agric Sustain 7(2):119–129. https://doi.org/10.3763/ijas.2009.0438
Vasileiadis VP, Sattin M, Otto S, Veres A, Pálinkás Z, Ban R, Pons X, Kudsk P, van der Weide R, Czembor E, Moonen AC, Kiss J (2011) Crop protection in European maize-based cropping systems: current practices and recommendations for innovative integrated pest management. Agric Syst 104(7):533–540. https://doi.org/10.1016/j.agsy.2011.04.002
Veres A, Tóth F, Kiss J, Fetykó K, Orosz S, Lavigne C, Otto S, Bohan D (2012) Spatio-temporal dynamics of Orius spp. (Heteroptera: Anthocoridae) abundance in the agricultural landscape. Agric Ecosyst Environ 162:45–51. https://doi.org/10.1016/j.agee.2012.08.009
Veres A, Petit S, Conord C, Lavigne C (2013) Does landscape composition affect pest abundance and their control by natural enemies? A review. Agric Ecosyst Environ 166:110–117. https://doi.org/10.1016/j.agee.2011.05.027
Vernon RS, van Herk WG, Clodius M, Tolman J (2016) Companion planting attract-and-kill method for wireworm management in potatoes. J Pest Sci 89(2):375–389. https://doi.org/10.1007/s10340-015-0707-6
Viscarret MM, López SN (2004) Biological studies on Encarsia porteri (Mercet) (Hymenoptera: Aphelinidae) an heterotrophic parasitoid of the Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) complex. Biol Control 30(2):236–240. https://doi.org/10.1016/j.biocontrol.2003.10.002
Vreysen MJB, Robinson AS, Hendrichs J (2007) Area-wide control of insect pests: from research to field implementation. Springer, Dordrecht, The Netherlands. https://doi.org/10.1007/978-1-4020-6059-5
Vuts J, Tolasch T, Furlan L, Csonka ÉB, Felföldi T, Márialigeti K, Toshova TB, Subchev M, Xavier A, Tóth M (2012) Agriotes proximus and A. lineatus (Coleoptera: Elateridae): a comparative study on the pheromone composition and cytochrome c oxidase subunit I gene sequence. Chemoecology 22(1):23–28. https://doi.org/10.1007/s00049-011-0091-5
Vuts J, Furlan L, Csonka ÉB, Woodcock CM, Caulfield JC, Mayon P, Pickett JA, Birkett MA, Tóth M (2014) Development of a female attractant for the click beetle pest Agriotes brevis. Pest Manag Sci 70(4):610–614. https://doi.org/10.1002/ps.3589
Ward DP, DeGooyer TA, Vaughn TT, Head GP, McKee MJ, Astwood JD, Pershing JC (2004) Genetically enhanced maize as a potential management option for corn rootworm: YieldGard rootworm maize case study. In: Vidal S, Kuhlmann U, Edwards CR (eds) Western corn rootworm: ecology and management. CABI, Wallingford, p 320. https://doi.org/10.1079/9780851998176.0000
Waterhouse DF (1998) Biological control of insect pests : Southeast Asian prospects / D.F. Waterhouse. Edited by Research Australian Centre for International Agricultural, ACIAR monograph series ; no. 51. Australian Centre for International Agricultural Research, Canberra
Wesseler J, Fall EH (2010) Potential damage costs of Diabrotica virgifera virgifera infestation in Europe – the ‘no control’ scenario. J Appl Entomol 134(5):385–394. https://doi.org/10.1111/j.1439-0418.2010.01510.x
Westphal C, Vidal S, Horgan FG, Gurr GM, Escalada M, Van Chien H, Tscharntke T, Heong KL, Settele J (2015) Promoting multiple ecosystem services with flower strips and participatory approaches in rice production landscapes. Basic Appl Ecol 16(8):681–689. https://doi.org/10.1016/j.baae.2015.10.004
Whitehorn PR, O’Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science. 336:351–352. https://doi.org/10.1126/science.1215025
Winarto YT (2004) Seeds of knowledge: the beginning of integrated pest management in Java.
Wu W, Piyaratne MKDK, Zhao H, Li C, Hu Z, Xiangshun H (2014) Butterfly catastrophe model for wheat aphid population dynamics: construction, analysis and application. Ecol Model 288:55–61. https://doi.org/10.1016/j.ecolmodel.2014.05.017
Wyckhuys K, Lu Y, Morales H, Vázquez LL Moreno JL, Eliopoulos P, Mahecha LMH (2013) Current status and potential of conservation biological control for agriculture in the developing world. Vol 65
Wyckhuys KAG, Burra DD, Tran DH, Graziosi I, Walter AJ, Nguyen TG, Trong HN, Le BV, Le TTN, Fonte SJ (2017) Soil fertility regulates invasive herbivore performance and top-down control in tropical agroecosystems of Southeast Asia. Agric Ecosyst Environ 249:38–49. https://doi.org/10.1016/j.agee.2017.08.006
Wyckhuys KAG, Bentley JW, Lie R, Nghiem LTP, Fredrix M (2018) Maximizing farm-level uptake and diffusion of biological control innovations in today’s digital era. BioControl 63(1):133–148. https://doi.org/10.1007/s10526-017-9820-1
Wyckhuys KAG, Heong KL, Sanchez-Bayo F, Bianchi FJJA, Lundgren JG, Bentley JW (2019a) Ecological illiteracy can deepen farmers’ pesticide dependency. Environ Res Lett 14(9):093004. https://doi.org/10.1088/1748-9326/ab34c9
Wyckhuys KAG, Hughes AC, Buamas C, Johnson AC, Vasseur L, Reymondin L, Deguine JP, Sheil D (2019b) Biological control of an agricultural pest protects tropical forests. Commun Biol 2(1):10. https://doi.org/10.1038/s42003-018-0257-6
Wyckhuys KAG, Pozsgai G, Lovei GL, Vasseur L, Wratten SD, Gurr GM, Reynolds OL, Goettel M (2019c) Global disparity in public awareness of the biological control potential of invertebrates. Sci Total Environ 660:799–806. https://doi.org/10.1016/j.scitotenv.2019.01.077
Xian X, Zhai B, Zhang X, Cheng X, Wang J (2007) Teleconnection between the early immigration of brown planthopper (Nilaparvata lugens Stål) and ENSO indices: implication for its medium- and long-term forecast. Acta Ecol Sin 27(8):3144–3154. https://doi.org/10.1016/S1872-2032(07)60069-9
Yang N-W, Wan F-H (2011) Host suitability of different instars of Bemisia tabaci biotype B for the parasitoid Eretmocerus hayati. Biol Control 59(2):313–317. https://doi.org/10.1016/j.biocontrol.2011.07.019
Yang Y-j, Dong B-q, Xu H-x, Zheng X-s, Heong KL, Zhong-xian L (2014) Susceptibility to insecticides and ecological fitness in resistant rice varieties of field Nilaparvata lugens Stål population free from insecticides in laboratory. Rice Sci 21(3):181–186. https://doi.org/10.1016/S1672-6308(13)60181-X
Yang L, Han Y, Li P, Wen L, Hou M (2017) Silicon amendment to rice plants impairs sucking behaviors and population growth in the phloem feeder Nilaparvata lugens (Hemiptera: Delphacidae). Sci Rep 7(1):1101. https://doi.org/10.1038/s41598-017-01060-4
Yao F-L, Yu Z, Zhao J-W, Desneux N, He Y-X, Weng Q-Y (2015) Lethal and sublethal effects of thiamethoxam on the whitefly predator Serangium japonicum (Coleoptera: Coccinellidae) through different exposure routes. Chemosphere 128:49–55. https://doi.org/10.1016/j.chemosphere.2015.01.010
Yin J-L, Xu H-W, Wu J-C, Hu J-H, Yang G-Q (2014) Cultivar and insecticide applications affect the physiological development of the brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae). Environ Entomol 37(1):206–212. https://doi.org/10.1603/0046-225x(2008)37[206:caiaat]2.0.co;2
Zhang X-m, Yang N-w, Wan F-h, Lövei GL (2014) Density and seasonal dynamics of Bemisia tabaci (Gennadius) Mediterranean on common crops and weeds around cotton fields in Northern China. J Integr Agric 13(10):2211–2220. https://doi.org/10.1016/S2095-3119(13)60613-9
Zhang X, Liao X, Mao K, Zhang K, Hu W, Li J (2016) Insecticide resistance monitoring and correlation analysis of insecticides in field populations of the brown planthopper Nilaparvata lugens (stål) in China 2012–2014. Pestic Biochem Physiol 132:13–20. https://doi.org/10.1016/j.pestbp.2015.10.003
Zhang H, Potts SG, Breeze T, Bailey A (2018) European farmers’ incentives to promote natural pest control service in arable fields. Land Use Policy 78:682–690. https://doi.org/10.1016/j.landusepol.2018.07.017
Zheng Y-L, Xu L, Wu J-C, Liu J-L, DuanMu H-L (2007) Time of occurrence of hopperburn symptom on rice following root and leaf cutting and fertilizer application with brown planthopper, Nilaparvata lugens (stål) infestation. Crop Prot 26(2):66–72. https://doi.org/10.1016/j.cropro.2006.04.001
Zhu Z-R, Cheng J-A, Jiang M-X, Zhang X-X (2004) Complex influence of rice variety, fertilization timing, and insecticide on population dynamics of Sogatella furcifera (Horvath) , Nilaparvata lugens (Stål) (Homoptera: Delphacidae) and their natural enemies in rice in Hangzhou, China. Vol 77
Zou Y, de Kraker J, Bianchi FJJA, van Telgen MD, Xiao H, van der Werf W (2017) Video monitoring of brown planthopper predation in rice shows flaws of sentinel methods. Sci Rep 7:42210–42210. https://doi.org/10.1038/srep42210
NAWQA (2014) https://water.usgs.gov/nawqa/pnsp/usage/maps/
PAN International’s list of highly hazardous pesticides (2010) http://pan-international.org/
USEPA (2014) https://www.epa.gov/pollinator-protection
The authors would like to thank the Stichting Triodos Foundation (The Netherlands) for funding the Task Force on Systemic Pesticides (TFSP) as a totally independent research group, for making this study and the relative open access possible. The Stichting Triodos Foundation received funds from the Umwelt Stiftung Greenpeace (Germany), Pollinis (France) and the M.A.O.C. Gravin van Bylandt Stichting (The Netherlands). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. In addition, the authors are very grateful to Finbarr Horgan for his valuable contribution about rice pests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Responsible editor: Philippe Garrigues
Electronic supplementary material
About this article
Cite this article
Veres, A., Wyckhuys, K.A.G., Kiss, J. et al. An update of the Worldwide Integrated Assessment (WIA) on systemic pesticides. Part 4: Alternatives in major cropping systems. Environ Sci Pollut Res (2020). https://doi.org/10.1007/s11356-020-09279-x
- Soil pests
- Brown planthopper
- Agricultural policy
- Biological control