Advertisement

Landscape ecology and expanding range of biocontrol agent taxa enhance prospects for diamondback moth management. A review

  • Geoff M. Gurr
  • Olivia L. Reynolds
  • Anne C. Johnson
  • Nicolas Desneux
  • Myron P. Zalucki
  • Michael J. Furlong
  • Zhenyu Li
  • Komivi S. Akutse
  • Junhui Chen
  • Xiwu Gao
  • Minsheng You
Open Access
Review Article
Part of the following topical collections:
  1. Pest control

Abstract

Diamondback moth (Plutella xylostella) is a globally significant pest of Brassicaceae crops that has attracted enormous research investment. It is typical of many agricultural pests, with insecticides remaining the most common method of control, despite frequent cases of resistance in pest populations and the potential for other management options such as natural enemies to provide suppression. Here we review scope to make better use of neglected natural enemy taxa and integrate recent work on landscape ecology to identify opportunities for more effective pest suppression. Our main findings are as follows: (1) relatively neglected taxa of natural enemies, especially predators and entomopathogens, are now attracting growing levels of research interest, although parasitoids remain most frequently used and researched; (2) knowledge of the spatio-temporal dynamics of populations at the landscape scale have advanced rapidly in the last decade; (3) ecological insights open new possibilities for exploiting spatial heterogeneity at scales larger than individual fields and even farms that influence pests and their natural enemies; (4) there is evidence for landscapes that selectively favor particular guilds and this knowledge could be developed to favor targeted natural enemies over pests in focal crops; and (5) landscape-scale effects can even over-ride field-scale management practices. The significance of these advances is that future management of diamondback moth and similar pests will benefit from a move away from reliance on the use of particular species of biological control agents, especially exotic parasitoids, and strategies that depend on use of broad-spectrum insecticides. Together with this move, we call for greater use of area-wide management that exploits the potential of landscapes to promote diverse assemblages of natural enemy species.

Keywords

Plutella xylostella Conservation biological control Habitat management Donor habitat Landscape connectivity Area-wide management Bacillus thuringiensis Entomopathogen Predator Parasitoid 

1 Introduction

The diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), is the most destructive insect pest of Brassica spp. crops worldwide (Furlong et al. 2013; Li et al. 2016a) and is estimated to cost the world economy US$4–5 billion a year (Zalucki et al. 2012). Its pest status in brassica vegetable crops increased dramatically following the widespread adoption of broad-spectrum insecticides (Ankersmit 1953) and the absence of effective natural enemies across several areas of its range (Talekar and Shelton 1993). More recently, it has become a major pest of the oil-seed crop, canola (Brassica napus L.), the production area of which has increased markedly in industrialized countries over recent decades (Furlong et al. 2008a). The importance of the diamondback moth as a global pest of brassica crops is reflected in publication metrics, with Web of Science holding over 3800 papers on this pest. More than 125 new papers have been added each year over the last decade. Critical reviews of this large volume of literature are, therefore, important to synthesize emerging knowledge of diamondback moth and integrate this with advances in related fields. Landmark reviews of this pest were published by Talekar and Shelton (1993) and Furlong et al. (2013), with reviews on biological control agents (Sarfraz et al. 2007), conservation biological control (Liu et al. 2014), multitrophic interactions (Verkerk and Wright 1996), and the ecology and management in the USA (Philips et al. 2014) and China (Li et al. 2016a) following suit. Each of these reviews contained information on the biology and use of various natural enemies.

Among taxa that attack diamondback moth, parasitoids have historically attracted the most research. Toxins derived from the entomopathogenic bacterium Bacillus thuringiensis (Bt) have been widely used against this pest but here we will not consider Bt to be a biological control agent. Although formulated Bt products may contain bacterial spores as well as crystal toxins (Crickmore 2006), and the spores enhance toxicity (Burges et al. 1976), they are more properly considered as insecticides, albeit non-synthetic. Here we widen attention by considering other biological control agent taxa, such as predators and various entomopathogens, to assess whether these are becoming better represented in the literature and the extent that they could complement parasitoids in future diamondback moth management approaches.

The second distinct gap that we explore is the prospect to use conservation biological control approaches that more effectively address the unmet need for control of diamondback moth using non-chemical, ecologically based approaches that enable sustainable management. Specifically, we explore the potential of habitat management approaches that promote natural enemy impact on pest densities (Gurr et al. 2017; Landis et al. 2000). These approaches tend to use diversification of the cropping system to provide resources such as source habitat, alternative prey, and plant foods to natural enemies. Resources for natural enemies are often lacking in brassica crop systems but can be provided by interventions that reintroduce aspects of diversity found in traditional agricultural systems (Fig. 1). Importantly, habitat management often operates at a spatial scale larger than individual fields and can extend to the landscape several kilometers from a focal field (Perović et al. 2010; Schmidt et al. 2005; Tscharntke et al. 2012). To date, landscape-scale research has been little considered in relation to biological control of diamondback moth, despite the strong dispersal capacity of the adults of this species (Furlong et al. 2013) and even their parasitoids (Dosdall et al. 2004) as well as the significance of this movement to insecticide resistance management in diamondback moth (Talekar and Shelton 1993; Sarfraz and Keddie 2005; Tabashnik et al. 1987). Accordingly, we assess the potential for exploiting advances in knowledge of spatial ecology to provide better biological control of this pest.
Fig. 1

Contrasting brassica vegetable production systems. Top: monoculture with bare ground, no weeds or non-crop vegetation, and amid urban infrastructure (Fujian Province, China). Bottom: polyculture with weeds, adjacent non-crop perennial vegetation, and little bare ground (Galapagos Islands, Ecuador). These factors can strongly influence the diversity of natural enemies and overall strength of biological control. (Photos: GM Gurr)

2 The global context

Arthropod pests continue to cause extensive crop loss and this drives the use of large amounts of synthetic insecticides (Bradshaw et al. 2016). Although biological control of pests has been actively pursued for over a century and the last decade has seen an acceleration of research efforts to better understand the biology and ecology of natural enemies, insecticides remain the mainstay of pest management in many crop systems (Adamson et al. 2014). Here we focus on diamondback moth as an example of a serious, globally distributed pest and consider how biological control and related cultural practices, especially at scales larger than individual fields, might be used more effectively. Diamondback moth is, however, not dissimilar to many other serious, cosmopolitan pests of crops other than brassicas such as Helicoverpa spp. (Downes et al. 2017), Bemisia whiteflies (Perring 2001; Brown et al. 1995), and Nilaparvata lugens (Bentur and Viraktamath 2008), in which vagility and propensity for developing insecticide resistance demand improved management strategies. Accordingly, notwithstanding the obvious need for pest management systems to be tuned to the specific ecology of a given pest, the present review of diamondback moth has wider relevance, providing insights and potentially fruitful leads for other pest species.

3 Diamondback moth movement and implications for biological control

Although movement of diamondback moth is typically trivial when host plants are available (Mo et al. 2003), the adult has the capacity to migrate large distances and rapidly colonize suitable hosts (Chapman et al. 2002). Recent research in China has demonstrated that annual northerly migrations can result in the movement of insecticide-resistant populations over thousands of kilometers (Wei et al. 2013; Li et al. 2016a). In North America, meteorological data provides strong evidence that the diamondback moth populations invading Canadian canola crops in summer can originate from vegetable crops as far away as northern Mexico and that the > 3000-km journey can be made over a matter of days (Dosdall et al. 2004). Similarly, there is indirect evidence that the diamondback moth adults reaching vegetable production areas in Tasmania in late spring/early summer originate from canola crops on mainland Australia (Schellhorn et al. 2008). The scale, intensity, and timing of these migrations may contribute to population increases and pest status (Li et al. 2016b).

In addition to multiplication within host crops, diamondback moth can persist and build up on brassicaceous weeds and native plant species that might be located great distances away from a focal crop which is the eventual site of economic impact (Niu et al. 2014). The diamondback moth populations of non-crop host plants can extend over vast areas (Furlong et al. 2008b) and managing them is difficult, especially in native brassica habitats. However, local/regional weather conditions such as temperatures and precipitation are strong drivers of diamondback moth population growth (Li et al. 2016b) and targeted monitoring of potential source populations when conditions for diamondback moth population growth are likely to be favorable (Zalucki and Furlong 2011) could provide useful management information. The development of bioclimatic simulation models linked to wind trajectory models has been advocated as an aid to forecasting possible diamondback moth outbreaks in vegetable and canola crops (Furlong et al. 2008b; Zalucki and Furlong 2011). Such an approach could predict the movement of diamondback moth into crop growing regions where local landscape management can be configured to ensure that endemic natural enemies are conserved.

Diamondback moth is a typical r-selected species; its high vagility and relatively high intrinsic rates of increase enable it to cope with seasonal unavailability of host plants in a given area and move to locate fresh resources. Associated with this dispersal capacity is the ability to evade natural enemies, as diamondback moth can leave habitats where it is under heavy attack, with enemies typically, but not always (Dosdall et al. 2004), lacking comparable powers of dispersal. This can result in the herbivore multiplying rapidly in new areas of (relatively) enemy-scarce habitat, especially as it moves from uncultivated to cultivated brassica host plants (Fox and Eisenbach 1992). This theme will be revisited below because a major challenge in achieving more consistently effective biological control is to facilitate two groups of ecological phenomena. The first of these is to maximize the persistence of diverse natural enemy assemblages in regions where brassica production takes place (meaning the non-crop habitat patches as well as the brassica fields), thereby increasing the likelihood that they might colonize nearby brassica crops. The second is the facilitation of rapid population increases of natural enemies on arrival in brassica habitat so that the establishment and maintenance of biological control is not impeded by factors such as insecticide use or the lack of complementary resources such as nectar.

4 Biological control and historical trends among agent types

There is considerable evidence that in brassica agroecosystems, diamondback moth is a secondary or induced pest and that in the absence of broad-spectrum insecticides, natural enemies (Furlong et al. 2013) and crop management (Li et al. 2016b) can suppress populations so that they can be effectively managed by more tactical interventions with selective compounds (Furlong et al. 2008a; Furlong et al. 2004b; Zalucki et al. 2009). The research literature on natural enemies of diamondback moth has grown dramatically over the last quarter century, from four papers published during 1992 to more than 50 during 2016 (Fig. 2). There was a marked escalation of the annual numbers of papers in 2004, due, in part, to the publication of a series of biological control papers from the fourth international workshop on diamondback moth. Shelton (2004) noted the changed emphasis from the previous three workshops in that series with an increasing trend towards research into biological control and IPM. However, in the 2006 and 2011 workshops, this trend was reversed reflecting increased research into the management of resistance to the suite of insecticides that had been introduced in the previous decade. Such inconsistency characterizes diamondback moth research over the past 40 years (Furlong et al. 2013).
Fig. 2

Historical trend in the research effort for contrasting diamondback moth natural enemies: orange, parasitoids; blue, predators; light green, entomopathogenic fungi; dark green, entomopathogenic nematodes

As Shelton (2004) predicted, following the rise in the number of crucifer monocultures, year-round production and the consequent control failures of diamondback moth, the need for “more sustainable and reliable strategies” would result in increasing efforts to understand the mechanisms of biological control and IPM strategies. As diamondback moth developed resistance to an increasing number of insecticides, various resistance management programs were proposed that included the judicious use of insecticides, area-wide rotation of insecticide groups with complimentary agronomic practices, and biological control (Sarfraz and Keddie 2005; Zhao et al. 2006; Talekar and Shelton 1993).

Partitioning research outputs according to the taxa and guilds of biological control agents reveal marked trends. Much effort has focused on parasitoids, several of which, particularly Diadegma semiclausum (Hellén) (Hymenoptera: Ichneumonidae), Diadromus collaris (Gravenhorst) (Hymenoptera: Ichneumonidae), and Cotesia vestalis (= plutellae) Haliday (Hymenoptera: Braconidae) have been widely introduced as classical biological agents (Sarfraz et al. 2007). Indeed, parasitoids have been the natural enemy guild that has consistently received the most research attention over the last 25 years. Searching Web of Science core collection for “parasitoid*” finds 357 papers on biological control of diamondback moth published since 1992 and at least a dozen each year over the last decade (Fig. 2). Predatory arthropods, in contrast, have received far less attention, a total of 118 papers over the same period. While the number of papers published each year on diamondback moth predators has increased to a greater extent than parasitoid-related papers, the annual number published remains low (Fig. 2). Predators can play an important role in controlling diamondback moth as shown in work in various countries including the USA (Muckenfuss et al. 1992), Australia (Furlong et al. 2004a), China (Liu et al. 2005), and North Korea (Furlong et al. 2008a), though their impact is contingent on avoiding pesticide-induced mortality of the agents. Recent work shows that diamondback moth predators, which principally attack early instars, and parasitoids which typically attack second instar and older larvae, can complement each other and that resource partitioning among these taxa can minimize intra-guild predation (Furlong et al. 2014).

The relative neglect of predators in preference for parasitoids reflects the research on a small number of parasitoid species that have been introduced to multiple countries in classical biological control programs (Sarfraz et al. 2007). Although parasitoids can be promoted by local habitat management (Lu et al. 2014; Gillespie et al. 2016), there is potential for enhancement of predators by habitat management at the landscape scale (Gonçalves et al. 2017). This is because a diversity of habitat vegetation promotes continuity of availability of food, especially prey (Gurr et al. 2017). This, in turn, provides opportunities for a diversity of predator guilds to persist in a landscape that are ready to exhibit prey switching to diamondback moth when brassica crops are present in sufficient numbers as prey populations begin to increase. The theme of promoting natural enemies by habitat management is explored in detail in the following section. In contrast to the volume of papers on arthropod biological control agents, only 57 papers were published on entomopathogenic fungi and just 35 on entomopathogenic nematodes. Notably, however, the numbers of papers on these entomopathogens have increased rapidly in the last 20 years (Fig. 2).

5 Habitat management, ecological interactions, and the importance of scale

Despite the clear potential for natural enemies to impact diamondback moth populations and serve as the foundation for integrated pest management (IPM), the level of adoption remains low (Furlong et al. 2013; Li et al. 2016a). A multiple-year regional study that quantified the effects of diamondback moth suppression by natural enemies in commercial brassica crops showed that the adoption of IPM based on the conservation of endemic natural enemies and the tactical application of selective insecticides could result in high crop yields with minimized insecticide inputs (Furlong et al. 2004b). Application of broad-spectrum insecticides caused significant disruption to the natural enemy complex; these effects persisted throughout the season and a single application of a pyrethroid or organophosphate insecticide inevitably necessitated further insecticide applications (Liu et al. 2005; Furlong et al. 2004b). Desneux et al. (2007) provide a comprehensive and broad review on acute and chronic toxicity of insecticides, as well as their sublethal effects. When broad-spectrum insecticides are used for diamondback moth management, high crop yields were possible but depended on frequent and significant application of synthetic insecticides (Furlong et al. 2004b). This is not only costly and harmful to the environment but also unsustainable, given the record of developing resistance to all insecticides deployed against this pest (Furlong et al. 2013; Li et al. 2016a; Verkerk and Wright 1997). By contrast, diamondback moth that migrated into brassica fields in North Korea were effectively managed by integrating endemic predators (Lycosidae and Carabidae) and parasitoids C. vestalis, D. collaris, and Oomyzus sokolowskii Kurdjumov (Eulophidae) with rational applications of Bt (Furlong et al. 2008a). That approach resulted in significantly improved yields compared with conventionally managed crops where frequent application of pyrethroid insecticide destroyed natural enemies, thereby promoting pest survival, resulting in extremely high densities of diamondback moth and other arthropod pests.

Local management at the farm scale can conserve endemic natural enemies, especially if Bt is used in place of more disruptive chemical insecticides. Accordingly, within the typically insecticide-intensive environments that brassica agroecosystems represent, elimination of chemical insecticides, especially broad-spectrum products, is a prerequisite to effective biological control. In order for biological control to operate to its maximum potential, two further aspects require attention. The first of these is the provision of key ecological resources that otherwise may limit the performance of individual natural enemies and their dynamics at population level. This approach to pest management is often referred to as conservation biological control (which generally includes avoidance of insecticide-induced natural enemy mortality) or, more narrowly, habitat management/manipulation (Landis et al. 2000; Gurr et al. 2017). A particularly well-researched category of the latter is nectar as food sources for adult parasitoids (Wäckers et al. 2006; Lu et al. 2014). The maintenance of landscape features such as effective refugia and habitat features that enhance connectivity (e.g., hedgerows) to serve as donor habitat and movement pathways for natural enemies (Perović et al. 2010; Schellhorn et al. 2008) can also be important. While a recent review has suggested that work on the significance of semi-natural habitats for biological control has tended to focus on the dynamics of the agents rather than the strength of the desired ecosystem service (Holland et al. 2017), there is a strong body of evidence that biological control in a focal crop can be heavily influenced by landscape-scale effects (Tscharntke et al. 2012). Australian studies have demonstrated, for example, that riparian vegetation, pastures composed of perennial native species, and remnant woodland close to farms can all serve as donor habitat for predators of diamondback moth. These natural enemies have been shown to move from such non-crop habitats to nearby brassica crops after spraying has reduced their numbers in the focal crop (Heimoana et al. 2017).

As is evident in the preceding section, the emphasis in habitat management of arthropod pests in general, as well as for diamondback moth in particular, is on the enhancement of impact by arthropod natural enemies through direct effects (i.e., predation and parasitism). The following two subsections aim to expand the scope of this theme by considering (i) the potential impacts of vegetation complexity on microbial natural enemies and the associated potential for habitat management by such agents and (ii) how indirect ecological interactions, i.e., those that operate via other species or are separate in time and space, may contribute to pest management.

5.1 Habitat management and entomopathogens

Entomopathogens are attracting increasing research interest for the suppression of diamondback moth (Fig. 2) as well as other key agricultural pests. Diamondback moth is attacked by a range of fungi, nematodes, bacteria, and viruses in the field. Research efforts, especially for fungi and nematodes, have focused on augmentation strategies to improve their impact (Stavely et al. 2004). The entomophthoralean fungi, Zoophthora radicans (Brefeld) Batko, Erynia spp. (Nowak. ex A. Batko) Remaud. & Hennebert., and Pandora blunckii (G. Lakon ex G. Zimm.) Humber can cause natural epizootics in diamondback moth populations, and methods have been developed for their dissemination (Furlong et al. 1995; Vandenberg et al. 1998; Vickers et al. 2004; Pell et al. 2001; Yeo et al. 2001). Diamondback moth is also susceptible to several species of Hyphomycetes including Beauveria bassiana (Bals.-Criv.) Vuill., Isaria fumosorosea (= Paecilomyces fumosoroseus) Wize, I. sinclairii (Berk.) Lloyd, Metarhizium anisopliae (Metchnikoff) Sorokin, Nomuraea rileyi (Farlow) Samson, and Lecanicillium muscarium R. Zare & W. Gams (Wilding 1986; Kirk et al. 2004; Cherry et al. 2004; Duarte et al. 2016) but these are less frequently associated with diamondback moth under natural conditions. Significant work has been done on the biology and utility of some of these fungi (Furlong and Pell 1997, 2001; Sarfraz et al. 2007). For example, B. bassiana formulated as Mycotrol® suppressed diamondback moth populations on seedlings grown in a nursery and on brassica crops in open fields in the USA (Vandenberg et al. 1998). Beauveria bassiana synergistically controlled three lepidopteran pests on brassicas when integrated with Bt (Vandenberg et al. 1999) and reduced the number of applications of Bt, so contributing to resistance management (Stavely et al. 2004).

Among the 24 identified entomopathogenic nematodes families, Steinernematidae and Heterorhabditidae in the order Rhabditida have been most widely researched as biological control agents. Steinernema sp. and Heterorhabditis indicus Poinar, Karunakar & David are reportedly effective against diamondback moth in Malaysia (Mason and Wright 1997) and studies in Pakistan (Ratnasinghe and Hague 1998) and Germany (Schroer and Ehlers 2005) report the effectiveness of S. carpocapsae (Weiser). Although ultra-low-volume applications of Steinernema sp. and Heterorhabditis sp. have been found effective in small-scale trials (Mason et al. 1999), application over larger open fields is constrained by susceptibility of these agents to abiotic factors especially exposure to UV radiation and low humidity (Grzywacz et al. 2010), reflecting that they naturally occur in soil. The spray equipment for foliar application of entomopathogenic nematodes is only slightly modified from chemical spray equipment. The optimal equipment and formulation requirements for maximizing coverage, placement, and timing to improve efficiency of foliar application and reduce restraints of abiotic factors have not received great attention (Wright et al. 2005).

Diamondback moth is susceptible to two types of lepidopteran-specific viruses, Nucleopolyhedroviruses (NPV; Alphabaculovirus spp.) and Granuloviruses (GV; Betabaculovirus spp.) and strains of both are commercially available (Sun and Peng 2007; Yang et al. 2012). In experiments in Kenya, PlxyGV controlled diamondback moth populations on kale more effectively than the available chemical insecticides (Grzywacz et al. 2004).

Typically, entomopathogens have been applied by conventional application of a formulated product. To maximize the efficacy of these agents, environmental factors need to be considered and habitat management provides a mechanism whereby the requisite microclimates might be provided. Most arthropod species, including diamondback moth, experience their habitat at spatial scales beyond the scale of an individual field, with movement between crops and between crop and non-crop vegetation (Perović et al. 2010; Paredes et al. 2015; Tscharntke and Brandl 2004; Saqib et al. 2017). Accordingly, habitat manipulation may promote entomopathogen survival and impact in a given system by providing shade from UV and moderated humidity and temperature (Fernández-Bravo et al. 2016), either within the focal crop or in nearby areas from which infected insects may move to the crop. This offers scope to address adverse effects on entomopathogen distribution, persistence, and infection (Jaronski 2010). For example, for entomopathogenic fungi, temperature (Roberts and Campbell 1977), moisture (Inglis et al. 2001), and UV radiation (Klein 1978; Blumthaler et al. 1994; Inglis et al. 2001; Gao and Garcia-Pichel 2011; Braga et al. 2001) affect the rates of key infection processes (e.g., germination of conidia, hyphal growth) as well as the production of conidia from mycosed cadavers.

Realizing the potential of entomopathogens for the management of insect pests demands an understanding of how vegetation structure affects entomopathogen communities, flux of inocula into specific host or crops species, and how pathogens regulate insect pest populations in relation to habitat fragmentation (Pell et al. 2010). Work in this area is in its infancy compared with the larger research effort historically directed at habitat management for arthropod natural enemies (Gurr et al. 2017; Landis et al. 2000) but the limited available literature on entomopathogen-landscape interactions is encouraging. For instance, a reservoir of entomopathogenic fungi in aphids of non-crop habitats may result in higher infection rates of aphids in crops when insects spillover between these habitats (Ekesi et al. 2005). Entomopathogens can persist in the soil in the absence of hosts and this opens other potentially useful strategies. Fungi such as B. bassiana and M. anisopliae are commonly found in both cultivated and undisturbed soils, although their distribution appears to be linked to habitat (Bidochka et al. 2001; Keller et al. 2003; Meyling and Eilenberg 2006; Meyling et al. 2009), and their populations in soil are highly influenced by agricultural practices (Meyling and Eilenberg 2007; Jaronski 2010; Jaronski 2007; Hummel et al. 2002). Clearly, refuge areas where soil populations are free of adverse effects from tillage and agrochemicals may help landscape-scale persistence and density and allow recolonization of adjacent arable fields (Schneider et al. 2012). Permanent grassland, forest margins, and field margins as well as hedgerows have been suggested as refuges for entomopathogenic fungi (Meyling and Eilenberg 2007; Pell et al. 2010). The suitability of these habitats can be enhanced by specific seeding and mowing schemes (Marshall 2002; Fuxa 1998; Lacey et al. 2001; Meyling and Eilenberg 2007; Shah and Pell 2003). A specific illustration of this effect comes from Swiss work with some Metarhizium species that were found to be present at higher densities in low-input permanent grassland and improved field margins (Schneider et al. 2012). Similarly, in a comparative study entomopathogenic fungi occurrence in the soil of mid-field woodlots and cultivated fields in a conventional and organic system, soil from the woodlots was characterized by a richer species composition of entomopathogenic fungi (Tkaczuk et al. 2014; Tkaczuk et al. 2012).

A key consideration is how entomopathogens in the soil may reach diamondback moth on the crop plant. One potential mechanism is that many entomopathogenic fungi can grow endophytically within plants as well as being present in the soil. Both B. bassiana and T. harzianum can establish in cabbage host plants. B. bassiana growing endophytically in cabbage retarded growth and development of larvae and reduced oviposition by diamondback moth (Zhang 2014). Larvae feeding on B. bassiana-inoculated plants exhibited slower development and a lower body weight and this was reflected in adult female choice, laying significantly more eggs on control plants compared to the endophyte-infected plants. Similar effects were reported by Raps and Vidal (1998) when exposing diamondback moth to cabbage inoculated with an endophytic strain of Sarocladium strictum (W. Gams) Summerb. The disturbance levels of many brassica production systems are likely to reduce the continuity of endophyte-infested crop plants but areas of non-crop vegetation that include endophyte host plants could fill this temporal gap.

Vegetation structure can also affect the field persistence and efficacy of entomopathogenic nematodes. To assess the effects of landscape types on the efficacy and population densities of entomopathogenic nematodes, Lawrence et al. (2006) conducted a series of investigations across four habitats (cultivated areas, grassy banks adjacent to cultivated areas, undisturbed shrub lands and forests) across the landscape of a vegetable production area in Ohio, USA. Entomopathogenic nematodes, Heterorhabditis bacteriophora Poinar and Steinernema feltiae (Filipjev), were detected only along grassy banks adjacent to the cultivated areas, an effect thought to be determined by soil moisture. More generally, a better understanding of nematode population dynamics in agricultural landscapes appears to be crucial for designing strategies to increase their occurrence, persistence, and effectiveness as biological control agents (Campbell et al. 1995; Campbell et al. 1998; Efron et al. 2001; Glazer et al. 1996; Lawrence et al. 2006).

5.2 Habitat management and indirect ecological interactions

As for other pests, much of the research on diamondback moth management has been conducted in the context of the local scale with the focus on an individual crop field or farm (Furlong et al. 2013). However, increased plant, microbe, and invertebrate diversity at farm and landscape scales promotes complex interactions among species, including indirect ones. Such interactions, although much less studied than more obvious direct interactions (Godfray 2011; Jervis and Kidd 1996; Wootton 1994), are actually major drivers in communities (Chailleux et al. 2014). By contrast to direct interactions, e.g., predation and parasitism, which are well characterized in many agroecosystems, indirect interactions have received much less attention, notably their possible impact on major ecosystem services in agroecosystems; this applies in the case of studies on interactions linked to the diamondback moth. Unlike direct ones, indirect interactions occur between species that can be separated in time and/or space and they require (at minimum) one additional mediating species (Holt 1977; Wootton 1994). For example, herbivore species that do not directly interact can negatively affect each other through interactions with a shared host plant (Mouttet et al. 2011; Mouttet et al. 2013) and/or natural enemy(ies) (Chailleux et al. 2014). Such indirect interactions are not well studied for diamondback moth but are likely to be significant. For example, the aphid B. brassicae as well as whiteflies can modulate attractiveness of diamondback moth-infested plants for the parasitoid D. semiclausum through changes in the synomones emitted by infested plants (Zhang et al. 2013; Li et al. 2017), thus affecting the risk of parasitism of diamondback moth. Crop type can also affect levels of parasitism, for example, parasitism of diamondback moth by D. semiclausum was higher in B. oleracea var. capitata crops than in B. rapa var. Pekinensis. (Verkerk and Wright 1997). In addition, plants pre-infested by Pieris spp. were less attractive to diamondback moth (Poelman et al. 2011). Diamondback moth also exhibited plant-mediated indirect interactions with Acremonium alternatum such that plants infested by this fungus prior to the arrival of the pest led to increased larval mortality and reduced growth rate (Raps and Vidal 1998). Plant volatiles from non-host species have also been investigated for their effects on diamondback moth sex pheromones with the aim of using plants for mating disruption (Wang et al. 2016; Philips et al. 2014).

Indirect effects likely take place in any community of three or more interacting species (Holt and Lawton 1994) and could have important impacts on crop yields (Wielgoss et al. 2012). They may represent a key mechanism in determining the strength of food web interactions in communities inhabiting agricultural landscapes (Barbosa et al. 1991), generating both short-term effects on species abundance and long-term effects on population dynamics (Wootton 1994; Abrams and Matsuda 1996; Tack et al. 2011). Thus, there are likely strong effects on biological control services provided by natural enemies inhabiting farmlands and neighboring habitats (Bompard et al. 2013; Chailleux et al. 2014), so these indirect effects need to be explicitly considered in future studies.

The nature and strength of the indirect interactions are strongly scale dependent (Koss et al. 2004; Tack et al. 2011; Chailleux et al. 2014). For example, predator aggregation to a single prey species in field studies proved consistent with indirect negative interactions between pests while cage experiments (smaller scale) had predicted positive indirect effects (Östman and Ives 2003). Heterogeneity at the landscape level promotes indirect interactions, for example, predator-mediated interactions among prey or other pests, alternative prey, non-pests, and natural enemies (Chailleux et al. 2014). This includes those organisms that are temporally and/or spatially distinct and that do not show overlap in the resources they used (Tack et al. 2011). Pests such as diamondback moth that specialize on a given crop taxon could still promote biological control services against other pests inhabiting other crops, as well as against other prey in neighboring non-cropped areas. If the diamondback moth leads to a build-up of generalist natural enemy populations including entomopathogens though some, such as Entomophthorales are relatively host specific, it follows that pest suppression could result from generalist enemies promoted by interventions in non-brassica crops or even in non-crop areas.

Spillover of biological control services from one habitat type to another can be considered as indirect interactions at the landscape level among pests that are present in various crops. Natural enemy populations can build up on a range of insect hosts in particular crops and then affect other pests in neighboring crops. This can occur through passive movement, by seasonal effects such as plant senescence, and by human intervention including harvesting events that trigger enemy dispersal and use of food sprays to attract enemies into a desired area (Wade et al. 2008). Such spillover likely involves more generalist natural enemies than those such as parasitoids that specialize on a single or few prey species (Meyling and Hajek 2010). In contrast to specialized natural enemies, a major benefit of polyphagy in generalist natural enemies is that they are loosely tied to any one particular resource and thereby buffered against spatio-temporal fluctuations in availability of that food type. This may be especially important in biological control of diamondback moth given its vagility. When seasonally absent in one location, predators may persist until the next season of brassica production by relying on various different prey and other foods. Switching diets allows such predators to persist locally, unlike specialists that are driven to local extinction. A caveat to this, however, is that the effects of polyphagous consumers, including spiders and other types of predators that are known to attack diamondback moth, may be reduced in complex food webs because their consumptive power is diluted across many weak trophic links (Halaj and Wise 2001; Denno and Finke 2006). This could limit their impact on the focal pest species though it has been suggested that not all predators are as polyphagous as generally assumed (Furlong and Zalucki 2010).

In contrast, specialist natural enemies such as the diamondback moth parasitoids mentioned above may disperse over longer distances (Dodsall et al. 2004) since they are less able to sustain themselves using resources present in non-brassica crops or close neighboring habitats than generalist natural enemies (Symondson et al. 2002). Using temporary plant infrastructures in non-cropped areas, for example, banker plants (Parolin et al. 2012) in hedgerows or wild plants showing characteristics enhancing natural enemy establishment and/or population build up, could help sustain natural enemies when target pest species are scarce or seasonal conditions are unsuitable for the persistence of specialist natural enemies (Huang et al. 2011).

6 Area-wide management: a platform for more effective biological control of diamondback moth

Moving from a crop or farm-scale paradigm for diamondback moth management to a larger, coordinated approach that can exploit landscape-scale effects to promote biological control is made easier by preexistence of the area-wide management (AWM) concept and its acceptance by farmers and authorities (Zalucki et al. 2009; Downes et al. 2017). AWM has a long history of use in a range of geographical areas against a variety of crop pests. In the case of diamondback moth, AWM has been suggested as important, particularly from the perspective of insecticide resistance management, cultural control and enhancement of biological control (Talekar and Shelton 1993). This is especially relevant here due to the migratory capacity of adult diamondback moth that can lead to the establishment of resistant populations, even in areas where there has been limited local selection for insecticide resistance (Zhao et al. 2006; Feng et al. 2011; Gao et al. 2016).

Globally, AWM is increasingly used for highly mobile pests, operating over a geographically defined area and characterized by being preventive (rather than reactive), as well as spatio-temporally coordinated (Hendrichs et al. 2007). The central premise of AWM is that all individuals of a pest population are managed, both in space and in time, in crops and in non-crop hosts, and year-round rather than only during the production season (Hendrichs et al. 2007). AWM does employ conservation biological control, especially against highly mobile species (Klassen 2005) and provides important guidance to natural enemy-focused efforts in terms of both scientific principles and the practical, management dimension. The more traditional field-by-field management approach is focused on remedial intervention triggered when a pest population reaches a certain threshold. Such localized control is suboptimal, particularly when exercising biological control through promotion of diverse taxa and guilds of natural enemies and when pests are mobile and making use of various host plants, as is the case for diamondback moth. The need to adopt a landscape-scale approach to promote natural enemies through habitat management is driven by (i) generalist species are often favored by continuity of availability of a range of prey species and plant-based foods; (ii) specialist species often exhibit life history omnivory, for example, adult stages of many parasitoids require access to nectar; (iii) food and shelter are required during periods when crops are either absent or are yet to be infested with pests; and (iv) while natural enemies have markedly differing dispersal ranges, they are often larger than the dimensions of a single crop and may be in the order of several kilometers (Tscharntke et al. 2012; Perović et al. 2010). Accordingly, the land uses immediately around crops and further afield become critical in providing appropriate resources to, and serving as donor habitat for, natural enemies.

Exploiting spatial barriers (even if semi-permeable) to the immigration of pests, especially mated females, into an area is key to AWM. Accordingly, geographically or topographically isolated locations or settings such as greenhouse complexes are good candidates (Casey et al. 2007). While some brassica crops are grown in greenhouses, they are in the minority so the vagility of diamondback moth adults means that barriers are of relatively low importance. Importantly, however, the reverse philosophy applies to the dynamics of natural enemies. For these beneficial species, barriers to immigration need to be minimized so that crops are rapidly colonized by large numbers of individuals from a range of guilds. Accordingly, a key challenge is to engineer landscapes that selectively promote population size and spatio-temporal flux of enemies while having the opposite effects on their prey. Achieving this is clearly challenging but work by Perović et al. (2010) suggests that perennial woody vegetation can promote landscape-scale connectivity for enemy immigration into cotton crops with no benefit to at least some herbivores (Macfadyen et al. 2015). More recent work in European managed grasslands showed that landscape simplification—a syndrome common in many agricultural areas (Fig. 1)—tends to favor arthropods with generalized feeding traits, larger body sizes, and longer seasonal activity periods (Gamez-Virues et al. 2015); all traits that could be predicted to allow persistence in habitats with larger patch sizes and carrying capacity. In contrast, landscape heterogeneity—as often evident in more traditional agricultural systems (Fig. 1)—tends to favor arthropods with more specialized feeding traits, smaller body sizes, and shorter activity periods. Importantly, this effect persists irrespective of high levels of management intensity within fields sited in such landscapes showing, essentially, that the landscape scale is more important than generally recognized, overriding differences at the more local scale (Gamez-Virues et al. 2015). Though that work took place in grasslands, it has direct implications for biological control of pests including diamondback moth. Landscape-scale strategies that are able to support a more diverse community of natural enemies would provide better pest suppression as a result of enemies partitioning the prey resource, thereby reducing intra-guild predation and competition. It also affords the system increased resilience to environmental disturbances, such as droughts or storms resulting from climate change (Yachi and Loreau 1999; Mori et al. 2013). Although the aforementioned work of European managed grasslands focused on arthropods, other results from the same large-scale study suggest that land use simplification has effects on multiple guilds and trophic levels and extend to below-ground taxa (Gossner et al. 2016; Perović et al. 2018). Accordingly, non-arthropod natural enemies of pests such as nematode and microbial entomopathogens may be adversely impacted by landscape simplification, but amenable to promotion by diversification strategies (Meyling and Eilenberg 2007; Pell et al. 2010) such as those mentioned in Section 5.1.

Although landscape-scale effects can over-ride local management, there remains an important complementary role for local interventions. For example, a brassica crop in a diverse landscape may enjoy higher levels of natural enemies if certain practices are employed. These include the use of nectar plants to nourish parasitoids, an impactful approach which reduced the need for spraying, increased grain yield and enhanced profits in Asian rice (Gurr et al. 2016). A complementary approach is the application of semiochemicals to attract natural enemy movement into crops from nearby donor habitat, an approach shown to have potential in Australian studies that included broccoli crops (Simpson et al. 2011a; Simpson et al. 2011b). Species of arthropod natural enemies respond differentially to different semiochemicals, so there is potential to use these in a selective manner to drive natural enemy distribution, not only spatially and temporally but also in a species-specific manner. Food sprays and banker plants can also be used to support natural enemies at the more local scale provided that the wider landscape has the capacity to function effectively as donor habitat (Huang et al. 2011; Wade et al. 2008). The integrated use of pest control approaches such as those described above is important for implementing any conceptual plan for biological control-based AWM, a challenge that landscape ecologists will need to embrace.

7 Conclusion and prospects

Despite diamondback moth being the subject of intense research efforts over multiple decades, it remains a major cause of crop loss and driver of production costs. Changing this will require changes to the pest management approaches used by growers and the nature of the research efforts undertaken to provide the evidence base (Fig. 3). Historically, most biological control studies have focused on specific potential agents, chiefly parasitoids. There has, however, been a growth in the absolute numbers and relative research effort regarding predators and entomopathogens of diamondback moth. A move towards using multiple agents and conservation biological control is necessary. Associated with this, the efficacy of biological control is dependent on avoiding insecticide-induced mortality of agents. While this can be done by switching from broad-spectrum to more selective active ingredients (or microbial insecticides such as Bt), forms of habitat management that provide refuges in the landscape from which surviving natural enemies can re-colonize a sprayed crop offer potential (Heimoana et al. 2017).
Fig. 3

Status of pest management for diamondback moth

Diamondback moth is highly vagile, and seasonal migrations allow exploitation of new brassica crops and subsequent rapid reproduction in enemy free space. As a consequence, landscape-scale programs are important so that diverse assemblages of natural enemies including entomopathogens can (i) persist in a given area during periods of pest absence and (ii) readily move into croplands and reproduce quickly to check pest build-up. Though farm- and local-scale interventions such as avoiding broad-spectrum insecticides, using nectar plant borders, semiochemical-mediated attraction, and banker plants have potential, they are contingent on the existence of sufficient donor habitat in the wider landscape from which natural enemies can move into the crop. Further, landscapes with high levels of vegetation diversity support a wider range of natural enemy taxa and guilds. This is advantageous in providing assemblages of natural enemies that can partition the prey resource (attacking all life stages for example) and able to cope with environmental change (higher temperatures and extreme weather events for example). Area-wide management is used successfully against various pests and offers the potential to be adapted as a delivery paradigm to improve biological control of diamondback moth. Components of this could include wider use of agroenvironment programs that are broadened in spatial extent to the landscape scale to motivate farmers and other stakeholders to adopt schemes beyond their individual farm (Gabriel et al. 2010). Similarly, certification programs for land stewardship that aim to maintain biodiversity and ecosystem services could be adapted to focus on the delivery of ecosystem services such as biological control to provide ecological intensification of agricultural systems (Geertsema et al. 2016). Essentially, these steps will move pest management from a reactive to preventative strategy. Finally, participatory approaches including the development and implementation of regional conservation programs should involve farmers so that multiple outcomes, including landscape-wide conservation of ecosystem service providers, are achieved (Westphal et al. 2015). While we believe these prospects apply strongly to diamondback moth, they have wider relevance to similarly r-selected pests, such as Helicoverpa spp. (Downes et al. 2017) and many Hemiptera pests, for which improved management is required.

Notes

Acknowledgements

We acknowledge the input of David Perovic & Sagrario Gamez-Virues in the early stages of planning this review.

Funding information

This project was supported by the National Natural Science Foundation of China (No. 31230061 and No. 31320103922). GMG was supported by the National Thousand Talents Fellowship, the Advanced Talents of SAEFA in China and a Graham Centre Research Fellowship. ND was supported by the project EUCLID (H2020-SFS-2014, grant number: 633999). OLR was supported by a Jinshan Scholar Fellowship at Fujian Agriculture and Forestry University (FAFU), China. KSA was supported as a postdoctoral fellow by the National Thousand Talents Fellowship at FAFU, China. Grants CS2/1998/089, HORT/2002/062, HORT/2004/063 and HORT/2010/090 from the Australian Centre for International Agricultural Research (ACIAR) have supported diamondback moth research by MJF and MPZ in China, Democratic Republic of Korea, Fiji, Samoa and Tonga.

References

  1. Abrams PA, Matsuda H (1996) Positive indirect effects between prey species that share predators. Ecology 77(2):610–616.  https://doi.org/10.2307/2265634 CrossRefGoogle Scholar
  2. Adamson D, Zalucki MP, Furlong MJ (2014) Pesticides and integrated pest management practice, practicality and policy in Australia. In: Peshin R, Pimentel D (eds) Integrated pest management: experiences with implementation, global overview, Vol.4. Springer Netherlands, Dordrecht, pp 387–411. doi: https://doi.org/10.1007/978-94-007-7802-3_16 Google Scholar
  3. Ankersmit G (1953) DDT-resistance in Plutella maculipennis (Curt.)(Lep.) in Java. Bull Entomol Res 44(03):421–425.  https://doi.org/10.1017/S0007485300025530 CrossRefGoogle Scholar
  4. Barbosa P, Krischik VA, Jones CG (1991) Microbial mediation of plant-herbivore interactions. John Wiley & Sons, New YorkGoogle Scholar
  5. Bentur JS, Viraktamath BC (2008) Rice planthoppers strike back. Curr Sci 95(4):441–443Google Scholar
  6. Bidochka MJ, Kamp AM, Lavender TM, Dekoning J, De Croos JNA (2001) Habitat association in two genetic groups of the insect-pathogenic fungus Metarhizium anisopliae: uncovering cryptic species? Appl Environ Microbiol 67(3):1335–1342.  https://doi.org/10.1128/aem.67.3.1335-1342.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Blumthaler M, Ambach W, Silbernagl R, Staehelin J (1994) Erythemal UV-B irradiance (Robertson-Berger sunburn meter data) under ozone deficiencies in winter/spring 1993. Photochem Photobiol 59(6):657–659.  https://doi.org/10.1111/j.1751-1097.1994.tb09672.x CrossRefGoogle Scholar
  8. Bompard A, Jaworski CC, Bearez P, Desneux N (2013) Sharing a predator: can an invasive alien pest affect the predation on a local pest? Popul Ecol 55(3):433–440.  https://doi.org/10.1007/s10144-013-0371-8 CrossRefGoogle Scholar
  9. Bradshaw CJA, Leroy B, Bellard C, Roiz D, Albert C, Fournier A, Barbet-Massin M, Salles J-M, Simard F, Courchamp F (2016) Massive yet grossly underestimated global costs of invasive insects. Nat Commun 7:12986.  https://doi.org/10.1038/ncomms12986 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Braga GUL, Flint SD, Messias CL, Anderson AJ, Roberts DW (2001) Effect of UV-B on conidia and germlings of the entomopathogenic hyphomycete Metarhizium anisopliae. Mycol Res 105(7):874–882.  https://doi.org/10.1017/S0953756201004270 CrossRefGoogle Scholar
  11. Brown J, Frohlich D, Rosell R (1995) The sweetpotato or silverleaf whiteflies: biotypes of Bemisia tabaci or a species complex? Annu Rev Entomol 40(1):511–534.  https://doi.org/10.1146/annurev.en.40.010195.002455 CrossRefGoogle Scholar
  12. Burges HD, Thomson EM, Latchford RA (1976) Importance of spores and δ-endotoxin protein crystals of Bacillus thuringiensis in Galleria mellonella. J Invertebr Pathol 27(1):87–94.  https://doi.org/10.1016/0022-2011(76)90032-X CrossRefGoogle Scholar
  13. Campbell JF, Lewis E, Yoder F, Gaugler R (1995) Entomopathogenic nematode (Heterorhabditidae and Steinernematidae) seasonal population dynamics and impact on insect populations in turfgrass. Biol Control 5(4):598–606.  https://doi.org/10.1006/bcon.1995.1071 CrossRefGoogle Scholar
  14. Campbell JF, Orza G, Yoder F, Lewis E, Gaugler R (1998) Spatial and temporal distribution of endemic and released entomopathogenic nematode populations in turfgrass. Entomologia Experimentalis et Applicata 86(1):1–11.  https://doi.org/10.1046/j.1570-7458.1998.00260.x CrossRefGoogle Scholar
  15. Casey C, Newman JP, Robb KL, Tjosvold SA, MacDonald JD, Parrella MP (2007) IPM program successful in California greenhouse cut roses. Calif Agric 61(2):71–78.  https://doi.org/10.3733/ca.v061n02p71 CrossRefGoogle Scholar
  16. Chailleux A, Mohl E, Teixeira-Alves M, Messelink G, Desneux N (2014) Natural enemy-mediated indirect interactions among prey species: potential for enhancing biocontrol services in agroecosystems. Pest Manag Sci 70:1769–1779.  https://doi.org/10.1002/ps.3916 CrossRefPubMedGoogle Scholar
  17. Chapman JW, Reynolds DR, Smith AD, Riley JR, Pedgley DE, Woiwod IP (2002) High-altitude migration of the diamondback moth Plutella xylostella to the U.K.: a study using radar, aerial netting, and ground trapping. Ecol Entomol 27(6):641–650.  https://doi.org/10.1046/j.1365-2311.2002.00472.x CrossRefGoogle Scholar
  18. Cherry AJ, Mercadier G, Meikle W, Castelo-Branco M, Schroer S (2004) The role of entomopathogens in DBM biological control. In: Kirk AA, Bordat D (eds) Improving biocontrol of Plutella xylostella: Proceedings of the International Symposium, Montpellier, France, 21–24 October, 2002. CIRAD, pp 51–70Google Scholar
  19. Crickmore N (2006) Beyond the spore—past and future developments of Bacillus thuringiensis as a biopesticide. J Appl Microbiol 101(3):616–619.  https://doi.org/10.1111/j.1365-2672.2006.02936.x CrossRefPubMedGoogle Scholar
  20. Denno RF, Finke DL (2006) Multiple predator interactions and food-web connectance: implications for biological control. In: Brodeur J, Boivin G (eds) Trophic and guild in biological interactions control. Springer, Berlin, pp 45–70CrossRefGoogle Scholar
  21. Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52(1):81–106.  https://doi.org/10.1146/annurev.ento.52.110405.091440 CrossRefPubMedGoogle Scholar
  22. Dosdall L, Mason P, Olfert O, Kaminski L, Keddie B (2004) The origins of infestations of diamondback moth, Plutella xylostella (L.), in canola in western Canada. In: Endersby N, Ridland PM (eds) The management of diamondback moth and other crucifer pests: Proceedings of the IV International workshop. The Regional Inst., Melbourne, pp 26–29Google Scholar
  23. Downes S, Kriticos D, Parry H, Paull C, Schellhorn N, Zalucki MP (2017) A perspective on management of Helicoverpa armigera: transgenic Bt cotton, IPM, and landscapes. Pest Manag Sci 73(3):485–492.  https://doi.org/10.1002/ps.4461 CrossRefPubMedGoogle Scholar
  24. Duarte RT, Gonçalves KC, Espinosa DJL, Moreira LF, De Bortoli SA, Humber RA, Polanczyk RA (2016) Potential of entomopathogenic fungi as biological control agents of diamondback moth (Lepidoptera: Plutellidae) and compatibility with chemical insecticides. J Econ Entomol 109(2):594–601.  https://doi.org/10.1093/jee/tow008 CrossRefPubMedGoogle Scholar
  25. Efron D, Nestel D, Glazer I (2001) Spatial analysis of entomopathogenic nematodes and insect hosts in a citrus grove in a semi-arid region in Israel. Environ Entomol 30(2):254–261.  https://doi.org/10.1603/0046-225X-30.2.254 CrossRefGoogle Scholar
  26. Ekesi S, Shah PA, Clark SJ, Pell JK (2005) Conservation biological control with the fungal pathogen Pandora neoaphidis: implications of aphid species, host plant and predator foraging. Agric For Entomol 7(1):21–30.  https://doi.org/10.1111/j.1461-9555.2005.00239.x CrossRefGoogle Scholar
  27. Feng X, Li ZY, Wu QJ, Chen AD, Wu YD, Hou YM, He YR, Li JH, Xie SH, Zhang JM, Fu W (2011) Research progress of the resistance management and sustainable control of diamondback moth (Plutella xylostella) in China. Chin J Appl Entomol 48(2):247–253Google Scholar
  28. Fernández-Bravo M, Garrido-Jurado I, Valverde-García P, Enkerli J, Quesada-Moraga E (2016) Responses to abiotic environmental stresses among phylloplane and soil isolates of Beauveria bassiana from two holm oak ecosystems. J Invertebr Pathol 141(Supplement C):6–17.  https://doi.org/10.1016/j.jip.2016.09.007 CrossRefPubMedGoogle Scholar
  29. Fox LR, Eisenbach J (1992) Contrary choices: possible exploitation of enemy-free space by herbivorous insects in cultivated vs. wild crucifers. Oecologia 89(4):574–579.  https://doi.org/10.1007/bf00317166 CrossRefPubMedGoogle Scholar
  30. Furlong MJ, Ju KH, Su PW, Chol JK, Il RC, Zalucki MP (2008a) Integration of endemic natural enemies and Bacillus thuringiensis to manage insect pests of Brassica crops in North Korea. Agric Ecosyst Environ 125(1):223–238.  https://doi.org/10.1016/j.agee.2008.01.003 CrossRefGoogle Scholar
  31. Furlong MJ, Pell JK (1997) The influence of environmental factors on the persistence of Zoophthora radicans conidia. J Invertebr Pathol 69(3):223–233.  https://doi.org/10.1006/jipa.1996.4649 CrossRefGoogle Scholar
  32. Furlong MJ, Pell JK (2001) Horizontal transmission of entomopathogenic fungi by the diamondback moth. Biol Control 22(3):288–299.  https://doi.org/10.1006/bcon.2001.0981 CrossRefGoogle Scholar
  33. Furlong MJ, Pell JK, Choo OP, Rahman SA (1995) Field and laboratory evaluation of a sex pheromone trap for the autodissemination of the fungal entomopathogen Zoophthora radicans (Entomophthorales) by the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Bull Entomol Res 85(03):331–337.  https://doi.org/10.1017/S0007485300036051 CrossRefGoogle Scholar
  34. Furlong MJ, Rowley DL, Murtiningsih R, Greenstone MH (2014) Combining ecological methods and molecular gut-content analysis to investigate predation of a lepidopteran pest complex of Brassica crops. Entomologia Experimentalis et Applicata 153(2):128–141.  https://doi.org/10.1111/eea.12231 CrossRefGoogle Scholar
  35. Furlong MJ, Shi Z-H, Liu S-S, Zalucki MP (2004a) Evaluation of the impact of natural enemies on Plutella xylostella L. (Lepidoptera: Yponomeutidae) populations on commercial Brassica farms. Agric For Entomol 6(4):311–322.  https://doi.org/10.1111/j.1461-9555.2004.00228.x CrossRefGoogle Scholar
  36. Furlong MJ, Spafford H, Ridland PM, Endersby NM, Edwards OR, Baker GJ, Keller MA, Paull CA (2008b) Ecology of diamondback moth in Australian canola: landscape perspectives and the implications for management. Aust J Exp Agric 48(12):1494–1505.  https://doi.org/10.1071/Ea07413 CrossRefGoogle Scholar
  37. Furlong MJ, Wright DJ, Dosdall LM (2013) Diamondback moth ecology and management: problems, progress, and prospects. Annu Rev Entomol 58:517–541.  https://doi.org/10.1146/annurev-ento-120811-153605 CrossRefPubMedGoogle Scholar
  38. Furlong MJ, Zalucki MP (2010) Exploiting predators for pest management: the need for sound ecological assessment. Entomologia Experimentalis et Applicata 135(3):225–236.  https://doi.org/10.1111/j.1570-7458.2010.00988.x CrossRefGoogle Scholar
  39. Furlong MJ, Zu-Hua S, Yin-Quan L, Shi-Jian G, Yao-Bin L, Shu-Sheng L, Zalucki MP (2004b) Experimental analysis of the influence of pest management practice on the efficacy of an endemic arthropod natural enemy complex of the diamondback moth. J Econ Entomol 97(6):1814–1827.  https://doi.org/10.1603/0022-0493-97.6.1814 CrossRefPubMedGoogle Scholar
  40. Fuxa JR (1998) Environmental manipulation for microbial control of insects. In: Barbosa P (ed) Conservation biological control. Academic Press, San Diego, USA, pp 255–268CrossRefGoogle Scholar
  41. Gabriel D, Sait SM, Hodgson JA, Schmutz U, Kunin WE, Benton TG (2010) Scale matters: the impact of organic farming on biodiversity at different spatial scales. Ecol Lett 13(7):858–869.  https://doi.org/10.1111/j.1461-0248.2010.01481.x CrossRefPubMedGoogle Scholar
  42. Gamez-Virues S, Perovic DJ, Gossner MM, Borschig C, Bluthgen N, de Jong H, Simons NK, Klein AM, Krauss J, Maier G, Scherber C, Steckel J, Rothenwohrer C, Steffan-Dewenter I, Weiner CN, Weisser W, Werner M, Tscharntke T, Westphal C (2015) Landscape simplification filters species traits and drives biotic homogenization. Nat Commun 6:8568.  https://doi.org/10.1038/ncomms9568 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Gao Q, Garcia-Pichel F (2011) Microbial ultraviolet sunscreens. Nat Rev Microbiol 9(11):791–802.  https://doi.org/10.1038/nrmicro2649 CrossRefPubMedGoogle Scholar
  44. Gao X, Yang J, Xu B, Yang F, Wu Q (2016) Insecticide resistance in diamondback moth populations in Beijing and Hebei. Chin J Appl Environ Biol 53:279–284Google Scholar
  45. Geertsema W, Rossing WAH, Landis DA, Bianchi FJJA, van Rijn PCJ, Schaminée JHJ, Tscharntke T, van der Werf W (2016) Actionable knowledge for ecological intensification of agriculture. Front Ecol Environ 14(4):209–216.  https://doi.org/10.1002/fee.1258 CrossRefGoogle Scholar
  46. Gillespie MA, Gurr GM, Wratten SD (2016) Beyond nectar provision: the other resource requirements of parasitoid biological control agents. Entomologia Experimentalis et Applicata 159:1–15.  https://doi.org/10.1111/eea.12424 CrossRefGoogle Scholar
  47. Glazer I, Kozodoi E, Salame L, Nestel D (1996) Spatial and temporal occurrence of natural populations of Heterorhabditis spp. (Nematoda: Rhabditida) in a semiarid region. Biol Control 6(1):130–136.  https://doi.org/10.1006/bcon.1996.0016 CrossRefGoogle Scholar
  48. Godfray HCJ (2011) Ecology, food and biodiversity. Science 333(6047):1231–1232.  https://doi.org/10.1126/science.1211815 CrossRefPubMedGoogle Scholar
  49. Gonçalves F, Carlos C, Aranha J, Torres L (2017) Does habitat heterogeneity affect the diversity of epigaeic arthropods in vineyards? Agric Forest Entomol:n/a-n/a doi: https://doi.org/10.1111/afe.12270 CrossRefGoogle Scholar
  50. Gossner MM, Lewinsohn TM, Kahl T, Grassein F, Boch S, Prati D, Birkhofer K, Renner SC, Sikorski J, Wubet T, Arndt H, Baumgartner V, Blaser S, Blüthgen N, Börschig C, Buscot F, Diekötter T, Jorge LR, Jung K, Keyel AC, Klein A-M, Klemmer S, Krauss J, Lange M, Müller J, Overmann J, Pašalić E, Penone C, Perović DJ, Purschke O, Schall P, Socher SA, Sonnemann I, Tschapka M, Tscharntke T, Türke M, Venter PC, Weiner CN, Werner M, Wolters V, Wurst S, Westphal C, Fischer M, Weisser WW, Allan E (2016) Land-use intensification causes multitrophic homogenization of grassland communities. Nature 540(7632):266–269.  https://doi.org/10.1038/nature20575 CrossRefPubMedGoogle Scholar
  51. Grzywacz D, Parnell D, Kibata G, Oduor G, Ogutu W, Miano D, Winstanley D (2004) The development of endemic baculoviruses of Plutella xylostella (diamondback moth, DBM) for control of DBM in East Africa. In: Endersby NM (ed) The management of diamondback moth and other crucifer pests: Proceedings of the Fourth International Workshop, Melbourne, Australia, 26-29 November 2001 2004. International Diamondback Moth Working Group, pp 197–206Google Scholar
  52. Grzywacz D, Rossbach A, Rauf A, Russell D, Srinivasan R, Shelton A (2010) Current control methods for diamondback moth and other brassica insect pests and the prospects for improved management with lepidopteran-resistant Bt vegetable brassicas in Asia and Africa. Crop Prot 29(1):68–79.  https://doi.org/10.1016/j.cropro.2009.08.009 CrossRefGoogle Scholar
  53. 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 LQ, Channoo C, Chengwattana N, Lan LP, Hai LH, Chaiwong J, Nicol HI, Perovic DJ, Wratten SD, Heong KL (2016) Multi-country evidence that crop diversification promotes ecological intensification of agriculture. Nature Plants 2:16014.  https://doi.org/10.1038/nplants.2016.14 CrossRefPubMedGoogle Scholar
  54. Gurr GM, Wratten SD, Landis DA, You M (2017) Habitat management to suppress pest populations: progress and prospects. Annu Rev Entomol 62(1):91–109.  https://doi.org/10.1146/annurev-ento-031616-035050 CrossRefPubMedGoogle Scholar
  55. Halaj J, Wise DH (2001) Terrestrial trophic cascades: how much do they trickle? Am Nat 157(3):262–281.  https://doi.org/10.1086/319190 CrossRefPubMedGoogle Scholar
  56. Heimoana V, Pilkington LJ, Raman A, Mitchell A, Nicol HI, Johnson AC, Gurr GM (2017) Integrating spatially explicit molecular and ecological methods to explore the significance of non-crop vegetation to predators of brassica pests. Agric Ecosyst Environ 239:12–19.  https://doi.org/10.1016/j.agee.2017.01.008 CrossRefGoogle Scholar
  57. Hendrichs J, Kenmore P, Robinson AS, Vreysen MJB (2007) Area-wide integrated pest management (AW-IPM): principles, practice and prospects. In: Vreysen MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests: from research to field implementation. Springer, Netherlands, Dordrecht, pp 3–33.  https://doi.org/10.1007/978-1-4020-6059-5_1 CrossRefGoogle Scholar
  58. Holland JM, Douma JC, Crowley L, James L, Kor L, Stevenson DRW, Smith BM (2017) Semi-natural habitats support biological control, pollination and soil conservation in Europe. A review. Agron Sustain Dev 37(4).  https://doi.org/10.1007/s13593-017-0434-x
  59. Holt R, Lawton J (1994) The ecological consequences of shared natural enemies. Annu Rev Ecol Syst 25(1):495–520.  https://doi.org/10.1146/annurev.es.25.110194.002431 CrossRefGoogle Scholar
  60. Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12(2):197–229.  https://doi.org/10.1016/0040-5809(77)90042-9 CrossRefPubMedGoogle Scholar
  61. Huang NX, Enkegaard A, Osborne LS, Ramakers PMJ, Messelink GJ, Pijnakker J, Murphy G (2011) The banker plant method in biological control. Crit Rev Plant Sci 30(3):259–278.  https://doi.org/10.1080/07352689.2011.572055 CrossRefGoogle Scholar
  62. Hummel RL, Walgenbach JF, Barbercheck ME, Kennedy GG, Hoyt GD, Arellano C (2002) Effects of production practices on soil-borne entomopathogens in western North Carolina vegetable systems. Environ Entomol 31(1):84–91.  https://doi.org/10.1603/0046-225X-31.1.84 CrossRefGoogle Scholar
  63. Inglis G, Goettel M, Butt T, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt T, Jackson C, Magan N (eds) Fungi as biocontrol agents. CAB International, Wallingford, UK, pp 23–69Google Scholar
  64. Jaronski ST (2007) Soil ecology of the entomopathogenic ascomycetes: a critical examination of what we (think) we know. In: Ekesi S, Maniania NK (eds) Use of entomopathogenic fungi in biological Pest management. Research SignPosts, Trivandrum, India, pp 91–144Google Scholar
  65. Jaronski ST (2010) Ecological factors in the inundative use of fungal entomopathogens. BioControl 55(1):159–185.  https://doi.org/10.1007/s10526-009-9248-3 CrossRefGoogle Scholar
  66. Jervis MA, Kidd N (1996) Insect natural enemies. Chapman Hall Australia, MelbourneCrossRefGoogle Scholar
  67. Keller S, Kessler P, Schweizer C (2003) Distribution of insect pathogenic soil fungi in Switzerland with special reference to Beauveria brongniartii and Metharhizium anisopliae. BioControl 48(3):307–319.  https://doi.org/10.1023/a:1023646207455 CrossRefGoogle Scholar
  68. Kirk A, Mercadier G, Bordat D, Delvare G, Pichon A, Arvanitakis L, Goudégnon A, Rincon C (2004) Variability in Plutella and its natural enemies: implications for biological control. In: Endersby N (ed) The management of diamondback moths and other crucifer pests: Proceedings of the Fourth International Workshop, Melbourne, Australia, 26-29 November, 2001 2004. Australian Entomological Society, pp 71–77Google Scholar
  69. Klassen W (2005) Area-wide integrated pest management and the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique: principles and practice in area-wide integrated pest management. Springer, Netherlands, Dordrecht, pp 39–68.  https://doi.org/10.1007/1-4020-4051-2_2 CrossRefGoogle Scholar
  70. Klein RM (1978) Plants and near-ultraviolet radiation. Bot Rev 44(1):1–127.  https://doi.org/10.1007/bf02860853 CrossRefGoogle Scholar
  71. Koss AM, Chang GC, Snyder WE (2004) Predation of green peach aphids by generalist predators in the presence of alternative, Colorado potato beetle egg prey. Biol Control 31(2):237–244.  https://doi.org/10.1016/j.biocontrol.2004.04.006 CrossRefGoogle Scholar
  72. Lacey LA, Frutos R, Kaya HK, Vail P (2001) Insect pathogens as biological control agents: do they have a future? Biol Control 21(3):230–248.  https://doi.org/10.1006/bcon.2001.0938 CrossRefGoogle Scholar
  73. 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 CrossRefPubMedGoogle Scholar
  74. Lawrence JL, Hoy CW, Grewal PS (2006) Spatial and temporal distribution of endemic entomopathogenic nematodes in a heterogeneous vegetable production landscape. Biol Control 37(3):247–255.  https://doi.org/10.1016/j.biocontrol.2006.02.002 CrossRefGoogle Scholar
  75. Li Y, Weldegergis BT, Chamontri S, Dicke M, Gols R (2017) Does aphid infestation interfere with indirect plant defense against lepidopteran caterpillars in wild cabbage? J Chem Ecol 43(5):493–505.  https://doi.org/10.1007/s10886-017-0842-z CrossRefPubMedPubMedCentralGoogle Scholar
  76. Li Z, Feng X, Liu S-S, You M, Furlong MJ (2016a) Biology, ecology, and management of the diamondback moth in China. Annu Rev Entomol 61:277–296.  https://doi.org/10.1146/annurev-ento-010715-023622 CrossRefPubMedGoogle Scholar
  77. Li Z, Zalucki MP, Yonow T, Kriticos DJ, Bao H, Chen H, Hu Z, Feng X, Furlong MJ (2016b) Population dynamics and management of diamondback moth (Plutella xylostella) in China: the relative contributions of climate, natural enemies and cropping patterns. Bull Entomol Res 106(2):197–214.  https://doi.org/10.1017/S0007485315001017 CrossRefPubMedGoogle Scholar
  78. Liu S, Shi Z, Furlong MJ, Zalucki M (2005) Conservation and enhancement of biological control helps to improve sustainable production of Brassica vegetables in China and Australia. In: Hoddle MS (ed) Second International Symposium on Biological Control of Arthropods, Davos, Switzerland, 2005. pp 254–266Google Scholar
  79. Liu Y-Q, Shi Z-H, Zalucki MP, Liu S-S (2014) Conservation biological control and IPM practices in Brassica vegetable crops in China. Biol Control 68(0):37–46.  https://doi.org/10.1016/j.biocontrol.2013.06.008 CrossRefGoogle Scholar
  80. Lu ZX, Zhu PY, Gurr GM, Zheng XS, Read DMY, Heong KL, Yang YJ, Xu HX (2014) Mechanisms for flowering plants to benefit arthropod natural enemies of insect pests: prospects for enhanced use in agriculture. Insect Sci 21(1):1–12.  https://doi.org/10.1111/1744-7917.12000 CrossRefPubMedGoogle Scholar
  81. Macfadyen S, Hopkinson J, Parry H, Neave MJ, Bianchi FJJA, Zalucki MP, Schellhorn NA (2015) Early-season movement dynamics of phytophagous pest and natural enemies across a native vegetation-crop ecotone. Agric Ecosyst Environ 200:110–118.  https://doi.org/10.1016/j.agee.2014.11.012 CrossRefGoogle Scholar
  82. Marshall EJP (2002) Introducing field margin ecology in Europe. Agric Ecosyst Environ 89(1):1–4.  https://doi.org/10.1016/S0167-8809(01)00314-0 CrossRefGoogle Scholar
  83. Mason JM, Matthews GA, Wright DJ (1999) Evaluation of spinning disc technology for the application of entomopathogenic nematodes against a foliar pest. J Invertebr Pathol 73(3):282–288.  https://doi.org/10.1006/jipa.1998.4832 CrossRefPubMedGoogle Scholar
  84. Mason JM, Wright DJ (1997) Potential for the control of Plutella xylostella larvae with entomopathogenic nematodes. J Invertebr Pathol 70(3):234–242.  https://doi.org/10.1006/jipa.1997.4695 CrossRefGoogle Scholar
  85. Meyling NV, Eilenberg J (2006) Isolation and characterisation of Beauveria bassiana isolates from phylloplanes of hedgerow vegetation. Mycol Res 110(2):188–195.  https://doi.org/10.1016/j.mycres.2005.09.008 CrossRefPubMedGoogle Scholar
  86. Meyling NV, Eilenberg J (2007) Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biol Control 43(2):145–155.  https://doi.org/10.1016/j.biocontrol.2007.07.007 CrossRefGoogle Scholar
  87. Meyling NV, Hajek AE (2010) Principles from community and metapopulation ecology: application to fungal entomopathogens. BioControl 55(1):39–54.  https://doi.org/10.1007/s10526-009-9246-5 CrossRefGoogle Scholar
  88. Meyling NV, Lübeck M, Buckley EP, Eilenberg J, Rehner SA (2009) Community composition, host range and genetic structure of the fungal entomopathogen Beauveria in adjoining agricultural and seminatural habitats. Mol Ecol 18(6):1282–1293.  https://doi.org/10.1111/j.1365-294X.2009.04095.x CrossRefPubMedGoogle Scholar
  89. Mo J, Baker G, Keller M, Roush R (2003) Local dispersal of the diamondback moth (Plutella xylostella (L.)) (Lepidoptera: Plutellidae). Environ Entomol 32(1):71–79CrossRefGoogle Scholar
  90. Mori AS, Furukawa T, Sasaki T (2013) Response diversity determines the resilience of ecosystems to environmental change. Biol Rev 88(2):349–364.  https://doi.org/10.1111/brv.12004 CrossRefPubMedGoogle Scholar
  91. Mouttet R, Bearez P, Thomas C, Desneux N (2011) Phytophagous arthropods and a pathogen sharing a host plant: evidence for indirect plant-mediated interactions. PLoS One 6(5):e18840.  https://doi.org/10.1371/journal.pone.0018840 CrossRefPubMedPubMedCentralGoogle Scholar
  92. Mouttet R, Kaplan I, Bearez P, Amiens-Desneux E, Desneux N (2013) Spatiotemporal patterns of induced resistance and susceptibility linking diverse plant parasites. Oecologia 173(4):1379–1386.  https://doi.org/10.1007/s00442-013-2716-6 CrossRefPubMedGoogle Scholar
  93. Muckenfuss A, Shepard B, Ferrer E (1992) Natural mortality of diamondback moth in coastal South Carolina. In: Talekar NS (ed) Diamondback moth and other crucifer pests: proceedings of the second international workshop, Tainan, Taiwan, 10–14 December 1990. Asian Vegetable Research and Development Center, pp 10–14Google Scholar
  94. Niu Y-Q, Sun Y-X, Liu T-X (2014) Development and reproductive potential of diamondback moth (Lepidoptera: Plutellidae) on selected wild crucifer species. Environ Entomol 43(1):69–74.  https://doi.org/10.1603/EN13206 CrossRefPubMedGoogle Scholar
  95. Östman Ö, Ives AR (2003) Scale-dependent indirect interactions between two prey species through a shared predator. Oikos 102(3):505–514.  https://doi.org/10.1034/j.1600-0706.2003.12422.x CrossRefGoogle Scholar
  96. Paredes D, Cayuela L, Gurr GM, Campos M (2015) Is ground cover vegetation an effective biological control enhancement strategy against olive pests? PLoS One 10(2):e0117265.  https://doi.org/10.1371/journal.pone.0117265 CrossRefPubMedPubMedCentralGoogle Scholar
  97. Parolin P, Bresch C, Poncet C, Desneux N (2012) Functional characteristics of secondary plants for increased pest management. Int J Pest Manag 58(4):369–377.  https://doi.org/10.1080/09670874.2012.734869 CrossRefGoogle Scholar
  98. Pell J, Eilenberg J, Hajek A, Steinkraus D (2001) Biology, ecology and pest management potential of Entomophthorales. In: Butt T, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential CABI International, Wallingford, pp 71–154Google Scholar
  99. Pell JK, Hannam JJ, Steinkraus DC (2010) Conservation biological control using fungal entomopathogens. BioControl 55(1):187–198.  https://doi.org/10.1007/s10526-009-9245-6 CrossRefGoogle Scholar
  100. Perović DJ, Gámez-Virués S, Landis DA, Wäckers F, Gurr GM, Wratten SD, You M-S, Desneux N (2018) Managing biological control services through multi-trophic trait interactions: review and guidelines for implementation at local and landscape scales. Biol Rev 93(1):306–321.  https://doi.org/10.1111/brv.12346 CrossRefPubMedGoogle Scholar
  101. Perović DJ, Gurr GM, Raman A, Nicol HI (2010) Effect of landscape composition and arrangement on biological control agents in a simplified agricultural system: a cost-distance approach. Biol Control 52(3):263–270.  https://doi.org/10.1016/j.biocontrol.2009.09.014 CrossRefGoogle Scholar
  102. Perring TM (2001) The Bemisia tabaci species complex. Crop Prot 20(9):725–737.  https://doi.org/10.1016/S0261-2194(01)00109-0 CrossRefGoogle Scholar
  103. Philips CR, Fu Z, Kuhar TP, Shelton AM, Cordero RJ (2014) Natural history, ecology, and management of diamondback moth (Lepidoptera: Plutellidae), with emphasis on the United States. J Integr Pest Manag 5(3):D1–D11.  https://doi.org/10.1603/IPM14012 CrossRefGoogle Scholar
  104. Poelman EH, Zheng S-J, Zhang Z, Heemskerk NM, Cortesero A-M, Dicke M (2011) Parasitoid-specific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores. Proce Nat Acad Sci USA 108(49):19647–19652.  https://doi.org/10.1073/pnas.1110748108 CrossRefGoogle Scholar
  105. Raps A, Vidal S (1998) Indirect effects of an unspecialized endophytic fungus on specialized plant—herbivorous insect interactions. Oecologia 114(4):541–547.  https://doi.org/10.1007/s004420050478 CrossRefPubMedGoogle Scholar
  106. Ratnasinghe G, Hague N (1998) The invasion, development and reproduction of Steinernema carpocapsae (Rhabditida: Steinernematidae) in the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Nematropica 28(1):1–6Google Scholar
  107. Roberts DW, Campbell AS (1977) Stability of entomopathogenic fungi. Misc Publ Entomol Soc Am 10:19–76Google Scholar
  108. Saqib HS, You M, Gurr GM (2017) Multivariate ordination identifies vegetation types associated with spider conservation in brassica crops. PeerJ Preprints 5:e3003v3001.  https://doi.org/10.7287/peerj.preprints.3003v1 CrossRefGoogle Scholar
  109. Sarfraz M, Keddie AB, Dosdall LM (2007) Biological control of the diamondback moth, Plutella xylostella: a review. Biocontrol Sci Tech 15(8):763–789.  https://doi.org/10.1080/09583150500136956 CrossRefGoogle Scholar
  110. Sarfraz M, Keddie BA (2005) Conserving the efficacy of insecticides against Plutella xylostella (L.) (Lep., Plutellidae). J Appl Entomol 129(3):149–157.  https://doi.org/10.1111/j.1439-0418.2005.00930.x CrossRefGoogle Scholar
  111. Schellhorn NA, Macfadyen S, Bianchi FJJA, Williams DG, Zalucki MP (2008) Managing ecosystem services in broadacre landscapes: what are the appropriate spatial scales? Aust J Exp Agric 48(12):1549–1559.  https://doi.org/10.1071/EA08112 CrossRefGoogle Scholar
  112. Schmidt MH, Roschewitz I, Thies C, Tscharntke T (2005) Differential effects of landscape and management on diversity and density of ground-dwelling farmland spiders. J Appl Ecol 42(2):281–287.  https://doi.org/10.1111/j.1365-2664.2005.01014.x CrossRefGoogle Scholar
  113. Schneider S, Widmer F, Jacot K, Kölliker R, Enkerli J (2012) Spatial distribution of Metarhizium clade 1 in agricultural landscapes with arable land and different semi-natural habitats. Appl Soil Ecol 52(Supplement C):20–28.  https://doi.org/10.1016/j.apsoil.2011.10.007 CrossRefGoogle Scholar
  114. Schroer S, Ehlers RU (2005) Foliar application of the entomopathogenic nematode Steinernema carpocapsae for biological control of diamondback moth larvae (Plutella xylostella). Biol Control 33(1):81–86.  https://doi.org/10.1016/j.biocontrol.2004.12.009 CrossRefGoogle Scholar
  115. Shah P, Pell J (2003) Entomopathogenic fungi as biological control agents. Appl Microbiol Biotechnol 61(5–6):413–423.  https://doi.org/10.1007/s00253-003-1240-8 CrossRefPubMedGoogle Scholar
  116. Shelton A (2004) Management of the diamondback moth: déjà vu all over again In: Endersby NM, Ridland P (eds) The management of diamondback moth and other crucifer pests: Proceedings of the 4th International Workshop, Melbourne, Australia, 26–29 November, 2001. The Regional Institute Ltd, pp 3–8Google Scholar
  117. Simpson M, Gurr GM, Simmons AT, Wratten SD, James DG, Leeson G, Nicol HI (2011a) Insect attraction to synthetic herbivore-induced plant volatile-treated field crops. Agric For Entomol 13(1):45–57.  https://doi.org/10.1111/j.1461-9563.2010.00496.x CrossRefGoogle Scholar
  118. Simpson M, Gurr GM, Simmons AT, Wratten SD, James DG, Leeson G, Nicol HI, Orre-Gordon GUS (2011b) Attract and reward: combining chemical ecology and habitat manipulation to enhance biological control in field crops. J Appl Ecol 48(3):580–590.  https://doi.org/10.1111/j.1365-2664.2010.01946.x CrossRefGoogle Scholar
  119. Stavely F, Pell J, Chapman B, Glare T, Yeo H, Suckling D, Walter M (2004) Insect pathogens for biological control of the diamondback moth with particular emphasis on the fungus Zoophthora radicans in New Zealand. In: Endersby N (ed) The management of diamondback moths and other crucifer pests: Proceedings of the Fourth International Workshop, Melbourne, Australia, 26-29 November, 2001 2004. Australian Entomological Society, pp 285–288Google Scholar
  120. Sun X, Peng H-Y (2007) Recent advances in biological control of pest insects by using viruses in China. Virol Sin 22(2):158–162.  https://doi.org/10.1007/s12250-007-0017-0 CrossRefGoogle Scholar
  121. Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47(1):561–594.  https://doi.org/10.1146/annurev.ento.47.091201.145240 CrossRefPubMedGoogle Scholar
  122. Tabashnik BE, Cushing NL, Johnson MW (1987) Diamondback moth (Lepidoptera: Plutellidae) resistance to insecticides in Hawaii: intra-island variation and cross-resistance. J Econ Entomol 80(6):1091–1099.  https://doi.org/10.1093/jee/80.6.1091 CrossRefGoogle Scholar
  123. Tack AJM, Gripenberg S, Roslin T (2011) Can we predict indirect interactions from quantitative food webs?—an experimental approach. J Anim Ecol 80(1):108–118.  https://doi.org/10.1111/j.1365-2656.2010.01744.x CrossRefPubMedGoogle Scholar
  124. Talekar N, Shelton A (1993) Biology, ecology, and management of the diamondback moth. Annu Rev Entomol 38(1):275–301.  https://doi.org/10.1146/annurev.en.38.010193.001423 CrossRefGoogle Scholar
  125. Tkaczuk C, Król A, Majchrowska-Safaryan A, Nicewicz Ł (2014) The occurrence of entomopathogenic fungi in soils from fields cultivated in a conventional and organic system. J Ecol Eng 15(4):137–144.  https://doi.org/10.12911/22998993.1125468 CrossRefGoogle Scholar
  126. Tkaczuk C, Krzyczkowski T, Wegensteiner R (2012) The occurrence of entomopathogenic fungi in soils from mid-field woodlots and adjacent small-scale arable fields. Acta Mycol 47(2):191–202CrossRefGoogle Scholar
  127. Tscharntke T, Brandl R (2004) Plant-insect interactions in fragmented landscapes. Ann Rev Entomol 49(1):405–430.  https://doi.org/10.1146/annurev.ento.49.061802.123339 CrossRefGoogle Scholar
  128. Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batary P, Bengtsson J, Clough Y, Crist TO, Dormann CF, Ewers RM, Frund J, Holt RD, Holzschuh A, Klein AM, Kleijn D, Kremen C, Landis DA, Laurance W, Lindenmayer D, Scherber C, Sodhi N, Steffan-Dewenter I, Thies C, van der Putten WH, Westphal C (2012) Landscape moderation of biodiversity patterns and processes—eight hypotheses. Biol Rev 87(3):661–685.  https://doi.org/10.1111/j.1469-185X.2011.00216.x CrossRefPubMedGoogle Scholar
  129. Vandenberg J, Griggs M, Wraight S, Shelton A (1999) Season-long management of lepidopteran pests of fresh-market cabbage using microbial control agents. Paper presented at the XXXIIth Annual Meeting of the Society for Invertebrate Pathology, Irvine, California, 22–27 August 1999Google Scholar
  130. Vandenberg JD, Shelton AM, Wilsey WT, Ramos M (1998) Assessment of Beauveria bassiana sprays for control of diamondback moth (Lepidoptera: Plutellidae) on crucifers. J Econ Entomol 91(3):624–630.  https://doi.org/10.1093/jee/91.3.624 CrossRefGoogle Scholar
  131. Verkerk RHJ, Wright DJ (1996) Multitrophic interactions and management of the diamondback moth: a review. Bull Entomol Res 86(3):205–216.  https://doi.org/10.1017/S0007485300052482 CrossRefGoogle Scholar
  132. Verkerk RHJ, Wright DJ (1997) Field-based studies with the diamondback moth tritrophic system in Cameron Highlands of Malaysia: implications for pest management. Int J Pest Manag 43(1):27–33.  https://doi.org/10.1080/096708797228942 CrossRefGoogle Scholar
  133. Vickers RA, Furlong MJ, White A, Pell JK (2004) Initiation of fungal epizootics in diamondback moth populations within a large field cage: proof of concept for auto-dissemination. Entomologia Experimentalis et Applicata 111(1):7–17.  https://doi.org/10.1111/j.0013-8703.2004.00140.x CrossRefGoogle Scholar
  134. Wäckers FL, Lee JC, Heimpel GE, Winkler K, Wagenaar R (2006) Hymenopteran parasitoids synthesize ‘honeydew-specific’ oligosaccharides. Funct Ecol 20(5):790–798.  https://doi.org/10.1111/j.1365-2435.2006.01158.x CrossRefGoogle Scholar
  135. Wade MR, Zalucki MP, Wratten SD, Robinson KA (2008) Conservation biological control of arthropods using artificial food sprays: current status and future challenges. Biol Control 45(2):185–199.  https://doi.org/10.1016/j.biocontrol.2007.10.024 CrossRefGoogle Scholar
  136. Wang F, Deng J, Schal C, Lou Y, Zhou G, Ye B, Yin X, Xu Z, Shen L (2016) Non-host plant volatiles disrupt sex pheromone communication in a specialist herbivore. Sci Rep 6:32666.  https://doi.org/10.1038/srep32666 CrossRefPubMedPubMedCentralGoogle Scholar
  137. Wei S-J, Shi B-C, Gong Y-J, Jin G-H, Chen X-X, Meng X-F (2013) Genetic structure and demographic history reveal migration of the diamondback moth Plutella xylostella (Lepidoptera: Plutellidae) from the southern to northern regions of China. PLoS One 8(4):e59654.  https://doi.org/10.1371/journal.pone.0059654 CrossRefPubMedPubMedCentralGoogle Scholar
  138. 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 CrossRefGoogle Scholar
  139. Wielgoss A, Clough Y, Fiala B, Rumede A, Tscharntke T (2012) A minor pest reduces yield losses by a major pest: plant-mediated herbivore interactions in Indonesian cacao. J Appl Ecol 49(2):465–473.  https://doi.org/10.1111/j.1365-2664.2012.02122.x CrossRefGoogle Scholar
  140. Wilding N (1986) The pathogens of diamondback moth and their potential for its control-a review. In: Talekar NS, Griggs TD (eds) Diamondback moth management: Proceedings of the First International Workshop, Tainan, Taiwan, 11–15 March 1985. The Asian Vegetable Research and Development Center, pp 219–232Google Scholar
  141. Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annu Rev Ecol Syst 25(1):443–466.  https://doi.org/10.1146/annurev.es.25.110194.002303 CrossRefGoogle Scholar
  142. Wright D, Peters A, Schroder S, Fife J (2005) Application technology. In: Grewal P, Ehlers R, Shapiro-Ilan D (eds) Nematodes as biocontrol agents. CAB International, Wallingford, UK, pp 91–106CrossRefGoogle Scholar
  143. Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Nat Acad Sci USA 96(4):1463–1468.  https://doi.org/10.1073/pnas.96.4.1463 CrossRefPubMedGoogle Scholar
  144. Yang MM, Li ML, an Zhang Y, Wang YZ, Qu LJ, Wang QH, Ding JY (2012) Baculoviruses and insect pests control in China. Afr J Agric Res 6(2):214–218.  https://doi.org/10.5897/AJMR11.1357 CrossRefGoogle Scholar
  145. Yeo H, Pell J, Walter M, Boyd-Wilson K, Snelling C, Suckling D (2001) Susceptibility of diamondback moth (Plutella xylostella (L.)) larvae to the entomopathogenic fungus, Zoophthora radicans (Brefeld) Batko. New Zealand. Plant Prot 54:47–50Google Scholar
  146. Zalucki M, Furlong M (2011) Predicting outbreaks of a migratory pest: an analysis of DBM distribution and abundance revisited. In: Srinivasan R, Shelton AM, Collins HL (eds) Proceedings of the 6th International Workshop on Management of the Diamondback Moth and Other Crucifer Insect Pests. Nakhon Pathom, Thailand, pp 8–14Google Scholar
  147. Zalucki MP, Adamson D, Furlong MJ (2009) The future of IPM: whither or wither? Aust J Entomol 48(2):85–96.  https://doi.org/10.1111/j.1440-6055.2009.00690.x CrossRefGoogle Scholar
  148. Zalucki MP, Shabbir A, Silva R, Adamson D, Shu-Sheng L, Furlong MJ (2012) Estimating the economic cost of one of the world's major insect pests, Plutella xylostella (Lepidoptera: Plutellidae): just how long is a piece of string? J Econ Entomol 105(4):1115–1129.  https://doi.org/10.1603/EC12107 CrossRefPubMedGoogle Scholar
  149. Zhang L (2014) Colonization pattern of crop plants by endophytic fungi. PhD, Georg-August-University Göttingen, GermanyGoogle Scholar
  150. Zhang P-J, Broekgaarden C, Zheng S-J, Snoeren TAL, van Loon JJA, Gols R, Dicke M (2013) Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana. New Phytol 197(4):1291–1299.  https://doi.org/10.1111/nph.12106 CrossRefPubMedGoogle Scholar
  151. Zhao JZ, Collins HL, Li YX, Mau RFL, Thompson GD, Hertlein M, Andaloro JT, Boykin R, Shelton AM (2006) Monitoring of diamondback moth (Lepidoptera: Plutellidae) resistance to spinosad, indoxacarb, and emamectin benzoate. J Econ Entomol 99(1):176–181. https://doi.org/10.1603/0022-0493(2006)099[0176:MODMLP]2.0.CO;2CrossRefPubMedGoogle Scholar

Copyright information

© The Author(s) 2018
corrected publication September 2018

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, duplication, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license and indicate if changes were made.

Authors and Affiliations

  • Geoff M. Gurr
    • 1
    • 2
    • 3
    • 4
  • Olivia L. Reynolds
    • 2
    • 4
    • 5
  • Anne C. Johnson
    • 4
  • Nicolas Desneux
    • 6
  • Myron P. Zalucki
    • 7
  • Michael J. Furlong
    • 7
  • Zhenyu Li
    • 8
  • Komivi S. Akutse
    • 1
    • 2
    • 3
    • 10
  • Junhui Chen
    • 1
    • 2
    • 3
  • Xiwu Gao
    • 9
  • Minsheng You
    • 1
    • 2
    • 3
  1. 1.State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Institute of Applied EcologyFujian Agriculture and Forestry UniversityFuzhouChina
  2. 2.Joint International Research Laboratory of Ecological Pest Control, Ministry of EducationFuzhouChina
  3. 3.Fujian-Taiwan Joint Innovation Centre for Ecological Control of Crop PestsFujian Agriculture and Forestry UniversityFuzhouChina
  4. 4.Graham Centre (an alliance between NSW Department of Primary Industries and Charles Sturt University)Wagga WaggaAustralia
  5. 5.NSW Department of Primary IndustriesElizabeth Macarthur Agricultural InstituteMenangleAustralia
  6. 6.INRA (French National Institute for Agricultural Research), CNRS, UMR 1355-7254 Institute Sophia AgrobiotechUniversité Côte d’AzurSophia-AntipolisFrance
  7. 7.School of Biological SciencesThe University of QueenslandSt LuciaAustralia
  8. 8.Institute of Plant Protection, Guangdong Academy of Agricultural Sciences and Guangdong Provincial Key Laboratory of High Technology for Plant ProtectionGuangzhouChina
  9. 9.Department of EntomologyChina Agricultural UniversityBeijingChina
  10. 10.International Centre of Insect Physiology and EcologyNairobiKenya

Personalised recommendations