Reduced soil tillage and insecticide use in pollen beetle management on oilseed rape in Finland

The pollen beetle, Meligethes aeneus (Fabricius) (syn. Brassicogethes aeneus (Fabricius)) is a major pest in the production of oilseed rape, Brassica napus L., in Europe. At high levels of crop infestation, adult beetles can cause severe economic damage by destroying the buds. Chemical control of this pest is biased due to the widely distributed pyrethroid resistance and a decreasing availability of insecticides with different modes of action. Effective insecticides are required not only to avoid yield losses by overwintered pollen beetles but also to minimize the reproduction rate of the beetle, thereby reducing the infestation pressure and the frequency of insecticide treatments in following years. The objectives of the present study were to determine the effects of the systemic neonicotinoid Biscaya (a.i. thiacloprid, 72 g ha -1 ) and the two contact pyrethroids Mavrik (tau-fluvalinate, 48 g ha -1 ) and Karate Zeon (lambda-cyhalothrin, 7.5 g ha -1 ) on population development of pollen beetle. In the years 2013-2015, field trials were established on crops of oilseed rape in the region of Braunschweig (northern Germany) and further locations in Germany. Recommended dose rates of the insecticides were applied at the bud stage, at the beginning of flowering or at full flowering of the crop. The effect of insecticide applications on overwintered pollen beetles was assessed by counting pollen beetles on plants before and up to two weeks after application. Furthermore, the impact of insecticide application at the bud stage on infestation of buds with eggs and larvae was investigated in field trials as well as in greenhouse experiments using plants and pollen beetles collected from untreated and Biscaya- or Mavrik-treated field plots. The effects of insecticides on larval instars and emergence of new generations of pollen beetles were studied in field trials. In addition, the impact of the insecticide treatments on parasitism rates of pollen beetle larvae by Tersilochus heterocerus and Phradis spp. was analysed by collecting samples of larvae from different field trials distributed over Germany. Application of Biscaya and Mavrik during the bud stage significantly reduced the abundance of the overwintered pollen beetles up to seven days after application. In contrast, application of Karate Zeon did not affect beetle numbers on plants. Consequently, the number of buds infested with eggs and larvae was reduced at least for 14 days after application of Biscaya and Mavrik compared to Karate Zeon-treated and untreated plots. Biscaya had a stronger effect on infestation of buds with eggs and larvae than Mavrik. Results of greenhouse experiments indicated that the lower number of infested buds found in Mavrik-treated plots resulted from a reduced number of overwintered pollen beetles, whereas in Biscaya-treated plots in addition to effects on overwintered pollen beetles a further reduction of bud infestation occurred. In all three experimental years the application of Biscaya at the beginning of flowering or full flowering resulted in significantly higher numbers of premature L1-larvae dropping down from the plants to the ground. This effect was only observed in Biscaya-treated plots, with up to 425% more L1-larvae dropping within one week compared to the control. Numbers of mature L2-larvae dropping down for pupation was reduced in plots treated with Mavrik and especially Biscaya. In Karate Zeon-treated plots the number of dropping L2-larvae was even higher than in control plots. In accordance with lower numbers of L2-larvae in Biscaya- and Mavrik-treated plots the number of emerging new generation beetles was reduced. No significant effect of insecticide application on parasitism rates of pollen beetle larvae by T. heterocerus and Phradis spp. was found. The parasitoid T. heterocerus was predominant with parasitized pollen beetle larvae occurring in all field trials and all experimental years, usually not earlier than in BBCH 65. In contrast Phradis spp. larvae were not detected in all field trials in 2015 and not before BBCH 67. Altogether, the results demonstrate that applications of Biscaya and Mavrik cause reductions of pollen beetle population growth. Especially the neonicotinoid Biscaya could form an important part of a resistance management program for controlling populations of pyrethroid resistant pollen beetles. Applications during the bud stage did not only reduce the overwintered pollen beetles, but in addition had sublethal effects on infestation of buds with eggs and larvae. Particularly Biscaya targeted for control of cabbage seedpod weevil or brassica pod midge during flowering has shown long-lasting effects on pollen beetle populations without affecting parasitization of pollen beetle larvae.

There is an urgent need to develop sustainable and environmentally benign integrated pest management (IPM) strategies for arable crops. The enhancement and manipulation of naturally occurring populations of the natural enemies of crop pests through habitat management for ‘conservation biological control’, as well as habitat management to manipulate populations of the pests themselves, have the potential to become major components of successful IPM strategies. We review the studies that have contributed to our current understanding of how the crop margin, local landscape, and regional landscape can influence pollen beetle Brassicogethes aeneus (syn. Meligethes aeneus) (Coleoptera: Nitidulidae) abundance and damage to oilseed rape crops (Brassica napus), and the efficacy of their natural enemies. We also discuss how habitat management across these multiple scales may improve pollen beetle control, reducing the need for insecticide use and contributing towards sustainable production of this important crop which is grown on increasing areas for both food and fuel.

An increase in the spread of pyrethroid resistance in the pollen beetle has been documented in many European countries. Pyrethroid resistance in the pollen beetle in the Czech Republic has been detected using a topical application bioassay. Resistance monitoring has been carried out during the implementation of insect resistance management. The susceptibilities of nine pollen beetle populations to four pyrethroids in 2009 - 2015 in the Czech Republic are presented in this paper. The highest resistance ratio (RR) values [based on the lethal dose for 50% of the population (LD50 )] obtained for deltamethrin, lambda-cyhalothrin, tau-fluvalinate and etofenprox were 500, 299, 108 and 66.9, respectively. Pollen beetle mortality after application of deltamethrin or lambda-cyhalothrin gradually decreased from 2009 to 2013. High cross-resistance between lambda-cyhalothrin and deltamethrin and low cross-resistance between lambda-cyhalothrin and etofenprox were demonstrated. A kdr mutation known to cause resistance in the pollen beetle was not detected. A high level of resistance was recorded in most of the nine populations of the pollen beetle in 2013. In the following 2 years, a decrease in resistance associated with a population density decrease of the pollen beetle was observed in all nine populations as a result of insect resistance management based on pyrethroid reduction in winter oilseed rape. © 2017 Society of Chemical Industry.

Previous work has characterised pyrethroid resistance in pollen beetle (Meligethes aeneus F.) as principally an oxidative mechanism. Piperonyl butoxide (PBO) can synergise this resistance in the field, but its effects on the honey bee are thought to be unacceptable. A field trial in Poland was conducted to show that a mixture of PBO and tau-fluvalinate at the registered rate gave increased and longer-lasting control of resistant pollen beetle. Four days after spraying with tau-fluvalinate, only 20% of pollen beetles were controlled, compared with 70% if the tau-fluvalinate/PBO mixture was used. No detriment to honey bee health was observed using the same mixture. PBO, if used in conjunction with a pyrethroid of relatively low bee toxicity, can successfully overcome pyrethroid resistance in pollen beetle without incurring an increased loss of honey bees, even if they are present at the time of spraying.

Molecular and functional characterization of CYP6BQ23, a cytochrome P450 conferring resistance to pyrethroids in European populations of pollen beetle, Meligethes aeneus

Pollen beetle, Meligethes aeneus F. (Coleoptera: Nitidulidae), is a major pest in European winter oilseed rape. Recently, control failures with pyrethroid insecticides commonly used to control this pest have been reported in many European countries. For resistance management purposes, the neonicotinoid insecticide thiacloprid was widely introduced as a new mode of action for pollen beetle control. A number of pollen beetle populations collected in Germany, France, Austria, Great Britain, Sweden, Denmark, Finland, Poland, Czech Republic and Ukraine were tested for pyrethroid resistance using lambda-cyhalothrin-coated glass vials (adult vial test). Most of the populations tested exhibited substantial levels of resistance to lambda-cyhalothrin, and resistance ratios ranged from < 10 to > 2000. A similar resistance monitoring bioassay for the neonicotinoid insecticide thiacloprid was developed and validated by assessing baseline susceptibility data for 88 European pollen beetle populations. A variation of less than fivefold in response to thiacloprid was detected. The thiacloprid adult vial bioassay is based on glass vials coated with an oil-dispersion-based formulation of thiacloprid, resulting in a much better bioavailability compared with technical material. Analytical measurements revealed a > 56 and 28 day stability of thiacloprid and lambda-cyhalothrin in coated glass vials at room temperature, respectively. No cross-resistance between thiacloprid and lambda-cyhalothrin based on log-dose probit-mortality data was detected. Pyrethroid resistance in many European populations of M. aeneus was confirmed, whereas all populations are susceptible to thiacloprid when tested in a newly designed and validated monitoring bioassay based on glass vials coated with oil-dispersion-formulated thiacloprid. Based on the homogeneous results, it is concluded that thiacloprid could be an important chemical tool for pollen beetle resistance management strategies in European winter oilseed rape.

Pollen beetle (Meligethes aeneus F.) has become the most important pest of oilseed rape in Europe, but its control has been greatly hindered by pyrethroid resistance. Target-site resistance has been implicated previously, and, whilst synergism has been found with piperonyl butoxide (PBO), the exact nature of metabolic resistance has remained unknown. The use of PBO, in conjunction with its analogue EN 16/5-1, has allowed the characterisation of metabolic resistance. In vitro assays in combination with in vivo studies using PBO and EN 16/5-1 showed that high synergism of pyrethroids was primarily correlated with an oxidative mechanism, although a limited contribution by esterases was implicated in one population. Differential synergism has enabled the characterisation of pyrethroid resistance in populations of M. aeneus. It was found to be principally due to an oxidative-based mechanism, and, if a synergist were to be used to inhibit this enzyme group, renewed control against resistant pests could be achieved.

Cytochrome P450 mediated pyrethroid resistance in European populations of Meligethes aeneus (Coleoptera: Nitidulidae)

To prevent damage by pollen beetles (Brassicogethes aeneus (Fabricius), syn. Meligethes aeneus (Fabricius)), frequent insecticide applications are often necessary. It would be an advantage if treatments for pollen beetle control would not only avoid yield losses by bud damage by overwintered pollen beetles, but also minimize pest reproduction, and also have side effects on the population development of other pests present in the crop. The effects of the neonicotinoid Biscaya (a.i. thiacloprid) and the pyrethroids Mavrik (tau-fluvalinate) and Karate Zeon (lambda-cyhalothrin) applied at different growth stages of winter oilseed rape on the abundance of overwintered pollen beetles were determined in field trials in Germany (2013–2015). In addition, effects on the two larval instars and new generation of adult pollen beetle were studied. Biscaya and Mavrik significantly reduced the number of overwintered pollen beetles up to seven days after application, whereas Karate Zeon had no effect. Application of Biscaya at the beginning of flowering resulted in a high mortality of L1-larvae in all years. The number of premature L1-larvae dropping down from the plants during the first week after application increased up to 425% compared to the control. The number of L2-larvae dropping down to the ground for pupation was significantly reduced by insecticide applications at different growth stages except for Karate Zeon. In Karate Zeon-treated plots, the number of L2-larvae dropping to the ground increased up to 42% compared to the control. In accordance with the reduced number of L2-larvae in Biscaya- and Mavrik-treated plots, fewer new-generation pollen beetles emerged in the field trials near Braunschweig, efficacy varying between 57 and 76% in Biscaya-treated plots and 32 and 57% in Mavrik-treated plots in 2014 and 2015, respectively. The results indicate that Mavrik, and especially Biscaya, are effective in controlling pollen beetles, reducing infestation pressure and thereby insecticide treatment frequency in following years.

Oilseed rape (Brassica napus) is a valuable crop, attacked by several insect pests, of which the pollen beetle (Meligethes aeneus) is one of the most widespread and important in Europe. The relative attractiveness for the pollen beetle of Brassica nigra, Eruca sativa and Raphanus sativus was compared with that of spring oilseed rape, to assess the potential of these plant species as trap crops for the pest. At early growth stages, B. nigra and R. sativus were more attractive to over-wintered adult pollen beetles than B. napus. At the bud and flowering stages, B. nigra was the most attractive while E. sativa was the least attractive. At flowering, B. nigra was more attractive for oviposition than the other species. Thus, of the species tested, B. nigra has the most potential as a prospective trap crop to protect spring oilseed rape before flowering when it is at its most vulnerable developmental phase, due to its faster development and its acceptability both for feeding and oviposition to overwintered pollen beetle adults. Raphanus sativus was accepted both for feeding and oviposition, but pollen beetle larvae failed to develop in its flowers; it therefore has the potential for use as a dead-end crop. At the end of the growing season, both E. sativa and R. sativus, as late-flowering species, attracted the new generation of pollen beetles and thereby have potential to extend the effectiveness of a trap-cropping system at this time.

Plant size is hypothesised to be a major driver of biotic interactions, as larger plants are more conspicuous and offer a wider range of resources and niches for associated animals. However, the role of interspecific differences in plant size for associated animals (antagonists or mutualists) and the resulting plant reproductive fitness is little explored. In this thesis effects of plant size on species richness of herbivores and their natural enemies as well as on species richness of pollinators were tested. Endophytic and ectophytic herbivores and their natural enemies were considered separately as were herbivores and their natural enemies associated with different plant components. Further, the effect of plant size was studied for feeding damage to different plant components and the associated impact on plant reproductive fitness parameters, namely seed number, thousand seed weight and total seed weight per plant individual. Finally, the focus was placed on the effect of plant size on antagonistic and mutualistic flower associated insects and their impact on plant reproductive fitness along the plant size gradient. A common garden experiment with an interspecific plant size gradient (from 10 to 130 cm length) among 21 annual Brassicaceae species was established. In this way, we realised a broad gradient in plant size across different plant species with standardisation of the habitat and the surrounding landscape features, overcoming a common problem flaw in the analysis of within-species variation and naturally grown plants. Plant size, number, biomass and the size of the different aboveground plant components (flowers, fruits, leaves and stems) were quantified along with flower cover and colour. Relative feeding damage to the different plant components and the resulting reproductive fitness of each plant species were assessed. Finally arthropods on and in flowers, fruits, leaves and stems were sampled, including herbivores, their natural enemies and pollinators. Plant size was positively related to the species richness of herbivores, of their natural enemies and to the species richness of pollinators. This was likewise true for endophagous and ectophagous herbivores and their natural enemies as well as for fruit and leaf associated herbivores and their natural enemies. Furthermore, data showed increasing feeding damage to flowers and fruits with increasing plant size, while feeding damage to leaves and stems was driven by their biomass rather than by plant size. Feeding damage to flowers had the strongest effect on reproductive fitness, decreasing seed number, thousand seed weight and total seed weight. Focusing on flower associated insects, plant size had a positive effect on abundance and species richness of pollinators (but only when flowers were not superabundant) and also on pollen beetle abundance, despite the associated higher rates of parasitism of pollen beetles. Pollen beetles reduced seed number and thousand seed weight. Pollinators positively affected seed number only. Overall, increasing plant size led to decreasing thousand seed weight but did not significantly alter seed number and total seed weight, indicating a balance between increasing pollen beetle damage and positive effects of increasing pollinator visits. In conclusion, increased detectability and attractiveness to herbivores leads to important fitness costs for large plants, including flower damage by pollen beetles, which had the strongest negative impact on plant reproductive fitness in terms of seed number, thousand seed weight and total seed weight. These fitness costs for large plants may be counteracted by their detectability and attractiveness to pollinators, which positively influenced seed number. Purely in terms of seed numbers, being large is advantageous in places dominated by pollinators, while being small is advantageous in places dominated by herbivorous flower visitors. Contrarily, plants suffer from being large with regard to their thousand seed weight, which was driven by herbivores only. In general, plant size is a hitherto underestimated driver of interactions, and its effects on plant fitness through interacting insects are highly complex.

Pollen beetles, Meligethes aeneus (Fabricius) (Coleoptera: Nitidulidae), are major pests in oilseed rape (OSR), Brassica napus L. (Brassicaceae). Among the predator species in the generalist predator complex present in OSR fields, wolf spiders (Araneae: Lycosidae) are found on the ground and cobweb spiders (Araneae: Theridiidae) build webs in the foliage. Here we study the incidence of predation of pollen beetles by these two spider groups using DNA-based molecular analysis. Wolf spiders of the genus Pardosa and the cobweb spider, Theridion impressum L. Koch, were each collected in three winter OSR fields over a period of about 3 weeks. Pollen beetle densities as well as the occurrence of predators and alternative prey were monitored. In total, 13.8% of the collected Pardosa spp. tested positive for pollen beetle DNA in the PCR analyses, whereas 51.7%T. impressum were positive. The likelihood of detecting pollen beetle DNA in the gut contents of both spider groups was positively related to pollen beetle larval density. The implications of these results for conservation biological control and future studies of food webs in OSR are discussed.

At a time of increasing demand for rapeseed oil for biofuel and food use and as increasing areas are grown, the risk of pollen beetle resistance to pyrethroids presents a significant threat to the sustainability of the oilseed rape crop and to farm incomes. Measures are urgently required to reduce the use of insecticides against pollen beetles, to preserve activity of the limited armoury of insecticides and minimise environmental pollution. In this paper, the status of pollen beetle resistance to pyrethroid insecticides and current control methods are presented from a UK perspective. Three ecological approaches to the control of pollen beetles that are based on research into their behaviour and ecology and that of their natural enemies are highlighted: use of monitoring, trap cropping and conservation biological control. These approaches have the potential to significantly reduce insecticide use against pollen beetles by helping to identify when spray thresholds have been breached, reducing pest incidence in the crop and increasing populations of natural enemies, respectively.

One of the main insect pests in oilseed rape is the pollen beetle (Brassicogethes aeneus (Fabricius), syn. Meligethes aeneus). To maximize efficiency of control of this pest, insecticides are required that ideally, not just prevent yield losses by bud feeding of overwintered pollen beetles, but simultaneously minimize the reproduction of the pest, thereby reducing the size of the following generation infesting next year’s oilseed rape. The neonicotinoid active substance thiacloprid is known to reduce bud infestation with eggs and larvae. However, the mechanisms by which this occurs as well as the effects of other active substances are not known. In this study, the effects of the neonicotinoid insecticide Biscaya (a.i. thiacloprid) and the pyrethroids Mavrik (tau-fluvalinate) and Karate Zeon (lambda-cyhalothrin) applied at the bud stage of winter oilseed rape with recommended field rates on infestation of buds with eggs and larvae of pollen beetles were tested in field trials in Germany in 2013–2015. In additional greenhouse experiments, it was investigated whether effects on bud infestation were caused by lethal effects on pollen beetle or by insecticidal residues on plants causing sublethal effects. In the field trials, application of Biscaya and Mavrik significantly reduced the percentage of buds containing eggs and larvae in contrast to Karate Zeon. In 2014 and 2015, 14 days after application, bud infestation on the main raceme was reduced by 86 and 82%, respectively, in Biscaya-treated plots and by 51 and 71%, respectively, in Mavrik-treated plots compared to the untreated plots. In the greenhouse experiments, the lowest percentage of bud infestation with eggs and larvae was recorded on Biscaya-treated plants whereas on Mavrik-treated plants, there was no significant difference compared with the control. The results of the field trials show that Biscaya and Mavrik reduced oilseed rape bud infestation with eggs and larvae of pollen beetles primarily by lethal effects on overwintered pollen beetles or by repellency. However, Biscaya had additional effects on egg laying, which was supported by the greenhouse experiments.

BACKGROUNDThe pollen beetle (Brassicogethes aeneus) is the most abundant pest of oilseed rape in spring and is potentially one of the most damaging. Adults feed on the pollen within closed flower buds and the damage leads to bud abscission, resulting in podless stalks and yield reduction. Several methods are currently used to monitor the pressure of this insect, such as counting the numbers of adults on the plants, quantifying the number of buds damaged by the insect before flowering or counting the number of podless stalks before harvest. We conducted experiments to evaluate the robustness of these sampling methods and compared their results. We also describe how pollen beetles damage the plants to understand the limitations of methods based on damage estimation.RESULTSMethods based on adult abundance lack robustness. We observed that most of the damage to buds is caused by pollen beetles feeding on small buds (< 3 mm), and that this damage can be quantified later in the season, indicating that methods based on the count of podless stalks are robust. Different methods gave consistent results and quantification of the pressure on the primary raceme can be a good proxy for pressure on the whole plant.CONCLUSIONSStandardised methods for assessment of pollen beetle pressure will enable comparison of pest management strategies between different studies and facilitate the development of alternative control strategies for this pest.© 2021 Rothamsted Research. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.