Meligethes aeneus oviposition preferences, larval parasitism rate and species composition of parasitoids on Brassica nigra, Raphanus sativus and Eruca sativa compared with on Brassica napus
Graphical abstract
Introduction
One of the most important principles of integrated pest management (IPM) is the prevention and/or suppression of harmful organisms, encouraging the use of non-chemical methods and target-specificity to control pest abundance (BiPRO, 2009). One of the tools that addresses these principles is the use of a trap crop strategy for the pests and their naturally-occurring biocontrol agents i.e. the natural enemies of pests, including parasitoids.
As phytophagous insects locate the crop by responding behaviorally to different visual and olfactory cues, manipulation of these cues and hence of pest behavior can be used to reduce or avoid pest damage to the crop. Trap cropping aims to reduce pest colonization in the main crop by attracting pests to areas of trap crop planted close to the main crop (Hokkanen, 1991, Cook et al., 2007a, Cook et al., 2007b, Cook et al., 2013). If the plant species used as a trap crop is also attractive to parasitoids and the percentage of parasitism is high enough to control the population size of their host insect, there is no need to destroy the trap crop or to treat it with insecticides. Under these circumstances, the trap crop can also perform as a parasitoid bank and support the increase of diversity and abundance of beneficial arthropods.
Oilseed rape (Brassica napus spp. oleifera L.) (Brassicaceae) is the third most widely grown crop in the European Union (FAO, 2013). In Estonia, the area grown has increased 82-fold over the past 20 years reaching 86 700 hectares in 2012 (Statistics Estonia, 2013). This increase has supported the population growth of crucifer-specialist pests. One of the most damaging pest throughout Europe is the pollen beetle (Meligethes aeneus (Fabricius) (Coleoptera: Nitidulidae)) (Alford et al., 2003, Cook and Denholm, 2008, Ekbom, 2010, Veromann et al., 2006a, Veromann et al., 2006c, Veromann et al., 2006b, Veromann et al., 2008, Williams, 2010). Adult pollen beetles feed on pollen from plants belonging to different families (Free and Williams, 1978, Fritzsche, 1957, Williams, 2010), but oviposit only in buds of brassicaceous plants (Ekbom and Borg, 1996, Free and Williams, 1978, Nilsson, 1989) although they have behavioral preferences for some Brassica species over others (Buechi, 1990, Ekbom and Borg, 1996).
Generally, the abundance of pollen beetles is controlled by applying synthetic insecticides (Thieme et al., 2010), which may not solve the pest problem (Hokkanen, 2000) and can even increase it (Veromann et al., 2008). Another problem is the development of pyrethroid resistance in pollen beetles (Hansen, 2003, Hansen, 2008, Heimbach et al., 2006, Cook and Denholm, 2008, Thieme et al., 2010, Tiilikainen and Hokkanen, 2008). Further, pesticides have a detrimental effect on parasitoids that are essential enemies of many crop pests and may act as keystone species in ecosystems (Murchie et al., 1997, Thies et al., 2003, Veromann et al., 2011).
In Europe, the key species of parasitoids controlling the abundance of pollen beetle are Phradis interstitialis Thomson, Phradis morionellus Holmgren, Tersilochus heterocerus Thomson (Hymenoptera: Ichneumonidae) and Diospilus capito Nees (Hymenoptera: Braconidae) (Nilsson, 2003). Of these, adults of T. heterocerus and P. morionellus commonly colonize the crop at the same time – at the beginning of flowering of either spring or winter oilseed rape varieties (Ulber and Nitzsche, 2006, Ulber et al., 2010, Williams, 2006) while D. capito is a multivoltine species which gains more importance when spring varieties start to flower (Miczulski, 1967, Nilsson, 2003). Tersilochus heterocerus, P. morionellus and D. capito oviposit into small larvae within buds and large second instar larvae in open flowers (Börner and Blunck, 1920, Nilsson, 2003, Osborne, 1960). Diospilus capito is mainly distributed in northern Europe and more common on spring oilseed rape (Hokkanen, 2008, Nilsson, 2003, Veromann et al., 2006a, Veromann et al., 2006b).
The average parasitism percentage of pollen beetle larvae varies between 25% and 50% in Europe (Ulber et al., 2010), but can reach 90% (Ulber et al., 2006). The abundance of this pest can be effectively lowered with a parasitism rate of 30–40% (Hokkanen, 2008). In Estonia, a parasitism rate of 48% has been reported (Veromann et al., 2013), although in conventional cropping systems it is more usually under 4% (Veromann et al., 2009).
The potential of trap cropping to reduce insecticide treatments and to avoid damage caused by pollen beetles in oilseed rape has been intensively studied (Buechi, 1990, Cook et al., 2006, Cook and Denholm, 2008, Ekbom and Borg, 1996, Veromann et al., 2012) as has the potential of parasitoids to control the pest (Ekbom, 2010, Ferguson et al., 2003, Hokkanen, 1989, Hokkanen, 1991, Hokkanen, 2006, Jönsson et al., 2004, Kromp and Kraus, 2006, Nilsson, 2003, Nilsson and Ahman, 2006, Nilsson and Andreasson, 1987, Nitzsche and Ulber, 1998, Osborne, 1960, Ulber et al., 2010). However, potential trap crops other than B. rapa have received only minor attention so far (Hokkanen et al., 1986, Kovács et al., 2013, Veromann et al., 2012) and the potential of parasitoids has only been investigated separately on plant species other than B. napus (Billqvist and Ekbom, 2001a, Billqvist and Ekbom, 2001b). The effects of potential trap crops on the efficiency and species composition of parasitoids remain unexplored.
In this study, we hypothesized that cruciferous plants differ in their attractiveness for oviposition to pollen beetle adults and their larval parasitoids. To test this hypothesis, we compared the oviposition preferences of the pollen beetle and its parasitoids for the potential cruciferous host plants Brassica nigra (L.) W. D. J. Koch (syn. Sinapis nigra L.), Raphanus sativus L. var. oleiformis Pers. and Eruca sativa Mill. (syn. Eruca vesicaria (L.) Cav.) with that for spring oilseed rape.
Section snippets
Study area and experimental design
Studies were carried out in an experimental field of the Estonian University of Life Sciences, Tartu, between summers 2009 and 2011. The experiment was laid out in a randomized complete block design with three replicates of each plant species: B. napus, R. sativus, B. nigra and E. sativa. Each plot was 1 × 5 m with 1 m wide bare soil buffer zone around each plot. Neither fertilizers nor pesticides were applied.
Plant material
Plots were sown on 7 May 2009, 12 May 2010 and 9 May 2011 at 250 seeds per m2. In 2009,
Results
Plant species had a significant influence on the abundance of pollen beetle larvae over the three-year study period (F = 14.07, df = 3, P < 0.0001) but year as a factor had no influence (F = 2.93, df = 2, P = 0.069). The effect of plant species was also significant each year (2009: F = 33.07, df = 3, P < 0.0001; 2010: F = 16.52, df = 3, P = 0.0009; 2011: F = 9.09, df = 3, P = 0.0059). For oviposition in 2009, B. nigra and B. napus were preferred over E. sativa and R. sativus (P ⩽ 0.001; Fig. 1); in 2010, the greatest number
Discussion
Visual and olfactory cues are both important in host plant location by phytophagous insects, including the pollen beetle (Blight and Smart, 1999, Cook et al., 2007a, Cook et al., 2007b, Cook et al., 2013, Döring et al., 2012, Giamoustaris and Mithen, 1996). In this study we found, that, for oviposition, the beetle preferred B. napus, B. nigra and R. sativus over E. sativa. This concurs with results from laboratory trials that also showed the beetle preferred B. nigra and B. napus over E. sativa
Conclusion
Our study shows that B. nigra has potential to reinforce the natural control of the pollen beetle. Not only was it attractive to this pest as an oviposition site, but it provided suitable hosts for parasitoid species not prevalent on oilseed rape. In addition to trapping pests, B. nigra could also act as a parasitoid bank, providing habitat for beneficial insects.
Acknowledgments
We thank the anonymous reviewer for the constructive suggestions of an earlier manuscript. This study was supported by grant 8895 of the Estonian Science Foundation, project No. P9003 PKPK and Estonian Ministry of Education and Research targeted financing project no SF 0170057s09.
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2023, Crop ProtectionCitation Excerpt :Other studies have employed trap cropping technique to manage pollen beetles (Brassicogethes spp, Coleoptera: Nitidulidae) in oilseed rape (Brassica napus). These studies tested several species of Brassicaceae, such as turnip rape (Brassica rapa) (Gotlin Čuljak et al., 2016; Hokkanen et al., 1986; Hokkanen, 1989), yellow mustard (Brassica juncea) (Kaasik et al., 2014b), black mustard (Brassica nigra) (Veromann et al., 2012; Kaasik et al., 2014a), and white mustard (Sinapis alba) (Kaasik et al., 2014b). Most of the tested plants could attract and retain the pest insects, which is an important characteristic for a trap crop to be successful, especially during the stages of the cash crops most susceptible to damage.
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2020, Crop ProtectionCitation Excerpt :Upon hatching, larvae feed on pollen within buds, and eventually within open flowers, followed by pupation under the soil surface below the plant (see review by Mauchline et al. (2018)). B. aeneus has evolved natural enemies, primarily hymenopteran parasitoids and coleopteran predators, that have been shown to be effective suppressors of B. aeneus populations (Thies and Tscharntke, 1999; Büchi, 2002; Riggi et al., 2017; Kaasik et al., 2014; Skellern and Cook, 2018). However, large-scale destruction and fragmentation of natural and seminatural habitats associated with large-scale conventional agriculture have resulted in a scenario where natural enemies of B. aeneus are often unable to deliver the biocontrol service effectively enough to control B. aeneus populations.
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2019, Crop ProtectionCitation Excerpt :The authors argue that the host-parasitoid interaction may be host density dependent and, therefore, plots with lower larval numbers are not as attractive as control plots. However, Kaasik et al. (2014) finds that the host searching of T. heterocerus is density independent and the parasitoid explores open flowers, independent of the abundance of pollen beetle larvae. Similarly, in our trials, there was a reduction of the parasitism rate, especially one week after the application of the conventional Biscaya treatment.
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2016, Crop ProtectionCitation Excerpt :However, B. rapa was preferred over B. napus when both species were in the bud stage, indicating some inherent preferences for B. rapa (Cook et al., 2007a). The effect of B. rapa attractiveness for pollen beetle isn't equal everywhere while B. rapa attracted similar number of adults as B. napus (Veromann et al., 2012; Kaasik et al., 2014a, 2014b). For optimal effectiveness in control of the main crop in the green bud stage (BBCH 50 – Biologische Bundesanstalt, Bundessortenamt und Chemische Industrie), when oilseed rape is most vulnerable, trap crop plants should be in the early flower stage when they are the most attractive to pollen beetle females.