Globally, numerous pests attack crops causing large economic damage without efficient conventional or biological control 1. Importantly, the control of pests through the application of chemical pesticides repeatedly fails to provide reliable conventional control and contributes to significant environmental harm 2.
For instance, the overuse of pesticides can lead to pest resurgence 3 , 4 , as well as population decline of beneficial insects like natural enemies 2 and pollinators 5 , 6. Therefore, there is an increasing interest in approaches that reconcile high crop yields with environmental sustainability through ecological intensification and the targeted management of ecosystem services in agriculture 7 , 8. Pest control by natural enemies arises as an ecologically and economically promising solution 9.
Among natural enemies, both predatory and parasitic insects have been shown to be effective in suppressing pest species 11 , Because these species coexist in natural communities, they are potentially involved in positive or negative interactions with each other that may influence the strength of pest regulation. In fact, empirical studies indicate that trophic interactions among diverse natural enemy assemblages may result in a full spectrum of outcomes including null, additive, antagonistic or synergistic effects For instance, parasitoids and predators can attack a pest during different periods of its occurrence in the field 14 , resulting in stronger pest suppression than a single-enemy species However, this additive effect may be diminished by antagonistic interactions between natural enemies such as intraguild predation This can occur when, for example, predators eat immature parasitoids within their prey, thus reducing parasitoid impact on the pest However, exactly how these positive and negative interactions among predators and parasitoids affect natural pest control often remains an open question.
Many studies consist of surveys that sample only one period of the pest occurrence in the field, or focus only on one enemy, making it difficult to understand the combined effects of complete natural enemy guilds on pest population dynamics. The landscape in which a field is embedded can also play a fundamental role in shaping the natural enemy community 18 , and consequently the delivery of natural pest control services 16 , 19 , Complex landscapes with a high density of uncultivated and perennial habitats are often found to enhance the natural enemy populations and support better biological control 12 , In addition, complex landscapes can potentially reduce antagonistic interactions among insect natural enemies, thereby allowing coexistence of species with overlapping functional niches However, studies are lacking that examine the combined contribution of natural enemy guilds to pest control across different periods of the pest occurrence in the field while addressing landscape scale effects in parallel.
We used a field exclusion experiment, to examine the degree to which different functional guilds of natural enemies can reduce a pest population. We quantified the combined effects of parasitoids and ground-dwelling predators on the population dynamics of pollen beetles in 18 oilseed rape OSR fields while simultaneously contrasting the landscape context of the fields Supplementary Fig. The pollen beetle, Meligethes aeneus F. To date, most previous studies have focused on parasitoids that attack pollen beetle larvae during the flowering stage 12 , 25 , Ground-dwelling predators may also exert a considerable pollen beetle mortality in OSR 27 , 28 as they attack mature larvae when they drop to the soil to pupate, but their actual predation rates have not been assessed.
In this context, OSR provides an interesting experimental case to better comprehend the strength of pest control exerted by different natural enemies acting on different periods of the pest occurrence in the field. Specifically, we aimed i to quantify the individual and combined effects of ground-dwelling predators and parasitoids on controlling pollen beetle densities in OSR, and ii to assess whether biological control efficacy is affected by the surrounding landscape.
Further, the average number of emerged OSR pest weevils Ceutorhynchus sp. Parasitism also correlated negatively with the proportion of pollen beetles emerging in both exclosure and the open treatments Fig. Effect of landscape context on pest density. The density of emerged pollen beetles was negatively correlated with parasitism in landscapes with a low or intermediate proportion of non-crop habitats, but disappeared in landscapes with a high proportion of non-crop habitats Fig. Our study explored the combined effect of parasitoids and ground-dwelling predators on the biological control of pollen beetles in oilseed rape fields OSR.
Combining an exclusion experiment with pollen beetle sampling over two life stages allowed us to directly assess the importance to pest control of two different natural enemy guilds and the surrounding landscape. Our results suggest temporal complementarity among natural enemies in controlling pollen beetle populations, likely due to parasitoids and ground-dwelling predators attacking different periods of the pest occurrence in the field.
We demonstrated that generalist predators exerted a considerable pest control and, complemented specialist parasitoids.
We also found that such benefits improved when an increasing proportions of the surrounding landscape was occupied by non-crop habitats. Although this study covered only one crop season, our results highlight the importance of contributions from different natural enemy guilds to pest regulation in crops. However, it would be interesting to verify these results over a longer temporal scale. Ground-dwelling predators, which prey on pollen beetle larvae as they drop to the soil to pupate, thus play a key role in reducing the density of adult beetles before they can pupate and emerge in summer.
Whereas the impact of ground-dwelling predators on cereal aphids is usually small compared to other natural enemies 30 , 31 , 32 , their impact appears in OSR strong enough to control both pollen beetles and weevils. Our results for weevils are in agreement with a previous study 28 , which reported ground-dwelling predators as playing a key role in controlling stem weevils in OSR.
Oilseed rape, a major crop in many parts of the world, is attacked by a wide range of insect pests, many of which are of considerable economic. Oilseed rape, a major crop in many parts of the world, is attacked by a wide range of insect pests, many of which are of considerable economic importance.
However, conventional pest management strategies can negatively affect predator populations, thereby reducing the efficacy of natural pest control Alternative farming practices, such as organic farming 34 or conservation tillage 35 , can potentially counteract these effects by sustaining more abundant populations of predators compared to intensively managed farming systems 36 , In addition to the effect of ground-dwelling predators, we also found a significant effect of parasitism on pollen beetles; even though parasitism averaging Significant negative interactions between natural enemies, such as intraguild predation of parasitized pollen beetle larvae by ground-dwellers, were not indicated in this study.
Overall, parasitoids and predators had an additive impact on pest suppression in OSR, suggesting niche partitioning among parasitoids and ground-dwelling predators, likely as a result of them consuming a different developmental stage of the pest, support higher biological control Adding a life history-related temporal dimension to biological control will allow us to better comprehend the flow and stability of pest control services in agro-ecosystems Landscape scale responses of pollen beetle densities and parasitism confirmed that non-crop habitats can be an important factor reducing pest pressure 12 , The density of pollen beetle larvae in OSR fields decreased with an increasing proportion of non-crop habitats in the landscape.
Previous studies have reported both a significant reduction of pollen beetle pressure 12 , 21 and a significant increase in pest pressure 40 , 41 with an increasing proportion of non-crop habitats in the landscape. Our finding is consistent with the hypothesis that complex landscapes containing a high proportion of non-crop habitats tend to reduce the density of pest populations compared to simple landscapes dominated by arable lands, due to better top-down control by natural enemies 18 , This is confirmed by the positive correlation between parasitism rate and the proportion of grasslands in the landscape.
Parasitoids benefit from the presence of uncultivated, perennial habitats that provide nectar resources, alternative hosts, and overwintering sites 18 , Therefore, perennial habitats, such as grasslands, can enhance the number and life span of parasitoids that migrate into neighbouring crop fields and contribute to the reduction of pests However, such effects cannot be generalised to all natural enemies. For instance, we found that ground-dwelling predators were not influenced by landscape context.
As other authors have noted 43 , 44 , 45 , not all natural enemy populations benefit from the availability of perennial habitats in the landscape because responses are species specific. Further studies focusing on the trait-specificity of landscape effects, for example, the role of feeding preferences, body size or dispersal capacity, might help to disentangle the different responses of natural enemies to landscape context 46 , Also, our results showed a strong effect of parasitism on pollen beetle control in landscapes with low or intermediate proportion of non-crop habitats, but not in landscapes with a high proportion of non-crop habitats.
This result may reflect the density-dependent relationship between host and parasitoid. In accordance with a recent review 48 , we found parasitism to be positively density dependent, i. This density-dependent parasitism, together with the lower density of pollen beetle larvae in landscapes with a high proportion of non-crop habitats could explain the neutral effect of parasitism on pollen beetle control in complex landscapes with a high density of perennial habitats.
Overall, our results underline the complementary impact of different natural enemy guilds in regulating pest population in crops. Both parasitoids and ground-dwelling predators are important biocontrol agents acting on different periods of the pest occurrence in the field. Landscapes with a large area in non-crop habitats support natural pest control with abundant suitable habitats for natural enemies, whereas landscapes dominated by arable land would benefit from the adoption of specific management practices that mitigate the negative effects of landscape simplification 37 , 49 , For example, the implementation of flower strips or hedgerows in crop fields could provide additional habitats for different natural enemy guilds 49 , 50 , 51 , Preservation of different natural enemy guilds may also become increasingly important as an insurance policy against potential new pest problems arising from climate change Different species will not respond equally to climate change and temporal complementarity among natural enemies might prove to be an important mechanism for ensuring stable pest control.
In conclusion, optimizing natural pest control could significantly reduce the dependence of modern agriculture on pesticide applications while maintaining high crop yields 7 , A better knowledge of the direct connections between alternative pest control strategies, crop damage reduction and yield benefits is needed to demonstrate the profitability of wildlife-friendly farming practices.
Field experiments were conducted between April and June In the study area, the proportion of OSR covered a range from 0. Among non-crop habitats, the proportion of forests covered a range from 0. The oilseed rape pollen beetle Meligethes aeneus F. As temperatures rise, adults disperse into winter OSR fields where they feed on and oviposit in the flower buds.
The larvae feed on pollen and, when mature, drop to the soil for pupation.
The next generation of adult beetles emerges during the summer, and these will overwinter Natural enemies comprise generalist ground-dwelling predators such as ground beetles, spiders and rove beetles, and specialised parasitic hymenoptera. The eggs or larvae of pollen beetle in Europe are parasitized by several species and among these Tersilochus heterocerus is one of the most important parasitoids specialized on pollen beetles in the study region After the pollen beetle larvae drop to the ground, T.
Pollen beetles are most vulnerable to predation when, as mature larvae, they drop to the soil to pupate, but predation rates are currently unknown. In each field, the contribution to natural pest control by ground-dwelling predators was quantified by establishing an exclusion experiment. A pitfall trap was placed in the middle of the exclosure treatment to trap accidentally enclosed predators. The experiment was set up at the beginning of April before oilseed rape started to flower. We measured the density of pollen beetle larvae dropping to the ground with white plastic trays surface area The plastic trays were set up during OSR flowering on the 4 th of May and emptied weekly for four weeks.
We determined parasitism rates by T. For each treatment exclosure and open , the number of pollen beetle adults emerging from the ground was surveyed with a photoeclector trap 0. In the open treatment, we put a pitfall trap inside the photoeclector to capture the ground-dwelling predators. In which way, we maintained comparable conditions between the two treatments during the survey of pollen beetle adult.
The trapping cups of the photoeclectors were filled with water and detergent. We emptied the photoeclector traps weekly from the end of May until the beginning of July.
Because we found other OSR pest species emerging from the ground in the exclusion experiment, we also determined their number. Specifically, we calculated the number of adult OSR pest weevils Ceutorhynchus sp. Kerndl GmbH -water-mixture with detergent as trapping liquid Crossed metal rods were placed over the cup opening to prevent small vertebrates from falling into the trap.
All pitfall traps were set up on the 4 th of April and emptied fortnightly until the beginning of July when the whole experimental setting was removed. We considered the abundance of carabid beetles, cursorial spiders and rove beetles as the total number of individuals for each sampling period per field. Because the density of cabbage stem flea beetles was low, this group was not analysed. The site ID was included in the model as a random factor.
Then, we tested the relative importance of parasitoids and ground-dwelling predators in controlling pollen beetle using the proportion of emerged pollen beetle adults i. A longer study period is required to show any possible impact of ICM on the relative intensity of entomopathogenic fungi, or on the prevalence of entomopathogens. Two different measures of the occurrence yielded different results: the relative intensity revealed the difference between the two different crop management methods, while prevalence did not.
The highest efficacy of S. When only the larval stage was targeted, the application method and dose had no significant effect. The CRS decreased the pest abundance significantly more than the surface application method. The strain survived for 7 months when it was applied in autumn in Germany, but its populations declined rapidly after winter. The examined biotic and abiotic factors had variable impacts on S. The two measures, prevalence and relative intensity of entomopathogens, gave valuable information for their use in biocontrol programs.
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