Cold winters drive consistent and spatially synchronous 8-year population cycles of cabbage stem flea beetle.

Population cycles have been observed in mammals as well as insects, but consistent population cycling has rarely been documented in agroecosystems and never for a beetle. We analysed the long-term population patterns of the cabbage stem flea beetle Psylliodes chrysocephala in winter oilseed rape over 50 years. Psylliodes chrysocephala larval density from 3045 winter oilseed rape fields in southern Sweden showed strong 8-year population cycles in regional mean density. Fluctuations in larval density were synchronous over time across five subregional populations. Subregional mean environmental variables explained 90.6% of the synchrony in P. chrysocephala populations at the 7-11 year time-scale. The number of days below -10°C showed strong anti-phase coherence with larval densities in the 7-11 year time-scale, such that more cold days resulted in low larval densities. High levels of the North Atlantic Oscillation weather system are coherent and anti-phase with cold weather in Scania, Sweden. At the field-scale, later crop planting date and more cold winter days were associated with decreased overwintering larval density. Warmer autumn temperatures, resulting in greater larval accumulated degree days early in the season, increased overwintering larval density. Despite variation in environmental conditions and crop management, 8-year cycles persisted for cabbage stem flea beetle throughout the 50 years of data collection. Moran effects, influenced by the North Atlantic Oscillation weather patterns, are the primary drivers of this cycle and synchronicity. Insect pest data collected in commercial agriculture fields is an abundant source of long-term data. We show that an agricultural pest can have the same periodic population cycles observed in perennial and unmanaged ecosystems. This unexpected finding has implications for sustainable pest management in agriculture and shows the value of long-term pest monitoring projects as an additional source of time-series data to untangle the drivers of population cycles.

Insect pest damage increases faba bean (Vicia faba) yield components but only in the absence of insect pollination.

Identifying and quantifying crop stressors interactions in agroecosystems is necessary to guide sustainable crop management strategies. Over the last 50 years, faba bean cropping area has been declining, partly due to yield instabilities associated with uneven insect pollination and herbivory. Yet, the effect of interactions between pollinators and a key pest, the broad bean beetle Bruchus rufimanus (florivorous and seed predating herbivore) on faba bean yield has not been investigated. Using a factorial cage experiment in the field, we investigated how interactions between two hypothesized stressors, lack of insect pollination by bumblebees and herbivory by the broad bean beetle, affect faba bean yield. Lack of bumblebee pollination reduced bean weight per plant by 15%. Effects of the broad bean beetle differed between the individual plant and the plant-stand level (i.e., when averaging individual plant level responses at the cage level), likely due to high variation in the level of herbivory among individual plants. At the individual plant level, herbivory increased several yield components but only in the absence of pollinators, possibly due to plant overcompensation and/or pollination by the broad bean beetle. At the plant-stand level, we found no effect of the broad bean beetle on yield. However, there was a tendency for heavier individual bean weight with bumblebee pollination, but only in the absence of broad bean beetle herbivory, possibly due to a negative effect of the broad bean beetle on the proportion of legitimate flower visits by bumblebees. This is the first experimental evidence of interactive effects between bumblebees and the broad bean beetle on faba bean yield. Our preliminary findings of negative and indirect associations between the broad bean beetle and individual bean weight call for a better acknowledgment of these interactions in the field in order to understand drivers of crop yield variability in faba bean.

CropPol: A dynamic, open and global database on crop pollination.

Seventy five percent of the world's food crops benefit from insect pollination. Hence, there has been increased interest in how global change drivers impact this critical ecosystem service. Because standardized data on crop pollination are rarely available, we are limited in our capacity to understand the variation in pollination benefits to crop yield, as well as to anticipate changes in this service, develop predictions, and inform management actions. Here, we present CropPol, a dynamic, open, and global database on crop pollination. It contains measurements recorded from 202 crop studies, covering 3,394 field observations, 2,552 yield measurements (i.e., berry mass, number of fruits, and fruit density [kg/ha], among others), and 47,752 insect records from 48 commercial crops distributed around the globe. CropPol comprises 32 of the 87 leading global crops and commodities that are pollinator dependent. Malus domestica is the most represented crop (32 studies), followed by Brassica napus (22 studies), Vaccinium corymbosum (13 studies), and Citrullus lanatus (12 studies). The most abundant pollinator guilds recorded are honey bees (34.22% counts), bumblebees (19.19%), flies other than Syrphidae and Bombyliidae (13.18%), other wild bees (13.13%), beetles (10.97%), Syrphidae (4.87%), and Bombyliidae (0.05%). Locations comprise 34 countries distributed among Europe (76 studies), North America (60), Latin America and the Caribbean (29), Asia (20), Oceania (10), and Africa (7). Sampling spans three decades and is concentrated on 2001-2005 (21 studies), 2006-2010 (40), 2011-2015 (88), and 2016-2020 (50). This is the most comprehensive open global data set on measurements of crop flower visitors, crop pollinators and pollination to date, and we encourage researchers to add more datasets to this database in the future. This data set is released for non-commercial use only. Credits should be given to this paper (i.e., proper citation), and the products generated with this database should be shared under the same license terms (CC BY-NC-SA).

Consequences of the neonicotinoid seed treatment ban on oilseed rape production - what can be learnt from the Swedish experience?

There has been great concern about negative effects on crop production resulting from the ban on insecticide seed treatments containing neonicotinoids. I examine how the neonicotinoid ban has affected crop protection and crop production in oilseed rape (Brassica napus L.) using Sweden as a case study and compare the Swedish situation with that in leading countries growing winter and spring oilseed rape, respectively. The cropping area of winter and spring oilseed rape in Sweden has increased by approximately 40% to around 100 000 ha and decreased by approximately 90% to around 4000 ha, respectively following the ban and there are trends for increased pest and disease pressure. Overall, however, the ban has not had any major impacts on total oilseed rape cropping area or crop yields per hectare of either winter or spring oilseed rape, which is in contrast to elsewhere in Europe. In Germany and the United Kingdom, for example, the cropping area has decreased following the ban on neonicotinoid seed treatments, attributed to increased insect pest pressure especially from cabbage stem flea beetle, Psylliodes chrysocephala. I conclude that winter oilseed rape has remained a viable crop to grow in Sweden without insecticide seed treatments, but that further investments into integrated pest management are needed for sustainable insect pest control in oilseed rape in the future. © 2021 The Author. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Water stress and insect herbivory interactively reduce crop yield while the insect pollination benefit is conserved.

Climate change is predicted to hamper crop production due to precipitation deficits and warmer temperatures inducing both water stress and increasing herbivory due to more abundant insect pests. Consequently, crop yields will be impacted simultaneously by abiotic and biotic stressors. Extensive yield losses due to such climate change stressors might, however, be mitigated by ecosystem services such as insect pollination. We examined the single and combined effects of water stress, insect herbivory and insect pollination on faba bean yield components and above- and belowground plant biomass under realistic field conditions. We used rainout shelters to simulate a scenario in line with climate change projections, with adequate water supply at sowing followed by a long period without precipitation. This induced a gradually increasing water stress, culminating around crop flowering and yield formation. We found that gradually increasing water stress combined with insect herbivory by aphids interactively shaped yield in faba beans. Individually, aphid herbivory reduced yield by 79% and water stress reduced yield by 52%. However, the combined effect of water stress and aphid herbivory reduced yield less (84%) than the sum of the individual stressor effects. In contrast, insect pollination increased yield by 68% independently of water availability and insect herbivory. Our results suggest that yield losses can be greatly reduced when both water stress and insect herbivory are reduced simultaneously. In contrast, reducing only one stressor has negligible benefits on yield as long as the crop is suffering from the other stressor. We call for further exploration of interactions among ecosystem services and biotic and abiotic stressors that simulate realistic conditions under climate change.

Wildflower plantings promote blue orchard bee, Osmia lignaria (Hymenoptera: Megachilidae), reproduction in California almond orchards.

Concerns over the availability of honeybees (Apis mellifera L.) to meet pollination demands have elicited interest in alternative pollinators to mitigate pressures on the commercial beekeeping industry. The blue orchard bee, Osmia lignaria (Say), is a commercially available native bee that can be employed as a copollinator with, or alternative pollinator to, honeybees in orchards. To date, their successful implementation in agriculture has been limited by poor recovery of bee progeny for use during the next spring. This lack of reproductive success may be tied to an inadequate diversity and abundance of alternative floral resources during the foraging period. Managed, supplementary wildflower plantings may promote O. lignaria reproduction in California almond orchards. Three wildflower plantings were installed and maintained along orchard edges to supplement bee forage. Plantings were seeded with native wildflower species that overlapped with and extended beyond almond bloom. We measured bee visitation to planted wildflowers, bee reproduction, and progeny outcomes across orchard blocks at variable distances from wildflower plantings during 2015 and 2016. Pollen provision composition was also determined to confirm O. lignaria wildflower pollen use. Osmia lignaria were frequently observed visiting wildflower plantings during, and after, almond bloom. Most O. lignaria nesting occurred at orchard edges. The greatest recovery of progeny occurred along the orchard edges having the closest proximity (80 m) to managed wildflower plantings versus edges farther away. After almond bloom, O. lignaria nesting closest to the wildflower plantings collected 72% of their pollen from Phacelia spp., which supplied 96% of the managed floral area. Phacelia spp. pollen collection declined with distance from the plantings, but still reached 17% 800 m into the orchard. This study highlights the importance of landscape context and proximity to supplementary floral resources in promoting the propagation of solitary bees as alternative managed pollinators in commercial agriculture.

Economic Injury Levels for Flea Beetles (Phyllotreta spp.; Coleoptera: Chrysomelidae) in Spring Oilseed Rape (Brassica napus; Brassicales: Brassicaceae).

Flea beetles (Phyllotreta spp.) are major insect pests in spring oilseed rape (SOSR; Brassica napus L.). Prohibited use of three neonicotinoid insecticides in the European Union means that there are currently no insecticide seed treatment options available. Insecticide spraying remains as a control option, but there is a need to estimate the economic threshold for crop injury. As a first step to this end, economic injury levels were determined for flea beetles in SOSR. Data from 16 field experiments were used to quantify the relationship between flea beetle crop injury and SOSR yield, and additional data from paired sprayed and unsprayed plots in 12 commercial SOSR fields were used to determine the reduction in crop injury from a pyrethroid spray. There was a strong linear negative effect of flea beetle injury with 19 kg/ha yield loss per percent crop injury to seedlings and a pyrethroid spray reduced crop injury by 39%. These results gave an economic injury level of 11% defoliation of SOSR seedlings under average oilseed rape prices and insecticide use costs in 2017. This is considerably lower than previously used nominal thresholds of 25-30% injury to cotyledons. Increased yields and increasingly cheaper pyrethroids might be the reason for the lower levels of crop injury that warrant chemical control. The economic injury levels presented here can be used to construct economic thresholds that preferably should also take into account crop growth stage, crop growth rate, and anticipated flea beetle activity.

Can Costs of Pesticide Exposure for Bumblebees Be Balanced by Benefits from a Mass-Flowering Crop?

Mass-flowering crops provide forage for bees but also contain pesticides. Such pesticide exposure can harm bees, but our understanding of how this cost is balanced by forage benefits is limited. To provide insights into benefits and costs, we placed bumblebee colonies in 18 landscapes with conventional red clover fields treated with the neonicotinoid thiacloprid (flowers + pesticide), untreated organic red clover fields (flowers), or landscapes lacking clover fields (controls). Colonies grew heavier near thiacloprid-treated clover compared to controls lacking clover, while colonies near untreated clover did not differ from colonies in neither of the other landscape types. Thiacloprid treatment effectively controlled pests and increased bumblebee crop visitation. However, colony production of queens and males did not differ among landscape types. In conclusion, thiacloprid application in clover appears to be of low risk for bumblebees. More generally, neonicotinoids may not be equally harmful when used in flowering crops and effective low-risk pest control in such crops could potentially benefit bumblebees and crop pollination.

Annual flower strips support pollinators and potentially enhance red clover seed yield.

Ecological intensification provides opportunity to increase agricultural productivity while minimizing negative environmental impacts, by supporting ecosystem services such as crop pollination and biological pest control. For this we need to develop targeted management solutions that provide critical resources to service-providing organisms at the right time and place. We tested whether annual strips of early flowering phacelia Phacelia tanacetifolia support pollinators and natural enemies of seed weevils Protapion spp., by attracting and offering nectar and pollen before the crop flowers. This was expected to increase yield of red clover Trifolium pratense seed. We monitored insect pollinators, pests, natural enemies and seed yields in a total of 50 clover fields along a landscape heterogeneity gradient, over 2 years and across two regions in southern Sweden. About half of the fields were sown with flower strips of 125-2,000 m2. The clover fields were pollinated by 60% bumble bees Bombus spp. and 40% honey bees Apis mellifera. The clover seed yield was negatively associated with weevil density, but was unrelated to bee species richness and density. Flower strips enhanced bumble bees species richness in the clover fields, with the strongest influence in heterogeneous landscapes. There were few detectable differences between crop fields with and without flower strips. However, long-tongued bumble bees were redistributed toward field interiors and during phacelia bloom honey bees toward field edges. Clover seed yield also increased with increasing size of the flower strip. We conclude that annual flower strips of early flower resources can support bumble bee species richness and, if sufficiently large, possibly also increase crop yields. However, clover seed yield was mainly limited by weevil infestation, which was not influenced by the annual flower strips. A future goal should be to design targeted measures for pest control.

Wildflower Plantings Do Not Compete With Neighboring Almond Orchards for Pollinator Visits.

The engineering of flowering agricultural field borders has emerged as a research and policy priority to mitigate threats to pollinators. Studies have, however, rarely addressed the potential that flowering field borders might compete with neighboring crops for pollinator visits if they both are in bloom at the same time, despite this being a concern expressed by growers. We evaluated how wildflower plantings added to orchard borders in a large (512 ha) commercial almond orchard affected honey bee and wild bee visitation to orchard borders and the crop. The study was conducted over two consecutive seasons using three large (0.48 ha) wildflower plantings paired with control orchard borders in a highly simplified agricultural landscape in California. Honey bee (Apis mellifera L.) and wild bee visitation to wildflower plots were at least an order of magnitude higher than to control plots, but increased honey bee visitation to wildflower plots did not lead to any detectable shifts in honey bee visitation to almond flowers in the neighboring orchard. Wild bees were rarely observed visiting almond flowers irrespective of border treatment, indicating a limited short-term potential for augmenting crop pollination using wild bees in highly simplified agricultural landscapes. Although further studies are warranted on bee visitation and crop yield from spatially independent orchards, this study indicates that growers can support bees with alternative forage in almond orchards without risking competition between the wildflower plantings and the crop.

Field Abundance Patterns and Odor-Mediated Host Choice by Clover Seed Weevils, Apion fulvipes and Apion trifolii (Coleoptera: Apionidae).

The clover seed weevils Apion fulvipes Geoffroy, 1785 and Apion trifolii L., 1768 (Coleoptera: Apionidae) cause major losses to seed production of white clover (Trifolium repens L.) and red clover (Trifolium pratense L.), respectively. Clover is important as animal forage and an alternative to inorganic fertilizers. Because clover is mainly pollinated by bees, the use of insecticides in management of these weevils is discouraged. To gain basic knowledge for development of alternative management strategies, we investigated weevil field abundance over two growing seasons, as well as feeding and olfactory host preferences by A. fulvipes and A. trifolii. Field trap catches in southern Sweden revealed that white clover was dominated by A. fulvipes and red clover by A. trifolii. For both weevil species, female catches were positively correlated to the number of clover buds and flowers in the field. In feeding and olfactory bioassays, females of A. fulvipes and A. trifolii showed a preference for T. repens and T. pratense, respectively. However, the feeding preference was lost when the antennae were removed, indicating a significant role of olfaction in host choice. Male weevils of both species did not show clear olfactory or feeding preferences for host plant species. The field study and laboratory bioassays demonstrate that, at least for female weevils, olfaction is important for selection of host plants. We discuss these novel results in the context of managing these important pests of clover by exploiting olfaction and behavioral attraction to host plant volatiles.

Neonicotinoid Insecticides and Their Impacts on Bees: A Systematic Review of Research Approaches and Identification of Knowledge Gaps.

It has been suggested that the widespread use of neonicotinoid insecticides threatens bees, but research on this topic has been surrounded by controversy. In order to synthesize which research approaches have been used to examine the effect of neonicotinoids on bees and to identify knowledge gaps, we systematically reviewed research on this subject that was available on the Web of Science and PubMed in June 2015. Most of the 216 primary research studies were conducted in Europe or North America (82%), involved the neonicotinoid imidacloprid (78%), and concerned the western honey bee Apis mellifera (75%). Thus, little seems to be known about neonicotinoids and bees in areas outside Europe and North America. Furthermore, because there is considerable variation in ecological traits among bee taxa, studies on honey bees are not likely to fully predict impacts of neonicotinoids on other species. Studies on crops were dominated by seed-treated maize, oilseed rape (canola) and sunflower, whereas less is known about potential side effects on bees from the use of other application methods on insect pollinated fruit and vegetable crops, or on lawns and ornamental plants. Laboratory approaches were most common, and we suggest that their capability to infer real-world consequences are improved when combined with information from field studies about realistic exposures to neonicotinoids. Studies using field approaches often examined only bee exposure to neonicotinoids and more field studies are needed that measure impacts of exposure. Most studies measured effects on individual bees. We suggest that effects on the individual bee should be linked to both mechanisms at the sub-individual level and also to the consequences for the colony and wider bee populations. As bees are increasingly facing multiple interacting pressures future research needs to clarify the role of neonicotinoids in relative to other drivers of bee declines.

When ecosystem services interact: crop pollination benefits depend on the level of pest control.

Pollination is a key ecosystem service which most often has been studied in isolation although effects of pollination on seed set might depend on, and interact with, other services important for crop production. We tested three competing hypotheses on how insect pollination and pest control might jointly affect seed set: independent, compensatory or synergistic effects. For this, we performed a cage experiment with two levels of insect pollination and simulated pest control in red clover (Trifolium pratense L.) grown for seed. There was a synergistic interaction between the two services: the gain in seed set obtained when simultaneously increasing pollination and pest control outweighed the sum of seed set gains obtained when increasing each service separately. This study shows that interactions can alter the benefits obtained from service-providing organisms, and this needs to be considered to properly manage multiple ecosystem services.

Towards integrated pest management in red clover seed production.

The development of integrated pest management is hampered by lack of information on how insect pest abundances relate to yield losses, and how pests are affected by control measures. In this study, we develop integrated pest management tactics for Apion spp. weevils (Coleoptera: Brentidae) in seed production of red clover, Trifolium pratense L. We tested a method to forecast pest damage, quantified the relationship between pest abundance and yield, and evaluated chemical and biological pest control in 29 Swedish red clover fields in 2008 and 2011. Pest inflorescence abundance, which had a highly negative effect on yield, could be predicted with pan trap catches of adult pests. In 2008, chemical control with typically one application of pyrethroids was ineffective both in decreasing pest abundances and in increasing yields. In 2011, when chemical control included applications of the neonicotinoid thiacloprid, pest abundances decreased and yields increased considerably in treated field zones. A post hoc analysis indicated that using pyrethroids in addition to thiacloprid was largely redundant. Infestation rates by parasitoids was higher and reached average levels of around 40% in insecticide treated field zones in 2011, which is a level of interest for biological pest control. Based on the data presented, an economic threshold for chemical control is developed, and guidelines are provided on minimum effective chemical pest control.

Characterization of olfactory sensory neurons in the white clover seed weevil, Apion fulvipes (Coleoptera: Apionidae).

Seed-eating Apion weevils (Coleoptera: Apionidae) cause large economic losses in white and red clover seed production across Europe. Monitoring and control of clover weevils would be facilitated by semiochemical-based methods. Until now, however, nothing was known about physiological or behavioral responses to semiochemicals in this insect group. Here we analyzed the antenna of the white clover (Trifolium repens L.) specialist Apion fulvipes Geoffroy with scanning electron microscopy, and used single sensillum recordings with a set of 28 host compounds to characterize 18 classes of olfactory sensory neurons (OSNs). Nine of the OSN classes responded strongly to synthetic compounds with high abundance in clover leaves, flowers, or buds. Eight classes responded only weakly to the synthetic stimuli, whereas one collective class responded exclusively to volatiles released from a crushed clover leaf. The OSNs showed a remarkable degree of specificity, responding to only one or a few chemically related compounds. In addition, we recorded a marked difference in the temporal dynamics of responses between different neurons, compounds, and doses. The identified physiologically active compounds will be screened for behavioral activity, with the ultimate goal to develop an odor-based control strategy for this pest.

Drastic historic shifts in bumble-bee community composition in Sweden.

The species richness of flower-visiting insects has declined in past decades, raising concerns that the ecosystem service they provide by pollinating crops and wild plants is threatened. The relative commonness of different species with shared ecological traits can play a pervasive role in determining ecosystem functioning, but information on changes in abundances of pollinators over time is lacking. We gathered data on relative abundances of bumble-bee species in Swedish red clover fields during three periods in the last 70 years (1940s, 1960s and present), and on clover seed yields since 1921. We found drastic decreases in bumble-bee community evenness, with potential consequences for level and stability of red clover seed yield. The relative abundances of two short-tongued bumble-bees have increased from 40 per cent in the 1940s to entirely dominate present communities with 89 per cent. Average seed yield declined in recent years and variation in yield doubled, suggesting that the current dependence on few species for pollination has been especially detrimental to stability in seed yield. Our results suggest a need to develop management schemes that promote not only species-rich but also more evenly composed communities of service-providing organisms.