Hedgerows surrounding organic apple orchards in north‐west Spain: potential to conserve beneficial insects

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Time since establishment drives bee and hoverfly diversity,abundance of crop-pollinating bees and aphidophagous hoverflies in perennial wildflower strips

Wildflower strips (WFS) are amongst the most commonly applied measures to promote pollinators and natural enemies of crop pests in agroecosystems. Their potential to enhance these functionally important insect groups may vary substantially with time since establishment of WFS. However, knowledge on their temporal dynamics remains scarce, hampering recommendations for optimized design and management. We therefore examined temporal dynamics of taxonomic and functional groups of bees and hoverflies in perennial WFS ranging from one to ≥6 years since sowing with a standardized species-rich seed mixture of flowering plants in 18 agricultural landscapes in Switzerland. The abundance of wild bees, honeybees and hoverflies declined after the second year by 89%, 62% and 72%, respectively. Declines in bee abundance and hoverfly species richness were linear and those of aphidophagous hoverflies exponential, while wild bee species richness peaked in the third year. Declines over time generally paralleled decreases in flower abundance (-83%) and flowering species richness (-61%) and an increase in grass cover (+70%) in WFS. Flowering plant species richness showed strong positive relationships with dominant crop-visiting wild bees and aphidophagous hoverflies. Furthermore, dominant crop-visiting wild bees, but not aphidophagous hoverflies, were positively related to the proportion of (semi-)open semi-natural habitat in the surrounding landscape (500 m radius), but negatively with forest. We conclude that the effectiveness of perennial WFS to promote pollinator diversity, crop-pollinating bees and aphidophagous hoverflies through foraging resources decreases after the first two to three years, probably due to a decline of diverse and abundant floral resources. Although older perennial WFS may still provide valuable nesting and overwintering opportunities for pollinators and natural enemies, our findings indicate that regular re-sowing of perennial WFS may be necessary to maintain adequate floral resource provisioning for effective pollinator conservation and promotion of crop pollination and natural pest control services in agricultural landscapes.     

Feeding preferences of the aphidophagous hoverfly Sphaerophoria rueppellii affect the performance of its offspring

Provision of additional floral resources in the crop is a successful strategy of conservation biological control for attracting several natural enemies including predatory syrphids. However, the selection of flower species is mainly based on visiting preferences, paying little attention to the link between preference and performance. In this study, we assess the influence of feeding on flowers of two insectary plants (sweet alyssum and coriander) and flowers of a crop species (sweet pepper) on performance of the parental and first generation of the syrphid Sphaerophoria rueppellii (Wiedemann) (Diptera: Syrphidae). We found that floral preference of the adults was linked to developmental performance of their offspring. Sweet alyssum was the flower most frequently visited by syrphid adults, enhancing adult body size and egg-to adult survival of the F1 generation.     

Threats and benefits of invasive alien plant species on pollinators

Invasive alien plant species are usually disliked due to their high pressure on native communities. However, their ecological effects on pollinators are complex: some species provide abundant floral resources, boosting the number of pollinators, while they often disrupt plant-pollinator interactions by outcompeting native plants. Our direct knowledge is mainly based on single-species studies, while understanding the mechanism of these complex ecological interactions needs multi-species field-based approaches. It is also imperative to clarify the pros and cons of invasive plants and drivers of invasion from the perspective of pollinators. We conducted a standard protocol-driven regional study in Central and Eastern Europe, comparing 6-7 invaded and non-invaded sites of 12 herbaceous invasive plant species. We sampled floral resources, bees, and hoverflies before and during the flowering of the invasive plants. We analysed the effects of plant invasion at the invasive plant species level and in combined analyses, and tested whether the life span (perennial vs. annual) and flowering time (early-, middle-, and late-flowering) of invasive plants affect the abundance, species richness, diversity and species composition of native plants and pollinators. The combined analyses showed lower abundance and species richness of flowering plants and pollinators before, and higher abundance of both during the flowering of invasive plants in invaded sites. However, invasive plants had significant species-specific effects. Perennial invasive plants had a stronger negative impact on floral resources and pollinators already before their flowering compared to annuals. Flowering time of invasive plants affected the pollinator guilds differently. We suggest that in certain critical time periods of the year, invasive plants might provide the dominant foraging resources for pollinators in an invaded ecosystem. But, they also often cause significant losses in native floral resources over the year. Instead of simple eradication, careful preparation and consideration might be needed during removal of invasive plants.     

Attractiveness of Michigan native plants to arthropod natural enemies and herbivores

The use of plants to provide nectar and pollen resources to natural enemies through habitat management is a growing focus of conservation biological control. Current guidelines frequently recommend use of annual plants exotic to the management area, but native perennial plants are likely to provide similar resources and may have several advantages over exotics. We compared a set of 43 native Michigan perennial plants and 5 frequently recommended exotic annual plants for their attractiveness to natural enemies and herbivores for 2 yr. Plant species differed significantly in their attractiveness to natural enemies. In year 1, the exotic annual plants outperformed many of the newly established native perennial plants. In year 2, however, many native perennial plants attracted higher numbers of natural enemies than exotic plants. In year 2, we compared each flowering plant against the background vegetation (grass) for their attractiveness to natural enemies and herbivores. Screening individual plant species allowed rapid assessment of attractiveness to natural enemies. We identified 24 native perennial plants that attracted high numbers of natural enemies with promise for habitat management. Among the most attractive are Eupatorium perfoliatum L., Monarda punctata L., Silphium perfoliatum L., Potentilla fruticosa auct. non L., Coreopsis lanceolata L., Spiraea alba Duroi, Agastache nepetoides (L.) Kuntze, Anemone canadensis L., and Angelica atropurpurea L. Subsets of these plants can now be tested to develop a community of native plant species that attracts diverse natural enemy taxa and provides nectar and pollen throughout the growing season.     

Visitation by wild and managed bees (Hymenoptera: Apoidea) to eastern U.S. native plants for use in conservation programs

Addition of floral resources to agricultural field margins has been shown to increase abundance of beneficial insects in crop fields, but most plants recommended for this use are non-native annuals. Native perennial plants with different bloom periods can provide floral resources for bees throughout the growing season for use in pollinator conservation projects. To identify the most suitable plants for this use, we examined the relative attractiveness to wild and managed bees of 43 eastern U.S. native perennial plants, grown in a common garden setting. Floral characteristics were evaluated for their ability to predict bee abundance and taxa richness. Of the wild bees collected, the most common species (62%) was Bombus impatiens Cresson. Five other wild bee species were present between 3 and 6% of the total: Lasioglossum admirandum (Sandhouse), Hylaeus affinis (Smith), Agapostemon virescens (F.), Halictus ligatus Say, and Ceratina calcarata/dupla Robertson/Say. The remaining wild bee species were present at <2% of the total. Abundance of honey bees (Apis mellifera L.) was nearly identical to that of B. impatiens. All plant species were visited at least once by wild bees; 9 were highly attractive, and 20 were moderately attractive. Honey bees visited 24 of the 43 plant species at least once. Floral area was the only measured factor accounting for variation in abundance and richness of wild bees but did not explain variation in honey bee abundance. Results of this study can be used to guide selection of flowering plants to provide season-long forage for conservation of wild bees.     

Wild bees and natural enemies prefer similar flower species and respond to similar plant traits

Designing wildflower habitats to support beneficial insects providing pollination and pest control services is important for supporting sustainable crop production. It is often desirable to support both groups of insects, making the selection of resource plants for insect conservation programs more challenging. Moreover, the process of selecting resource plants is complicated by the array of possible options in each region, and the need to provide resources over the entire growing season. Identifying traits shared by resource plants that are attractive to both bees and natural enemies can reduce the need to evaluate new plants in each region, by providing a guide for the types of plants expected to be rewarding to these insects. Using insect visitation data collected from replicated common garden plantings of native wildflower and shrub species from the Great Lakes region of the United States, we found a high degree of correlation between the abundance of bees and natural enemies visiting native plant species. These results were used to identify a set of 15 plant species that can provide resources for these insects throughout the summer. Across all tested species, pollen quantity per flower and the week of bloom were positively correlated with some, but not all, taxonomic groupings of beneficial insects. In contrast, floral area was consistently positively associated with visitation of both natural enemies and wild bees. This trait is easy to document and can allow for efficient local testing of potential resource plants, providing a faster path to implementing insect conservation in working landscapes.     

Contrasting impacts of highly invasive plant species on flower-visiting insect communities

Invasive alien plants threaten biodiversity, ecosystems and service provision worldwide. They can have positive and negative direct and indirect effects on herbivorous insects, including those that provide pollination services. Here, we quantify how three highly invasive plant species (Heracleum mantegazzianum, Impatiens glandulifera and Fallopia japonica) influence the availability of floral resources and flower-visiting insect communities. We compared invaded with comparable uninvaded areas to assess floral resources and used pan-trapping to quantify insect communities. Only F. japonica influenced floral resource availability: sites invaded by this species had a higher flowering plant species richness and abundance of open floral units than uninvaded sites, probably due to its late flowering and the paucity of other flowering species at this time of year. Fallopia japonica was also associated with higher abundances of bumblebees, higher overall insect diversity and higher hoverfly diversity than uninvaded areas. Differences in pollinator communities were also associated with I. glandulifera and H. mantegazzianum, despite there being no detectable differences in floral resources at these sites. Specifically, there were more bumblebees and solitary bees in I. glandulifera sites, and a higher overall diversity of insects, particularly hoverflies. By contrast, H. mantegazzianum sites had a lower abundance of solitary bees and hoverflies. These findings confirm that invasive plant species have a range of species-specific effects on ecological communities. This supports the emerging view that control of invasive species, as required under international obligations, is not simple and that potential losses and gains for biodiversity must be carefully evaluated on a case-by-case basis.     

Attractiveness of single and multiple species flower patches to beneficial insects in agroecosystems

The provision of floral resources for the enhancement of beneficial insect populations has shown promise as a strategy to enhance biological control and pollination in agroecosystems. One approach involves the provision of a single flower species while a second involves the multiple flower species, but the two have never been compared experimentally. Here we examine the influence of single and multiple species flower treatments on the abundance and foraging behaviour of key beneficial insects in two agricultural agroecosystems (broccoli and lucerne crops). The five flower treatments comprised buckwheat only, phacelia only, a simple mixture of buckwheat and phacelia, a complex mixture of buckwheat, phacelia and a commercial seed blend or the existing crop as a control. The abundance of bumble‐bees (Bombus hortorum) and honey bees (Apis mellifera) was highest in the three treatments that contained phacelia, while hoverfly (Melanostoma fasciatum) numbers were high in all four flower treatments. Bumble‐bees and honey bees probed almost exclusively phacelia flowers, even when provided with a choice of other flower species in the simple and complex mixture treatments. In contrast, hoverflies probed the flowers of all plant species in single and multiple species treatments, with no apparent difference in acceptance. However, in mixture treatments, the majority of individual bumble‐bees, honey bees and hoverflies probed the flowers from only one species, despite the presence of alternative flower species. Our results illustrate how an appreciation of insect floral attractiveness can be used to customise the species composition of floral patches to potentially maximise biological control and pollination in targeted agroecosystems.     

The attractiveness of flowering herbaceous plants to bees (Hymenoptera: Apoidea) and hoverflies (Diptera: Syrphidae) in agro‐ecosystems of Central Spain

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Non-crop vegetation associated with chili pepper agroecosystems promote the abundance and survival of aphid predators

Habitat manipulation has long been used as strategy to enhance beneficial insects in agroecosystems. Non-crop weed strips have the potential of supplying food resources to natural enemies, even when pest densities are low. However, in tropical agroecosystems there is a paucity of information pertaining to the resources provided by non-crop weeds and their interactions with natural enemies. In this study we evaluated (a) whether weeds within chili pepper fields affect the diversity and abundance of aphidophagous species; (b) whether there are direct interactions between weeds and aphidophagous arthropods; and (c) the importance of weed floral resources for survival of a native and exotic coccinellid in chili pepper agroecosystems. In the field, aphidophagous arthropods were dominated by Coccinellidae, Syrphidae, Anthocoridae, Neuroptera and Araneae, and these natural enemies were readily observed preying on aphids, feeding on flowers or extrafloral nectaries, and using plant structures for oviposition and/or protection. Survival of native Cycloneda sanguinea (Coleoptera: Coccinellidae) differed between plant species, with significantly greater survival on Ageratum conyzoides and Bidens pilosa. However, no evidence was gathered to suggest that weed floral resources provided any nutritional benefit to the exotic Harmonia axyridis (Coleoptera: Coccinellidae). This research has provided evidence that naturally growing weeds in chili pepper agroecosystems can affect aphid natural enemy abundance and survival, highlighting the need for further research to fully characterize the structure and function of plant resources in these and other tropical agroecosystems.     

Larger patches of diverse floral resources increase insect pollinator density,diversity, and their pollination of native wildflowers

Native wildflower plantings can be used to provide nutritional resources to support pollinating insects, yet the effects of planting size and bloom richness on the density, diversity, and function of these insects are not well understood. We established stands of twelve native flowering perennial plant species in replicated plots ranging in size from 1 to 100 m². These plots were sampled for insect pollinators, bloom richness, and seed production by three wildflower species. Honeybees, wild bees, and hoverflies all responded positively to increasing flower richness, whereas particular insect pollinator groups responded differently to the size of the flowering plant area. The density of honeybees and hoverflies was not affected by increasing flowering patch size, whereas in general, wild bees were observed at higher density and diversity in the 30 and 100 m² patches. Increasing wildflower patch size, and thus wild bee density, resulted in greater seed set in the sampled wildflowers. These results indicate that wild bees are sensitive to the area and richness of floral resources in patches, even at relatively small scales. Therefore, larger wildflower plantings with more diverse flower species mixes are more suitable for the conservation of wild pollinators and reproduction of sown species.     

Sowing of margin strips rich in floral resources improves herbivore control in adjacent crop fields

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An entomophage park to promote natural enemy diversity

Undisturbed habitats of natural vegetation near agricultural areas protect and enhance specific natural enemies and provide them with resources such as nectar, pollen, physical refuge, alternative prey, alternative hosts and mating sites. In order to reduce the pesticide-induced mortality of natural enemies and to improve natural enemy fitness and effectiveness, one such area (termed an ‘entomophage park’) was established at the Sher-e-Kashmir University of Agricultural Sciences and Technology of Jammu, at Chatha, India in 2007. Naturally occurring plants, weeds, cultivated crops and flowers were monitored regularly for natural enemies. Seven sampling methods were employed to compare the abundance of natural enemies in the entomophage park and adjoining crop fields. Both entomophage diversity and abundance in the park were much higher than in the adjacent agricultural fields of vegetables and cereals. A total of 61 species of natural enemies were recovered from the entomophage park, as compared to 22 and 20 species in cereal and vegetable fields, respectively. The abundance of parasitoids (ichneumonids, braconids, scelionids and chalcidoids) was significantly higher in the park as compared to surveyed agricultural fields, as was egg parasitism by scelionids (Telenomus spp.) and trichogrammatids, and parasitisation by the larval parasitoid Campoletis chlorideae on Helicoverpa armigera. The entomophage park also significantly enhanced the fecundity and survival of the ichneumonid C. chlorideae, when compared to individuals collected from vegetable and cereal fields. Seventeen species of plants were recorded as ‘insectary plants' (one providing substantial floral resources) in the entomophage park. Such parks may play an important role in maintaining the biodiversity of natural enemies and enhancing natural pest control.     

The relation between oilseed rape and pollination of later flowering plants varies across plant species and landscape contexts

Increasing cultivation of oilseed rape may have consequences for pollinators and wild plant pollination. By providing pollinating insects with pollen and nectar, oilseed rape benefits short-tongued, generalist insect species. Long-tongued bumble bee species, specialized to other flower types, may instead be negatively affected by increased competition from the generalists (e.g. due to nectar-robbing of long-tubed flowers) after oilseed rape flowering has ceased. We expected that the increased abundance of short-tongued pollinators and reduced abundance of long-tongued bumble bees in landscapes with a high proportion of oilseed rape would impact the pollination of later flowering wild plant species. In addition, we expected contrasting effects on plants pollinated by short-tongued pollinators and those pollinated by long-tongued bumble bees. We predicted that semi-natural grasslands, which provide insects with alternative floral resources, would reduce both negative and positive effects on pollination by mitigating competition between pollinators.In 16 semi-natural grasslands, surrounded by agricultural landscapes, with a variation in both the proportion of oilseed rape and the proportion of semi-natural grassland within 1 km, we studied reproductive output in two species of potted plants with different pollination strategies: the woodland strawberry (Fragaria vesca) and red clover (Trifolium pratense). The first species is mainly pollinated by short-tongued pollinators, e.g. hoverflies and solitary bees, and the latter by long-tongued bumble bees. Both species flowered after oilseed rape.Strawberry weight was higher in landscapes with a high proportion of oilseed rape, but only in landscapes with a low proportion of semi-natural grassland. The proportion of developed achenes was also positively related to the proportion of oilseed rape, but only during the latest flowering period. In contrast, red clover seed set was unrelated to the proportion of oilseed rape. Whereas the discrepancy between the two strawberry measurements calls for further research, this study suggests that oilseed rape can affect later flowering plants and that the impact differs among species.     

Hoverflies (Diptera: Syrphidae) benefit from a cultivation of the bioenergy crop Silphium perfoliatum L. (Asteraceae) depending on larval feeding type,landscape composition and crop management

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Comparing existing weeds and commonly used insectary plants as floral resources for a parasitoid

The potential consequences of deploying weed and non-weed floral resources in a three trophic-level system were evaluated in the laboratory. Four flowering plants were used: the two common weeds shepherd’s purse Capsella bursa-pastoris (globally widespread) and white rocket Diplotaxis erucoides (a common weed in Europe) and two common flowering plants: buckwheat Fagopyrum esculentum and alyssum Lobularia maritima. Adults of the aphid parasitoid Diaeretiella rapae were exposed to flowering buckwheat and survived 4–5 times longer than those in the control (water only) and 2–3 times longer than when provided with flowering alyssum, or the other two species. All plant species significantly increased parasitoid longevity, egg load and achieved fecundity compared with the control, with buckwheat having the greatest effect. This work illustrates that the functional diversity of ‘weeds’, if appropriately managed, has potential to enhance biological control efficacy without the need for agronomic and other challenges which are involved in adding specific non-crop flowering plants such as buckwheat to agroecosystems. In the field, factors such as the plants’ phenology, agronomy and competitiveness with the crop will need to be evaluated before they can be truly ranked.     

Flowering banker plants for the delivery of multiple agroecosystem services

Ecosystem services provided by agricultural ecosystems include natural pest control and pollination, and these are important to ensure crop productivity. This study investigates the use of the banker plant Calendula officinalis L. to provide multiple ecosystem services by increasing the abundance of natural enemies for biological control of tomato pests, providing forage resources to wild bees, and improving crop yield. C. officinalis was selected for this experiment as it is used as a banker plant for Dicyphini (Hemiptera: Miridae) predators. Strips of flowering C. officinalis were established in the field edges of tomato fields and arthropod visitation to C. officinalis strips and tomato was measured. Crop damage from multiple pests of tomato was assessed in fields with C. officinalis strips and control sites. The contribution of pollination to crop yield was assessed through a pollinator exclusion experiment. The inclusion of C. officinalis in tomato fields was associated with increased abundance of Dicyphini, parasitoids, bees and other arthropod groups within these strips. A reduction in the total leaf crop damage from Lepidoptera pests was recorded in fields with C. officinalis strips. Increased fruit set and biomass were recorded in open-pollinated tomato but this was not significantly different between control and C. officinalis fields. Results presented here demonstrate that the inclusion of a companion plant can improve the conservation of beneficial arthropods and the delivery of agroecosystem services but efficacy is likely to be improved with the addition of plants, with different functional traits, and with improved attractiveness to crop pollinators.     

Effects of spontaneous field margin vegetation on the regulation of herbivores in two winter crops

Non-crop vegetation of field margins provides resources for natural enemies of crop herbivores. However, it is still not well known whether this resource provisioning effect is strong enough to improve herbivore regulation within crop fields and which plant species and functional groups favour this ecosystem service. A better understanding of the interactions between field margin vegetation and herbivore regulation is crucial to evaluate management strategies and to design suppressive plant mixtures. We surveyed 64 wheat and oilseed rape fields of Western France for two years (16 fields per year and crop) in order (1) to identify plant diversity or group effects on herbivore regulation within crop fields and (2) to identify species within plant groups that improve regulation. Herbivores, herbivore damage and natural enemies were monitored on crop plants at a distance of 5 and 50 m from the field margin. At the same time, the cover and phenological stage of all vascular plants were estimated in the adjacent field margin. The study demonstrated a positive relationship between the cover of entomophilous plant species that were flowering at the survey date and response variables related to herbivore regulation. Plant species richness and the cover of plant species taxonomically close to crop plants had a small influence on herbivores and natural enemies in wheat whereas related wild Brassicaceae increased herbivory and decreased herbivore regulation in oilseed rape. Within the entomophilous flowering plants, several species were significantly related to a better herbivore regulation in univariate analyses. Multivariate ordination techniques allowed the identification of plant species influencing several response variables of herbivore regulation at the same time. Our study demonstrated the importance of entomophilous species that flowered at peak infestation of crop herbivores. Spontaneous field margins rich in flowering entomophilous species provide an important ecosystem service without expensive sowing of seed mixtures.     

A multi-site experiment to test biocontrol effects of wildflower strips in different French climate zones

Sowing of wildflower strips has been integrated in agri-environment schemes of several European countries. Their beneficial effects on natural enemies of pest insects are well documented but (1) the desired spill-over into crop fields has not always been demonstrated, and (2) the need to adapt sown mixtures to regional climatic differences has been rarely addressed.We set up a multi-site experiment in different French climatic regions to compare effects of a wildflower strip with a grass mixture and spontaneous vegetation. The design included five regions, three to five fields per region and the three strip treatments being repeated in each field. We tested strip treatment effects on vegetation (plant species richness, plant and flower cover) and on natural enemies (hoverflies, ladybirds, aphid predation). In a subset, we further analysed the spill-over into winter wheat fields including natural enemies and pest insects (cereal aphids, leaf beetles).The wildflower strip mixture developed well in all regions and increased plant species richness and flower cover compared with grass strips and spontaneous vegetation. We found a corresponding higher hoverfly abundance and aphid predation in wildflower strips that were consistent in all regions, whereas ladybird abundance was not affected. A significantly higher hoverfly abundance, aphid predation and aphid parasitism in wheat fields close to wildflower strips indicated a spill-over. No corresponding margin treatment effects were observed for aphid and leaf beetle abundance in the field. A multivariate analysis comparing the influence of climate and vegetation parameters showed that floral cover better explained variation in natural enemy abundance and predation than climate. Our results demonstrated that similar mixtures of native plants can be used over large climatic gradients to improve biocontrol. Further research is needed to improve spill-over into crop fields and to obtain consistently strong effects in different climate zones.