Rachael Winfree

Stability of pollination services decreases with isolation from natural areas despite honey bee visits

Sustainable agricultural landscapes by definition provide high magnitude and stability of ecosystem services, biodiversity and crop productivity. However, few studies have considered landscape effects on the stability of ecosystem services. We tested whether isolation from florally diverse natural and semi-natural areas reduces the spatial and temporal stability of flower-visitor richness and pollination services in crop fields. We synthesised data from 29 studies with contrasting biomes, crop species and pollinator communities. Stability of flower-visitor richness, visitation rate (all insects except honey bees) and fruit set all decreased with distance from natural areas. At 1 km from adjacent natural areas, spatial stability decreased by 25, 16 and 9% for richness, visitation and fruit set, respectively, while temporal stability decreased by 39% for richness and 13% for visitation. Mean richness, visitation and fruit set also decreased with isolation, by 34, 27 and 16% at 1 km respectively. In contrast, honey bee visitation did not change with isolation and represented > 25% of crop visits in 21 studies. Therefore, wild pollinators are relevant for crop productivity and stability even when honey bees are abundant. Policies to preserve and restore natural areas in agricultural landscapes should enhance levels and reliability of pollination services.

A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems

Bees provide essential pollination services that are potentially affected both by local farm management and the surrounding landscape. To better understand these different factors, we modelled the relative effects of landscape composition (nesting and floral resources within foraging distances), landscape configuration (patch shape, interpatch connectivity and habitat aggregation) and farm management (organic vs. conventional and local-scale field diversity), and their interactions, on wild bee abundance and richness for 39 crop systems globally. Bee abundance and richness were higher in diversified and organic fields and in landscapes comprising more high-quality habitats; bee richness on conventional fields with low diversity benefited most from high-quality surrounding land cover. Landscape configuration effects were weak. Bee responses varied slightly by biome. Our synthesis reveals that pollinator persistence will depend on both the maintenance of high-quality habitats around farms and on local management practices that may offset impacts of intensive monoculture agriculture.

Delivery of crop pollination services is an insufficient argument for wild pollinator conservation

There is compelling evidence that more diverse ecosystems deliver greater benefits to people, and these ecosystem services have become a key argument for biodiversity conservation. However, it is unclear how much biodiversity is needed to deliver ecosystem services in a cost-effective way. Here we show that, while the contribution of wild bees to crop production is significant, service delivery is restricted to a limited subset of all known bee species. Across crops, years and biogeographical regions, crop-visiting wild bee communities are dominated by a small number of common species, and threatened species are rarely observed on crops. Dominant crop pollinators persist under agricultural expansion and many are easily enhanced by simple conservation measures, suggesting that cost-effective management strategies to promote crop pollination should target a different set of species than management strategies to promote threatened bees. Conserving the biological diversity of bees therefore requires more than just ecosystem-service-based arguments.

Modelling pollination services across agricultural landscapes

BACKGROUND AND AIMS Crop pollination by bees and other animals is an essential ecosystem service. Ensuring the maintenance of the service requires a full understanding of the contributions of landscape elements to pollinator populations and crop pollination. Here, the first quantitative model that predicts pollinator abundance on a landscape is described and tested. METHODS Using information on pollinator nesting resources, floral resources and foraging distances, the model predicts the relative abundance of pollinators within nesting habitats. From these nesting areas, it then predicts relative abundances of pollinators on the farms requiring pollination services. Model outputs are compared with data from coffee in Costa Rica, watermelon and sunflower in California and watermelon in New Jersey-Pennsylvania (NJPA). KEY RESULTS Results from Costa Rica and California, comparing field estimates of pollinator abundance, richness or services with model estimates, are encouraging, explaining up to 80 % of variance among farms. However, the model did not predict observed pollinator abundances on NJPA, so continued model improvement and testing are necessary. The inability of the model to predict pollinator abundances in the NJPA landscape may be due to not accounting for fine-scale floral and nesting resources within the landscapes surrounding farms, rather than the logic of our model. CONCLUSIONS The importance of fine-scale resources for pollinator service delivery was supported by sensitivity analyses indicating that the models predictions depend largely on estimates of nesting and floral resources within crops. Despite the need for more research at the finer-scale, the approach fills an important gap by providing quantitative and mechanistic model from which to evaluate policy decisions and develop land-use plans that promote pollination conservation and service delivery.

Climate-associated phenological advances in bee pollinators and bee-pollinated plants

The phenology of many ecological processes is modulated by temperature, making them potentially sensitive to climate change. Mutualistic interactions may be especially vulnerable because of the potential for phenological mismatching if the species involved do not respond similarly to changes in temperature. Here we present an analysis of climate-associated shifts in the phenology of wild bees, the most important pollinators worldwide, and compare these shifts to published studies of bee-pollinated plants over the same time period. We report that over the past 130 y, the phenology of 10 bee species from northeastern North America has advanced by a mean of 10.4 ± 1.3 d. Most of this advance has taken place since 1970, paralleling global temperature increases. When the best available data are used to estimate analogous rates of advance for plants, these rates are not distinguishable from those of bees, suggesting that bee emergence is keeping pace with shifts in host-plant flowering, at least among the generalist species that we investigated.

Historical changes in northeastern US bee pollinators related to shared ecological traits.

Pollinators such as bees are essential to the functioning of terrestrial ecosystems. However, despite concerns about a global pollinator crisis, long-term data on the status of bee species are limited. We present a long-term study of relative rates of change for an entire regional bee fauna in the northeastern United States, based on >30,000 museum records representing 438 species. Over a 140-y period, aggregate native species richness weakly decreased, but richness declines were significant only for the genus Bombus. Of 187 native species analyzed individually, only three declined steeply, all of these in the genus Bombus. However, there were large shifts in community composition, as indicated by 56% of species showing significant changes in relative abundance over time. Traits associated with a declining relative abundance include small dietary and phenological breadth and large body size. In addition, species with lower latitudinal range boundaries are increasing in relative abundance, a finding that may represent a response to climate change. We show that despite marked increases in human population density and large changes in anthropogenic land use, aggregate native species richness declines were modest outside of the genus Bombus. At the same time, we find that certain ecological traits are associated with declines in relative abundance. These results should help target conservation efforts focused on maintaining native bee abundance and diversity and therefore the important ecosystems services that they provide.

Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms

Ecological restoration of plant-pollinator interactions has received surprisingly little attention, despite animal-mediated pollination underpinning reproduction of the majority of higher plants. Here, we offer a conceptual and practical framework for the ecological restoration of pollination mutualisms. Through the use of targeted restoration plantings to attract and sustain pollinators and increased knowledge of the ecological requirements of pollinators, we propose that pollination could be successfully restored in degraded ecosystems. The challenge for pollination biologists is to integrate their findings with those of plant restoration ecologists to ensure sustainable pollination in restored ecosystems.

Abundance of common species, not species richness, drives delivery of a real‐world ecosystem service

Biodiversity-ecosystem functioning experiments have established that species richness and composition are both important determinants of ecosystem function in an experimental context. Determining whether this result holds for real-world ecosystem services has remained elusive, however, largely due to the lack of analytical methods appropriate for large-scale, associational data. Here, we use a novel analytical approach, the Price equation, to partition the contribution to ecosystem services made by species richness, composition and abundance in four large-scale data sets on crop pollination by native bees. We found that abundance fluctuations of dominant species drove ecosystem service delivery, whereas richness changes were relatively unimportant because they primarily involved rare species that contributed little to function. Thus, the mechanism behind our results was the skewed species-abundance distribution. Our finding that a few common species, not species richness, drive ecosystem service delivery could have broad generality given the ubiquity of skewed species-abundance distributions in nature.

The conservation and restoration of wild bees

Bees pollinate most of the worlds wild plant species and provide economically valuable pollination services to crops; yet knowledge of bee conservation biology lags far behind other taxa such as vertebrates and plants. There are few long‐term data on bee populations, which makes their conservation status difficult to assess. The best‐studied groups are the genus Bombus (the bumble bees), and bees in the EU generally; both of these are clearly declining. However, it is not known to what extent these groups represent the approximately 20,000 species of bees globally. As is the case for insects in general, bees are underrepresented in conservation planning and protection efforts. For example, only two bee species are on the global IUCN Red List, and no bee is listed under the U.S. Endangered Species Act, even though many bee species are known to be in steep decline or possibly extinct. At present, bee restoration occurs mainly in agricultural contexts, funded by government programs such as agri‐environment schemes (EU) and the Farm Bill (USA). This is a promising approach given that many bee species can use human‐disturbed habitats, and bees provide valuable pollination services to crops. However, agricultural restorations only benefit species that persist in agricultural landscapes, and they are more expensive than preserving natural habitat elsewhere. Furthermore, such restorations benefit bees in only about half of studied cases. More research is greatly needed in many areas of bee conservation, including basic population biology, bee restoration in nonagricultural contexts, and the identification of disturbance‐sensitive bee species.

Non-bee insects are important contributors to global crop pollination

Significance Many of the world’s crops are pollinated by insects, and bees are often assumed to be the most important pollinators. To our knowledge, our study is the first quantitative evaluation of the relative contribution of non-bee pollinators to global pollinator-dependent crops. Across 39 studies we show that insects other than bees are efficient pollinators providing 39% of visits to crop flowers. A shift in perspective from a bee-only focus is needed for assessments of crop pollinator biodiversity and the economic value of pollination. These studies should also consider the services provided by other types of insects, such as flies, wasps, beetles, and butterflies—important pollinators that are currently overlooked. Wild and managed bees are well documented as effective pollinators of global crops of economic importance. However, the contributions by pollinators other than bees have been little explored despite their potential to contribute to crop production and stability in the face of environmental change. Non-bee pollinators include flies, beetles, moths, butterflies, wasps, ants, birds, and bats, among others. Here we focus on non-bee insects and synthesize 39 field studies from five continents that directly measured the crop pollination services provided by non-bees, honey bees, and other bees to compare the relative contributions of these taxa. Non-bees performed 25–50% of the total number of flower visits. Although non-bees were less effective pollinators than bees per flower visit, they made more visits; thus these two factors compensated for each other, resulting in pollination services rendered by non-bees that were similar to those provided by bees. In the subset of studies that measured fruit set, fruit set increased with non-bee insect visits independently of bee visitation rates, indicating that non-bee insects provide a unique benefit that is not provided by bees. We also show that non-bee insects are not as reliant as bees on the presence of remnant natural or seminatural habitat in the surrounding landscape. These results strongly suggest that non-bee insect pollinators play a significant role in global crop production and respond differently than bees to landscape structure, probably making their crop pollination services more robust to changes in land use. Non-bee insects provide a valuable service and provide potential insurance against bee population declines.