Theoretical and simulation studies predict that the order of species loss from mutualist networks with respect to how linked species are to other species within the network will determine the rate at which networks collapse. However, the empirical order of species loss with respect to linkage has rarely been investigated. Furthermore, a species' linkage is a composite of its diet breadth and its abundance, yet the relative importance of these two factors in determining species loss order is poorly known. Here we explore the order of pollinator species loss in two contrasting study systems undergoing land-use intensification, using >20,000 pollinator specimens. We found that a pollinator species' linkage, as measured independently within plant-pollinator networks, positively predicted its persistence at human-disturbed sites in three of four analyses. The strongest predictor of persistence in all analyses was pollinator species abundance. In contrast, diet breadth poorly predicted persistence. Overall, our results suggest that community disassembly order buffers plant-pollinator networks against environmental change by retaining the highly linked species that make a disproportionate contribution to network robustness. Furthermore, these highly linked species likely persist because they are also the most common species, not because they are dietary generalists.
Bacterial gut symbiont communities are critical for the health of many insect species. However, little is known about how microbial communities vary among host species or how they respond to anthropogenic disturbances. Bacterial communities that differ in richness or composition may vary in their ability to provide nutrients or defenses. We used deep sequencing to investigate gut microbiota of three species in the genus Bombus (bumble bees). Bombus are among the most economically and ecologically important non-managed pollinators. Some species have experienced dramatic declines, probably due to pathogens and land-use change. We examined variation within and across bee species and between semi-natural and conventional agricultural habitats. We categorized as 'core bacteria' any operational taxonomic units (OTUs) with closest hits to sequences previously found exclusively or primarily in the guts of honey bees and bumble bees (genera Apis and Bombus). Microbial community composition differed among bee species. Richness, defined as number of bacterial OTUs, was highest for B. bimaculatus and B. impatiens. For B. bimaculatus, this was due to high richness of non-core bacteria. We found little effect of habitat on microbial communities. Richness of non-core bacteria was negatively associated with bacterial abundance in individual bees, possibly due to deeper sampling of non-core bacteria in bees with low populations of core bacteria. Infection by the gut parasite Crithidia was negatively associated with abundance of the core bacterium Gilliamella and positively associated with richness of non-core bacteria. Our results indicate that Bombus species have distinctive gut communities, and community-level variation is associated with pathogen infection.
Climate change has the potential to alter the phenological synchrony between interacting mutualists, such as plants and their pollinators. However, high levels of biodiversity might buffer the negative effects of species-specific phenological shifts and maintain synchrony at the community level, as predicted by the biodiversity insurance hypothesis. Here, we explore how biodiversity might enhance and stabilise phenological synchrony between a valuable crop, apple and its native pollinators. We combine 46 years of data on apple flowering phenology with historical records of bee pollinators over the same period. When the key apple pollinators are considered altogether, we found extensive synchrony between bee activity and apple peak bloom due to complementarity among bee species activity periods, and also a stable trend over time due to differential responses to warming climate among bee species. A simulation model confirms that high biodiversity levels can ensure plant-pollinator phenological synchrony and thus pollination function.
If climate change affects pollinator-dependent crop production, this will have important implications for global food security because insect pollinators contribute to production for 75% of the leading global food crops. We investigate whether climate warming could result in indirect impacts upon crop pollination services via an overlooked mechanism, namely temperature-induced shifts in the diurnal activity patterns of pollinators. Using a large data set on bee pollination of watermelon crops, we predict how pollination services might change under various climate change scenarios. Our results show that under the most extreme IPCC scenario (A1F1), pollination services by managed honey bees are expected to decline by 14.5%, whereas pollination services provided by most native, wild taxa are predicted to increase, resulting in an estimated aggregate change in pollination services of +4.5% by 2099. We demonstrate the importance of native biodiversity in buffering the impacts of climate change, because crop pollination services would decline more steeply without the native, wild pollinators. More generally, our study provides an important example of how biodiversity can stabilize ecosystem services against environmental change.
More diverse biological communities may provide ecosystem services that are less variable over space or time. However, the mechanisms underlying this relationship are rarely investigated empirically in real-world ecosystems. Here, we investigate how a potentially important stabilising mechanism, response diversity, the differential response to environmental change among species, stabilises pollination services against land-use change. We measured crop pollination services provided by native bees across land-use gradients in three crop systems. We found that bee species responded differentially to increasing agricultural land cover in all three systems, demonstrating that response diversity occurs. Similarly, we found response diversity in pollination services in two of the systems. However, there was no evidence that response diversity, in general, stabilised ecosystem services. Our results suggest that either response diversity is not the primary stabilising mechanism in our system, or that new measures of response diversity are needed that better capture the stabilising effects it provides.
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.
The diversity and abundance of wild insect pollinators have declined in many agricultural landscapes. Whether such declines reduce crop yields, or are mitigated by managed pollinators such as honey bees, is unclear. We found universally positive associations of fruit set with flower visitation by wild insects in 41 crop systems worldwide. In contrast, fruit set increased significantly with flower visitation by honey bees in only 14% of the systems surveyed. Overall, wild insects pollinated crops more effectively; an increase in wild insect visitation enhanced fruit set by twice as much as an equivalent increase in honey bee visitation. Visitation by wild insects and honey bees promoted fruit set independently, so pollination by managed honey bees supplemented, rather than substituted for, pollination by wild insects. Our results suggest that new practices for integrated management of both honey bees and diverse wild insect assemblages will enhance global crop yields.
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.
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.
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.
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.
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.
Pollinators may be declining globally, a matter of concern because animal pollination is required by most of the worlds plant species, including many crop plants. Human land use and the loss of native habitats is thought to be an important driver of decline for wild, native pollinators, yet the findings of published studies on this topic have never been quantitatively synthesized. Here we use meta-analysis to synthesize the literature on how bees, the most important group of pollinators, are affected by human disturbances such as habitat loss, grazing, logging, and agriculture. We obtained 130 effect sizes from 54 published studies recording bee abundance and/or species richness as a function of human disturbance. Both bee abundance and species richness were significantly, negatively affected by disturbance. However, the magnitude of the effects was not large. Furthermore, the only disturbance type showing a significant negative effect, habitat loss and fragmentation, was statistically significant only in systems where very little natural habitat remains. Therefore, it would be premature to draw conclusions about habitat loss having caused global pollinator decline without first assessing the extent to which the existing studies represent the status of global ecosystems. Future pollinator declines seem likely given forecasts of increasing land-use change.
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.
Biological diversity could enhance ecosystem service provision by increasing the mean level of services provided, and/or by providing more consistent (stable) services over space and time. Ecological theory predicts that when an ecosystem service is provided by many species, it will be stabilized against disturbance by a variety of stabilizing mechanisms. However, few studies have investigated whether stabilizing mechanisms occur in real landscapes affected by human disturbance. We used two datasets on crop pollination by wild native bees to screen for and differentiate among three stabilizing mechanisms: density compensation (negative co-variance among species abundances); response diversity (differential response to environmental variables among species); and cross-scale resilience (response to the same environmental variable at different scales by different species). In both datasets, we found response diversity and cross-scale resilience, but not density compensation. We conclude that stabilizing mechanisms may contribute to the stability of pollination services in our study areas, emphasizing the insurance value of seemingly redundant species. Furthermore, the absence of density compensation that we found at the landscape scale contrasts with findings of previous small-scale experimental and modelling work, suggesting that we should not assume that density compensation will stabilize ecosystem services in real landscapes.
Human activity causes abrupt changes in resource availability across the landscape. In order to persist in human-altered landscapes organisms need to shift their habitat use accordingly. Little is known about the mechanisms by which whole communities persist in human-altered landscapes, including the role of complementary habitat use. We define complementary habitat use as the use of different habitats at different times by the same group of species during the course of their activity period. We hypothesize that complementary habitat use is a mechanism through which native bee species persist in human-altered landscapes. To test this idea, we studied wild bee communities in agro-natural landscapes and explored their community-level patterns of habitat and resource use over space and time. The study was conducted in six agro-natural landscapes in the eastern United States, each containing three main bee habitat types (natural habitat, agricultural fields, and old fields). Each of the three habitats exhibited a unique seasonal pattern in amount, diversity, and composition of floral resources, and together they created phenological complementarity in foraging resources for bees. Individual bee species as well as the bee community responded to these spatiotemporal patterns in floral availability and exhibited a parallel pattern of complementary habitat use. The majority of wild bee species, including all the main crop visitors, used fallow areas within crops early in the season, shifted to crops in mid-season, and used old-field habitats later in the season. The natural-forest habitat supported very limited number of bees, mostly visitors of non-crop plants. Old fields are thus an important feature in these arable landscapes for maintaining crop pollination services. Our study provides a detailed examination of how shifts in habitat and resource use may enable bees to persist in highly dynamic agro-natural landscapes, and points to the need for a broad cross-habitat perspective in managing these landscapes.
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