Modeling the status, trends, and impacts of wild bee abundance in the United States.

Wild bees are highly valuable pollinators. Along with managed honey bees, they provide a critical ecosystem service by ensuring stable pollination to agriculture and wild plant communities. Increasing concern about the welfare of both wild and managed pollinators, however, has prompted recent calls for national evaluation and action. Here, for the first time to our knowledge, we assess the status and trends of wild bees and their potential impacts on pollination services across the coterminous United States. We use a spatial habitat model, national land-cover data, and carefully quantified expert knowledge to estimate wild bee abundance and associated uncertainty. Between 2008 and 2013, modeled bee abundance declined across 23% of US land area. This decline was generally associated with conversion of natural habitats to row crops. We identify 139 counties where low bee abundances correspond to large areas of pollinator-dependent crops. These areas of mismatch between supply (wild bee abundance) and demand (cultivated area) for pollination comprise 39% of the pollinator-dependent crop area in the United States. Further, we find that the crops most highly dependent on pollinators tend to experience more severe mismatches between declining supply and increasing demand. These trends, should they continue, may increase costs for US farmers and may even destabilize crop production over time. National assessments such as this can help focus both scientific and political efforts to understand and sustain wild bees. As new information becomes available, repeated assessments can update findings, revise priorities, and track progress toward sustainable management of our nation's pollinators.

A generalizable energetics-based model of avian migration to facilitate continental-scale waterbird conservation.

Conserving migratory birds is made especially difficult because of movement among spatially disparate locations across the annual cycle. In light of challenges presented by the scale and ecology of migratory birds, successful conservation requires integrating objectives, management, and monitoring across scales, from local management units to ecoregional and flyway administrative boundaries. We present an integrated approach using a spatially explicit energetic-based mechanistic bird migration model useful to conservation decision-making across disparate scales and locations. This model moves a Mallard-like bird (Anas platyrhynchos), through spring and fall migration as a function of caloric gains and losses across a continental-scale energy landscape. We predicted with this model that fall migration, where birds moved from breeding to wintering habitat, took a mean of 27.5 d of flight with a mean seasonal survivorship of 90.5% (95% Cl = 89.2%, 91.9%), whereas spring migration took a mean of 23.5 d of flight with mean seasonal survivorship of 93.6% (95% CI = 92.5%, 94.7%). Sensitivity analyses suggested that survival during migration was sensitive to flight speed, flight cost, the amount of energy the animal could carry, and the spatial pattern of energy availability, but generally insensitive to total energy availability per se. Nevertheless, continental patterns in the bird-use days occurred principally in relation to wetland cover and agricultural habitat in the fall. Bird-use days were highest in both spring and fall in the Mississippi Alluvial Valley and along the coast and near-shore environments of South Carolina. Spatial sensitivity analyses suggested that locations nearer to migratory endpoints were less important to survivorship; for instance, removing energy from a 1036 km2 stopover site at a time from the Atlantic Flyway suggested coastal areas between New Jersey and North Carolina, including the Chesapeake Bay and the North Carolina piedmont, are essential locations for efficient migration and increasing survivorship during spring migration but not locations in Ontario and Massachusetts. This sort of spatially explicit information may allow decision-makers to prioritize their conservation actions toward locations most influential to migratory success. Thus, this mechanistic model of avian migration provides a decision-analytic medium integrating the potential consequences of local actions to flyway-scale phenomena.

Modeling with uncertain science: estimating mitigation credits from abating lead poisoning in Golden Eagles.

Challenges arise when renewable energy development triggers "no net loss" policies for protected species, such as where wind energy facilities affect Golden Eagles in the western United States. When established mitigation approaches are insufficient to fully avoid or offset losses, conservation goals may still be achievable through experimental implementation of unproven mitigation methods provided they are analyzed within a framework that deals transparently and rigorously with uncertainty. We developed an approach to quantify and analyze compensatory mitigation that (1) relies on expert opinion elicited in a thoughtful and structured process to design the analysis (models) and supplement available data, (2) builds computational models as hypotheses about cause-effect relationships, (3) represents scientific uncertainty in stochastic model simulations, (4) provides probabilistic predictions of "relative" mortality with and without mitigation, (5) presents results in clear formats useful to applying risk management preferences (regulatory standards) and selecting strategies and levels of mitigation for immediate action, and (6) defines predictive parameters in units that could be monitored effectively, to support experimental adaptive management and reduction in uncertainty. We illustrate the approach with a case study characterized by high uncertainty about underlying biological processes and high conservation interest: estimating the quantitative effects of voluntary strategies to abate lead poisoning in Golden Eagles in Wyoming due to ingestion of spent game hunting ammunition.

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.

Mapping the margin: comparing marginal values of tropical forest remnants for pollination services.

Natural ecosystems benefit human communities by providing ecosystem services such as water purification and crop pollination. Mapping ecosystem service values has become popular, but most are static snapshots of average value. Estimating instead the economic impacts of specific ecosystem changes can better inform typical resource decisions. Here we develop an approach to mapping marginal values, those resulting from the next unit of ecosystem change, across landscapes. We demonstrate the approach with a recent model of crop pollination services in Costa Rica, simulating deforestation events to predict resulting marginal changes in pollination services to coffee farms. We find that marginal losses from deforestation vary from zero to US$700/ha across the landscape. Financial risks for farmers from these losses and marginal benefits of forest restoration show similar spatial variation. Marginal values are concentrated in relatively few forest parcels not identified using average value. These parcels lack substitutes: nearby forest parcels that can supply services in the event of loss. Indeed, the marginal value of forest parcels declines exponentially with the density of surrounding forest cover. The approach we develop is applicable to any ecosystem service. Combined with information on costs, it can help target conservation or restoration efforts to optimize benefits to people and biodiversity.

Marginal value analysis reveals shifting importance of migration habitat for waterfowl under a changing climate.

Migratory waterfowl are an important resource for consumptive and non-consumptive users alike and provide tremendous economic value in North America. These birds rely on a complex matrix of public and private land for forage and roosting during migration and wintering periods, and substantial conservation effort focuses on increasing the amount and quality of target habitat. Yet, the value of habitat is a function not only of a site's resources but also of its geographic position and weather. To quantify this value, we used a continental-scale energetics-based model of daily dabbling duck movement to assess the marginal value of lands across the contiguous United States during the non-breeding period (September to May). We examined effects of eliminating each habitat node (32 × 32 km) in both a particularly cold and a particularly warm winter, asking which nodes had the largest effect on survival. The marginal value of habitat nodes for migrating dabbling ducks was a function of forage and roosting habitat but, more importantly, of geography (especially latitude and region). Irrespective of weather, nodes in the Southeast, central East Coast, and California made the largest positive contributions to survival. Conversely, nodes in the Midwest, Northeast, Florida, and the Pacific Northwest had consistent negative effects. Effects (positive and negative) of more northerly nodes occurred in late fall or early spring when climate was often severe and was most variable. Importance and effects of many nodes varied considerably between a cold and a warm winter. Much of the Midwest and central Great Plains benefited duck survival in a warm winter, and projected future warming may improve the value of lands in these regions, including many National Wildlife Refuges, for migrating dabbling ducks. Our results highlight the geographic variability in habitat value, as well as shifts that may occur in these values due to climate change.

Effects of weather variation on waterfowl migration: Lessons from a continental-scale generalizable avian movement and energetics model.

We developed a continental energetics-based model of daily mallard (Anas platyrhynchos) movement during the non-breeding period (September to May) to predict year-specific migration and overwinter occurrence. The model approximates movements and stopovers as functions of metabolism and weather, in terms of temperature and frozen precipitation (i.e., snow). The model is a Markov process operating at the population level and is parameterized through a review of literature. We applied the model to 62 years of daily weather data for the non-breeding period. The average proportion of available habitat decreased as weather severity increased, with mortality decreasing as the proportion of available habitat increased. The most commonly used locations during the course of the non-breeding period were generally consistent across years, with the most inter-annual variation present in the overwintering area. Our model revealed that the distribution of mallards on the landscape changed more dramatically when the variation in daily available habitat was greater. The main routes for avian migration in North America were predicted by our simulations: the Atlantic, Mississippi, Central, and Pacific flyways. Our model predicted an average of 77.4% survivorship for the non-breeding period across all years (range = 76.4%-78.4%), with lowest survivorship during autumn (90.5 ± 1.4%), intermediate survivorship in winter (91.8 ± 0.7%), and greatest survivorship in spring (93.6 ± 1.1%). We provide the parameters necessary for exploration within and among other taxa to leverage the generalizability of this migration model to a broader expanse of bird species, and across a range of climate change and land use/land cover change scenarios.

Putting pesticides on the map for pollinator research and conservation.

Wild and managed pollinators are essential to food production and the function of natural ecosystems; however, their populations are threatened by multiple stressors including pesticide use. Because pollinator species can travel hundreds to thousands of meters to forage, recent research has stressed the importance of evaluating pollinator decline at the landscape scale. However, scientists' and conservationists' ability to do this has been limited by a lack of accessible data on pesticide use at relevant spatial scales and in toxicological units meaningful to pollinators. Here, we synthesize information from several large, publicly available datasets on pesticide use patterns, land use, and toxicity to generate novel datasets describing pesticide use by active ingredient (kg, 1997-2017) and aggregate insecticide load (kg and honey bee lethal doses, 1997-2014) for state-crop combinations in the contiguous U.S. Furthermore, by linking pesticide datasets with land-use data, we describe a method to map pesticide indicators at spatial scales relevant to pollinator research and conservation.

Efficiency of incentives to jointly increase carbon sequestration and species conservation on a landscape.

We develop an integrated model to predict private land-use decisions in response to policy incentives designed to increase the provision of carbon sequestration and species conservation across heterogeneous landscapes. Using data from the Willamette Basin, Oregon, we compare the provision of carbon sequestration and species conservation under five simple policies that offer payments for conservation. We evaluate policy performance compared with the maximum feasible combinations of carbon sequestration and species conservation on the landscape for various conservation budgets. None of the conservation payment policies produce increases in carbon sequestration and species conservation that approach the maximum potential gains on the landscape. Our results show that policies aimed at increasing the provision of carbon sequestration do not necessarily increase species conservation and that highly targeted policies do not necessarily do as well as more general policies.

Adaptive management in the U.S. National Wildlife Refuge System: science-management partnerships for conservation delivery.

Adaptive management is an approach to recurrent decision making in which uncertainty about the decision is reduced over time through comparison of outcomes predicted by competing models against observed values of those outcomes. The National Wildlife Refuge System (NWRS) of the U.S. Fish and Wildlife Service is a large land management program charged with making natural resource management decisions, which often are made under considerable uncertainty, severe operational constraints, and conditions that limit ability to precisely carry out actions as intended. The NWRS presents outstanding opportunities for the application of adaptive management, but also difficult challenges. We describe two cooperative programs between the Fish and Wildlife Service and the U.S. Geological Survey to implement adaptive management at scales ranging from small, single refuge applications to large, multi-refuge, multi-region projects. Our experience to date suggests three important attributes common to successful implementation: a vigorous multi-partner collaboration, practical and informative decision framework components, and a sustained commitment to the process. Administrators in both agencies should consider these attributes when developing programs to promote the use and acceptance of adaptive management in the NWRS.

County-level analysis reveals a rapidly shifting landscape of insecticide hazard to honey bees (Apis mellifera) on US farmland.

Each year, millions of kilograms of insecticides are applied to crops in the US. While insecticide use supports food, fuel, and fiber production, it can also threaten non-target organisms, a concern underscored by mounting evidence of widespread decline of pollinator populations. Here, we integrate several public datasets to generate county-level annual estimates of total 'bee toxic load' (honey bee lethal doses) for insecticides applied in the US between 1997-2012, calculated separately for oral and contact toxicity. To explore the underlying components of the observed changes, we divide bee toxic load into extent (area treated) and intensity (application rate x potency). We show that while contact-based bee toxic load remained relatively steady, oral-based bee toxic load increased roughly 9-fold, with reductions in application rate outweighed by disproportionate increases in potency (toxicity/kg) and extent. This pattern varied markedly by region, with the greatest increase seen in Heartland (121-fold increase), likely driven by use of neonicotinoid seed treatments in corn and soybean. In this "potency paradox", farmland in the central US has become more hazardous to bees despite lower volumes of insecticides applied, raising concerns about insect conservation and highlighting the importance of integrative approaches to pesticide use monitoring.

Local adaptation and rapid evolution of aphids in response to genetic interactions with their cottonwood hosts.

Several studies have demonstrated the ecological consequences of genetic variation within a single plant species. For example, these studies show that individual plant genotypes support unique composition of the plants' associated arthropod community. By contrast, fewer studies have explored how plant genetic variation may influence evolutionary dynamics in the plant's associated species. Here, we examine how aphids respond evolutionarily to genetic variation in their host plant. We conducted two experiments to examine local adaptation and rapid evolution of the free-feeding aphid Chaitophorus populicola across genetic variants of its host plant, Populus angustifolia. To test for local adaptation, we collected tree cuttings and aphid colonies from three sites along an elevation/climate gradient and conducted a reciprocal transplant experiment. In general, home aphids (aphids transplanted onto trees from the same site) produced 1.7-3.4 times as many offspring as foreign aphids (aphids transplanted onto trees from different sites). To test for rapid evolution, we used 4 clonally replicated aphid genotypes and transplanted each onto 5 clonally replicated P. angustifolia genotypes. Each tree genotype started with the same aphid genotype composition. After 21 days (~two aphid generations), aphid genotype composition changed (i.e., aphids evolved) and some tree genotypes supported unique evolutionary trajectories of aphids. These results suggest that plant evolution in response to human perturbation, such as climate change and invasive species, will also result in evolutionary responses in strongly interacting species that could cascade to affect whole communities.

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 model's 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.

Pesticides and pollinators: A socioecological synthesis.

The relationship between pesticides and pollinators, while attracting no shortage of attention from scientists, regulators, and the public, has proven resistant to scientific synthesis and fractious in matters of policy and public opinion. This is in part because the issue has been approached in a compartmentalized and intradisciplinary way, such that evaluations of organismal pesticide effects remain largely disjoint from their upstream drivers and downstream consequences. Here, we present a socioecological framework designed to synthesize the pesticide-pollinator system and inform future scholarship and action. Our framework consists of three interlocking domains-pesticide use, pesticide exposure, and pesticide effects-each consisting of causally linked patterns, processes, and states. We elaborate each of these domains and their linkages, reviewing relevant literature and providing empirical case studies. We then propose guidelines for future pesticide-pollinator scholarship and action agenda aimed at strengthening knowledge in neglected domains and integrating knowledge across domains to provide decision support for stakeholders and policymakers. Specifically, we emphasize (1) stakeholder engagement, (2) mechanistic study of pesticide exposure, (3) understanding the propagation of pesticide effects across levels of organization, and (4) full-cost accounting of the externalities of pesticide use and regulation. Addressing these items will require transdisciplinary collaborations within and beyond the scientific community, including the expertise of farmers, agrochemical developers, and policymakers in an extended peer community.

Plant-soil microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms.

Although soil microbial communities are known to play crucial roles in the cycling of nutrients in forest ecosystems and can vary by plant species, how microorganisms respond to the subtle gradients of plant genetic variation is just beginning to be appreciated. Using a model Populus system in a common garden with replicated clones of known genotypes, we evaluated microbial biomass and community composition as quantitative traits. Two main patterns emerged. (1) Plant genotype influenced microbial biomass nitrogen in soils under replicated genotypes of Populus angustifolia, F1, and backcross hybrids, but not P. fremontii. Genotype explained up to 78% of the variation in microbial biomass as indicated by broad-sense heritability estimates (i.e., clonal repeatability). A second estimate of microbial biomass (total phospholipid fatty acid) was more conservative and showed significant genotype effects in P. angustifolia and backcross hybrids. (2) Plant genotype significantly influenced microbial community composition, explaining up to 70% of the variation in community composition within P. angustifolia genotypes alone. These findings suggest that variation in above- and belowground traits of individual plant genotypes can alter soil microbial dynamics, and suggests that further investigations of the evolutionary implications of genetic feedbacks are warranted.

Ecology and Economics of Using Native Managed Bees for Almond Pollination.

Native managed bees can improve crop pollination, but a general framework for evaluating the associated economic costs and benefits has not been developed. We conducted a cost-benefit analysis to assess how managing blue orchard bees (Osmia lignaria Say [Hymenoptera: Megachildae]) alongside honey bees (Apis mellifera Linnaeus [Hymenoptera: Apidae]) can affect profits for almond growers in California. Specifically, we studied how adjusting three strategies can influence profits: (1) number of released O. lignaria bees, (2) density of artificial nest boxes, and (3) number of nest cavities (tubes) per box. We developed an ecological model for the effects of pollinator activity on almond yields, validated the model with published data, and then estimated changes in profits for different management strategies. Our model shows that almond yields increase with O. lignaria foraging density, even where honey bees are already in use. Our cost-benefit analysis shows that profit ranged from -US$1,800 to US$2,800/acre given different combinations of the three strategies. Adding nest boxes had the greatest effect; we predict an increase in profit between low and high nest box density strategies (2.5 and 10 boxes/acre). In fact, the number of released bees and the availability of nest tubes had relatively small effects in the high nest box density strategies. This suggests that growers could improve profits by simply adding more nest boxes with moderate number of tubes in each. Our approach can support grower decisions regarding integrated crop pollination and highlight the importance of a comprehensive ecological economic framework for assessing these decisions.

Patch aging and the S-Allee effect: breeding system effects on the demographic response of plants to habitat fragmentation.

We used empirical and modeling approaches to examine effects of plant breeding systems on demographic responses to habitat fragmentation. Empirically, we investigated effects of local flowering plant density on pollination and of population size on mate availability in a common, self-incompatible purple coneflower, Echinacea angustifolia, growing in fragmented prairie habitat. Pollination and recruitment increased with weighted local density around individual flowering plants. This positive density dependence is an Allee effect. In addition, mean mate compatibility between pairs of plants increased with population size. Based on this empirical study, we developed an individual-based, spatially explicit demographic model that incorporates autosomal loci and an S locus. We simulated habitat fragmentation in populations identical except for their breeding system, self-incompatible (SI) or self-compatible (SC). Both populations suffered reduced reproduction in small patches because of scarcity of plants within pollination distance (potential mates) and inbreeding depression. But SI species experienced an additional, genetic contribution to the Allee effect (S-Allee effect) caused by allele loss at the S locus, which reduces mate availability, thereby decreasing reproduction. The strength of the S-Allee effect increases through time (i.e., patches age) because random genetic drift reduces S-allele richness. We investigate how patch aging influences extinction and discuss how the S-Allee effect influences communities in fragmented habitat.

Do capuchin monkeys (Sapajus apella) prefer symmetrical face shapes?

In humans, facial symmetry has been linked to an individual's genetic quality, and facial symmetry has a small yet significant effect on ratings of facial attractiveness. The same evolutionary processes underlying these phenomena may also convey a selective advantage to symmetrical individuals of other primate species, yet to date, few studies have examined sensitivity to facial symmetry in nonhuman primates. Here we presented images of symmetrical and asymmetrical human and monkey faces to tufted capuchin monkeys (Sapajus apella) and hypothesized that capuchins would visually prefer symmetrical faces of opposite-sex conspecifics. Instead, we found that male capuchins preferentially attended to symmetrical male conspecific faces, whereas female capuchins did not appear to discriminate between symmetrical and asymmetrical faces. These results suggest that male capuchin monkeys may use facial symmetry to judge male quality in intramale competition. (PsycINFO Database Record

Strategic Grassland Bird Conservation throughout the Annual Cycle: Linking Policy Alternatives, Landowner Decisions, and Biological Population Outcomes.

Grassland bird habitat has declined substantially in the United States. Remaining grasslands are increasingly fragmented, mostly privately owned, and vary greatly in terms of habitat quality and protection status. A coordinated strategic response for grassland bird conservation is difficult, largely due to the scope and complexity of the problem, further compounded by biological, sociological, and economic uncertainties. We describe the results from a collaborative Structured Decision Making (SDM) workshop focused on linking social and economic drivers of landscape change to grassland bird population outcomes. We identified and evaluated alternative strategies for grassland bird conservation using a series of rapid prototype models. We modeled change in grassland and agriculture cover in hypothetical landscapes resulting from different landowner decisions in response to alternative socio-economic conservation policy decisions. Resulting changes in land cover at all three stages of the annual cycle (breeding, wintering, and migration) were used to estimate changes in grassland bird populations. Our results suggest that successful grassland bird conservation may depend upon linkages with ecosystem services on working agricultural lands and grassland-based marketing campaigns to engage the public. With further development, spatial models that link landowner decisions with biological outcomes can be essential tools for making conservation policy decisions. A coordinated non-traditional partnership will likely be necessary to clearly understand and systematically respond to the many conservation challenges facing grassland birds.