A test of balanced fitness limitations theory: Pollen limitation in plants.

When reproductive success is determined by the relative availabilities of a series of essential, non-substitutable resources, the theory of balanced fitness limitations predicts that the cost of harvesting a particular resource shapes the likelihood that a shortfall of that resource will constrain realized fitness. Plant reproduction through female function offers a special opportunity to test this theory; essential resources in this context include, first, the pollen received from pollinators or abiotic vectors that is used to fertilize ovules, and, second, the resources needed to provision the developing seeds and fruit. For many plants realized reproductive success through female function can be readily quantified in the field, and one key potential constraint on fitness, pollen limitation, can be assessed experimentally by manually supplementing pollen receipt. We assembled a comparative dataset of pollen limitation using only studies that supplement pollen to all flowers produced over the plant's reproductive lifespan. Pre- and post-pollination costs were estimated using the weight of flowers and fruits and estimates of fruit set. Consistent with expectations, we find self-incompatible plants make greater pre-pollination investments and experience greater pollen limitation. However, contrary to theoretical expectations, when variation due to self-compatibility is accounted for by including self-compatibility in the statistical model as a covariate, we find no support for the prediction that plants that invest more heavily in pre-pollination costs are subject to greater pollen limitation. Strong within-species, between-population variation in the expression of pollen limitation makes the quantification of mean pollen limitation difficult. We urge plant ecologists to conduct more studies of pollen limitation using whole-plant pollen supplementation to produce a richer comparative dataset that would support a more robust test of the balanced limitations hypothesis.

Wildflower plantings enhance nesting opportunities for soil-nesting bees.

Ongoing declines of bees and other pollinators are driven in part by the loss of critical floral resources and nesting substrates. Most conservation/restoration efforts for bees aim to enhance floral abundance and continuity but often assume the same actions will bolster nesting opportunities. Recent research suggests that habitat plantings may not always provide both forage and nesting resources. We evaluated wildflower plantings designed to augment floral resources to determine their ability to enhance nesting by soil-nesting bees over 3 study years in Northern California agricultural landscapes. We established wildflower plantings along borders of annual row crops and paired each with an unplanted control border. We used soil emergence traps to assess nest densities and species richness of soil-nesting bees from spring through late summer at paired field borders planted with wildflowers or maintained conventionally as bare or sparsely vegetated areas, as is typical for the region. We also quantified soil-surface characteristics and flower resources among borders. Wildflower plantings significantly increased nest densities and the richness of bee species using them. Such benefits occurred within the first year of planting and persisted up to 4 years post establishment. The composition of nesting bee communities also differed between wildflower and unenhanced borders. Wildflower plantings differed from controls in multiple characteristics of the soil surface, including vegetation cover, surface microtopography and hardness. Surprisingly, only vegetation cover significantly affected nest densities and species richness. Wildflower plantings are a widespread habitat action with the potential to support wild bees. The demonstrated benefit wildflower plantings had for increasing the nesting of soil-nesting bees greatly augments their relevance for the conservation of wild bee communities in agricultural and other landscapes. Identifying soil-surface characteristics that are important for nesting provides critical information to guide the implementation and management of habitats for bees.

Evidence of exploitative competition between honey bees and native bees in two California landscapes.

Human-mediated species introductions provide real-time experiments in how communities respond to interspecific competition. For example, managed honey bees Apis mellifera (L.) have been widely introduced outside their native range and may compete with native bees for pollen and nectar. Indeed, multiple studies suggest that honey bees and native bees overlap in their use of floral resources. However, for resource overlap to negatively impact resource collection by native bees, resource availability must also decline, and few studies investigate impacts of honey bee competition on native bee floral visits and floral resource availability simultaneously. In this study, we investigate impacts of increasing honey bee abundance on native bee visitation patterns, pollen diets, and nectar and pollen resource availability in two Californian landscapes: wildflower plantings in the Central Valley and montane meadows in the Sierra. We collected data on bee visits to flowers, pollen and nectar availability, and pollen carried on bee bodies across multiple sites in the Sierra and Central Valley. We then constructed plant-pollinator visitation networks to assess how increasing honey bee abundance impacted perceived apparent competition (PAC), a measure of niche overlap, and pollinator specialization (d'). We also compared PAC values against null expectations to address whether observed changes in niche overlap were greater or less than what we would expect given the relative abundances of interacting partners. We find clear evidence of exploitative competition in both ecosystems based on the following results: (1) honey bee competition increased niche overlap between honey bees and native bees, (2) increased honey bee abundance led to decreased pollen and nectar availability in flowers, and (3) native bee communities responded to competition by shifting their floral visits, with some becoming more specialized and others becoming more generalized depending on the ecosystem and bee taxon considered. Although native bees can adapt to honey bee competition by shifting their floral visits, the coexistence of honey bees and native bees is tenuous and will depend on floral resource availability. Preserving and augmenting floral resources is therefore essential in mitigating negative impacts of honey bee competition. In two California ecosystems, honey bee competition decreases pollen and nectar resource availability in flowers and alters native bee diets with potential implications for bee conservation and wildlands management.

Sublethal behavioral impacts of resource limitation and insecticide exposure reinforce negative fitness outcomes for a solitary bee.

Contemporary landscapes present numerous challenges for bees and other beneficial insects that play critical functional roles in natural ecosystems and agriculture. Pesticides and the loss of food resources from flowering plants are two stressors known to act together to impair bee fitness. The impact of these stressors on key behaviors like foraging and nesting can limit pollination services and population persistence, making it critical to understand these sublethal effects. We investigated the effects of insecticide exposure and floral resource limitation on the foraging and nesting behavior of the solitary blue orchard bee, Osmia lignaria. Bees in field cages foraged on wildflowers at high or low densities, some treated with the common insecticide, imidacloprid, in a fully crossed design. Both stressors influenced behavior, but they had differential impacts. Bees with limited food resources made fewer, but longer foraging trips and misidentified their nests more often. Insecticide exposure reduced bee foraging activity. Additionally, insecticides interacted with bee age to influence antagonistic behavior among neighboring females, such that insecticide-exposed bees were less antagonistic with age. Our findings point towards mechanisms underlying effects on populations and ecosystem function and reinforce the importance of studying multiple drivers to understand the consequences of anthropogenic change.

Rare and declining bee species are key to consistent pollination of wildflowers and crops across large spatial scales.

Biodiversity promotes ecosystem function (EF) in experiments, but it remains uncertain how biodiversity loss affects function in larger-scale natural ecosystems. In these natural ecosystems, rare and declining species are more likely to be lost, and function needs to be maintained across space and time. Here, we explore the importance of rare and declining bee species to the pollination of three wildflowers and three crops using large-scale (72 sites across 5000 km2 ), multi-year datasets. Half of the sampled bee species (82/164) were rare or declining, but these species provided only ~15% of overall pollination. To determine the number of species important to EF, we used two methods of "scaling up," both of which have previously been used for biodiversity-function analysis. First, we summed bee species' contributions to pollination across space and time and then found the minimum set of species needed to provide a threshold level of function across all sites; according to this method, effectively no rare and declining bee species were important to pollination. Second, we account for the "insurance value" of biodiversity by finding the minimum set of bee species needed to simultaneously provide a threshold level of function at each site in each year. The second method leads to the conclusion that 25 rare and eight declining bee species (36% and 53% of all rare and declining bee species, respectively) are included in the minimum set. Our findings provide some of the strongest evidence yet that rare and declining species are key to meeting threshold levels of EF, thereby providing a more direct link between real-world biodiversity loss and EF.

Honey bee introductions displace native bees and decrease pollination of a native wildflower.

Introduced species can have cascading effects on ecological communities, but indirect effects of species introductions are rarely the focus of ecological studies. For example, managed honey bees (Apis mellifera) have been widely introduced outside their native range and are increasingly dominant floral visitors. Multiple studies have documented how honey bees impact native bee communities through floral resource competition, but few have quantified how these competitive interactions indirectly affect pollination and plant reproduction. Such indirect effects are hard to detect because honey bees are themselves pollinators and may directly impact pollination through their own floral visits. The potentially huge but poorly understood impacts that non-native honey bees have on native plant populations combined with increased pressure from beekeepers to place hives in U.S. National Parks and Forests makes exploring impacts of honey bee introductions on native plant pollination of pressing concern. In this study, we used experimental hive additions, field observations, as well as single-visit and multiple-visit pollination effectiveness trials across multiple years to untangle the direct and indirect impacts of increasing honey bee abundance on the pollination of an ecologically important wildflower, Camassia quamash. We found compelling evidence that honey bee introductions indirectly decrease pollination by reducing nectar and pollen availability and competitively excluding visits from more effective native bees. In contrast, the direct impact of honey bee visits on pollination was negligible, and, if anything, negative. Honey bees were ineffective pollinators, and increasing visit quantity could not compensate for inferior visit quality. Indeed, although the effect was not statistically significant, increased honey bee visits had a marginally negative impact on seed production. Thus, honey bee introductions may erode longstanding plant-pollinator mutualisms, with negative consequences for plant reproduction. Our study calls for a more thorough understanding of the indirect effects of species introductions and more careful coordination of hive placements.

Greater bee diversity is needed to maintain crop pollination over time.

The current biodiversity crisis underscores the need to understand how biodiversity loss affects ecosystem function in real-world ecosystems. At any one place and time, a few highly abundant species often provide the majority of function, suggesting that function could be maintained with relatively little biodiversity. However, biodiversity may be critical to ecosystem function at longer timescales if different species are needed to provide function at different times. Here we show that the number of wild bee species needed to maintain a threshold level of crop pollination increased steeply with the timescale examined: two to three times as many bee species were needed over a growing season compared to on a single day and twice as many species were needed over six years compared to during a single year. Our results demonstrate the importance of pollinator biodiversity to maintaining pollination services across time and thus to stable agricultural output.

A contemporary survey of bumble bee diversity across the state of California.

Bumble bees (genus Bombus) are important pollinators with more than 260 species found worldwide, many of which are in decline. Twenty-five species occur in California with the highest species abundance and diversity found in coastal, northern, and montane regions. No recent studies have examined California bumble bee diversity across large spatial scales nor explored contemporary community composition patterns across the state. To fill these gaps, we collected 1740 bumble bee individuals, representing 17 species from 17 sites (~100 bees per site) in California, using an assemblage monitoring framework. This framework is intended to provide an accurate estimate of relative abundance of more common species without negatively impacting populations through overcollection. Our sites were distributed across six ecoregions, with an emphasis on those that historically hosted high bumble bee diversity. We compared bumble bee composition among these sites to provide a snapshot of California bumble bee biodiversity in a single year. Overall, the assemblage monitoring framework that we employed successfully captured estimated relative abundance of species for most sites, but not all. This shortcoming suggests that bumble bee biodiversity monitoring in California might require multiple monitoring approaches, including greater depth of sampling in some regions, given the variable patterns in bumble bee abundance and richness throughout the state. Our study sheds light on the current status of bumble bee diversity in California, identifies some areas where greater sampling effort and conservation action should be focused in the future, and performs the first assessment of an assembly monitoring framework for bumble bee communities in the state.

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

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

Early resources lead to persistent benefits for bumble bee colony dynamics.

Conditions experienced early in development can affect the future performance of individuals and populations. Demographic theories predict persistent population impacts of past resources, but few studies have experimentally tested such carry-over effects across generations or cohorts. We used bumble bees to test whether resource timing had persistent effects on within-colony dynamics over sequential cohorts of workers. We simulated a resource pulse for field colonies either early or late in their development and estimated colony growth rates during pulse- and non-pulse periods. During periods when resources were not supplemented, early-pulse colonies grew faster than late-pulse colonies; early-pulse colonies grew larger as a result. These results revealed persistent effects of past resources on current growth and support the importance of transient dynamics in natural ecological systems. Early-pulse colonies also produced more queen offspring, highlighting the critical nature of resource timing for the population, as well as colony, dynamics of a key pollinator.

Past insecticide exposure reduces bee reproduction and population growth rate.

Pesticides are linked to global insect declines, with impacts on biodiversity and essential ecosystem services. In addition to well-documented direct impacts of pesticides at the current stage or time, potential delayed "carryover" effects from past exposure at a different life stage may augment impacts on individuals and populations. We investigated the effects of current exposure and the carryover effects of past insecticide exposure on the individual vital rates and population growth of the solitary bee, Osmia lignaria Bees in flight cages freely foraged on wildflowers, some treated with the common insecticide, imidacloprid, in a fully crossed design over 2 y, with insecticide exposure or no exposure in each year. Insecticide exposure directly to foraging adults and via carryover effects from past exposure reduced reproduction. Repeated exposure across 2 y additively impaired individual performance, leading to a nearly fourfold reduction in bee population growth. Exposure to even a single insecticide application can have persistent effects on vital rates and can reduce population growth for multiple generations. Carryover effects had profound implications for population persistence and must be considered in risk assessment, conservation, and management decisions for pollinators to mitigate the effects of insecticide exposure.

A meta-analysis of single visit pollination effectiveness comparing honeybees and other floral visitors.

PREMISE: Many animals provide ecosystem services in the form of pollination including honeybees, which have become globally dominant floral visitors. A rich literature documents considerable variation in single visit pollination effectiveness, but this literature has yet to be extensively synthesized to address whether honeybees are effective pollinators. METHODS: We conducted a hierarchical meta-analysis of 168 studies and extracted 1564 single visit effectiveness (SVE) measures for 240 plant species. We paired SVE data with visitation frequency data for 69 of these studies. We used these data to ask three questions: (1) Do honeybees (Apis mellifera) and other floral visitors differ in their SVE? (2) To what extent do plant and pollinator attributes predict differences in SVE between honeybees and other visitors? (3) Is there a correlation between visitation frequency and SVE? RESULTS: Honeybees were significantly less effective than the most effective non-honeybee pollinators but were as effective as the average pollinator. The type of pollinator moderated these effects. Honeybees were less effective compared to the most effective and average bird and bee pollinators but were as effective as other taxa. Visitation frequency and SVE were positively correlated, but this trend was largely driven by data from communities where honeybees were absent. CONCLUSIONS: Although high visitation frequencies make honeybees important pollinators, they were less effective than the average bee and rarely the most effective pollinator of the plants they visit. As such, honeybees may be imperfect substitutes for the loss of wild pollinators, and safeguarding pollination will benefit from conservation of non-honeybee taxa.

Larger workers outperform smaller workers across resource environments: An evaluation of demographic data using functional linear models.

Behavior and organization of social groups is thought to be vital to the functioning of societies, yet the contributions of various roles within social groups toward population growth and dynamics have been difficult to quantify. A common approach to quantifying these role-based contributions is evaluating the number of individuals conducting certain roles, which ignores how behavior might scale up to effects at the population-level. Manipulative experiments are another common approach to determine population-level effects, but they often ignore potential feedbacks associated with these various roles.Here, we evaluate the effects of worker size distribution in bumblebee colonies on worker production in 24 observational colonies across three environments, using functional linear models. Functional linear models are an underused correlative technique that has been used to assess lag effects of environmental drivers on plant performance. We demonstrate potential applications of this technique for exploring high-dimensional ecological systems, such as the contributions of individuals with different traits to colony dynamics.We found that more larger workers had mostly positive effects and more smaller workers had negative effects on worker production. Most of these effects were only detected under low or fluctuating resource environments suggesting that the advantage of colonies with larger-bodied workers becomes more apparent under stressful conditions.We also demonstrate the wider ecological application of functional linear models. We highlight the advantages and limitations when considering these models, and how they are a valuable complement to many of these performance-based and manipulative experiments.

Pesticide and resource stressors additively impair wild bee reproduction.

Bees and other beneficial insects experience multiple stressors within agricultural landscapes that act together to impact their health and diminish their ability to deliver the ecosystem services on which human food supplies depend. Disentangling the effects of coupled stressors is a primary challenge for understanding how to promote their populations and ensure robust pollination and other ecosystem services. We used a crossed design to quantify the individual and combined effects of food resource limitation and pesticide exposure on the survival, nesting, and reproduction of the blue orchard bee Osmia lignaria. Nesting females in large flight cages accessed wildflowers at high or low densities, treated with or without the common insecticide, imidacloprid. Pesticides and resource limitation acted additively to dramatically reduce reproduction in free-flying bees. Our results emphasize the importance of considering multiple drivers to inform population persistence, management, and risk assessment for the long-term sustainability of food production and natural ecosystems.

The effectiveness of flower strips and hedgerows on pest control, pollination services and crop yield: a quantitative synthesis.

Floral plantings are promoted to foster ecological intensification of agriculture through provisioning of ecosystem services. However, a comprehensive assessment of the effectiveness of different floral plantings, their characteristics and consequences for crop yield is lacking. Here we quantified the impacts of flower strips and hedgerows on pest control (18 studies) and pollination services (17 studies) in adjacent crops in North America, Europe and New Zealand. Flower strips, but not hedgerows, enhanced pest control services in adjacent fields by 16% on average. However, effects on crop pollination and yield were more variable. Our synthesis identifies several important drivers of variability in effectiveness of plantings: pollination services declined exponentially with distance from plantings, and perennial and older flower strips with higher flowering plant diversity enhanced pollination more effectively. These findings provide promising pathways to optimise floral plantings to more effectively contribute to ecosystem service delivery and ecological intensification of agriculture in the future.

Wildfire reveals transient changes to individual traits and population responses of a native bumble bee Bombus vosnesenskii.

Fire-induced changes in the abundance and distribution of organisms, especially plants, can alter resource landscapes for mobile consumers driving bottom-up effects on their population sizes, morphologies and reproductive potential. We expect these impacts to be most striking for obligate visitors of plants, like bees and other pollinators, but these impacts can be difficult to interpret due to the limited information provided by forager counts in the absence of survival or fitness proxies. Increased bumble bee worker abundance is often coincident with the pulses of flowers that follow recent fire. However, it is unknown if observed postfire activity is due to underlying population growth or a stable pool of colonies recruiting more foragers to abundant resource patches. This distinction is necessary for determining the net impact of disturbance on bumble bees: are there population-wide responses or do just a few colonies reap the rewards? We estimated colony abundance before and after fire in burned and unburned areas using a genetic mark-recapture framework. We paired colony abundance estimates with measures of body size, counts of queens, and estimates of foraging and dispersal to assess changes in worker size, reproductive output, and landscape-scale movements. Higher floral abundance following fire not only increased forager abundance but also the number of colonies from which those foragers came. Importantly, despite a larger population size, we also observed increased mean worker size. Two years following fire, queen abundance was higher in both burned and unburned sites, potentially due to the dispersal of queens from burned into unburned areas. The effects of fire were transient; within two growing seasons, worker abundance was substantially reduced across the entire sampling area and body sizes were similar between burned and unburned sites. Our results reveal how disturbance can temporarily release populations from resource limitation, boosting the genetic diversity, body size, and reproductive output of populations. Given that the effects of fire on bumble bees acted indirectly through pulsed resource availability, it is likely our results are generalizable to other situations, such as habitat restorations, where resource density is enhanced within the landscape.

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

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

Mismatched outcomes for biodiversity and ecosystem services: testing the responses of crop pollinators and wild bee biodiversity to habitat enhancement.

Supporting ecosystem services and conserving biodiversity may be compatible goals, but there is concern that service-focused interventions mostly benefit a few common species. We use a spatially replicated, multiyear experiment in four agricultural settings to test if enhancing habitat adjacent to crops increases wild bee diversity and abundance on and off crops. We found that enhanced field edges harbored more taxonomically and functionally abundant, diverse, and compositionally different bee communities compared to control edges. Enhancements did not increase the abundance or diversity of bees visiting crops, indicating that the supply of pollination services was unchanged following enhancement. We find that actions to promote crop pollination improve multiple dimensions of biodiversity, underscoring their conservation value, but these benefits may not be spilling over to crops. More work is needed to identify the conditions that promote effective co-management of biodiversity and ecosystem services.

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.