Plant-pollinator network architecture does not impact intraspecific microbiome variability.

Variation in how individuals interact with food resources can directly impact, and be affected by, their microbial interactions due to the potential for transmission. The degree to which this transmission occurs, however, may depend on the structure of forager networks, which determine the community-scale transmission opportunities. In particular, how the community-scale opportunity for transfer balances individual-scale barriers to transmission is unclear. Examining the bee-flower and bee-microbial interactions of over 1000 individual bees, we tested (1) the degree to which individual floral visits predicted microbiome composition and (2) whether plant-bee networks with increased opportunity for microbial transmission homogenized the microbiomes of bees within that network. The pollen community composition carried by bees was associated with microbiome composition at some sites, suggesting that microbial transmission at flowers occurred. Contrary to our predictions, however, microbiome variability did not differ based on transfer opportunity: bee microbiomes in asymmetric networks with high opportunity for microbial transfer were similarly variable compared to microbiomes in networks with more evenly distributed links. These findings suggest that microbial transmission at flowers is frequent enough to be observed at the community level, but that community network structure did not substantially change the dynamics of this transmission, perhaps due to filtering processes in host guts.

Floral resources shape parasite and pathogen dynamics in bees facing urbanization.

Urbanization is associated with increases in impervious land cover, which alters the distribution of resources available to wildlife and concentrates activity in unbuilt spaces such as parks and gardens. How resource shifts alter the dynamics of parasite and pathogen transmission has not been addressed for many important species in urban systems. We focus on urban gardens, resource-rich "islands" within the urban matrix, to examine how the availability of floral resources at local and landscape scales influences the prevalence of six RNA viruses and three parasites in honey bees and bumble bees. Because parasites and pathogens are transmitted at flowers between visitors, we expected that floral abundance would concentrate bees within gardens, amplifying infection rates in pollinators, unless increases in floral resources would enhance bee diversity enough to dilute transmission. We found that garden size and flowering perennial plant abundance had a positive, direct effect on parasite and pathogen richness in bumble bees, suggesting that resource provisioning amplifies transmission. We also found that parasitism rates in honey bees were positively associated with parasites and pathogens in bumble bees, suggesting spillover between species. Encouragingly, we found evidence that management may mitigate parasitism through indirect effects: garden size had a positive impact on bee diversity, which in turn was negatively associated with parasite and pathogen richness in bumble bees. Unexpectedly, we observed that that parasite and pathogen richness in honey bees had no significant predictors, highlighting the complexity of comparing transmission dynamics between species. Although floral resources provide bees with food, we suggest more research on the tradeoffs between resource provisioning and disease transmission to implement conservation plantings in changing landscapes.

Mass-flowering monoculture attracts bees, amplifying parasite prevalence.

As the global agricultural footprint expands, it is increasingly important to address the link between the resource pulses characteristic of monoculture farming and wildlife epidemiology. To understand how mass-flowering crops impact host communities and subsequently amplify or dilute parasitism, we surveyed wild and managed bees in a monoculture landscape with varying degrees of floral diversification. We screened 1509 bees from 16 genera in sunflower fields and in non-crop flowering habitat across 200 km2 of the California Central Valley. We found that mass-flowering crops increase bee abundance. Wild bee abundance was subsequently associated with higher parasite presence, but only in sites with a low abundance of non-crop flowers. Bee traits related to higher dispersal ability (body size) and diet breadth (pollen lecty) were also positively related to parasite presence. Our results highlight the importance of non-crop flowering habitat for supporting bee communities. We suggest monoculture alone cannot support healthy bees.

Pollinator interaction flexibility across scales affects patch colonization and occupancy.

Global change alters ecological communities and may disrupt ecological interactions and the provision of ecosystem functions. As ecological communities respond to global change, species may either go locally extinct or form novel interactions. To date, few studies have assessed how flexible species are in their interaction patterns, mainly due to the scarcity of data spanning long time series. Using a ten-year species-level dataset on the assembly of mutualistic networks from the Central Valley in California, we test whether interaction flexibility affects pollinators' colonization and persistence and their resulting habitat occupancy in a highly modified landscape. We propose three metrics of interaction flexibility associated with different scales of organization within ecological communities and explore which species' traits affect them. Our results provide empirical evidence linking species' ability to colonize habitat patches across a landscape to the role they play in networks. Phenological breadth and body size had contrasting effects on interaction flexibility. We demonstrate the relationship between mutualistic networks and species' ability to colonize and persist in the landscape, suggesting interaction flexibility as a potential mechanism for communities to maintain ecosystem function despite changes in community composition.

Pyrodiversity promotes interaction complementarity and population resistance.

Theory predicts that network characteristics may help anticipate how populations and communities respond to extreme climatic events, but local environmental context may also influence responses to extreme events. For example, altered fire regimes in many ecosystems may significantly affect the context for how species and communities respond to changing climate. In this study, I tested whether the responses of a pollinator community to extreme drought were influenced by the surrounding diversity of fire histories (pyrodiversity) which can influence their interaction networks via changing partner availability. I found that at the community level, pyrodiverse landscapes promote functional complementarity and generalization, but did not consistently enhance functional redundancy or resistance to simulated co-extinction cascades. Pyrodiversity instead supported flexible behaviors that enable populations to resist perturbations. Specifically, pollinators that can shift partners and network niches are better able to take advantage of the heterogeneity generated by pyrodiversity, thereby buffering pollinator populations against changes in plant abundances. These findings suggest that pyrodiversity is unlikely to improve community-level resistance to droughts, but instead promotes population resistance and community functionality. This study provides unique evidence that resistance to extreme climatic events depends on both network properties and historical environmental context.

One size does not fit all: Customizing MCMC methods for hierarchical models using NIMBLE.

Improved efficiency of Markov chain Monte Carlo facilitates all aspects of statistical analysis with Bayesian hierarchical models. Identifying strategies to improve MCMC performance is becoming increasingly crucial as the complexity of models, and the run times to fit them, increases. We evaluate different strategies for improving MCMC efficiency using the open-source software NIMBLE (R package nimble) using common ecological models of species occurrence and abundance as examples. We ask how MCMC efficiency depends on model formulation, model size, data, and sampling strategy. For multiseason and/or multispecies occupancy models and for N-mixture models, we compare the efficiency of sampling discrete latent states vs. integrating over them, including more vs. fewer hierarchical model components, and univariate vs. block-sampling methods. We include the common MCMC tool JAGS in comparisons. For simple models, there is little practical difference between computational approaches. As model complexity increases, there are strong interactions between model formulation and sampling strategy on MCMC efficiency. There is no one-size-fits-all best strategy, but rather problem-specific best strategies related to model structure and type. In all but the simplest cases, NIMBLE's default or customized performance achieves much higher efficiency than JAGS. In the two most complex examples, NIMBLE was 10-12 times more efficient than JAGS. We find NIMBLE is a valuable tool for many ecologists utilizing Bayesian inference, particularly for complex models where JAGS is prohibitively slow. Our results highlight the need for more guidelines and customizable approaches to fit hierarchical models to ensure practitioners can make the most of occupancy and other hierarchical models. By implementing model-generic MCMC procedures in open-source software, including the NIMBLE extensions for integrating over latent states (implemented in the R package nimbleEcology), we have made progress toward this aim.

Proximity of restored hedgerows interacts with local floral diversity and species' traits to shape long-term pollinator metacommunity dynamics.

Disconnected habitat fragments are poor at supporting population and community persistence; restoration ecologists, therefore, advocate for the establishment of habitat networks across landscapes. Few empirical studies, however, have considered how networks of restored habitat patches affect metacommunity dynamics. Here, using a 10-year study on restored hedgerows and unrestored field margins within an intensive agricultural landscape, we integrate occupancy modelling with network theory to examine the interaction between local and landscape characteristics, habitat selection and dispersal in shaping pollinator metacommunity dynamics. We show that surrounding hedgerows and remnant habitat patches interact with the local floral diversity, bee diet breadth and bee body size to influence site occupancy, via colonisation and persistence dynamics. Florally diverse sites and generalist, small-bodied species are most important for maintaining metacommunity connectivity. By providing the first in-depth assessment of how a network of restored habitat influences long-term population dynamics, we confirm the conservation benefit of hedgerows for pollinator populations and demonstrate the importance of restoring and maintaining habitat networks within an inhospitable matrix.

Opportunistic attachment assembles plant-pollinator networks.

Species and interactions are being lost at alarming rates and it is imperative to understand how communities assemble if we have to prevent their collapse and restore lost interactions. Using an 8-year dataset comprising nearly 20 000 pollinator visitation records, we explore the assembly of plant-pollinator communities at native plant restoration sites in an agricultural landscape. We find that species occupy highly dynamic network positions through time, causing the assembly process to be punctuated by major network reorganisations. The most persistent pollinator species are also the most variable in their network positions, contrary to what preferential attachment - the most widely studied theory of ecological network assembly - predicts. Instead, we suggest assembly occurs via an opportunistic attachment process. Our results contribute to our understanding of how communities assembly and how species interactions change through time while helping to inform efforts to reassemble robust communities.

Pyrodiversity begets plant-pollinator community diversity.

Fire has a major impact on the structure and function of many ecosystems globally. Pyrodiversity, the diversity of fires within a region (where diversity is based on fire characteristics such as extent, severity, and frequency), has been hypothesized to promote biodiversity, but changing climate and land management practices have eroded pyrodiversity. To assess whether changes in pyrodiversity will have impacts on ecological communities, we must first understand the mechanisms that might enable pyrodiversity to sustain biodiversity, and how such changes might interact with other disturbances such as drought. Focusing on plant-pollinator communities in mixed-conifer forest with frequent fire in Yosemite National Park, California, we examine how pyrodiversity, combined with drought intensity, influences those communities. We find that pyrodiversity is positively related to the richness of the pollinators, flowering plants, and plant-pollinator interactions. On average, a 5% increase in pyrodiversity led to the gain of approximately one pollinator and one flowering plant species and nearly two interactions. We also find that a diversity of fire characteristics contributes to the spatial heterogeneity (ß-diversity) of plant and pollinator communities. Lastly, we find evidence that fire diversity buffers pollinator communities against the effects of drought-induced floral resource scarcity. Fire diversity is thus important for the maintenance of flowering plant and pollinator diversity and predicted shifts in fire regimes to include less pyrodiversity compounded with increasing drought occurrence will negatively influence the richness of these communities in this and other forested ecosystems. In addition, lower heterogeneity of fire severity may act to reduce spatial turnover of plant-pollinator communities. The heterogeneity of community composition is a primary determinant of the total species diversity present in a landscape, and thus, lower pyrodiversity may negatively affect the richness of plant-pollinator communities across large spatial scales.

On-farm habitat restoration counters biotic homogenization in intensively managed agriculture.

To slow the rate of global species loss, it is imperative to understand how to restore and maintain native biodiversity in agricultural landscapes. Currently, agriculture is associated with lower spatial heterogeneity and turnover in community composition (ß-diversity). While some techniques are known to enhance α-diversity, it is unclear whether habitat restoration can re-establish ß-diversity. Using a long-term pollinator dataset, comprising ∼9,800 specimens collected from the intensively managed agricultural landscape of the Central Valley of California, we show that on-farm habitat restoration in the form of native plant 'hedgerows', when replicated across a landscape, can boost ß-diversity by approximately 14% relative to unrestored field margins, to levels similar to some natural communities. Hedgerows restore ß-diversity by promoting the assembly of phenotypically diverse communities. Intensively managed agriculture imposes a strong ecological filter that negatively affects several important dimensions of community trait diversity, distribution, and uniqueness. However, by helping to restore phenotypically diverse pollinator communities, small-scale restorations such as hedgerows provide a valuable tool for conserving biodiversity and promoting ecosystem services.

Temporal dynamics influenced by global change: bee community phenology in urban, agricultural, and natural landscapes.

Urbanization and agricultural intensification of landscapes are important drivers of global change, which in turn have direct impacts on local ecological communities leading to shifts in species distributions and interactions. Here, we illustrate how human-altered landscapes, with novel ornamental and crop plant communities, result not only in changes to local community diversity of floral-dependent species, but also in shifts in seasonal abundance of bee pollinators. Three years of data on the spatio-temporal distributions of 91 bee species show that seasonal patterns of abundance and species richness in human-altered landscapes varied significantly less compared to natural habitats in which floral resources are relatively scarce in the dry summer months. These findings demonstrate that anthropogenic environmental changes in urban and agricultural systems, here mediated through changes in plant resources and water inputs, can alter the temporal dynamics of pollinators that depend on them. Changes in phenology of interactions can be an important, though frequently overlooked, mechanism of global change.

Habitat restoration promotes pollinator persistence and colonization in intensively managed agriculture.

Widespread evidence of pollinator declines has led to policies supporting habitat restoration including in agricultural landscapes. Yet, little is yet known about the effectiveness of these restoration techniques for promoting stable populations and communities of pollinators, especially in intensively managed agricultural landscapes. Introducing floral resources, such as flowering hedgerows, to enhance intensively cultivated agricultural landscapes is known to increase the abundances of native insect pollinators in and around restored areas. Whether this is a result of local short-term concentration at flowers or indicative of true increases in the persistence and species richness of these communities remains unclear. It is also unknown whether this practice supports species of conservation concern (e.g., those with more specialized dietary requirements). Analyzing occupancies of native bees and syrphid flies from 330 surveys across 15 sites over eight years, we found that hedgerow restoration promotes rates of between-season persistence and colonization as compared with unrestored field edges. Enhanced persistence and colonization, in turn, led to the formation of more species-rich communities. We also find that hedgerows benefit floral resource specialists more than generalists, emphasizing the value of this restoration technique for conservation in agricultural landscapes.

Diversification practices reduce organic to conventional yield gap.

Agriculture today places great strains on biodiversity, soils, water and the atmosphere, and these strains will be exacerbated if current trends in population growth, meat and energy consumption, and food waste continue. Thus, farming systems that are both highly productive and minimize environmental harms are critically needed. How organic agriculture may contribute to world food production has been subject to vigorous debate over the past decade. Here, we revisit this topic comparing organic and conventional yields with a new meta-dataset three times larger than previously used (115 studies containing more than 1000 observations) and a new hierarchical analytical framework that can better account for the heterogeneity and structure in the data. We find organic yields are only 19.2% (±3.7%) lower than conventional yields, a smaller yield gap than previous estimates. More importantly, we find entirely different effects of crop types and management practices on the yield gap compared with previous studies. For example, we found no significant differences in yields for leguminous versus non-leguminous crops, perennials versus annuals or developed versus developing countries. Instead, we found the novel result that two agricultural diversification practices, multi-cropping and crop rotations, substantially reduce the yield gap (to 9 ± 4% and 8 ± 5%, respectively) when the methods were applied in only organic systems. These promising results, based on robust analysis of a larger meta-dataset, suggest that appropriate investment in agroecological research to improve organic management systems could greatly reduce or eliminate the yield gap for some crops or regions.