Berry J. Brosi

The phenology of organisms worldwide is shifting in response to changes in environmental conditions. There is growing concern that resulting timing mismatches among interacting species will negatively impact system-level properties, yet there is no general framework for evaluating community responses to changes in phenology. To address this gap, we developed a mathematical framework based on local stability analysis and used it to assess the resilience implications of phenological perturbations with a multi-year, highly time-resolved empirical dataset on subalpine plant-pollinator communities. The forecasted effects of phenological perturbations were largely independent of perturbations to species densities, indicating the potential for even small changes in phenology to disrupt the functioning of ecosystems that are otherwise highly stable.

Biodiversity in human-dominated landscapes is declining, but evidence-based conservation targets to guide international policies for such landscapes are lacking. We present a framework for informing habitat conservation policies based on the enhancement of habitat quantity and quality and define thresholds of habitat quantity at which it becomes effective to also prioritize habitat quality. We applied this framework to insect pollinators, an important part of agroecosystem biodiversity, by synthesizing 59 studies from 19 countries. Given low habitat quality, hoverflies had the lowest threshold at 6% semi-natural habitat cover, followed by solitary bees (16%), bumble bees (18%), and butterflies (37%). These figures represent minimum habitat thresholds in agricultural landscapes, but when habitat quantity is restricted, marked increases in quality are required to reach similar outcomes.

Land use change threatens global biodiversity and compromises ecosystem functions, including pollination and food production. Reduced taxonomic α‐diversity is often reported under land use change, yet the impacts could be different at larger spatial scales (i.e., γ‐diversity), either due to reduced β‐diversity amplifying diversity loss or increased β‐diversity dampening diversity loss. Additionally, studies often focus on taxonomic diversity, while other important biodiversity components, including phylogenetic diversity, can exhibit differential responses. Here, we evaluated how agricultural and urban land use alters the taxonomic and phylogenetic α‐, β‐, and γ‐diversity of an important pollinator taxon—bees. Using a multicontinental dataset of 3117 bee assemblages from 157 studies, we found that taxonomic α‐diversity was reduced by 16%–18% in both agricultural and urban habitats relative to natural habitats. Phylogenetic α‐diversity was decreased by 11%–12% in agricultural and urban habitats. Compared with natural habitats, taxonomic and phylogenetic β‐diversity increased by 11% and 6% in urban habitats, respectively, but exhibited no systematic change in agricultural habitats. We detected a 22% decline in taxonomic γ‐diversity and a 17% decline in phylogenetic γ‐diversity in agricultural habitats, but γ‐diversity of urban habitats was not significantly different from natural habitats. These findings highlight the threat of agricultural expansions to large‐scale bee diversity due to systematic γ‐diversity decline. In addition, while both urbanization and agriculture lead to consistent declines in α‐diversity, their impacts on β‐ or γ‐diversity vary, highlighting the need to study the effects of land use change at multiple scales.

Synopsis: Understanding how the structure of biological systems impacts their resilience (broadly defined) is a recurring question across multiple levels of biological organization. In ecology, considerable effort has been devoted to understanding how the structure of interactions between species in ecological networks is linked to different broad resilience outcomes, especially local stability. Still, nearly all of that work has focused on interaction structure in presence-absence terms and has not investigated quantitative structure, i.e., the arrangement of interaction strengths in ecological networks. We investigated how the interplay between binary and quantitative structure impacts stability in mutualistic interaction networks (those in which species interactions are mutually beneficial), using community matrix approaches. We additionally examined the effects of network complexity and within-guild competition for context. In terms of structure, we focused on understanding the stability impacts of nestedness, a structure in which more-specialized species interact with smaller subsets of the same species that more-generalized species interact with. Most mutualistic networks in nature display binary nestedness, which is puzzling because both binary and quantitative nestedness are known to be destabilizing on their own. We found that quantitative network structure has important consequences for local stability. In more-complex networks, binary-nested structures were the most stable configurations, depending on the quantitative structures, but which quantitative structure was stabilizing depended on network complexity and competitive context. As complexity increases and in the absence of within-guild competition, the most stable configurations have a nested binary structure with a complementary (i.e., anti-nested) quantitative structure. In the presence of within-guild competition, however, the most stable networks are those with a nested binary structure and a nested quantitative structure. In other words, the impact of interaction overlap on community persistence is dependent on the competitive context. These results help to explain the prevalence of binary-nested structures in nature and underscore the need for future empirical work on quantitative structure.

Honey bee parasites remain a critical challenge to management and conservation. Because managed honey bees are maintained in colonies kept in apiaries across landscapes, the study of honey bee parasites allows the investigation of spatial principles in parasite ecology and evolution. We used a controlled field experiment to study the relationship between population growth rate and virulence (colony survival) of the parasite Varroa destructor (Anderson and Trueman). We used a nested design of 10 patches (apiaries) of 14 colonies to examine the spatial scale at which Varroa population growth matters for colony survival. We tracked Varroa population size and colony survival across a full year and found that Varroa populations that grow faster in their host colonies during the spring and summer led to larger Varroa populations across the whole apiary (patch) and higher rates of neighboring colony loss. Crucially, this increased colony loss risk manifested at the patch scale, with mortality risk being related to spatial adjacency to colonies with fast-growing Varroa strains rather than with Varroa growth rate in the colony itself. Thus, within-colony population growth predicts whole-apiary virulence, demonstrating the need to consider multiple scales when investigating parasite growth-virulence relationships.

Premise: Changes to flowering time caused by climate change could affects plant fecundity, but studies that compare the individual‐level responses of phenologically distinct, co‐occurring species are lacking. We assessed how variation in floral phenology affects the fecundity of individuals from three montane species with different seasonal flowering times, including in snowmelt acceleration treatments to increase variability in phenology.Methods: We collected floral phenology and seed set data for individuals of three montane plant species (Mertensia fusiformis, Delphinium nuttallianum, Potentilla pulcherrima). To examine the drivers of seed set, we measured conspecific floral density and conducted pollen limitation experiments to isolate pollination function. We advanced the phenology of plant communities in a controlled large‐scale snowmelt acceleration experiment.Results: Differences in individual phenology relative to the rest of the population affected fecundity in our focal species, but effects were species‐specific. For our early‐season species, individuals that bloomed later than the population peak bloom had increased fecundity, while for our midseason species, simply blooming before or after the population peak increased individual fecundity. For our late‐season species, blooming earlier than the population peak increased fecundity. The early and midseason species were pollen‐limited, and conspecific density affected seed set only for our early‐season species.Conclusions: Our study shows that variation in individual phenology affects fecundity in three phenologically distinct montane species, and that pollen limitation may be more influential than conspecific density. Our results suggest that individual‐level changes in phenology are important to consider for understanding plant reproductive success.

Broadcast spraying of antibiotics in crops is widely used for controlling bacterial plant pathogens. The effects of antibiotics on non-target (and especially beneficial) organisms in cropping systems, however, are not well studied. Pollinators are of particular concern because in pear and apple crops, antibiotics for controlling fire blight ( Erwinia amylovora ) are sprayed during bloom, likely exposing pollinators. This is especially relevant as laboratory evidence suggests that antibiotics could have sublethal effects on bee foraging behavior and colony health. But to our knowledge these potential impacts have not been studied in field settings. Here, we compared the effects of two fire blight control methods, a single spray of an antibiotic (oxytetracycline) and a biological antagonist ( Aureobasidium pullulans ), on honey bee ( Apis mellifera ) foraging, pollination, and fruit set in pear orchards. Complementing these field assessments, we conducted laboratory experiments to examine the effects of these treatments on locomotion and foraging behavior of the bumble bee species, Bombus vosnesenskii . We found that honey bees visited fewer flowers and foraged longer on each flower in orchards sprayed with antibiotics than with biological product, but there were no differences in pollination and seed set. The pear cultivars we worked in, however, can self-pollinate. In the lab, we found that feeding on high doses of either the antibiotic or the biological antagonist reduced bumble bee foraging behavior relative to controls. The limited impact of antibiotics on pear pollination observed in this study suggest that antibiotics pose a low economic risk to pear growers, especially for self-compatible cultivars. Still, crops with higher pollinator dependence may be more affected by reductions in pollinator visitation. Future studies should examine the impacts of multiple antibiotic sprays within a season, which are common during warm springs, and their long-term health impacts on both individual bees and colonies. Highlights: Antibiotics are sprayed on many crops to control plant bacterial pathogens. The impacts of antibiotics on beneficial organisms in agriculture are unknown. We studied antibiotic impacts on bee behavior and pollination function in pears. Bees exposed to antibiotics visit fewer flowers and this could impact bee fitness. Despite decreased bee visitation, we did not detect a reduction in crop pollination. Graphical

The timing of life history events is being altered by climate change and other anthropogenic environmental changes, with potential functional consequences. Such changes may be particularly important in mutualisms, such as plant-pollinator interactions, where timing mismatches can impact fitness in both plants and pollinators. Numerous studies have examined how changes in flowering phenology could impact the seed set of individual species, yet it is the changes to relative fitness among species that shape coexistence and community composition. To understand how phenological change can affect plant community seed set, we conducted a large-scale snowmelt acceleration experiment to advance flowering phenology in eight montane meadow communities across two valleys in the Rocky Mountains of Colorado, USA. Each snowmelt acceleration plot (10 m x 14 m) was paired with an adjacent control plot without snowmelt manipulation (16 plots total). In six plots and their adjacent controls, we measured how phenological change altered the fecundity of eight co-occurring plant species, evaluating pollen limitation in five species using hand pollination treatments. Although accelerating flowering phenology resulted in lower overall fecundity and greater pollen limitation in the examined assemblage of focal species, these changes occurred in different directions depending on the species. Species-dependent responses were also reflected in a significant change in the relative proportions of seeds produced by different plants. Our results suggest potential impacts on future plant community composition resulting from early snowmelt, and underscore the importance of studying the impacts of phenological change at a community level.

Given widespread concerns over human-mediated bee declines in abundance and species richness, conservation efforts are increasingly focused on maintaining natural habitats to support bee diversity in otherwise resource-poor environments. However, natural habitat patches can vary in composition, impacting landscape-level heterogeneity and affecting plant-pollinator interactions. Plant-pollinator networks, especially those based on pollen loads, can provide valuable insight into mutualistic relationships, such as revealing the degree of pollination specialization in a community; yet, local and landscape drivers of these network indices remain understudied within urbanizing landscapes. Beyond networks, analyzing pollen collection can reveal key information about species-level pollen preferences, providing plant restoration information for urban ecosystems. Through bee collection, vegetation surveys, and pollen load identification across ~350 km of urban habitat, we studied the impact of local and landscape-level management on plant-pollinator networks. We also quantified pollinator preferences for plants within urban grasslands. Bees exhibited higher foraging specialization with increasing habitat heterogeneity and visited fewer flowering species (decreased generality) with increasing semi-natural habitat cover. We also found strong pollinator species-specific flower foraging preferences, particularly for Asteraceae plants. We posit that maintaining native forbs and supporting landscape-level natural habitat cover and heterogeneity can provide pollinators with critical food resources across urbanizing ecosystems.

Many tropical seed-dispersing frugivores are facing extinction, but the consequences of the loss of endangered frugivores for seed dispersal is not well understood. We investigated the role of frugivore endangerment status via robustness-to-coextinction simulations (in this context, more accurately described as robustness-to-partner-loss simulations) using data from the Brazilian Atlantic Forest biodiversity hotspot. By simulating the extinction of endangered frugivores, we found a rapid and disproportionate loss of tree species with dispersal partners in the network, and this surprisingly surpassed any other frugivore extinction scenario, including the loss of the most generalist frugivores first. A key driver of this pattern is that many specialist plants rely on at-risk frugivores as seed-dispersal partners. Moreover, interaction compensation in the absence of endangered frugivores may be unlikely because frugivores with growing populations forage on fewer plant species than frugivores with declining populations. Therefore, protecting endangered frugivores could be critical for maintaining tropical forest seed dispersal, and their loss may have higher-than-expected functional consequences for tropical forests, their regeneration processes, and the maintenance of tropical plant diversity