Understanding effects of floral products on bee parasites: Mechanisms, synergism, and ecological complexity.

Floral nectar and pollen commonly contain diverse secondary metabolites. While these compounds are classically thought to play a role in plant defense, recent research indicates that they may also reduce disease in pollinators. Given that parasites have been implicated in ongoing bee declines, this discovery has spurred interest in the potential for 'medicinal' floral products to aid in pollinator conservation efforts. We review the evidence for antiparasitic effects of floral products on bee diseases, emphasizing the importance of investigating the mechanism underlying antiparasitic effects, including direct or host-mediated effects. We discuss the high specificity of antiparasitic effects of even very similar compounds, and highlight the need to consider how nonadditive effects of multiple compounds, and the post-ingestion transformation of metabolites, mediate the disease-reducing capacity of floral products. While the bulk of research on antiparasitic effects of floral products on bee parasites has been conducted in the lab, we review evidence for the impact of such effects in the field, and highlight areas for future research at the floral product-bee disease interface. Such research has great potential both to enhance our understanding of the role of parasites in shaping plant-bee interactions, and the role of plants in determining bee-parasite dynamics. This understanding may in turn reveal new avenues for pollinator conservation.

Can Conflicting Selection from Pollinators and Nectar-Robbing Antagonists Drive Adaptive Pollen Limitation? A Conceptual Model and Empirical Test.

AbstractPollen limitation is widespread, despite predictions that it should not be. We propose a novel mechanism generating pollen limitation: conflicting selection by pollinators and antagonists on pollinator attraction traits. We introduce a heuristic model demonstrating antagonist-induced adaptive pollen limitation and present a field study illustrating its occurrence in a wild population. For antagonist-induced adaptive pollen limitation to occur, four criteria must be met: (1) correlated attraction of pollinators and antagonists; (2) greater response by antagonists than pollinators to altered investment in attraction traits; (3) reduced investment in pollinator attraction, leading to pollen limitation; and (4) higher fitness for plants with reduced investment in pollinator attraction. We surveyed nectar robbery and reproductive output for 109 Odontonema cuspidatum (Acanthaceae) plants in a pollen-limited population over 2 years and used experimental floral arrays to evaluate how flower number affects pollination and nectar robbery. Both pollinators and nectar robbers preferred larger floral displays and nectar robbery reduced reproductive output, suggesting conflicting selection. Survey and experimental data agreed closely on the optimum flower number under antagonist-induced pollen limitation; this number was substantially overrepresented in the population. While criteria for antagonist-induced adaptive pollen limitation are restrictive, the necessary conditions may often be realized. Considering interactions beyond the plant-pollinator dyad illuminates previously overlooked mechanisms generating pollen limitation.

Light availability influences the intensity of nectar robbery and its effects on reproduction in a tropical shrub via multiple pathways.

PREMISE: The multiple exogenous pathways by which light availability affects plant reproduction (e.g., via influence on attraction of mutualists and antagonists) remain surprisingly understudied. The light environment experienced by a parent can also have transgenerational effects on offspring via these same pathways. METHODS: We evaluated (a) the influence of light availability on floral traits in Odontonema cuspidatum, (b) the relative importance of the pathways by which light influences nectar robbery and reproductive output, and (c) the role of parental light environment in mediating these relationships. We conducted a reciprocal translocation experiment using clonally propagated ramets and field surveys of naturally occurring plants. RESULTS: Light availability influenced multiple floral traits, including flower number and nectar volume, which in turn influenced nectar robbery. But nectar robbery was also directly influenced by light availability, due to light effects on nectar robber foraging behavior or neighborhood floral context. Parental light environment mediated the link between light availability and nectar robber attraction, suggesting local adaptation to low-light environments in floral visitor attraction. However, we found no transgenerational effect on reproduction. CONCLUSIONS: Our findings demonstrate that exogenous pathways by which light influences plants (particularly through effects on floral antagonists) can complicate the positive relationship between light availability and plant reproduction. Our results are among the first to document effects of light on floral antagonists and clonal transgenerational effects on flower visitor attraction traits.

Does urbanization favour exotic bee species? Implications for the conservation of native bees in cities.

A growing body of research indicates that cities can support diverse bee communities. However, urbanization may disproportionately benefit exotic bees, potentially to the detriment of native species. We examined the influence of urbanization on exotic and native bees using two datasets from Michigan, USA. We found that urbanization positively influenced exotic-but not native-bee abundance and richness, and that this association could not be explained by proximity to international ports of entry, prevalence of exotic flora or urban warming. We found a negative relationship between native and exotic bee abundance at sites with high total bee abundance, suggesting that exotic bees may negatively affect native bee populations. These effects were not driven by the numerically dominant exotic honeybee, but rather by other exotic bees. Our findings complicate the emerging paradigm of cities as key sites for pollinator conservation.

Changes in adult sex ratio in wild bee communities are linked to urbanization.

Wild bees are indispensable pollinators, supporting global agricultural yield and angiosperm biodiversity. They are experiencing widespread declines, resulting from multiple interacting factors. The effects of urbanization, a major driver of ecological change, on bee populations are not well understood. Studies examining the aggregate response of wild bee abundance and diversity to urbanization tend to document minor changes. However, the use of aggregate metrics may mask trends in particular functional groups. We surveyed bee communities along an urban-to-rural gradient in SE Michigan, USA, and document a large change in observed sex ratio (OSR) along this gradient. OSR became more male biased as urbanization increased, mainly driven by a decline in medium and large bodied ground-nesting female bees. Nest site preference and body size mediated the effects of urbanization on OSR. Our results suggest that previously documented negative effects of urbanization on ground-nesting bees may underestimate the full impact of urbanization, and highlight the need for improved understanding of sex-based differences in the provision of pollination services by wild bees.

Urbanization-mediated context dependence in the effect of floral neighborhood on pollinator visitation.

Context dependence in ecological interactions is widespread, but our ability to predict how environmental variation will mediate the effects of a given interaction remains poor. Co-flowering plants can influence visitation of shared pollinators to one another; the effect of these interactions varies with ecological context. While research has investigated the effect of local biotic conditions on such interactions, little is known about how land use change, specifically urbanization, affects them. I tested how the interaction of urbanization and neighborhood floral density (NFD) and richness affected pollinator visitation rates to two crop species, cucumber and sunflower by placing experimental arrays of each species in paired high- (garden) and low- (lawn) floral density neighborhoods along an urban-to-rural gradient. Pollinator visitation to flowers was monitored over 2 years, as was NFD and richness. The two plant species showed contrasting responses to both urbanization and floral neighborhood density, with only cucumber experiencing context dependence in the effect of floral neighborhood. These contrasting responses to urbanization and floral neighborhood are likely due to differences between species in floral visitor community composition. Plants grown in gardens experienced higher pollinator visitation regardless of floral neighborhood. This study highlights the need for better understanding of genus- or species-specific pollinator responses to urbanization to predict the effect of urbanization on plant-pollinator interactions.

Big city Bombus: using natural history and land-use history to find significant environmental drivers in bumble-bee declines in urban development.

Native bee populations are critical sources of pollination. Unfortunately, native bees are declining in abundance and diversity. Much of this decline comes from human land-use change. While the effects of large-scale agriculture on native bees are relatively well understood, the effects of urban development are less clear. Understanding urbanity's effect on native bees requires consideration of specific characteristics of both particular bee species and their urban landscape. We surveyed bumble-bee (Bombus spp.) abundance and diversity in gardens across multiple urban centres in southeastern Michigan. There are significant declines in Bombus abundance and diversity associated with urban development when measured on scales in-line with Bombus flight ability. These declines are entirely driven by declines in females; males showed no response to urbanization. We hypothesize that this is owing to differing foraging strategies between the sexes, and it suggests reduced Bombus colony density in more urban areas. While urbanity reduced Bombus prevalence, results in Detroit imply that 'shrinking cities' potentially offer unique urban paradigms that must be considered when studying wild bee ecology. Results show previously unidentified differences in the effects of urbanity on female and male bumble-bee populations and suggest that urban landscapes can be managed to support native bee conservation.