Anthropogenic environmental changes present multiple stressors that together impact biodiversity and ecosystem function. Among these, pesticide exposure and the loss of flowering plants are ubiquitous across contemporary landscapes and threaten the persistence of bee populations. In this dissertation, I explored the individual and combined effects of pesticide and floral resource stressors on bee behavior, reproduction, and population persistence, as well as a potential strategy for mitigating these impacts. I used a combination of manipulative field cage experiments and landscape studies to examine these stressors and their impacts at different scales.

Because bees often experience pesticide and resource stressors simultaneously, I first examined the potential for interactive effects of these stressors, as well as their individual impacts on wild bees. I established a fully crossed design in field cages; nesting female Osmia lignaria, the solitary blue orchard bee, accessed wildflowers at high or low densities, treated with or without the common insecticide, imidacloprid. In Chapter 1, I showed that pesticide exposure and floral resource scarcity combined additively to dramatically alter multiple vital rates, including reduced reproduction and a male-biased offspring sex ratio. In Chapter 2, I quantified behavioral responses in the same experiment, revealing that the resource and pesticide stressors had differential impacts with consequences for bee populations and potentially for pollination services through individual behavioral changes. Limited floral resources required bees to make fewer, longer foraging trips as well as misidentify their nests more often upon return from these trips. Bees exposed to pesticides made shorter foraging trips and did not compensate for this by taking more trips, reducing their overall foraging activity. Pesticide exposure also interacted with age to affect antagonistic behavior.

In Chapter 3, I examined the carryover effects of past pesticide exposure on wild bees. Using the offspring from the previous cage experiment with known pesticide exposure backgrounds, I re-established the field cages and released bees in a crossed design with pesticide exposure or no exposure in each year. Thus, some bees experienced pesticides over two generations and others not at all. Regardless of the past exposure history, pesticides in the second year reduced reproduction. For bees that were also exposed in the past, the exposure over two years additively impaired individual performance, leading to a nearly fourfold estimated reduction in bee population growth. Furthermore, even past exposure by itself, regardless of exposure in the second year, led to a decline in offspring production.

In Chapter 4, I collaborated with Maj Rundlöf to investigate the potential for wildflower plantings to mitigate the negative effects of pesticide exposure in agricultural landscapes. We assessed the nesting and reproduction of O. lignaria and the bumble bee Bombus vosnesenskii in replicate agricultural landscapes, half of which contained a wildflower planting next to the nest or colony. We collected pollen from foraging bees to determine resource use and pesticide residues. The wildflower plantings were a source of pesticide exposure, especially for O. lignaria, but also supported O. lignaria nesting. The landscape-level floral resources better predicted B. vosnesenskii colony success, but the local flower resources mitigated the negative effects of pesticides on their reproduction.

These chapters together show that two common environmental stressors combine to negatively impact bees. They also reveal potential mechanisms underlying impacts of the stressors on reproduction and population growth. My dissertation highlights the importance of mitigating the negative effects of pesticides and floral resource limitation, especially in agricultural landscapes where the two stressors often co-occur. Finally, this work offers insight into how the stressors could be mitigated through an emerging strategy to diversity agricultural landscapes.

Globalization and industrial agriculture have led to a severe homogenization of ecological communities. European honey bees are now present on every continent expect Antarctica and are rapidly replacing native bees as plant visitors. Maintaining global crop productivity requires that we support honey bees, but honey bees may be unsuitable replacements for native pollinators, and agricultural intensification should not come at the expense of plant and animal biodiversity. This dissertation examines how increasing honey bee abundance impacts native bees and their interactions with plants. In Chapter 1, I investigate the impacts of increasing honey bee abundance on native bee visitation patterns, native bee pollen diets, and nectar and pollen resource availability in two California landscapes: wildflower plantings in the Central Valley and montane meadows in the Sierra. I find that, in both ecosystems, honey bee competition increases niche overlap between honey bees and native bees, leading to important shifts in the network of interactions between plants and pollinators. In the Sierra, native bees re-shuffle their interactions to escape competition, but honey bee abundance decreases pollen and nectar availability in both systems. This suggests that, although native bees can adapt to competition, increasing honey bee abundance may reduce native bee pollen and nectar collection with negative repercussions for native bee populations when floral resources are limiting. Increasing honey bee abundance and associated shifts in plant-pollinator interaction patterns may also have important functional consequences for plants. However, assessing the overall impact of honey bee introductions on pollination is complicated because abundant honey bees can influence pollination directly, through their own floral visits, but also indirectly, by competitively influencing visits from other pollinators. In Chapter 2, I disentangle the direct and indirect impacts of increasing honey bee abundance on the pollination of an ecologically important wildflower, Camassia quamash. I find compelling evidence that honey bee introductions indirectly decrease pollination by competitively excluding visits from more effective native bees, suggesting that hive introductions in sensitive ecosystems should be approached with extreme caution. Although I focus on just one plant species in Chapter 2, I expect that replacing native bees with honey bees might decrease pollination for other plant species, particularly when honey bees are ineffective pollinators. In Chapter 3 (originally published in the American Journal of Botany), I assess the pollination effectiveness of honey bees compared to other floral visitors using a hierarchical meta-analysis and find that honey bees are less effective than the average bee and rarely the most effective pollinator of plants globally. As such, honey bees may be imperfect substitutes for the loss of wild pollinators. Taken together, my dissertation demonstrates that increasing honey bee abundance may erode longstanding plant-pollinator mutualisms with negative consequences for plant reproduction and native bee floral resource collection. However, negative impacts for native bees will depend on whether their population growth is limited by floral resource availability and negative impacts for plant species will depend on the relative effectiveness of honey bees as pollinators. Improving our understanding of when, where, and how honey bee competition negatively impacts native bee and plant populations will be crucial for calibrating the balance between biodiversity conservation and agricultural production.

Soil transitions underly many terrestrial landscapes and are well-established drivers of plant community structure. Yet, edaphic characteristics are frequently excluded from hypotheses of how environmental features structure ecological communities for higher trophic levels. In this dissertation, I test whether a particular type of soil, serpentine, structures bee communities and the flowers they depend on. Building on a foundation of classic ecological studies, I establish where and why flowers and bees distribute themselves across the mosaic landscapes of California serpentine soils by using both community and functional ecology tools. Functional trait ecology plays a key role in revealing what mechanisms filter local bee communities. And finally, I categorize how these bee and flower communities produce emergent patterns of interaction using network approaches. This dissertation demonstrates that soil, and perhaps many other underlying environmental conditions, not only filter and structure plant communities, but also the wild bee communities that visit them.

Chapter One documents and categorizes wild bee and flower communities across serpentine and non-serpentine meadows in California’s coastal mountain ranges. Soil characteristics are well-established environmental drivers of local plant community diversity and composition, but their effects on mobile organisms in higher trophic levels are less well understood. We analyzed whether pollinator (mostly wild bee) and floral communities—distributed across a discrete serpentine soil boundary in California’s coast ranges—differed according to the underlying soil type (serpentine or non-serpentine). We found that wild bee richness and abundance were significantly lower in non-serpentine meadows, but the taxonomic composition of bee communities did not differ between soil types. Spring floral richness, abundance, and composition were also lower in non-serpentine meadows, but floral communities had different compositions on the two soil types. In both bee and floral communities, there were strong phenological effects on abundance, richness, and composition over the course of the spring season that were parallel. Both bees and flowers were markedly more diverse and abundant in serpentine meadows, particularly in the late spring when non-serpentine meadows stopped flowering.

Chapter Two utilizes a functional trait framework to test whether soil characteristics affect the functional diversity of wild bee communities, either directly or indirectly via changes to vegetation-related nesting and foraging habitat quality. We demonstrate that soil type affects the functional diversity of bee communities, with those on serpentine soils being more functionally rich. Rather than direct soil-bee impacts, soil type appears to indirectly filter bee communities via interactions between vegetation-based habitat quality and bee nesting and foraging traits. We use a fourth-corner analysis to show that nesting and foraging habitat quality correlates with particular bee functional traits. Specifically, above-ground nesting bees are filtered out of serpentine meadows, and late-flying bees are filtered out of non-serpentine meadows. Despite a growing literature on landscape drivers affecting bee community functional richness, the indirect pathways filtering bees are rarely quantified. In contrast to the strong direct filters that infertile soils exert on plant communities via functional response traits, the indirect effects on pollinators are more complex. Soil fertility’s indirect effects of “cascading up” to structure the functional diversity of other higher trophic communities may be a broader pattern, but evidence is scant.

Chapter Three takes a network perspective to understand how interactions (and not only species) turn over across serpentine and non-serpentine grasslands. Ecologists have long sought to understand and dissect interaction networks among co-occurring species and to understand if these interactions assemble into networks with common emergent properties like nestedness, modularity, and specialization. In addition, how interactions turn over—and consequently affect network structure and resilience to perturbations—across other environmental gradients is a field of important, and current, focus. We analyzed how soil type affected the network structure and interaction turnover of plant-pollinator communities. We demonstrate that plant-pollinator network structure differed significantly between serpentine and non-serpentine meadows. We also utilized a parallel analysis of network microstructure, where we focused on the turnover of interactions between networks. The difference in overall network structure appears to be driven by interaction turnover; serpentine networks exhibited lower interaction turnover between themselves than non-serpentine networks, and interaction rewiring—when shared species switch interaction partners—contributed to turnover between serpentine networks more frequently. Interaction rewiring contributed very little to interaction turnover in general, and only ~20% of interaction turnover between sites was among shared species. And when compared to a regional pooled meta-web, serpentine networks were more unique than non-serpentine networks. Although serpentine meadows are more unique in a regional context, the more frequent rewiring and lower interaction turnover between serpentine meadows drives less specialized, more resilient plant-pollinator networks in these low-resource environments.

Climate change and climate instability driven by anthropogenic fossil fuel emissions areincreasing the frequency and severity of extreme weather events. One such event, heat waves, are becoming more frequent, intense and prolonged (Meehl and Tebaldi 2004; Stillman 2019; Thiery et al. 2021). Extreme heat associated with these heat waves may be particularly damaging to critical species life-history events such as reproduction and mating, and also interactions between organisms (Vasseur et al. 2014; Harvey et al. 2023). Heat may especially impact plant- pollinator interactions and the mating of flowering plants, as heat may disrupt the process of pollination and alter the stable dynamics of mating (Hedhly et al. 2009; Walters et al. 2022; Hemberger et al. 2023). Importantly, heat may disrupt plant-pollinator interactions and successful mating directly through heat’s effects on flower gamete production and performance (Hedhly et al. 2009), but also indirectly through heat’s effects on foraging pollinators (Walters et al. 2022; Hemberger et al. 2023). My dissertation is divided into three chapters with the aim of understanding methodically how heat impacts the ecology of pollination and floral reproduction. Chapter 1 used experimental pollination treatments explicitly focusing on the perspective of the plant to understand how heat affects the dynamics of pollen limitation-the reduction in potential seed production through insufficient receipt of or pollen that is incapable of fertilizing ovules. It evaluates how heat may simultaneously influence the quantity of pollen grains produced and the quality of those pollen grains in addition to pollen quality effects inherent to pollen origin (self versus outcross). I found that heat dramatically limited pollen production, and the quality of pollen grains measured as its viability and performance to grow pollen tubes and fertilize ovules. Although outcross pollen was of higher quality than self pollen under control conditions, heat diminished these differences. These results suggest that heat primes plants to have a high risk of quantitative and qualitative pollen limitation and can disrupt plant mating strategies. Chapter 2 used experiments to quantify the relative contributions of direct (through flowers) and indirect (through pollinator foraging and flower visitation) effects of extreme heat on pollination, post- pollination, and reproduction. The experiments involved bumble bee foraging in heated chambers to allow bumble bees to disperse pollen between flowers. I found that heat strongly limited pollination, the success of those dispersed pollen grains (post-pollination) and reproduction through direct and indirect effects, and that direct effects of heat in post-pollination caused outright reproductive failure. Importantly, these effects were additive. Although both direct and indirect effects are highly limiting, the presence of direct effects dominated heat’s indirect effects on pollination, post-pollination, and reproduction. Chapter 3 used mathematical modelling to explore the sensitivity of pollination and plant reproduction to heat based on models of pollination dynamics and thermal performance curves. Due to logistical challenges that emerge in experimentation, mathematical models allowed me to overcome them and fully explore the parameter space to understand which temperatures specifically would be deleterious, and whether this depended on direct and indirect effects. Furthermore, this chapter also explored whether altering the density of pollinators could offset the negative effects of heat on flowers for pollination and post-pollination processes. My results demonstrated that pollination and reproduction respond non-linearly at high temperatures as pollination and reproduction abruptly collapse. This collapse was largely driven by decreasing pollen production, and therefore increasing pollinator abundance did not compensate for how flowers respond to heat. The collection of these chapters builds upon previous work that suggests that pollination should be highly vulnerable to heat. My results underscore the broad detrimental effect that heat has at each stage of the reproductive process (pollination and post-pollination), and that there is little to no resilience in pollination systems to the effects of heat. When plants mate during periods of extreme heat, it will likely severely limit the reproduction of plants through direct and indirect pathways (Walters et al. 2022; Hemberger et al. 2023), which threatens the persistence of plant populations and the security of food production (Battisti and Naylor 2009; Lesk et al. 2016).

Native California bees and other wild pollinators, which are essential to many fruit and vegetable crops, are being threatened by climate change, pesticides and habitat degradation. Carbon farming, a set of practices that sequester carbon in the soil or woody biomass, can create habitat that supports these pollinators. This paper focuses on habitat management and farming practices that both increase carbon sequestration and benefit pollinator communities. By incentivizing and supporting conservation practices that incorporate carbon farming, we can protect wild pollinators and increase the resilience of California agriculture in the face of ongoing climate change.