From Soil Fungi to Bees: Fertile Grounds for Agroecology in California’s San Joaquin Valley

All the ecological components of a farm are tightly interlinked – influencing each other, negatively orpositively, through multiple divergent pathways. Belowground, roots can form a well-developed network with arbuscular mycorrhizal fungi (AMF) for greater nutrient uptake. Aboveground, floral resources (pollen and nectar) influence bee visitation needed for crop pollination. In this way, AMF could positively influence crop pollination through improving nutrient uptake. However, agricultural intensification, characterized by high nutrient inputs, low crop diversity, and high tillage frequency, have been linked to biodiversity loss, negatively impacting multiple species interactions. While diversifying crops could help to promote these beneficial ecological interactions, it is poorly understood how changes in crop diversity impact bees that specialize on limited floral resources or mycorrhizal fungi that exhibit preferential host associations. By partnering with small-scale farmers of color, my dissertation focused on understanding the mechanisms in which crop diversity influences below- and above-ground interactions, and their connections (AMF to pollination).The first part of my dissertation examined how crop diversity (monoculture versus polycultures)affected AMF and pollinator communities in the intensively managed agricultural region in California’s San Joaquin Valley. I examined how crop diversity influences several aspects of AMF communities: (1) richness and diversity, (2) composition, and (3) colonization. I demonstrate that crop diversity enriches AMF communities, counteracting the negative effects of agricultural intensification, providing the potential to increase agroecosystem functioning and sustainability. Next, to investigate the impact of on-farm diversification on pollinator communities, I focused on how specialist squash bees (Peponapis genera) responded to crop diversity (monoculture versus polyculture) using squash (Cucurbita pepo) as the focal crop. I hypothesized that squash bees would be more abundant on monocultures, due to greater numbers of squash flowers, than polycultures. Despite this, I found that increasing non-squash floral resource diversity in polycultures supports a greater abundance of squash bees. On-farm diversification may be an important refuge for specialist bees that are vulnerable in landscapes dominated by agriculture.The second part of my dissertation sought to more closely characterize mechanisms that enhancepollination services critical to promoting food security. While aboveground floral visitors provide pollination services to plants, belowground AMF could enhance the quality of floral resources (pollen and nectar). Yet, the effect of the AMF community composition on pollination is still unclear because existing studies consist of a single AMF species or disregard the interacting effect of soil nutrient availability. Therefore, in a controlled greenhouse and field experiment, I investigated how different levels of AMF diversity and nutrient availability impacted floral resources and pollinator visitation. Our results demonstrate that greater AMF diversity, regardless of nutrient availability, has the largest positive effect on floral resource quality and pollinator visitation, an indicator of pollination services.Altogether, this dissertation points to the effects of crop diversity on belowground and abovegroundbiodiversity that could bolster ecosystem functions. By working directly with small-scale farmers of color, this research also outlines potential pathways that farmers can take towards harnessing beneficial ecosystem functions. Importantly, the results demonstrate that crop diversification could help to recover biodiversity from below- to above-ground even in the intensively managed region in California’s San Joaquin Valley

On-Farm Diversification in an Agriculturally-Dominated Landscape Positively Influences Specialist Pollinators

Agricultural practices can either contribute to pollinator decline or provide opportunities to support pollinator communities. At the landscape-scale, agriculture can have negative impacts on pollinators, especially pollinators that specialize on limited floral or nesting resources. While increasing floral resources at the field-scale is positive for pollinator communities, little is known about how it affects specialist bees that depend on a specific pollen source (oligoleges). We studied pollinators on small-scale farms that contrasted in crop diversity (monocultures vs. polycultures), embedded in the intensively managed agriculture region of the San Joaquin Valley in California, to understand how wild bee communities and specialist bees would respond to field-scale diversification practices. We used squash (Cucurbita pepo) as our focal crop, because it is visited by both specialist pollinators, “squash bees” in the genera Peponapis and Xenoglossa, and by generalist bees like those in the genera Apis and Agapostemon. We hypothesized that there would be a greater number of squash bees on monoculture farms, which have abundant squash flowers, than on polyculture farms. Contrary to our predictions, we found that increasing the number of non-squash floral resources at the field-scale in agroecosystems supports a greater abundance of squash bees but has no effect on the diversity of bees visiting squash flowers. This pattern of increased abundance was consistent for other wild bees and the total number of bees (i.e., including honey bees), but not for honey bee abundance alone. Further, the abundance of pollinators increased or remained the same on polyculture farms throughout the morning while decreasing on monoculture farms, suggesting that as squash flowers start to close in midmorning, bees on the monocultures go elsewhere because no other floral resources co-occur. However, they remain on the polycultures where other resources co-occur. Thus, on-farm diversification may be an important refuge for both specialist bees and other pollinator species that are vulnerable to floral resource simplification as a result of development, especially through monoculture agriculture

On-Farm Diversification in an Agriculturally-Dominated Landscape Positively Influences Specialist Pollinators

Agricultural practices can either contribute to pollinator decline or provide opportunities to support pollinator communities. At the landscape-scale, agriculture can have negative impacts on pollinators, especially pollinators that specialize on limited floral or nesting resources. While increasing floral resources at the field-scale is positive for pollinator communities, little is known about how it affects specialist bees that depend on a specific pollen source (oligoleges). We studied pollinators on small-scale farms that contrasted in crop diversity (monocultures vs. polycultures), embedded in the intensively managed agriculture region of the San Joaquin Valley in California, to understand how wild bee communities and specialist bees would respond to field-scale diversification practices. We used squash (Cucurbita pepo) as our focal crop, because it is visited by both specialist pollinators, “squash bees” in the genera Peponapis and Xenoglossa, and by generalist bees like those in the genera Apis and Agapostemon. We hypothesized that there would be a greater number of squash bees on monoculture farms, which have abundant squash flowers, than on polyculture farms. Contrary to our predictions, we found that increasing the number of non-squash floral resources at the field-scale in agroecosystems supports a greater abundance of squash bees but has no effect on the diversity of bees visiting squash flowers. This pattern of increased abundance was consistent for other wild bees and the total number of bees (i.e., including honey bees), but not for honey bee abundance alone. Further, the abundance of pollinators increased or remained the same on polyculture farms throughout the morning while decreasing on monoculture farms, suggesting that as squash flowers start to close in midmorning, bees on the monocultures go elsewhere because no other floral resources co-occur. However, they remain on the polycultures where other resources co-occur. Thus, on-farm diversification may be an important refuge for both specialist bees and other pollinator species that are vulnerable to floral resource simplification as a result of development, especially through monoculture agriculture

Neonicotinoid Sunflower Seed Treatment, While Not Detected in Pollen and Nectar, Still Impacts Wild Bees and Crop Yield

Neonicotinoid seed treatments are commonly used in agricultural production even though their benefit to crop yield and their impact on pollinators, particularly wild bees, remains unclear. Using an on-farm matched pair design in which half of each field was sown with thiamethoxam treated seed and half without, we assessed honey bee and wild bee exposure to pesticides in sunflower fields by analyzing pesticide residues in field soil, sunflower pollen and nectar, pollen-foraging and nectar-foraging honey bees, and a sunflower specialist wild bee (Melissodes agilis). We also quantified the effects of thiamethoxam-treated seed on wild bee biodiversity and crop yield. M. agilis abundance was significantly lower with thiamethoxam treatment and overall wild bee abundance trending lower but was not significantly different. Furthermore, crop yield was significantly lower in plots with thiamethoxam treatment, even though thiamethoxam was only detected at low concentrations in one soil sample (and its primary metabolite, clothianidin, was never detected). Conversely, wild bee richness was significantly higher and diversity was marginally higher with thiamethoxam treatment. Nectar volumes harvested from the nectar-foraging honey bees were also significantly higher with thiamethoxam treatment. Several pesticides that were not used in the sunflower fields were detected in our samples, some of which are known to be deleterious to bee health, highlighting the importance of the landscape scale in the assessment of pesticide exposure for bees. Overall, our results suggest that thiamethoxam seed treatments may negatively impact wild bee pollination services in sunflower. Importantly, this study highlights the advantages of the inclusion of other metrics, such as biodiversity or behavior, in pesticide risk analysis, as pesticide residue analysis, as an independent metric, may erroneously miss the impacts of field realistic pesticide exposure on bees

Crop diversity enriches arbuscular mycorrhizal fungal communities in an intensive agricultural landscape

Arbuscular mycorrhizal fungi (AMF) are keystone symbionts of agricultural soils but agricultural intensification has negatively impacted AMF communities. Increasing crop diversity could ameliorate some of these impacts by positively affecting AMF. However, the underlying relationship between plant diversity and AMF community composition has not been fully resolved. We examined how greater crop diversity affected AMF across farms in an intensive agricultural landscape, defined by high nutrient input, low crop diversity and high tillage frequency. We assessed AMF communities across 31 field sites that were either monocultures or polycultures (growing > 20 different crop types) in three ways: richness, diversity and composition. We also determined root colonization across these sites. We found that polycultures drive the available AMF community into richer and more diverse communities while soil properties structure AMF community composition. AMF root colonization did not vary by farm management (monocultures vs polycultures), but did vary by crop host. We demonstrate that crop diversity enriches AMF communities, counteracting the negative effects of agricultural intensification on AMF, providing the potential to increase agroecosystem functioning and sustainability

Crop diversity enriches arbuscular mycorrhizal fungal communities in an intensive agricultural landscape.

Arbuscular mycorrhizal fungi (AMF) are keystone symbionts of agricultural soils but agricultural intensification has negatively impacted AMF communities. Increasing crop diversity could ameliorate some of these impacts by positively affecting AMF. However, the underlying relationship between plant diversity and AMF community composition has not been fully resolved. We examined how greater crop diversity affected AMF across farms in an intensive agricultural landscape, defined by high nutrient input, low crop diversity and high tillage frequency. We assessed AMF communities across 31 field sites that were either monocultures or polycultures (growing > 20 different crop types) in three ways: richness, diversity and composition. We also determined root colonization across these sites. We found that polycultures drive the available AMF community into richer and more diverse communities while soil properties structure AMF community composition. AMF root colonization did not vary by farm management (monocultures vs polycultures), but did vary by crop host. We demonstrate that crop diversity enriches AMF communities, counteracting the negative effects of agricultural intensification on AMF, providing the potential to increase agroecosystem functioning and sustainability

Narrow and Brittle or Broad and Nimble? Comparing Adaptive Capacity in Simplifying and Diversifying Farming Systems

Humanity faces a triple threat of climate change, biodiversity loss, and global food insecurity. In response, increasing the general adaptive capacity of farming systems is essential. We identify two divergent strategies for building adaptive capacity. Simplifying processes seek to narrowly maximize production by shifting the basis of agricultural production toward centralized control of socially and ecologically homogenized systems. Diversifying processes cultivate social-ecological complexity in order to provide multiple ecosystem services, maintain management flexibility, and promote coordinated adaptation across levels. Through five primarily United States focused cases of distinct agricultural challenges—foodborne pathogens, drought, marginal lands, labor availability, and land access and tenure—we compare simplifying and diversifying responses to assess how these pathways differentially enhance or degrade the adaptive capacity of farming systems in the context of the triple threat. These cases show that diversifying processes can weave a form of broad and nimble adaptive capacity that is fundamentally distinct from the narrow and brittle adaptive capacity produced through simplification. We find that while there are structural limitations and tradeoffs to diversifying processes, adaptive capacity can be facilitated by empowering people and enhancing ecosystem functionality to proactively distribute resources and knowledge where needed and to nimbly respond to changing circumstances. Our cases suggest that, in order to garner the most adaptive benefits from diversification, farming systems should balance the pursuit of multiple goals, which in turn requires an inclusive process for active dialogue and negotiation among diverse perspectives. Instead of locking farming systems into pernicious cycles that reproduce social and ecological externalities, diversification processes can enable nimble responses to a broad spectrum of possible stressors and shocks, while also promoting social equity and ecological sustainability

What are mycorrhizal traits?

Traits are inherent properties of organisms, but how are they defined for organismal networks such as mycorrhizal symbioses? Mycorrhizal symbioses are complex and diverse belowground symbioses between plants and fungi that have proved challenging to fit into a unified and coherent trait framework. We propose an inclusive mycorrhizal trait framework that classifies traits as morphological, physiological, and phenological features that have functional implications for the symbiosis. We further classify mycorrhizal traits by location – plant, fungus, or the symbiosis – which highlights new questions in trait-based mycorrhizal ecology designed to charge and challenge the scientific community. This new framework is an opportunity for researchers to interrogate their data to identify novel insights and gaps in our understanding of mycorrhizal symbioses.The iCOMET workshop was supported by the Natural Environmental Research Council (grant number NE/S008543/1). V.B.C. is supported by the National Science Foundation (award DEB-1844531)