Elsevier

Food Webs

Volume 27, June 2021, e00194
Food Webs

Interactions between plants and pollinators across urban and rural farming landscapes

https://doi.org/10.1016/j.fooweb.2021.e00194Get rights and content

Abstract

Arthropods are responsible for pollinating the majority of food and fuel crops worldwide. However, global declines in bee populations threaten the delivery of pollination services in both managed and natural ecosystems. Alternative pollinators such as flies, butterflies, beetles, and wasps may provide a buffer that protects agriculture from bee population declines. Flower-visiting flies are abundant in both rural and urban agricultural settings, and in some cases may pollinate plants avoided by bees. Here we explored the structure of plant-pollinator networks for both bee and non-bee pollinator communities across rural and urban farms in western Washington State, USA. We identified several broad groups of pollinators comprising 13 morphogroups of insects and arthropods. While bees were the pollinators observed on reproductive parts of flowers most frequently, syrphid flies contributed to a high number of arthropod-flower visits. We also found that syrphid flies visited four plant types not visited by bees, and that urban and rural farm settings were characterized by different syrphid fly communities. When comparing the networks of plant-arthropod interactions, urban farm settings had more diverse networks overall, with a greater richness of plant-arthropod interactions for both bee and non-bee pollinators. These findings underscore the need for greater focus on alternative pollinators as contributors to pollination services, particularly in urban settings where pollination services may be more impacted by bee declines and habitat loss. Our work will inform specific pollinator conservation efforts in the Pacific Northwest region and more broadly across the United States.

Introduction

Arthropods pollinate the majority of fruit, vegetable, and nut crops consumed around the world (Klein et al., 2007). Honey bees (Apis mellifera) are key pollinators in agriculture because they can be managed within large colonies, and they effectively pollinate many crops (Garibaldi et al., 2013). However, the number of honey bee colonies has dramatically declined in recent years due to factors such as agricultural intensification, habitat loss, and disease (Tylianakis et al., 2007; Goulson et al., 2015). In turn, researchers have increasingly begun to assess the importance of alternative pollinators, although nearly all of this research has focused on wild bee species (Rader et al., 2009; Garibaldi et al., 2013). Unfortunately, wild bee species have also experienced widespread declines in abundance and diversity (Tylianakis, 2013; Goulson et al., 2015).

The drastic decline in bee populations threatens global food security and sustainable agriculture. Accordingly, an increased understanding of the role that non-bee arthropods play as pollinators on farms may benefit agricultural productivity and inform conservation efforts. Many species of flies (Diptera), moths and butterflies (Lepidoptera), wasps (Hymenoptera), and beetles (Coleoptera) can function as pollinators in certain crop systems (Listabarth, 2001; Rader et al., 2012). If non-bee arthropods provide effective pollination services, they could promote sustainable crop pollination while providing insurance against ongoing bee losses. It is worth noting that populations of non-bee pollinators are also declining, but they are present in many different types of ecosystems and a number of studies have shown that pollinator-friendly habitats support non-bee arthropods as well as bees (Bates et al., 2011; Winfree et al., 2011; Rader et al., 2016). Few studies, however, have examined the role of non-bee pollinators or their impacts in real-world farming systems.

In addition to pollinating crops, non-bee arthropods may provide complementary pollination services to bees in space or time (Rader et al., 2012). Wild bees often complement honey bees by pollinating different crops, and can promote pollination efficiency when they encourage competition with honey bees. The presence of wild bees has been shown to increase honey bee movement through crops (Garibaldi et al., 2013). If non-bee species similarly complement bees by increasing overall pollinator visitation, or increasing bee pollination through competition, their presence could promote sustainable crop pollination. Non-bee arthropods might also indirectly affect pollination services by mediating bee behavior. This could serve as another form of competition, through the use of resources. For example, bees use olfactory cues to detect whether a flower has already been visited by another bee or fly in an effort to determine if the nectar resources are already depleted and thus increasing the efficiency of their foraging trip, known as exploitive competition (Goulson et al., 2001; Reader et al., 2005).

Patterns of insect-plant interactions are often indirectly impacted by landscape factors, such that landscape context might communities of bees and non-bee pollinators (Bloom et al., 2019). For example, while urban areas typically have less habitat and nesting sites for ground dwelling bees, landscaped areas and community gardens often provide a rich diversity of different types of flowers throughout a season (Ahrné et al., 2009; Bates et al., 2011). More diverse flower communities could drive increased diversity in arthropod communities (Fründ et al., 2010). In contrast, rural areas often provide less diversity, but greater overall floral resource availability, particularly in areas with mass-flowering crop fields (Bates et al., 2011). These areas also tend to offer more nesting sites due to reduced paved areas, but floral resources in less rich plant communities may only available for short time periods (Choate et al., 2018) . Each of these settings may thus support different arthropod communities (Ahrné et al., 2009), where urban areas with higher floral diversity may support a greater number of specialist arthropods, whereas rural areas with a flush of food resources may support a higher diversity of generalists. Interactions between bees and non-bees might thus differ across urban and rural landscapes due in part to the potential interactions being different solely based on the makeup of insect and plant communities. Characterizing plant-pollinator networks across various landscape contexts can be used to assess the relationships between plants and pollinators, where networks with more unique links and more complementary links are more robust (Ibanez, 2012).

Here, we compared communities of pollinating arthropods, and plant-pollinator network structure, in urban and rural farming systems. Our work was conducted in collaboration with a network of organic diversified vegetable farms in western Washington State, USA. These farms support diverse communities of bee and non-bee pollinators (Crowder et al., 2012; Bloom et al., 2019). As the demand for organic food increases globally (Kristiansen et al., 2006), a better understanding of bee and non-bee pollinators on organic farms could help guide development of sustainable crop pollination strategies. Because the majority of farms in our study system require pollination of many different plant types during a season, stable pollinator communities are essential. Based on the dynamic availability of resources on these different farm types, we hypothesized that urban farms would support a higher richness of pollinating arthropods due to the increased floral richness, while rural farms would support a higher abundance due to increased floral abundance. Further, we expected these farms to support different communities based on the different availabilities of habitat and food resources. Finally, we anticipated strong differences in the networks of non-bee arthropods and plants in these different farm types, again being driven by the differences in plants and arthropods at each landscape type.

Section snippets

Farm selection

We conducted our research on 24 diversified produce farms in 2015. In 2016, we resampled 22 of those 24 farms, and we added an additional 13 farms in 2016, for a total of 35 farms in 2016, and 37 unique farms across both years across urban and rural landscape types in western Washington State, USA (Fig. 1). Each farm was less than 10 ha and either certified organic or used only practices associated with organic production (i.e., no synthetic inputs). Each farm produced at least one variety each

Characterizing the plant and arthropod communities in rural and urban farms

In 2015, we extensively sampled the entire pollinator community and recorded a total of 2405 arthropod visits to the reproductive structures of flowers. Bees of all morphogroups made up ~61% of these visits, followed by flies with ~35% of the visits. Visits by other groups of non-bee arthropods including wasps, lacewings, spiders, butterflies, dragonflies, beetles, and ants were relatively rare, making up the remaining ~4% of visits. We recorded a total of 46 different types of flowering plants

Discussion

We observed support for the hypotheses we tested in this study, seeing greater richness and diversity of flowers and pollinators on urban farm sites, but greater abundance of flowers and pollinators on rural farms. Our study showed that the floral communities are different on urban and rural farms, and thus should promote different pollinator communities. We saw vastly different fly communities between the two landscape types, which we expected based on the differences in resources available,

Declaration of competing interest

The authors whose names are listed immediately below certify that they have NO affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers' bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in

Acknowledgements

Funding was provided by Western SARE (Graduate Grant GW16-033), USDA AFRI (Awards 2014-51106-22096 and 2018-67011-28021) and USDA Hatch Project 1014754. We would like to thank our grower partners as well as P.B. Ironhorse, C. Looney, E. Bloom, H. Harris, A. Blattenbauer, and M. Bernstein who assisted with data collection for this project, and M. Sherwood and R. Ryan for their support in preparing this manuscript. Finally, we would like to thank our friends and family.

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