The Pennsylvania State University The Graduate School Intercollege Graduate Degree Program in Ecology PLANT-POLLINATOR MUTUALISMS: COMMUNITY STRUCTURE, FUNCTION AND MANAGEMENT A Dissertation in Ecology by Laura Russo 2013 Laura Russo Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2013 The dissertation of Laura Russo was reviewed and approved* by the following: Katriona Shea Professor of Biology Dissertation Advisor Co-Chair of Committee David Mortensen Professor of Plant Sciences Co-chair of Committee John Tooker Assistant Professor of Entomology Ottar Bjørnstad Professor of Entomology and Biology David Eissenstat Professor of Woody Plant Physiology Chair of the Intercollege Graduate Degree Program in Ecology *Signatures are on file in the Graduate School iii ABSTRACT This thesis combines both experimental work and theoretical models to address the taxonomic and phenological structure of mutualistic interactions between plants and pollinators, implications for management and conservation of ecosystem services in agroecosystems, and potential impacts of perturbations on the structure of these interactions. I explore the utility of network theoretical models in quantifying, visually representing, and analyzing mutualistic community structure, as well as the potential for such models to direct management objectives. The first chapter is an introduction that gives an overview and definitions of frequently used terms in the work. It is followed by an investigation of the importance of taxonomy in structuring mutualistic interactions (chapter two). Using a large legacy dataset of plants and insect visitors, I provide evidence that specialization at the regional level is lineage-specific and find that patterns of significant taxonomic conservatism are common; in other words, closely related species are more likely to interact with similar partners. I also identify groups of plant species and their insect visitors that have correlated taxonomies, suggesting subsets of strongly interacting groups within the whole. Communities of wild bees have been shown to be capable of fully supplying the pollination requirements of agricultural fields. For this reason, many land managers seek to supplement the pollination services provided by honeybees by supporting the diversity and abundance of wild bees. In chapter three, I identify plant species capable of provisioning communities of wild bees with floral resources, and demonstrate how floral iv provisioning habitat can be targeted to support individual species, or groups of species, over time. In chapter four, I construct theoretical models to explore the impact of the integration of a novel plant species into a community of interacting plants and pollinators. I find that the impact of a novel species on community structure is mediated both by the number and type of interactions it forms with native species. Testing experimental data from a community of plants and pollinators, I find that certain network properties are reliably predicted by these interaction models, while more complex properties are dependent on link identity. Though much of this work focuses on communities of pollinators specifically adapted to the collection of floral resources, I also demonstrate that groups of lesser- known taxa can contribute to pollination services, and that their association with plants can be important for one or both of the interacting organisms. In chapter five, I therefore emphasize the importance of capturing and examining groups of species other than those which are commonly thought to be the most important floral visitors as a way of quantifying the diversity of arthropods. I have also found that disturbances, such as species invasions, do not always necessarily have negative connotations for mutualistic partners. Indeed, I show in chapter six that the weed species that persist in marginal habitat may be strongly preferred by groups of threatened pollinators, and therefore may contribute significantly to the persistence of pollinator communities. Thus, the invasion of non-native species may have both detrimental and beneficial effects. v Finally, in chapter seven, I find that structural properties of the interactions between plants and insects can be manipulated on a community level. In addition, I find that subtle manipulations can lead to large changes in the composition of plant-pollinator communities. I also show that insects forage opportunistically and respond rapidly to perceived changes in the quality and attractiveness of flowers. Thus, the identity of the species in the community does strongly influence the structure of interactions. Using community-level approaches, as I do in this thesis, demonstrates that networks can be a useful tool for studying emergent ecosystem services, such as pollination. I synthesize my findings in a conclusion chapter (chapter eight). Overall, I find that the structure of mutualisms between plants and insect visitors can provide insights into both fundamental ecological questions and applied contemporary challenges. vi TABLE OF CONTENTS List of Figures .............................................................................................................. ix List of Tables ............................................................................................................... xiv Acknowledgements ...................................................................................................... xvi Chapter 1 Introduction ................................................................................................. 1 References ..................................................................................................... 8 Chapter 2 The taxonomic structuring and conservatism of plants and their insect visitors................................................................................................................... 15 Abstract ................................................................................................................. 15 Introduction ................................................................................................... 16 Materials and Methods .................................................................................. 19 Results ........................................................................................................... 23 Discussion ...................................................................................................... 25 Acknowledgements ....................................................................................... 30 Author contributions ...................................................................................... 31 References ..................................................................................................... 31 Tables ............................................................................................................ 37 Figures ........................................................................................................... 39 Chapter 3 Supporting crop pollinators with floral resources: network-based phenological matching .......................................................................................... 43 Abstract ................................................................................................................. 43 Introduction ................................................................................................... 44 Material and Methods .................................................................................... 48 Results ........................................................................................................... 54 Discussion ...................................................................................................... 59 Conclusions ................................................................................................... 63 Acknowledgements ....................................................................................... 64 Author contributions ...................................................................................... 65 References ..................................................................................................... 65 Tables ............................................................................................................ 72 Figures ........................................................................................................... 75 Chapter 4 Patterns of novel species interaction formation affect network structure in plant-pollinator communities ............................................................................ 83 vii Abstract ................................................................................................................. 83 Introduction ................................................................................................... 84 Methods ......................................................................................................... 87 Results ........................................................................................................... 95 Discussion ...................................................................................................... 98 Acknowledgments ......................................................................................... 103 Author contributions .....................................................................................