UNIVERSITY of CALIFORNIA, SAN DIEGO Effects of Habitat Fragmentation and Introduced Species on the Structure and Function Of

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UNIVERSITY of CALIFORNIA, SAN DIEGO Effects of Habitat Fragmentation and Introduced Species on the Structure and Function Of UNIVERSITY OF CALIFORNIA, SAN DIEGO Effects of Habitat Fragmentation and Introduced Species on the Structure and Function of Plant-Pollinator Interactions A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Biology by Keng-Lou James Hung Committee in charge: Professor David A. Holway, Chair Professor Joshua R. Kohn Professor Lisa A. Levin Professor Jean-Bernard H. Minster Professor James C. Nieh 2017 © Keng-Lou James Hung, 2017 All rights reserved. The Dissertation of Keng-Lou James Hung is approved, and it is acceptable in quality and form for publication on microfilm and electronically: Chair University of California, San Diego 2017 iii DEDICATION This dissertation is dedicated to my parents, who stopped at nothing to nurture my intellectual curiosity; to my brother, who was my ever-reliable field assistant and encourager; and to my wife, who gave up everything she had to make this venture a reality. This dissertation is as much a product of my hard work as it is your unconditional love, support, and prayers. This dissertation is also dedicated to the 43,000 bees, wasps, flies, and other insects whose curtailed lives will be forever immortalized in data that will one day be used to secure a brighter future for their kind. You took one for the team; thank you for your sacrifice. iv TABLE OF CONTENTS Signature Page ................................................................................................................. iii Dedication ........................................................................................................................ iv Table of Contents .............................................................................................................. v List of Figures .................................................................................................................. vi List of Tables ................................................................................................................ viii Acknowledgments ............................................................................................................. x Vita ................................................................................................................................. xiii Abstract of the Dissertation ........................................................................................... xiv Chapter 1: Urbanization-Induced Habitat Fragmentation Erodes Multiple Components of Temporal Diversity in a Southern California Native Bee Assemblage .................................................................................................... 1 Chapter 2: Parallel Loss of Taxonomic and Functional Diversity in Native Bee Assemblages Inhabiting Fragments of Well-Preserved Scrub Habitat in Southern California .............................................................................. 32 Chapter 3: Plant-Pollinator Interaction Networks in Fragmented Habitats Retain Structural Robustness in Spite of Pollinator Diversity Loss ................................................................................................................................. 82 Chapter 4: The Worldwide Importance of Honey Bees as Pollinators in Natural Habitats ............................................................................................................ 119 v LIST OF FIGURES Figure 1-1. Hypothetical scenarios of disturbance impacting temporal gamma, alpha, and beta diversity of an assemblage. ..................................................... 21 Figure 1-2. Temporal gamma diversity of native bees in reserve (gray boxes) and fragment plots (white boxes). ...................................................................... 22 Figure 1-3. Temporal alpha diversity of native bees in reserve and fragment plots in 2011 (A-D) and 2012 (E-H). ............................................................. 23 Figure 1-4. Temporal beta diversity of native bees in reserve (gray boxes) and fragment plots (white boxes). ........................................................................ 24 Figure 2-1. Alpha diversity of native bees in reserve and fragment plots. ................................................................................................................................ 56 Figure 2-2. Non-metric multidimensional scaling (NMDS) ordination plots of bee assemblages in reserve plots (gray circles) and fragment plots (white circles), with respect to taxonomic (A-B) and functional (C-D) composition. ........................................................................................................ 57 Figure 2-3. Bee faunas in reserve and fragment plots with respect to the relative representation of each functional trait. ........................................................ 58 Figure 2-4. Average range sizes of bee assemblages in reserves and fragments. ........................................................................................................................ 59 Figure 2-S1. Distribution of P-values from comparisons of beta diversity (A-B) and assemblage composition (C-D) between reserve and fragment plots in the 2012 dataset (n = 1,000 permutations). ................................. 64 Figure 3-1. Plant-pollinator interaction network metrics that responded to habitat fragmentation, pollinator diversity loss, or both. .......................................... 105 Figure 3-2. The role of honey bees in plant-pollinator interaction networks. ....................................................................................................................... 106 Figure 3-3. Year-to-year variation in the network statistics examined in our study. ....................................................................................................................... 107 Figure 4-1. Relative visitation frequencies of the western honey bee in 80 plant-pollinator interaction networks in natural habitats worldwide. ...................... 137 vi Figure 4-2. The distribution of plant species with respect to the proportion of their total recorded floral visits contributed by honey bees. .............................................................................................................................. 138 Figure 4-3. Relative efficiency of honey bees compared to other studied pollinators with respect to the ability to deposit pollen or effect fruit or seed set with a single visit. ............................................................................... 139 vii LIST OF TABLES Table 1-S1. List of utilized study plots in coastal sage scrub reserves and habitat fragments. .................................................................................................... 26 Table 2-1. Functional traits of native bees used in analyses of functional diversity. ...................................................................................................... 60 Table 2-2. Variance of functional traits for the taxonomic ranks of family, subfamily, and genus. ......................................................................................... 60 Table 2-3. Spearman rank correlations among functional traits. .................................... 61 Table 2-4. Results of two-sample t-tests comparing bee assemblages in reserve and fragment plots with respect to the relative representation of each functional trait. ........................................................................................................ 61 Table 2-5. Bee species and functional groups exhibiting significant associations with scrub reserve plots in each study year. ............................................... 62 Table 2-S1. Functional traits, functional group membership, and range size of each bee species and morphospecies included in our study. ............................... 65 Table 2-S2. Results of main analyses performed on the full dataset (i.e., with the inclusion of both bee specimens collected via aerial net and bowl traps) and on genus-level data (genus-level mean or modal averages were used for functional traits and range size). ............................................... 72 Table 2-S3. Results of analyses of taxonomic and functional beta diversity and assemblage composition, performed with the exclusion of indicator species associated with reserves. ................................................................. 73 Table 3-S1. List of utilized study plots in coastal sage scrub reserves and habitat fragments. .................................................................................................. 108 Table 3-S2. Re-analyses examining the impact of pollinator diversity loss on structural properties of plant-pollinator interaction networks, with honey bees excluded from the dataset. ................................................................. 110 Table 4-1. The best multiple linear regression model relating environmental variables to honey bee relative visitation frequency in plant-pollinator interaction networks worldwide (n = 54 networks where honey bees were present). ................................................................................. 140 Table 4-S1. Pollination networks (n = 80) used in addressing research questions 1 through 4. .................................................................................................. 141 viii Table 4-S2. The best zero-inflated multiple beta regression model relating environmental variables to the distribution of honey bee relative
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