UC Santa Cruz UC Santa Cruz Electronic Theses and Dissertations
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UC Santa Cruz UC Santa Cruz Electronic Theses and Dissertations Title Competitive context drives pollinator behavior: linking foraging plasticity, natural pollen deposition, and plant reproduction Permalink https://escholarship.org/uc/item/50t4x0nx Author Briggs, Heather Mae Publication Date 2016 Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California UNIVERSITY OF CALIFORNIA SANTA CRUZ COMPETITIVE CONTEXT DRIVES POLLINATOR BEHAVIOR: LINKING FORAGING PLASTICITY, NATURAL POLLEN DEPOSITION, AND PLANT REPRODUCTION A dissertation submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in ENVIRONMENTAL STUDIES by Heather Mae Briggs June 2016 The Dissertation of Heather Mae Briggs is approved: __________________________________ Professor Gregory Gilbert, chair __________________________________ Professor Ingrid Parker __________________________________ Associate Professor Berry J. Brosi __________________________________ Professor Brent Haddad _____________________________ Tyrus Miller Vice Provost and Dean of Graduate Studies Table of Contents List of Figures iv List of Tables v Abstract vi Acknowledgements ix Introduction 1 Chapter 1 7 Single pollinator species losses reduce floral fidelity and plant reproductive function. Chapter 2 31 Heterospecific pollen deposition in Delphinium barbeyi: linking stigmatic pollen loads to reproductive output in the field. Chapter 3 59 Reponses of pollinators to reductions in interspecific competition are context-dependent and correlated with bee tongue length. Chapter 4 89 Not all interactions are positive: testing the robustness of plant-pollinator networks to extinction simulations after incorporating negative interactions. Discussion 123 iii List of Figures 1-1. Floral fidelity and pollination function. 27 1-2. Floral fidelity, pollen carriage, and stigmatic pollen deposition. 28 1-3. Seed production 29 2-1. Natural pollen deposition in Delphinium barbeyi. 53 2-2. Relationship between heterospecific pollen and conspecific pollen. 54 2-3. Effect of conspecific and heterospecific pollen deposition on 55 probability of viable seed production. 3-1. Random intercept coefficient estimates for each site from M3. 80 3-2. Predicted values of the three fixed effects 81 (tongue length, manipulated tongue length and state) from M4. 3S-1. Random permutation of tongue length values across sites. 82 4-1. Extinction patterns for the three pollination networks (a) Dupont, 113 (b) Arroyo and (c) Clemens. 4-2. Effects of negative interactions on network robustness during 114 pollinator knockout simulations for different extinction orders and starting networks. 4-3. Effects of negative interactions on total number of extinction cascades 115 occurring during pollinator knockout simulations for different extinction orders and starting networks. iv List of Tables 1-1. Statistical results 31 2-1. Results of generalized mixed-effects models with binomial errors. 56 3-1. Tongue lengths of sympatric Bombus spp. 83 3-2. Results of generalized linear mixed-effects models with binomial errors. 85 4-1. Results of network robustness (R) GLMs 116 for each network separately. 4-2. Results of network robustness (R) GLMs 117 for each extinction order separately. 4-3. GLM results for total number of cascades vs. PNI 118 for each network separately. 4-4. GLM results for total number of cascades vs. PNI 119 for each order separately. v Abstract Competitive Context Drives Pollinator Behavior: Linking Foraging Plasticity, Natural Pollen Deposition, And Plant Reproduction With ongoing global pollinator declines it is important to understand the functional impact of pollinator species losses. While network-based simulation models of pollinator declines predict that plant communities will be robust to losses of pollinator species, these predictions have never been tested empirically. In four chapters, my dissertation uses both empirical and modeling approaches to explore the impacts of losing pollinator species in alpine plant communities. First, I test the hypothesis that interspecific interactions among pollinators (rather than fixed species roles) dynamically alter the functional contribution of species in a community and that these dynamic roles can sometimes reduce plant reproductive function. Experimental removal of the most abundant bumble bee pollinator species from an alpine bumblebee community led to a reduction in floral fidelity in the remaining pollinators. Importantly, this behavioral response in the remaining pollinators reduced plant reproduction by increasing the transfer of ineffective heterospecific pollen. Second, I evaluate how patterns of naturally deposited heterospecific pollen relate to the reproductive output of Delphinium barbeyi, a common subalpine perennial herb in the Rocky Mountains. I found a significant negative interaction between conspecific pollen and the amount of heterospecific pollen whereby the vi relationship between conspecific pollen and viable seed production became weaker with increasing heterospecific pollen deposition on stigmas. Third, I explore how traits—specifically pollinator tongue length, which dictates pollinator resource partitioning—influences how pollinators responded to reduced interspecific competition. I found that bees vary in their baseline floral fidelity and that their tongue length explained a large part of this variation. Bees with shorter tongues moved between plant species (floral infidelity) more often than bees with longer tongues. I did not find significant variation in how bee species responded to reduced interspecific competition, but rather saw a guild-wide reduction in floral fidelity in response to the removal of the dominant bee species. Interestingly, I found that competitive context determines the floral fidelity of the pollinators in a community. In this case, as the tongue length of the most abundant bee increases, the site level foraging fidelity decreases. Network model simulations predict plant populations will be resilient when faced with pollinator extinctions. Importantly, these models are built on the assumption that all interactions in networks are positive, potentially overestimating the resilience of plant-pollinator networks. A wide range of studies (including my field work) have shown that many pollinators are actually ineffective at pollinating plant species they visit, and can therefore have negative consequences for plant reproduction. Fourth, I used interaction network simulations to understand how the addition of negative interactions impacts the predictions of resilience when plant communities are faced with pollinator species losses. I found that the addition of vii negative interactions makes networks less robust to pollinator extinctions, but not always in the same way. This work suggests metrics specific to interaction networks may be important in determining how robust plant-pollinator interactions are to extinctions. Finally I provide overview on some of the causes and consequences of pollinator decline in the US and offer insight in to how my basic research in to pollinator ecology can help pinpoint vulnerable species and communities that should be targeted for conservation efforts. viii To PTH and LJH — the brightest lights at the end of the tunnel. ix Acknowledgements The path was anything but direct, but I found my way to the end of this dissertation through the help and dedication of many friends, loved ones, and colleagues. Thank you to my committee who exhibited patience and encouragement throughout this process. To Brent Haddad, thank you for encouraging me through to the end. Your guidance and calm nature was much appreciated. To Ingrid Parker, thank you for your invaluable advice and suggestions. Your dedication to your family and your work are inspiring and something that I will refer back to throughout my life and I thank you for that. To Berry Brosi, thank you for introducing me to the Rocky Mountain Biological Lab back in 2010. RMBL was and will remain a place of solace, of friendship, of dance parties and dinner parties, of love and loss. Thank you for letting me be a part of your vision. I learned so much up in those mountains and I appreciate you helping me become a part of that community. To Greg Gilbert, thank you for adopting me early on despite my unrelated interests and hard headedness. You have helped me become a better communicator in life and in science and that is an invaluable skill. Thank you. To the staff of the Rocky Mountain Biological Laboratory, you make beautiful things happen for so many aspiring scientists. Thank you for doing what you do. To the lovely and inspiring friends I made while completing this work at RMBL, Paul Caradonna, Amy Iler, Ross Brennan, Sarah Richman, Kara Cromwell, billy barr, Jane Oglive, Will Petry, Nick Waser and Mary Price. Thank you for your love and guidance. Lucy Anderson, you are the single best research assistant on the planet. x Your enthusiasm for life and love is incredible and contagious. You continue to inspire me daily and I am so grateful for what has grown in to a very special friendship. Thank you to both Dan Papaj and Judie Bronstein for giving me an intellectual home in Tuscon. To my fantastic cohort, Sarah Carvill, Sharifa Crandall, Costanza Rampini, Lewis Reed, Tiffany Wise-West, Catherine Wade and Veronica Yovovich. You ladies are a constant inspiration. To my patient and loving family. Thank you for supporting me through grad school even though it