University of Vermont ScholarWorks @ UVM Graduate College Dissertations and Theses Dissertations and Theses 2018 Investigating The ffecE ts Of Ant-Hemipteran Mutualisms On The nI vertebrate Community Structure And Their oH st Plant, Honey Mesquite (prosopis Glandulosa) Nabil Nasseri University of Vermont Follow this and additional works at: https://scholarworks.uvm.edu/graddis Part of the Botany Commons, Ecology and Evolutionary Biology Commons, and the Entomology Commons Recommended Citation Nasseri, Nabil, "Investigating The Effects Of Ant-Hemipteran Mutualisms On The nI vertebrate Community Structure And Their osH t Plant, Honey Mesquite (prosopis Glandulosa)" (2018). Graduate College Dissertations and Theses. 971. https://scholarworks.uvm.edu/graddis/971 This Dissertation is brought to you for free and open access by the Dissertations and Theses at ScholarWorks @ UVM. It has been accepted for inclusion in Graduate College Dissertations and Theses by an authorized administrator of ScholarWorks @ UVM. For more information, please contact [email protected]. INVESTIGATING THE EFFECTS OF ANT-HEMIPTERAN MUTUALISMS ON THE INVERTEBRATE COMMUNITY STRUCTURE AND THEIR HOST PLANT, HONEY MESQUITE (PROSOPIS GLANDULOSA) A Dissertation Presented by Nabil Nasseri to The Faculty of the Graduate College of The University of Vermont In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Specializing in Biology October, 2018 Defense Date: March 23, 2018 Dissertation Examination Committee: Alison K. Brody, Ph.D. Advisor Josef H. Görres, Ph.D., Chairperson Sara Helms Cahan, Ph.D Nicholas J. Gotelli, Ph.D Cynthia J. Forehand, Ph.D., Dean of the Graduate College ABSTRACT Ants are ubiquitous in most communities and many form opportunistic mutualisms with honeydew-producing hemipterans (e.g. treehoppers). Hemipterans excrete honeydew, a carbohydrate rich substance, that ants harvest and, in return, ants protect their honeydew- producing partners from parasitoids, predators, and competitors. Given the efficacy of tending ants in removing hemipteran antagonists, and the strong roles that ants play within their communities as predators, competitors, and seed dispersers, surprisingly little is known of the effects of ant-hemipteran mutualisms (AHM) on the invertebrate communities in which they are embedded or on the plants that host AHM. Using observational and manipulative field experiments, I examined the long-term effect of AHM on their host plant’s, honey mesquite (Prosopis glandulosa), reproductive potential and quality. In addition, I measured how the presence of AHM affects the abundance, richness, diversity, and composition of the invertebrate communities living on honey mesquite. Plants hosting AHM may indirectly benefit (through the removal of herbivore arthropods) or suffer (through the loss pollinators) due to the defensive behavior of tending ants. To determine the effects of AHM on their host plant, I established a four-year press experiment in which I removed AHM from 50 randomly trees, while leaving 50 as controls. In addition, I marked and followed 30 trees from which AHM were naturally absent. To assess if mesquite quality differed between trees hosting AHM and trees in which AHM were naturally absent, in 2012 I assayed foliar condensed tannin concentrations, a secondary defense compound, and, in 2015, I measured foliar nitrogen, phosphorous, potassium, magnesium, and iron as they are essential for growth and reproduction. I compared the reproductive potential between AHM present and removed trees by counting flowers and fruits across all 4 years of the study. Mesquite that hosted AHM contained significantly less condensed tannins and significantly higher concentrations of N%, Mg, and Fe. Furthermore, over the duration of the study mesquite hosting AHM contained significantly more flowers than those from which AHM were removed or naturally absent. My results indicate that AHM select trees of high quality and their continued presence is associated with high levels of reproductive potential. Most studies that have evaluated community-level effects of AHM compare total abundance and species richness in communities (or host plants) with and without AHMs. However, both measures are dependent on sampling effort, complicating comparisons across different studies. To examine the effects of AMH on the arthropod community in mesquite, I first compared family richness and alpha diversity using standardized rarefaction and extrapolation curves. I then measured beta diversity and turnover in community composition from one year to the next. The removal of AHM increased invertebrate diversity and significantly altered community composition. Although treatments did not statistically differ in turnover rates, replacements occurred among treatments at the family level which may be biologically meaningful. Furthermore, herbivore and predator populations increased, and pollinator populations decreased following the removal of AHM. These results suggest that the presence of AHM can alter the composition of arthropod communities and food-web dynamics. However, these effects were significant in some years and not others, suggesting the importance of temporal variation in drivers of communities. Overall, my work demonstrates that AHM can be drivers of community composition and illustrate the importance of examining their effects across multiple seasons. ACKNOWLEDGEMENTS First and foremost, I would like to thank Dr. Alison Brody for being a remarkable advisor, mentor and friend. I cannot bake her enough mandelbrots for all she has done and more importantly, for her patience. Thanks to my amazing committee: Sara Helms Cahan for her guidance in establishing my experimental design and introducing me to the joy and wonder of digging red harvester ant nests and their stings, Nick Gotelli for hammering home the importance of displaying the variation in the data and pushing me to embrace R…still deliberating which is more painful, harvester ant stings or R’s learning curve, Josef H. Görres for being an astounding chairperson by always being supportive and reminding me that there is light at the end and it is reachable. A special thank you to my Welder family: Terry Donovan, Selma Glasscock, Angela Garcia, Irma Tamez, Adam Mitchell, Meg Streich, Kelsey Griffin, Sarah Cusser, Nick Cano, Olivia Kost. A very special thank you to Sarah Kahlich, the “nemies!” and I are forever grateful! Thank you to all the graduate students and friends that truly provided me with the social and intellectual support I needed. You are too numerous to list, but special thanks to my G-chat colleagues (A.N., L.O., F.L., M.G.) for the laughs, coffee breaks, and stat/R discussions, Ally2 and Co. (A.D., C.D., D.D., A.N., D.K., Z.N-K.) for hysterical game nights – “OXY-GEN!”, Steak and Drake camping brother, L.B., for the piece and quite in wild Maine, Wed/Thurs Night Cards (C.I., V.I. G.F, B.D., H.K.,S.D.) that encouraged “Nabiling it”. To N.S. for letting me crash on your sofa or spare bed after late nights of ii writing. Thanks to all the undergraduates that helped in the lab; with a special thanks to Luke McCartin for all the extra time and work he put in. Thank you to my mom (Elyce) and baba (Naim) for their unwavering support and guidance. For instilling in me the importance of education and bettering myself. My brothers (Quddus, Collin, and Fugita), thank you so much for providing me with strong, positive role models to look up to and being there for me when I needed you. To Emily Koella for providing me with unconditional love and support, and always being there to help pull me out of rabbit holes. Lastly, I would like to thank the Rob and Bessie Welder Wildlife Refuge Foundation for allowing me to conduct my research at the refuge and for selecting me as a Welder Fellow, Sigma Xi’s Grant-in-Aid of Research fund, Botanical Society of America Graduate Student Research Award, University of Vermont’s Ronald Suiter Award and Carolyn M. Glass ’83 Award, and Parker Lumber in Sinton, TX and Air Energy in Houston, TX for donating research supplies. iii TABLE OF CONTENTS Page ACKNOWLEDGEMENTS ................................................................................................ ii LIST OF TABLES ............................................................................................................ vii LIST OF FIGURES ......................................................................................................... viii Chapter 1: The structuring of communities through direct and indirect interactions derived from ant protection mutualisms: A review and prospectus ................................... 1 1.1. Abstract .................................................................................................................... 1 1.2. Introduction .............................................................................................................. 2 1.3. Community level effects of ant-protection mutualisms ........................................... 4 1.4. Temporal indirect effects of APM on communities ................................................ 6 1.4. Effect of APM presence on pollinator behavior and efficacy .................................. 7 1.5. Long-term effect of ant-protection mutualisms on the reproductive potential of host plants ................................................................................................................... 8 1.6. Conclusion: Importance of Incorporating Indirect Interactions