University of Missouri, St. Louis IRL @ UMSL Theses Graduate Works 11-26-2012 The slo‘ w-growth-high-mortality’ hypothesis: how plant species, leaf quality, and the third trophic level contribute to the mortality of two common leaf- tying microlepidopteran herbivores Kirk Lee Barnett University of Missouri-St. Louis, [email protected] Follow this and additional works at: http://irl.umsl.edu/thesis Recommended Citation Barnett, Kirk Lee, "The slo‘ w-growth-high-mortality’ hypothesis: how plant species, leaf quality, and the third trophic level contribute to the mortality of two common leaf-tying microlepidopteran herbivores" (2012). Theses. 47. http://irl.umsl.edu/thesis/47 This Thesis is brought to you for free and open access by the Graduate Works at IRL @ UMSL. It has been accepted for inclusion in Theses by an authorized administrator of IRL @ UMSL. For more information, please contact [email protected]. Barnett, Kirk L, 2012, UMSL, p. 1 The ‘slow-growth-high-mortality’ hypothesis: how plant species, leaf quality, and the third trophic level contribute to the mortality of two common leaf-tying microlepidopteran herbivores Kirk L. Barnett B.S., Biology, University of Missouri – St. Louis, 2008 A Thesis submitted to The Graduate School at the University of Missouri – St. Louis in partial fulfillment of the requirements for the degree Master of Science in Biology November 2012 Advisory Committee Robert Marquis, Ph.D. Chairperson Zuleyma Tang-Martinez, Ph.D. Robert Ricklefs, Ph.D. Barnett, Kirk L, 2012, UMSL, p. 2 TABLE OF CONTENTS Acknowledgments 4 Thesis Abstract 5 Chapter 1: Anti-herbivore plant defenses and the third trophic level: combined effects on insect herbivores: The Consequences of Being an Herbivore and the Feeding Strategies to Overcome Poor Leaf Quality Introduction 6 Plants as a Food Source for Herbivores 8 Effects of Plant Defenses on Insect Growth and Survivorship 19 Behavior of Shelter Building 24 Why Actively Build a Shelter? 27 Slow-Growth-High-Mortality 34 Literature Cited 39 Chapter 2: The ‘slow-growth-high-mortality’ hypothesis: how plant species, leaf quality, and the third trophic level contribute to mortality of two common leaf-tying microlepidopteran herbivores. Abstract 59 Introduction 60 Barnett, Kirk L, 2012, UMSL, p. 3 Methods 63 Results 71 Discussion 76 Literature Cited 84 Tables 91 Figures 97 Barnett, Kirk L, 2012, UMSL, p. 4 ACKNOWLEDGEMENTS I would like to take this opportunity to thank my advisor, Dr. Robert Marquis, without whom I would have never progressed as far I have as a graduate student. He has helped me both with my undergraduate and graduate projects and his ideas have contributed significantly to the evolution of me as a researcher. I would also like to thank the other members of my committee, Dr. Zuleyma Tang- Martinez, Dr. Amy Zanne, and Dr. Robert Ricklefs for their valuable insight and, above all, patience with the formulation, execution, and conclusion of my thesis. In addition, I would like to thank the Marquis Lab group, the members of which have provided ideas and constructive criticism that made my research what it is today. I am also extremely grateful for financial help that Dr. Patrick Osbourne and the Whitney Harris World Ecology Center had provided me with both in my undergraduate and graduate career, in addition to the National Science Foundation. Without their support, this research would of most likely not of been possible. I am also in debt to Mr. Bruce Schuette at Cuivre River State Park, who gave permission to us to use the park as the primary research area. Lastly, I would like to thank my friends and colleagues who assisted me with field work when it was needed and who have inspired me to go on to do greater things. Barnett, Kirk L, 2012, UMSL, p. 5 THESIS ABSTRACT I investigated how the survivorship, abundance, and development of two common microlepidoteran leaf-tiers on four species of oak change in response to leaf quality and exposure to the third trophic level, and used those results to validate predictions under the slow-growth-high-mortality hypothesis. In chapter 1, I begin with a review of the literature by examining the components of plant traits that contribute to the success of insect herbivores and how plants can alter both defensive compounds and nutritional quality in order to deter herbivory. I then describe how changes in leaf quality and defense can be overcome by insect herbivores, one means by which is shelter building. Finally, I introduce the slow-growth-high-mortality hypothesis and describe how plant quality, ecosystem engineering, and the third trophic level can be used to validate the predictions of said hypothesis. In chapter 2, I present the results of an experiment that examined the bottom-up and top-down effects on two common leaf-tying microlepidopterans on four species of oaks by manipulating their exposure to the third trophic level. I found that the two leaf-tier species experienced the first trophic level differently but responded similarly to the third trophic level. Plant traits differed among oak species and changed from one generation of leaf-tier to the next. However, plant traits, measured as principal components, were for the most part uncorrelated with measures of survivorship, development, and parasitism, and were, at the very most, inconsistent between the two leaf-tier species. The patterns of mortality for both leaf-tiers did not reflect the effects of tree identity on larval development and, hence, did not follow the predictions of the slow-growth-high-mortality hypothesis. Barnett, Kirk L, 2012, UMSL, p. 6 CHAPTER 1. Anti-herbivore plant defenses and the third trophic level: combined effects on insect herbivores. INTRODUCTION Interactions of plants and herbivores are complex and involve both evolutionary responses in behavior and physiology of plants and the herbivores that attack them (Ehrlich and Raven 1964, Opler 1974). Plants can alter the patterns of attack of phytophagous insects by varying leaf quality, both constitutively and as a response to herbivory, and through apparency to herbivores (Feeny 1976, Rhoades and Cates 1976, Price et al. 1980, Coley et al. 1985). Because nitrogen is very often a limiting resource in insects and plant nitrogen content is low, phytophagous insects are forced to consume plant material many times their own body weight (Allen et al. 1974, Mattson 1980). In addition, water availability can be somewhat unreliable and has been shown to be important in insect growth (Scriber 1984); hence plants have been speculated to vary this resource to increase the mortality of their attackers (Mattson 1980). Both water and nitrogen are vital to plant growth and reproduction, however, their variation may not in all cases be in response to herbivory. Those plant products that are produced directly by all plants are called primary metabolites and are vital for metabolic function. Those compounds that are often restricted to specific plant groups and are not vital to growth and reproduction are called secondary metabolites (Pichersky and Gang 2000). These compounds are both induced and constitutive and have been viewed strictly as an herbivore deterrent (Fraenkel 1959); however, there is some evidence that they might Barnett, Kirk L, 2012, UMSL, p. 7 also be allopathic in plant-plant competition (Siemens et al. 2002). Anti-herbivore defenses range from qualitative, such as highly toxic glucosinolates, to quantitative, such as tannins and phenolics (Schoonhoven et al. 2005). These can vary in their effectiveness and concentration, but, in spite of or as a result of their presence, some herbivores have evolved ways to negate these defenses (Rhoades 1985). In addition to chemical defenses, plants employ a wide variety of physical defenses, such as trichomes and waxy cuticles (Jetter et al. 2000, Valverde et al. 2001). When an herbivorous insect consumes a plant, it has to convert that material to energy, which is then used for growth and reproduction (Waldbauer 1968). Some plant compounds have been shown to slow this conversion by reducing digestibility (Rhoades 1979). This has led many researchers to propose that plants use a strategy in which they delay insect growth to increase mortality from abiotic forces and the third trophic level (Champagne et al. 1986, Fordyce and Shapiro 2003). This has been termed the ‘slow- growth - high-mortality’ hypothesis, for which there is both supporting and refuting evidence (Williams 1999). Besides detoxification and sequestration, herbivorous insects also have been able to overcome some chemical defenses through behavioral responses. These responses include trenching, shelter-building, and, in the case of tropical herbivores, feeding phenology (Dussourd and Eisner 1987, Cappuccino 1993, Coley and Barone 1996). Here I will discuss how plants are utilized as food by herbivorous insects and how those plants, in turn, are thought to defend themselves against attack. I will then describe how delayed growth of an herbivore may be a consequence of plant defense and describe the various methods herbivores use to overcome these defenses. Finally, I will discuss the Barnett, Kirk L, 2012, UMSL, p. 8 behavior of shelter-building and how it relates to the ‘slow-growth-high-mortality’ hypothesis. THE CONSEQUENCES OF BEING AN HERBIVORE AND THE FEEDING STRATEGIES TO OVERCOME POOR LEAF QUALITY Plants as a Food Source for Herbivores The relationship between plants and their insect herbivores is one of a constant battle. This is because as one tries to prevent the other from attack, the other is selected to evolve new strategies to get around those barriers. The opponents, at first glance, seem unequally matched. Plants are immobile and seemingly cannot actively fight back, for the most part have long generations, and have been shown to possess low recombination rates. Insects, on the other hand, are generally highly mobile, relatively small, and have a high reproduction rate.