STOCHASTIC MODELING OF ORB-WEB CAPTURE MECHANICS SUPPORTS THE IMPORTANCE OF RARE LARGE PREY FOR SPIDER FORAGING SUCCESS AND SUGGESTS HOW WEBS SAMPLE AVAILABLE BIOMASS A Thesis Presented to The Graduate Faculty of The University of Akron In Partial Fulfillment of the Requirements for the Degree Master of Science Samuel C. Evans December, 2013 STOCHASTIC MODELING OF ORB-WEB CAPTURE MECHANICS SUPPORTS THE IMPORTANCE OF RARE LARGE PREY FOR SPIDER FORAGING SUCCESS AND SUGGESTS HOW WEBS SAMPLE AVAILABLE BIOMASS Samuel C. Evans Thesis Approved: Accepted: ____________________________ ____________________________ Advisor Department Chair Dr. Todd A. Blackledge Dr. Monte E. Turner ____________________________ ____________________________ Committee Member Dean of the College Dr. Randall J. Mitchell Dr. Chand Midha ____________________________ ____________________________ Committee Member Dean of the Graduate School Dr. Steven C. Weeks Dr. George R. Newkome ____________________________ Date ii ABSTRACT Strong selective pressures can be exerted by events that occur extremely rarely and unpredictably during an organism's lifetime. The importance of such rare events may elude detection if the fitness consequences are not immediately observable, such as in the form of missed foraging opportunities. For orb-weaving spiders, fitness may depend almost exclusively on securing one or a few large, rarely-encountered, difficult-to-capture prey. Here, we present a stochastic individual-based model simulating foraging, growth, and survival of various-sized spiders in environments varying in distribution of biomass among prey sizes. We use this model to assess the degree to which foraging success is determined by the outcome of a small subset of foraging opportunities, and ascertain the architectural and biomechanical properties most crucial to deciding the outcomes of these rare events. Although our deterministic model suggests spiders should, on average, gain the most biomass from small prey sizes, spiders in stochastic simulations grew the most by capturing a single large and difficult-to-capture prey comprising the majority of their diets. The mechanics involved in stopping and retaining flying prey were more important in determining foraging success compared to those involved in encountering and contacting prey. Spiders lost the raw majority of biomass they encountered by failing to stop prey. However, prey retention exhibited the highest rate of biomass loss—spiders lost over 90% of successfully stopped biomass by failing to retain prey, but failed to stop only 40-80% of prey biomass their webs successfully contacted. Our results support the rare large prey hypothesis of Venner and Casas (2005), and reinforce the hypothesis that iii orb webs are pervasively selected for their potential to arrest large amounts of energy. However, certain factors such as prey availability and the biomechanics of prey retention in webs warrant further investigation, as these may be crucial to the plausibility of alternative foraging strategies. iv DEDICATION To the scores of people who, as I struggled to rein in the thoughts culminating in this thesis, supplied the scaffolding around which my character was built in ways I never expected. v ACKNOWLEDGEMENTS Steve Weeks and Randy Mitchell provided insight and support as SCE's thesis committee members. Michael Barton, Jeremy Prokop, Zhong-Hui Duan, and Charles van Tilberg contributed computational resources. Mohammad Marhabaie, Bor-Kai Hsiung, Gaurav Amarpuri, Thomas Beatman, Shagun Sharma, and Andrew Shall contributed helpful comments on the manuscript. Rafael Maia provided insightful discussions of the model and particularly valuable support with R syntax. vi TABLE OF CONTENTS Page LIST OF FIGURES --------------------------------------------------------------------------------------------- viii CHAPTER I. INTRODUCTION ----------------------------------------------------------------------------------------------- 1 II. MATERIALS AND METHODS ------------------------------------------------------------------------- 9 The model -------------------------------------------------------------------------------------------------- 9 Prey availability ------------------------------------------------------------------------------------------ 9 The spiders ------------------------------------------------------------------------------------------------ 13 Prey capture process ----------------------------------------------------------------------------------- 14 Prey-web contact --------------------------------------------------------------------------------------- 15 Prey stopping -------------------------------------------------------------------------------------------- 16 Prey retention -------------------------------------------------------------------------------------------- 18 Biomass assimilation ---------------------------------------------------------------------------------- 19 Metabolism and survival ----------------------------------------------------------------------------- 19 Deterministic model ----------------------------------------------------------------------------------- 21 Simulation and analyses ----------------------------------------------------------------------------- 22 III. RESULTS ------------------------------------------------------------------------------------------------------ 24 IV. DISCUSSION ------------------------------------------------------------------------------------------------ 33 REFERENCES ---------------------------------------------------------------------------------------------------- 39 APPENDIX --------------------------------------------------------------------------------------------------------- 44 vii LIST OF FIGURES Figure Page 1 Diagram of a typical orb web ........................................................................................... 5 2 Biomass and abundance distributions of prey simulated in the model .................. 10 3 Flowcharts representing (a) a single spider in the model, and (b) the daily prey capture process for that spider ................................................ 12 4 Deterministic distributions of percent of total captured biomass acquired from each prey size .......................................................................................... 25 5 Histograms of spider growth in the stochastic model ................................................ 26 6 Relationships between spider growth and single largest prey captured ................. 27 7 Scatterplots showing positive relationships between spider growth and percent of total captured biomass from the single largest prey captured ............... 28 8 Relationships between spider growth and the size difference between the largest and second-largest individual prey items captured................................. 29 9 Fate of total biomass encountered by spiders .............................................................. 30 10 Proportion of prey biomass entering each capture stage that was lost vs. sustained to the next stage ................................................................. 31 11 Relationships between total biomass encountered and total biomass stopped by webs, for all surviving spiders .......................................... 32 viii CHAPTER I INTRODUCTION Much of evolutionary ecology research seeks to describe the selective forces that influence how organisms acquire resources to maximize fitness (Stearns 1977; Houston et al. 1988). Such traits might be shaped primarily via events that occur extremely rarely and unpredictably during an organism's lifetime. Aberrant climatic events can drastically alter distributions of phenotypes within entire populations (Brown and Brown 2011). Recent discoveries of novel genera subsisting on nutrient bonanzas from rarely- encountered deep-sea whale and wood falls indirectly suggests that such organisms can only reproduce on a detectable scale in such rare instances (Amon et al. 2013; Bienhold et al. 2013). Moreover, organisms possessing phenotypes that are well beyond adequate for surviving and foraging in “average” scenarios are of curious interest because the likely high energetic costs of such phenotypes would presumably render them inefficient and have negative relative fitness consequences, yet these persist in some lineages (Gaines and Denny 1993; Foelix 2011). However, a rare event that determines individual foraging success may elude detection as a significant selective force because its consequences for the forager may not be immediately observable. Spiders that build viscid orb webs (Araneae: Orbiculariae: Araneoidea) are particularly useful model organisms for testing hypotheses of natural selection shaping traits via rare, cryptic events. These spiders represent a diverse, worldwide-distributed 1 clade of several thousand species ranging from 1mg to over 1g in adult body size (Blackledge et al. 2009). As sit-and-wait foragers, orb-weaving spiders provide a complete blueprint of their foraging strategy in the characteristics of their orb webs. Moreover, these spiders rebuild their webs daily, affording the opportunity to alter foraging effort in response to exogenous factors (Blackledge et al. 2011). Therefore, more complete and accurate measurements can be made of these organisms' life history traits and their underlying mechanics. Indeed, much data exists regarding orb-weaver energetic investment in foraging (Peakall and Witt 1976; Sherman 1994), foraging potential (Venner and Casas 2005; Blackledge