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The Role of Wolf Spiders (Araneae: Lycosidae) on The THE ROLE OF WOLF SPIDERS (ARANEAE: LYCOSIDAE) ON THE BIOLOGICAL CONTROL OF THE BOLLWORM HELICOVERPA SPP. (LEPIDOPTERA: NOCTUIDAE) IN COTTON CROPS Dalila Rendon (B.Sc, M.Sc) Macquarie University Department of Biological Sciences Supervisor: Associate professor Phillip Taylor Commonwealth Scientific and Industrial Research Organization (CSIRO) Agricultural Flagship Supervisor: Dr. Mary Whitehouse Thesis submitted for the degree of Doctor of Philosophy January 2016 STATEMENT OF CANDIDATE I certify that the work in this thesis entitled “THE ROLE OF WOLF SPIDERS (ARANEAE: LYCOSIDAE) ON THE BIOLOGICAL CONTROL OF THE BOLLWORM HELICOVERPA SPP. (LEPIDOPTERA: NOCTUIDAE) IN COTTON CROPS” has not previously been submitted for a degree nor has it been submitted as part of requirements for a degree to any other university or institution other than Macquarie University. I also certify that the thesis is an original piece of research and it has been written by me. Any help and assistance that I have received in my research work and the preparation of the thesis itself have been appropriately acknowledged. In addition, I certify that all information sources and literature used are indicated in the thesis. The research presented in this thesis did not require Macquarie University Ethics Review Committee approval, since all the experiments presented here were done with arthropods. Signature Dalila Rendon Student ID 42243262 July 10 2015 i ii THESIS ABSTRACT Cotton bollworm larvae (Lepidoptera: Noctuidae, Helicoverpa spp.) that survive on genetically modified ‘Bt cotton’ contribute to the risk of widespread resistance to Bt toxins. A resistance management technique in cotton fields involves deep tilling of the soil to kill overwintering pupae (‘pupae busting’), which is incompatible with the agronomic practice of minimum tillage. As a biological control alternative in minimum-tillage cotton fields, ground predators can kill Helicoverpa spp. Larvae as they descend from the plant to pupate in the soil, or moths emerging from underground. In this thesis, I examine the impact of biological control from wolf spiders (Araneae: Lycosidae) on ground-dwelling stages of Helicoverpa spp., as a strategy for Bt resistance management in minimum tillage fields. Wolf spider diversity was higher in complex minimum-tillage cotton plots compared to simple tilled cotton plots. Predation events of general prey were rare to observe in the field, and gut- content tests revealed that a low proportion of wolf spiders (2.1%) potentially killed IgG- marked Helicoverpa spp. larvae, but this is likely due to the low rate of spider recapture in cotton plots due to migration. In enclosed containers, the three largest and abundant species of wolf spiders Tasmanicosa leuckartii, Hogna crispipes, and Hogna kuyani all kill high proportions of 5th instar Helicoverpa spp. larvae on the soil. Tasmanicosa killed Helicoverpa before and after pupation; in glasshouse enclosures, a single Tasmanicosa can reduce by 38% the number of larvae surviving to pupation, and by 66% the number of larvae surviving to moth emergence. The increase in abundance (one or two Tasmanicosa or Hogna individuals) in glasshouse enclosures did not increase Helicoverpa mortality. Increasing spider abundance and diversity (Tasmanicosa + Hogna) in glasshouse enclosures reduced Helicoverpa survival compared to one Tasmanicosa only, but this effect was not additive, suggesting that antagonistic intraguild interactions between wolf spiders can limit biological control on Helicoverpa. In the presence of the ground cricket Teleogryllus commodus (a prey commonly observed in the field), Tasmanicosa still killed high proportions of Helicoverpa larvae in iii laboratory containers. However, transient acquired toxicity by Teleogryllus which let to spider mortality can disrupt biological control of Helicoverpa. In addition to consumptive effects of direct predation, wolf spiders also exerted non-consumptive effects on Helicoverpa; in laboratory containers, Helicoverpa larvae spent less time on a cotton boll and more time on the soil in the presence of a spider. Additionally, increased loss of cotton boll mass likely reflects changes in Helicoverpa foraging behaviour induced by the presence of spiders. Considering the setting (laboratory, glashouse, field), and the interactions with intraguild predators and alternative prey, wolf spiders showed various strengths and limitations in their capacity to control Helicoverpa. Given the high diversity and abundance of wolf spiders in cotton fields throughout the cropping season, and the high proportion of Helicoverpa spp. larvae and moths that spiders kill even in the presence of alternative prey, wolf spiders should be considered important biological control agents when implementing pest and Bt resistance management strategies. iv ACKNOWLEDGEMENTS This thesis would not have been possible without the trust that many people deposited in me and encouraged me along the way. Phil Taylor and Mary Whitehouse were the ultimate “Ying-Yang” supervising combo; With Phil’s never-ending patience, and Mary’s motherly support, this challenging learning experience became incredibly fulfilling. Thanks for guiding me along the process, I consider myself very lucky to have you as my mentors. I received multiple funding sources along my candidature. My PhD program was funded by an Endeavour Postgraduate Award. The department of Biological Sciences at Macquarie University provided all research related funding. Two minor grants contributed to the development of the experiments: A Rice Memorial Field Research Award provided assistance for field survey equipment, and a Linnean Society of NSW Joyce Vickery Award provided assistance for laboratory recording equipment. Travel to the United States to learn gut-content analysis methods in Kentucky and Arizona was funded by the Macquarie University Postgraduate Research Fund, and the Cotton Research and Development Corporation. I am indebted to all the staff at the Australian Cotton Research Institute for the great amount of support and help that you offered me. To all the entomology team, thanks for your help in the lab, glasshouse and field, for being the “funnest” group at ACRI, and for your enthusiasm for dress-up parties! Many thanks too to the administrative staff at the Biological Sciences department at Macquarie University for making everyone’s life so much easier and productive. Thanks also to my peers and officemates at the Behavioural Biology group for your support, feedback, advice, and making work life in general so pleasant. Besides four productive years of research, what really made this worth it were the friends I made along the way. On my first week of my PhD, Sam Collins took me indoor rock climbing for the first time in my life. Little did I know, this was going to become my favourite v hobby, and the best way to blow off PhD-related stress. Thanks to all those climbing enthusiasts who were ‘on belay’ and supported me, both on and off the wall, for making this journey so enjoyable. Also to my colleagues who became friends and shared laughs, drinks, dances, advice, tears and fun, particularly Peri, Marianne, Julieta, Marcela, Silvia, Peter, Matt, Sam, Naila, Eirik, Daniel, and the list goes on...Thanks to Katie and Simone, who became my family in a remote country town, and whose recipes will be very missed. I would like to give an unusual acknowledgement to all the things that went wrong! Like the times I got bogged in the flooded fields and had to be rescued....or that time when I put diesel in a petrol car...or when the roof of my glasshouse got ripped off in a storm....or when the air conditioning broke and all my animals and cotton plants got baked at 60C, therefore losing an entire trial....or when my videorecording system stopped working because I mixed up the power adaptors...or when I killed a whole batch of pupae by accidentally washing them with ethanol instead of bleach. This taught me that I will never stop learning and still have so many more mistakes to make, but regardless of them, I can still keep on going...And it also made me jump with joy whenever things went smoothly! The last (and most important) mention of honour goes to my family. My loving husband, Ewald, who as a blessing in disguise was also writing a doctoral thesis at the same time as me, understood my long erratic hours and my absences during fieldwork. Thanks for being in this together with me. My dad and mom, who never doubted me, and instilled in me a passion for discovery, adventure and travel. Thanks for encouraging to keep taking the next step when I decided to follow such an unusual career! Most importantly, this thesis is dedicated to my Abuela (grandmother), my favourite TV game-show teammate. vi TABLE OF CONTENTS STATEMENT OF CANDIDATE ............................................................................................ i THESIS ABSTRACT ............................................................................................................. iii ACKNOWLEDGEMENTS ..................................................................................................... v LIST OF FIGURES ................................................................................................................ ix LIST OF TABLES ................................................................................................................ xiii INTRODUCTION ...................................................................................................................
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