This file is part of the following reference: Manicom, Carryn (2010) Beyond abundance: the direct and indirect effects of predation in a terrestrial trophic web. PhD thesis, James Cook University. Access to this file is available from: http://eprints.jcu.edu.au/19007 Beyond Abundance: The direct and indirect effects of predation in a terrestrial trophic web Thesis submitted by Carryn Manicom BSc (Hons) University of Cape Town March 2010 for the degree of Doctor of Philosophy in the School of Marine and Tropical Biology James Cook University Clockwise from top: The study site at Ramsey Bay, Hinchinbrook Island, picture taken from Nina Peak towards north; juvenile Carlia storri; varanid access study plot in Melaleuca woodland; spider Argiope aethera wrapping a march fly; mating pair of Carlia rubrigularis; male Carlia rostralis eating huntsman spider (Family Sparassidae). C. Manicom i Abstract We need to understand the mechanism by which species interact in food webs to predict how natural ecosystems will respond to disturbances that affect species abundance, such as the loss of top predators. The study of predator-prey interactions and trophic cascades has a long tradition in ecology, and classical views have focused on the importance of lethal predator effects on prey populations (direct effects on density), and the indirect transmission of effects that may cascade through the system (density-mediated indirect interactions). However, trophic cascades can also occur without changes in the density of interacting species, due to non-lethal predator effects on prey traits, such as behaviour (trait-mediated indirect interactions). Studies of direct and indirect predation effects have traditionally considered predator control of herbivore populations; however, top predators may also control smaller predators. Due to their versatility and high predation rates, intermediate-level predators (mesopredators) may have disproportionably larger effects on lower trophic levels than top predators. Despite knowledge of the importance of indirect predation effects, and the effects of mesopredators, there is little evidence of the relative importance of density- and trait-mediated effects of predation in complex terrestrial trophic systems. My study consisted of a manipulative field experiment where the effects of top predators and mesopredators were both simultaneously and individually isolated. I manipulated the access of varanids (top predators) and skinks (mesopredators) to areas at my study site using large (200 m2) fenced study plots, and determined the effects of these predators on spiders (lower-order mesopredators), other arthropods and primary producers. To appreciate the impact that predation had on fauna, a detailed understanding of the ecology of the prey species was needed. Small skinks dominated the faunal community at my study site and thus were likely to make a large contribution to energy flow in the system, both as prey to higher trophic levels and as predators of lower trophic levels. Current knowledge of the demography, ecology and life history strategies of small, tropical skinks was inadequate. I described the population structure, survival rates, reproductive seasons and recruitment patterns of the dominant skink species at my study site, and I defined their growth patterns, age at maturity, ii sexual dimorphism and relationship with ectoparasites. I found that these closely-related, sympatric skinks shared similarities in many aspects of their life history, but that different mechanisms acted on juvenile skinks to cause various amounts of sexual dimorphism of adult body size. Observations of skink activity, use of microhabitat and behaviour revealed that skinks were highly active; suggesting that they were efficient and effective foragers, but also conspicuous and highly vulnerable to predators. From diet analysis, I determined that skinks were selective in their prey choice, consuming certain prey types and sizes that were in short supply in the environment. The species varied in the prey they consumed, but spiders and orthopterans were consistent prey types for all skinks. Skinks were found to have a strong direct effect on spider abundance in study plots; they reduced the density of cursorial spiders and of web-building spiders close to the ground. The number of web-building spiders was, in turn, negatively correlated with the abundance of aerial arthropods. Herbivore damage to leaves was reduced in skink access plots. The selective removal by skinks of other predators (spiders) and herbivores (orthopterans) from the trophic system was thus shown to have far-reaching indirect effects that cascaded through the system to alter the composition of the arthropod community, and the amount of damage to local vegetation. Varanids did not directly alter the abundance of skinks or arthropods, but did have strong indirect effects. Skinks significantly reduced their activity in the presence of varanids, likely leading to lower energetic requirements and less foraging. The cascading effects of predation on skink activity were evident when comparing arthropod community composition among study plots: skinks directly altered the structure of the arthropod community by consumption and in the presence of varanids, skink foraging was restricted. In the absence of varanids, however, skinks were ‘released’ from predation threat, and only those arthropod taxa rarely consumed by skinks were abundant. Varanids thus indirectly altered arthropod community composition by altering skink behaviour, clear evidence of a trait-mediated indirect effect of predation. This is the first study, to my knowledge, to experimentally show the effect of behaviourally mediated mesopredator release on lower trophic levels, and such behavioural predator effects may be very influential in community ecology. The results of my study reveal iii the strength and importance of indirect predation effects, and show that measuring more than just the abundance of individuals is vital to determine the full effects of predator removal. iv Statements of access and sources I, the undersigned, author of this thesis, understand that James Cook University will make this thesis available for use within the University library and, via the Australian Digital Theses network, for use elsewhere. I understand that, as an unpublished work, a thesis has significant protection under the Copyright Act and I do not wish to place any further restriction on access to this work. ------------------------- ------------------ (Signature) (Date) Declaration I declare that this thesis is my own work and has not been submitted in any form for another degree or diploma at any university or other institution of tertiary education. Information derived from the published or unpublished work of others has been acknowledged in the text and a list of references is given. ------------------------- ------------------ (Signature) (Date) v Declaration on Ethics The research presented and reported in this thesis was conducted within the guidelines for research ethics outlined in the National Statement on Ethics Conduct in Research Involving Humans (1999), the Joint NHMRC/AVCC Statement and Guidelines on Research Practice (1997), the James Cook University Policy on Experimentation Ethics. Standard Practices and Guidelines (2001), and the James Cook University Statement and Guidelines on Research Practice (2001). The proposed research methodology received clearance from the James Cook University Experimentation Ethics Review Committee (approval number A677). ------------------------- ------------------ (Signature) (Date) vi Preface The only data used in this thesis that I did not collect myself were spider counts collected by Joanne Bussey (Honours student, James Cook University, 2005) in April – May 2005, and July – August 2005 (Chapter 9). I collected data from April 2003 to December 2004 during seven field trips to my study site on Hinchinbrook Island as part of my job as a research officer for the School of Tropical Biology, James Cook University. Chapter 7 (Diet and prey selection of sympatric tropical skinks) is currently in press (Austral Ecology), myself and Lin Schwarzkopf are authors. The manuscript presented as Appendix B (Self-made shelters protect spiders from predation) was written by myself, with co-authors Lin Schwarzkopf, Ross Alford and Thomas Schoener, and was published in 2008 (Proceedings of the National Academy of Sciences 105 [39]: 14903–14907). The manuscript presented as Appendix C (The cost of failing to thermoregulate is higher in the tropics: A conceptual model and empirical test) was written by Mathew Vickers, with myself and Lin Schwarzkopf as co-authors. It is currently under review (The American Naturalist). vii Acknowledgements My most sincere thanks and gratitude to my supervisors, Lin Schwarzkopf and Ross Alford. Thank you for securing the funding for this research, and for your help, guidance and encouragement throughout my PhD candidature. I have learnt so much from your knowledge and experience, and feel very fortunate to have been your student. Thank you, Ross, for your thoughtful advice, kindness, encouragement and for all your great ideas. Thank you for coming out into the field with me, I enjoyed and benefited greatly from our discussions, and really appreciate the time you spent helping me with analysis. Lin, I cannot begin to tell you how much your support (both moral and academic) has meant to me over the years. Thank you for your motivation, faith, encouragement,