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Bucciarelli, Gary Dissertation 2015 UNIVERSITY OF CALIFORNIA Los Angeles Phenotypic variation of toxin levels in a chemically defended amphibian: The ecological and evolutionary significance of tetrodotoxin A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Biology by Gary Bucciarelli 2015 ABSTRACT OF THE DISSERTATION Phenotypic variation in space and time of toxin levels in an amphibian: The ecological and evolutionary significance of tetrodotoxin by Gary Bucciarelli Doctor of Philosophy in Biology University of California, Los Angeles, 2015 Professor Howard Bradley Shaffer, Chair The!global!decline!of!amphibian!populations!is!well!documented,!yet!researchers!have!only! begun!to!understand!how!these!declines!may!affect!biological,!environmental,!ecological,! and!evolutionary!processes.!In!the!first!chapter,!recently!published!primary!literature!is! reviewed!to!describe!the!complexities!of!amphibian!population!declines,!with!a!focus!on! the!interactions!of!nonnative!species,!anthropogenic!disturbances,!and!climate!change.!To! begin!to!understand!the!potential!consequences!of!the!decline!of!endemic!California! herpetofauna,!the!ecological!role!of!a!Species!of!Special!Concern,!the!California!newt! (Taricha'torosa)!was!evaluated!in!streams!of!the!Santa!Monica!Mountains.!The!California! newt!possesses!a!potent!neurotoxin,!tetrodotoxin!(TTX),!which!is!known!to!elicit! antipredator!behavior!in!conspecific!larvae.!Given!these!results,!potential!variation!of! individual!and!breeding!population!TTX!levels!may!affect!ecological!and!evolutionary! processes.!In!chapter!2,!TTX!levels!of!adult!T.'torosa'from!three!breeding!localities!in!the! ii!! Santa!Monica!Mountains!were!quantified!to!test!for!variation!in!amounts!of!TTX!between! sites!using!a!novel!nonFdestructive!sampling!method,!a!newly!developed!technique!to! extract!TTX,!and!an!adapted!high!performance!liquid!chromatography!system!with!a! detection!limit!of!48!picograms!TTX!(0.15!picomoles).!The!amounts!of!TTX!from!newts!in! these!three!streams!suggest!fine!geographic!variation!in!toxin!levels.!In!chapter!3,!the! potential!ecological!effects!of!newts!and!TTX!were!tested!using!field!and!laboratory! bioassays!to!determine!if!newt!chemical!cues!and!TTX!affect!the!foraging!behavior!of! macroinvertebrates.!Field!bioassays!indicate!that!macroinvertebrates!move!away!from! point!sources!of!newt!chemical!cues,!while!laboratory!bioassays!show!that!predatory! odonate!nymphs!exposed!to!TTX!reduce!predation!rates,!mean!velocities!when!striking! prey,!and!mean!angular!velocities!when!compared!to!controls.!In!the!final!chapter,!male! site!fidelity!and!individual!TTX!levels!were!tracked!in!situ!over!four!breeding!seasons.!Data! reveal!fluctuations!in!individual!and!breeding!population!TTX!levels,!suggesting!that!TTX!is! not!a!stable!trait.!Furthermore,!statistical!analyses!indicate!that!fidelity!to!a!pool!is! significantly!linked!to!relative!TTX!concentrations.!Collectively,!these!results!demonstrate!a! striking!ecological!role!for!T.'torosa!and!TTX,!and!imply!that!the!loss!of!this!amphibian'in! our!study!system!may!have!wideFreaching!ecological!consequences.!! !! iii! ! The dissertation of Gary Bucciarelli is approved. David B. Green Gregory F. Grether Lee B. Kats Thomas B. Smith Howard Bradley Shaffer, Committee Chair University of California, Los Angeles 2015 iv! ! For those who have dared to think differently..... v!! TABLE OF CONTENTS CHAPTER 1. Invasion Complexities: The diverse impacts of nonnative species on amphibians.................................................................................................................................. 1 References.................................................................................................................................. 16 CHAPTER 2. Quantifying tetrodotoxin levels in the California newt using a non-destructive sampling method............................................................................................... 24 References................................................................................................................................... 30 CHAPTER 3. Effects of newt chemical cues on the distribution and foraging behavior of stream macroinvertebrates...................................................................................................... 36 References................................................................................................................................... 42 CHAPTER 4. Individual fluctuations in toxin levels affect breeding site fidelity in a chemically defended amphibian.................................................................................................. 46 References................................................................................................................................... 74 vi! ! LIST OF TABLES 4.1. Individual TTX measurements of recaptured newts............................................................ 71 4.2. Mean TTX concentrations of all sampled newts................................................................. 72 4.3. Estimated p-values for model predictors............................................................................. 73 ! vii! ! LIST OF FIGURES 4.1. Individual and daily mean TTX concentrations from 2011 - 2014..................................... 65 4.2. Breeding pool fidelity and TTX chronologies of 21 recaptured individuals ...................... 67 4.3. Tree regression and random forest results from 21 individuals sampled more than once............................................................................................................................ 68 4.4. Tree regression and random forest results from 56 individuals sampled only once..................................................................................................................................... 69 4.5. Null distribution of permuted importance scores for the relative TTX predictor............................................................................................................................. 70 viii! ! ACKNOWLEDGEMENTS Chapter One is a reproduction of: Bucciarelli, GM, Blaustein AR, Garcia TS, & Kats LB. 2014. Invasion Complexities: The Diverse Impacts of Nonnative Species on Amphibians. Copeia 4 611 - 632. doi: 10.1643/OT-14-014. GMB reviewed literature, drafted and revised the manuscript, and created graphics. ARB, TSG, and LBK helped to conceive subtopics and revise drafts of the manuscript. Chapter Two is a reproduction of: Bucciarelli, GM, Li A, Kats, LB, & Green DB. 2014. Quantifying tetrodotoxin levels in the California newt using a non-destructive sampling method. Toxicon 80 87 - 93. doi:10.1016/j.toxicon.2014.01.009 GMB designed experiments, conducted field work, performed statistical analyses, drafted and revised the manuscript, and created graphics. AL helped to design experiments, perform laboratory experiments, and assist with revisions. LBK and DBG helped to design the experiments and revise the manuscript. Chapter Three is a reproduction of: Bucciarelli, GM, & Kats LB. 2015. Effects of newt chemical cues on the distribution and foraging behavior of stream macroinvertebrates. Hydrobiologia 749 69 - 81. doi: 10.1007/s10750-014-2146-4 GMB designed experiments, performed field work, laboratory experiments, and statistical ix! ! analyses, created graphics, and drafted and revised the manuscript. LBK helped design experiments and helped to revise the manuscript. Chapter Four is a version of a manuscript submitted for publication. GMB performed laboratory and field work, data analyses, conceived of and designed the study, and drafted the manuscript. DBG assisted with laboratory work and helped revise the manuscript. HBS participated in the design of the study and helped to revise the manuscript. LBK assisted with the design of the study, data collection, and helped revise the manuscript. x!! VITA EDUCATION Antioch College, B.A., Interdisciplinary Cultural Studies, 2002 PROFESSIONAL EXPERIENCE 2013 - Present Public Outreach Coordinator, UCLA La Kretz Center for California Conservation Science 2013 (Spring) Research Scientist, Graniterock 2009 - 2012 Research Assistant, La Selva Biological Preserve, Costa Rica 2005 - 2010 Manager, Apple Inc., Los Angeles, CA TEACHING EXPERIENCE 2013 - Present University of California, Los Angeles: Teaching Assistant Consultant 2012 University of California, Los Angeles: Introduction to Evolution 2011 University of California, Los Angeles: Ecological Responses to Environmental Challenges 2002 Antioch College: Media Literacy and Production GRANTS, FELLOWSHIPS, AWARDS 2015 UCLA Departmental Dissertation Year Fellowship 2014 The National Park Service, Southern California Research Learning: $7,500 2014 The Malibu Institute: $15,000 2013 La Kretz Graduate Student Research Grant 2013 Mildred E. Mathias Graduate Research Grant 2012 UCLA Award of Distinction in Teaching 2011 NSF Graduate Research Fellowship Program Honorable Mention 2011 UCLA Departmental Fellowship: $13,000 1998 Horace Mann Scholarship: $20,000 per year PUBLICATIONS (*undergraduate) Bucciarelli, GM & Kats LB. 2015. Effects of newt predator cues on the distribution and foraging of stream macroinvertebrates. Hydrobiologia 749 69-81. xi! ! Bucciarelli, GM, Blaustein AR, Garcia T. & Kats LB. 2014. Invasion complexities: The diverse impacts of invasive species on amphibians. Copeia 4 611-632. Bucciarelli, GM, *Li A, Kats LB, & Green DB. 2014. Quantifying tetrodotoxin levels in
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