Old Dominion University ODU Digital Commons Biological Sciences Theses & Dissertations Biological Sciences Spring 2016 A Hitchhiker’s Guide to Invasion Biology: Describing the Ecological Mechanisms Underlying the Range Expansions of Two Ixodid Tick Species Robyn M. Nadolny Old Dominion University, [email protected] Follow this and additional works at: https://digitalcommons.odu.edu/biology_etds Part of the Biology Commons, Ecology and Evolutionary Biology Commons, and the Entomology Commons Recommended Citation Nadolny, Robyn M.. "A Hitchhiker’s Guide to Invasion Biology: Describing the Ecological Mechanisms Underlying the Range Expansions of Two Ixodid Tick Species" (2016). Doctor of Philosophy (PhD), Dissertation, Biological Sciences, Old Dominion University, DOI: 10.25777/cs2c-sx53 https://digitalcommons.odu.edu/biology_etds/11 This Dissertation is brought to you for free and open access by the Biological Sciences at ODU Digital Commons. It has been accepted for inclusion in Biological Sciences Theses & Dissertations by an authorized administrator of ODU Digital Commons. For more information, please contact [email protected]. A"HITCHHIKER’S"GUIDE"TO"INVASION"BIOLOGY:"DESCRIBING"THE"ECOLOGICAL" MECHANISMS"UNDERLYING"THE"RANGE"EXPANSIONS"OF"TWO"IXODID"TICK"SPECIES" ! by! ! ! Robyn!M.!Nadolny! B.S.!May!2008,!Beloit!College! M.S.!August!2011,!Old!Dominion!University! ! ! A!Dissertation!Submitted!to!the!Faculty!of!! Old!Dominion!University!in!Partial!Fulfillment!of!the!! Requirements!for!the!Degree!of! ! ! DOCTOR!OF!PHILOSOPHY! ! ECOLOGICAL!SCIENCES! ! OLD!DOMINION!UNIVERSITY! May!2016" " " " " " " " " " " Approved!by:! ! Holly!D.!Gaff!(Director)! ! David!T.!Gauthier!(Member)! ! Wayne!L.!Hynes!(Member)! ! Elsa!N.!Schaefer!(Member)! ! Eric!L.!Walters!(Member)! " " " " " " " " ! ! ! ABSTRACT" A!HITCHHIKER’S!GUIDE!TO!INVASION!BIOLOGY:!DESCRIBING!THE!ECOLOGICAL! MECHANISMS!UNDERLYING!THE!RANGE!EXPANSIONS!OF!TWO!IXODID!TICK!SPECIES! ! Robyn!M.!Nadolny! Old!Dominion!University,!2016! Director:!Dr.!Holly!D.!Gaff!" ! Increasing!incidence!of!many!tickZborne!diseases!have!been!linked!to!recent! expansions!of!tick!species!distributions.!Many!tick!species!are!expanding!their!ranges! because!of!anthropogenic!changes!in!the!landscape,!shifting!climatic!variables,!and! increasing!populations!of!suitable!host!species!and!tick!habitat.!Few!empirical!studies!have! been!performed,!however,!investigating!the!ecological!mechanisms!underlying!these!range! expansions.!Ticks!are!parasitic!organisms!that!disperse!across!landscape!by!hitchhiking!on! hosts,!but!must!then!survive!in!the!environment!for!long!periods!of!time!between! bloodmeals.!Two!species!of!ixodid!tick,!Ixodes'affinis!and!Amblyomma'maculatum,!are! simultaneously!expanding!their!ranges!throughout!the!MidZAtlantic!region!of!the!United! States,!and!provide!a!case!study!from!which!to!examine!the!relative!importance!of!host! choice!and!apparent!habitat!preference!in!the!resulting!patterns!of!range!expansion.! The!first!objective!of!this!research!was!to!use!field!studies!to!describe!the!life!history! of!each!of!these!species!in!Virginia,!and!determine!important!host!and!habitat! characteristics!for!the!survival!and!expansion!of!these!species!in!the!MidZAtlantic.!Tick! surveillance!data!were!collected!over!five!years!in!a!variety!of!habitats!throughout! southeastern!Virginia.!These!data!were!used!to!answer!basic!natural!history!questions! about!these!ticks!in!novel!habitats,!including!determining!tick!abundance!and!phenology,!as! well!as!habitat!and!host!preferences.!Although!both!tick!species!parasitized!many!of!the! same!host!species,!differences!in!the!habitat!conditions!necessary!for!tick!population! establishment!resulted!in!different!patterns!of!invasion.!Understanding!how!and!where! these!ticks!establish!is!useful!in!understanding!the!public!health!risks!associated!with!areas! being!invaded.! The!second!objective!of!this!research!was!to!determine!the!ancestry!of!the!northern! populations!of!these!ticks,!using!genetic!connectivity!among!populations!to!determine!the! mostly!likely!pathways!for!dispersal!from!ancestral!populations!to!the!MidZAtlantic.! Despite!overlapping!host!preferences!throughout!ontogeny,!each!species!exhibited!very! different!genetic!and!geographic!patterns!of!population!establishment!and!connectivity.! Genetic!evidence!suggests!that!these!species!may!rely!on!different!key!life!stages!to! disperse!successfully!into!novel!environments,!and!that!host!vagility,!habitat!stability!and! habitat!connectivity!all!play!critical!roles!in!the!establishment!of!new!tick!populations.! The!third!objective!of!this!research!was!to!use!metrics!derived!from!field!and! genetic!studies!to!parameterize!agentZbased!models,!simulating!tick!range!expansions! under!different!habitat!and!host!conditions.!Incorporating!parameter!values!specific!to!I.' affinis!and!A.'maculatum!life!history,!host!ranges,!habitat!preferences,!and!genetic!diversity! allowed!for!hypothesis!testing!on!whether!habitats!or!hosts!have!greater!influences!on!the! invasions!of!these!species!in!the!MidZAtlantic.!This!research!describes!the!first!comparative! case!study!of!two!tick!species!with!unique!host!and!habitat!preferences!dispersing! simultaneously!across!a!landscape,!and!increases!our!understanding!of!the!relative! importance!of!hosts!and!habitat!in!hitchhiker!invasions. iv ! ! ! ! ! ! ! Copyright,!2016,!by!Robyn!M.!Nadolny!and!Holly!D.!Gaff,!All!Rights!Reserved.! " v This!dissertation!is!dedicated!to!my!husband,!Tucker,!for!his!unwavering!support,! encouragement!and!love.!Also!to!my!mother,!father!and!sister,!for!always!believing!in!me,! and!for!always!making!time!to!listen.!! vi ACKNOWLEDGMENTS" " This!research!would!not!have!been!possible!without!the!tireless!assistance!and! guidance!of!many!mentors!and!friends!along!the!way.!First,!I!would!like!to!thank!my! advisor,!Dr.!Holly!Gaff,!for!her!countless!hours!of!patience,!friendship,!and!support!in!the! field,!lab,!and!beyond.!She!has!gone!above!and!beyond!in!every!way!to!help!me!succeed,! and!I!am!forever!grateful.!Dr.!David!Gauthier!was!my!mentor!in!the!lab,!and!the!population! genetics!component!of!this!dissertation!would!have!been!impossible!without!his!guidance.! His!humor!and!thoughtful!commentary!have!been!invaluable!throughout!this!process,!and! he!is!also!deserving!of!special!thanks.!Thanks!also!to!my!stalwart!committee!members;!Dr.! Wayne!Hynes,!microbiologist!extraordinaire;!Dr.!Eric!Walters,!ecological!theory!expert,! maker!of!wisecracks,!and!statistician;!and!Dr.!Elsa!Schaefer,!modeler,!mathematician,!and! cheerleader,!for!their!patience,!insight,!and!diligent!red!pens.!Special!thanks!also!to!my!ad' hoc!committee!member,!Ellen!Stromdahl,!who!continues!to!be!a!wonderful!professional! mentor!and!friend.!Gratitude!also!to!the!man!himself,!Dr.!Dan!Sonenshine,!for!being!willing! to!answer!strange!questions!about!tick!biology!at!odd!hours,!and!for!showing!us!all!how!it’s! done.! My!grad!student!family!at!ODU!was!also!instrumental!in!helping!me!persevere! through!this!doctoral!adventure.!Thank!you!to!my!lab!mates!Chelsea!Wright,!Lexi!White,! Pam!Kelman,!Amy!Johnson,!Erin!Heller,!and!Lindsey!Bidders!for!their!friendship,! camaraderie,!and!general!mischiefZmaking!in!the!lab!and!way,!way!beyond.!Special!thanks! to!fellow!ecology!grad!students!Ben!Gutzler,!Anna!Brownson,!Natasha!Hagemeyer,!and! Carly!York,!for!always!being!willing!to!listen,!laugh,!or!grab!a!beverage!over!the!last!five! vii years.!! This!PhD!was!made!possible!by!the!generous!support!of!the!SMART!(Science,! Mathematics,!and!Research!for!Transformation)!scholarship!through!the!American!Society! for!Engineering!Education!and!the!Department!for!Defense,!specifically!my!supporting! institution,!the!Army!Public!Health!Center.!This!research!was!also!supported!by!the! National!Institutes!of!Health,!grant!number!K25AI067791.!Thanks!also!to!the!Virginia! Academy!of!Science,!the!Entomological!Society!of!America,!and!the!Jayne!Koskinas!and!Ted! Giovannis!Foundation!for!Health!Policy!for!supporting!this!research.!A!final!thank!you!to! the!army!of!undergraduates!and!others!who!came!out!to!the!field!to!help!collect!data!–! without!you,!none!of!this!would!be!possible.! ! ! viii TABLE"OF"CONTENTS! " Page! ! LIST!OF!TABLES!..........................................................................................................................................!x! ! LIST!OF!FIGURES!.....................................................................................................................................!xii" ! INTRODUCTION!.........................................................................................................................................!1! ! ECOLOGY!AND!PUBLIC!HEALTH!RELEVANCE!OF!IXODES'AFFINIS!.....................!5! ! ECOLOGY!AND!PUBLIC!HEALTH!RELEVANCE!OF!! ! AMBLYOMMA'MACULATUM!....................................................................................................!8! !!!!!!!!!! BIOLOGICAL!INVASIONS!.......................................................................................................!11! !!!!!!!!!! TOOLS!FOR!MEASURING!BIOLOGICAL!INVASIONS!...................................................!14! ! RESEARCH!AIMS!........................................................................................................................!18! ! DEFINITION!OF!KEY!TERMS!................................................................................................!20! " IXODES'AFFINIS!IN!SOUTHEASTERN!VIRGINIA!AND!IMPLICATIONS!! FOR!THE!SPREAD!OF!BORRELIA'BURGDORFERI,'THE!AGENT!OF!!
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