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The Nuances of Locomotor Strategies in Suspensory Primates (Apes

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The Nuances of Locomotor Strategies in Suspensory Primates (Apes The$Nuances$of$Locomotor$Strategies$in$Suspensory$Primates$(Apes):$$$ $ Locomotor$Costs$in$Terms$of$Skeletal$Injury$ ! ! A$thesis$submitted$to$the$$ Graduate$School$ of$the$University$of$Cincinnati$ in$partial$fulfillment$of$the$$ requirements$for$the$degree$of$ $ Master$of$Arts$ $ In$the$Department$of$Anthropology$ of$the$College$of$Arts$and$Sciences$ by$ $ Jessica$Lynn$Hughes$ $ B.S.$Clemson$University$ December$2008$ $ Committee$Chair:$Katherine$Whitcome,$Ph.D.$ $ ABSTRACT$ Injury$may$be$a$significant$locomotor$cost,$in$that$a$severely$injured$animal$may$be$ unable$to$secure$enough$food$to$maintain$normal$activities,$avoid$predation,$or$find$mates.$ Thus,$safety$is$as$likely$as$energetics$to$be$the$impetus$of$natural$selection,$and$both$have$ potential$to$impact$reproductive$fitness$(Pontzer$and$Wrangham,$2004;$Thorpe,$2005).$The$ purpose$of$this$study$is$twofold.$First,$to$assess$fracture$patterns$relative$to$variation$in$ locomotion,$ecology,$and$body$mass$among$suspensory$apes.$Second,$to$quantify$change$in$ compact$bone$geometry$associated$with$bone$fracture$and$bone$remodeling$in$suspensory$ apes.$$ To$obtain$the$first$goal,$fracture$frequency,$severity,$and$remodeling$are$examined$ in$limb$bones$from$skeletons$of$141$wildZcaught$primates$according$to$four$major$ predictions.$First,$the$suspensory$genera$will$show$a$greater$percentage$of$limb$bone$ fractures$than$quadrupedal$baboons.$Second,$among$suspensory$apes,$the$brachiating$ gibbons$will$have$the$highest$fracture$frequency$and$the$most$severe$fractures,$the$ quadrumanus$orangutans$will$have$frequent$and$severe$fractures,$but$fewer$than$the$ brachiators,$and$the$climbing$and$knuckleZwalking$chimpanzees$will$have$the$lowest$ fracture$occurrence$and$severity.$As$a$corollary,$terrestrial$quadrupedal$baboons$will$have$ the$lowest$fracture$frequency$and$severity.$Third,$fractures$will$be$more$prevalent$in$ species$with$larger$bodies.$Fourth,$fracture$rate$and$severity$will$be$greatest$in$species$that$ travel$on$substrates$higher$in$the$forest$canopy.$The$results$show$that$body$size$is$a$ significant$predictor$of$fracture$frequency.$Increases$in$body$size$increase$the$likelihood$of$ fracture.$Travel$height$and$locomotor$strategy$are$not$significant$predictors$of$fracture$ frequency.$However,$the$dual$locomotor$strategy$and$low$travel$heights$used$by$Pan$have$a$ ! ii! ! negative$relationship$with$deformity$and$remodeling.$Such$strategies$may$provide$an$ evolutionary$advantage,$as$fractures$incurred$by$Pan$are$less$likely$to$be$severely$ deformed$and$are$more$likely$to$have$obtain$more$complete$remodeling.$ The$second$part$of$this$study$investigates$differences$in$the$internal$bone$geometry$ of$fractured$and$unfractured$corresponding$elements.$I$test$three$major$hypotheses.$First,$ animals$that$frequently$use$terrestrial$quadrupedal$locomotion,$such$as$baboons$and$ chimpanzees,$will$show$larger$differences$in$crossZsectional$area$(CSA)$when$affected$by$ fracture$than$those$that$are$more$suspensory.$Second,$elements$that$are$consistently$ weight$bearing$in$the$preferred$locomotor$strategy$will$show$the$most$difference$in$CSA.$ For$example,$the$difference$in$CSA$of$the$fractured$foreZlimbs$of$the$highly$suspensory$ gibbons$and$orangutans$will$be$greater$than$that$of$the$more$terrestrial$chimpanzees$and$ baboons.$Third,$body$size$will$be$positively$correlated$with$fracture$severity$and$will$have$ an$impact$on$the$difference$in$CSA$between$fractured$limbs$and$their$corresponding$ elements.$The$results$of$this$study$demonstrate$that$chimpanzees$have$a$lower$mean$CSA$ for$fractured$elements$than$unfractured$elements.$This$difference$in$bone$geometry$could$ be$related$the$chimpanzee’s$ability$to$engage$in$the$dual$locomotor$behaviors$of$ suspensory$locomotion$and$knuckleZwalking,$that$promote$reduction$in$body$mass$and$ impact$load$on$the$injured$limb.$! ! ! iii! ! ! ! ! ! ! ! Copyright!by! Jessica!Hughes! 2012! ! ! ! ! ! ! ! ! ! iv! ! ! ! ! ! ! For!my!grandfather,!Wayne!Burns,!! who!taught!me!strength,!perseverance,!and!patience.! ! ! ! v! ! Acknowledgements. I"would"like"to"first"thank"the"chair"of"my"thesis"committee"Dr."Katherine"Whitcome." When"I"walked"into"her"office"two"years"ago,"I"had"never"taken"an"anthropology"class,"but" Katherine’s"infectious"enthusiasm"for"exploring"the"world"around"her"through"the"lenses" provided"by"physical"anthropology"caught"hold"of"me"very"quickly."Without"her" unwavering"support"and"inspiring"work,"it"would"not"have"been"possible"to"complete"this" master’s"degree."A"special"thank"you"to"committee"member"Dr."Brooke"Crowley."Her"insight" on"ecology"and"behavior"was"crucial"to"writing"this"master’s"thesis."Gabby"Waesch,"your" tireless"assistance"in"data"analysis"was"essential"to"my"finishing"this"work"in"a"timely" manner."I"hope"to"work"further"with"you"in"the"future."To"Jeremy"Koster,"I"thank"you"for" your"help"with"my"statistical"analysis."Becoming"fluent"in"the"R"software"language"was"a" huge"feat"and"I"could"not"have"done"it"without"you."A"big"thank"you"to"Dr."Liza"Shapiro" (UTA),"Lyman"Jellema"(CMNH),"Darrin"Lunde"(NMNH),"Dr."Matthew"Colbert"(UTA),"Dr." Jessie"Maisano"(UTA),"Dr."Bruno"Frolich"(NMNH),"and"the"Case"Western"Radiology" Department"for"allowing"me"access"to"wonderful"skeletal"collections"and"helping"me" accomplish"my"data"collection."Finally,"I"would"like"to"thank"my"family"and"friends."Without" you"I"would"not"have"laughter,"sanity,"or"a"master’s"degree."" . ! vi! ! TABLE!OF!CONTENTS! ABSTRACT……………………………………………………………………………………………………………………..$ii$ DEDICATION………………………………………………………………………………………………………………….$v$ ACKNOWLEDGEMENTS………………………………………………………………………………………………...$vi$ LIST$OF$TABLES$……………………………………………………………………………………………………...……xii$ LIST$OF$FIGURES……………………………………………………………………………………..…………..………xiii$ PART!1:!Bone!Fractures! CHAPTER!1:!Introduction………………………………………………………………………………………….!1! 1.1 Suspensory$Locomotion$and$Hominoid$Ecology………………………………………………$3$ 1.2 Limb$Fracture$in$Suspensory$Primates……………………………………………………………$6$ 1.2.1 Suspensory$Locomotion$and$Risk$of$Injury……………………………………………………...$8$ 1.2.2 Safety$Features…………………………………………………………………………………………….$13$ 1.3 Hypotheses………………………………………………………………………………………………….$15$ 1.3.1 Locomotion$Hypotheses……………………………………………………………………………….$16$ 1.3.1.a Fracture$Occurrence$and$Severity$of$Fractures$will$be$Lowest$in$Quadrupedal$ Primates………………………………………………………………………………………………………$16$ 1.3.1.b Fracture$Occurrence$and$Severity$will$be$Related$to$Suspensory$Behavior……..$16$ 1.3.2 Ecological$Hypotheses………………………………………………………………………………….$16$ 1.3.2.a Fracture$Occurrence$and$Severity$will$Increase$with$Increasing$Body$Size……..$16$ !vii! ! 1.3.2.b Fracture$Occurrence$and$Severity$will$be$Highest$for$Animals$Foraging$ (Traveling$and$Feeding)$Higher$in$the$Canopy………………………………………………$17$ 1.4 Explanation$of$Predictions……………………………………………………………………………$17$ 1.5 Biomechanics$of$Locomotor$Support$in$Suspensory$Primates………………………..$18$ 1.5.1 Bone$Composition………………………………………………………………………………………..$18$ 1.5.2 Modes$of$Loading…………………………………………………………………………………………$20$ 1.5.3 Stress$and$Strain………………………………………………………………………………………….$21$ 1.6 Bone$Repair………………………………………………………………………………………………...$24$ CHAPTER!2:!Materials!and!Methods……………………………………………………………………..…!27! 2.1 Sample……………………………………………………………………………………………………...…$27$ 2.2 Visual$Assessment$of$Fracture$Severity$and$Bone$Deformation……………………...$29$ 2.3 Statistical$Analyses………………………………………………………………………………………$31$ CHAPTER!3:!Results……………………………………………………………………………………………..…!40! 3.1 Descriptive$Statistics……………………………………………………………………………………$40$ 3.1.1 Fracture$Frequencies……………………...……………………………………………………………$40$ 3.1.2 Remodeling…………………………………………………………………………………………….……$43$ 3.1.3 Deformation…………………………..……………………………………………………………….……$43$ 3.2 Locomotion$and$Ecology…………………………..…………………………………………………..$45$ 3.2.1 Comparison$Between$Quadrupedal$and$Suspensory$Locomotor$Modes…...……..$45$ 3.2.2 Locomotor$Comparison$Among$Suspensory$Apes…...............................................……..$45$ 3.2.3 Body$Size…...………………………………………………………………………………………………..$45$ 3.2.4 Canopy$Height……………………………………………………………………………………………..$46$ !viii! ! 3.3 Deformation$and$Remodeling………………………………………………….…………..………..$46$ 3.3.1 Deformation$and$Locomotor$Modes……………………………………….……………………..$46$ 3.3.2 Deformation$and$Body$Size…………………………………………………………………………..$47$ 3.3.3 Deformation$and$Canopy$Height……………………………………………….…………………..$48$ 3.3.4 Remodeling$and$Locomotor$Modes……………………………………………..………………..$48$ 3.3.5 Remodeling$and$Body$Size……………………………………………………..……………………..$48$ 3.3.6 Remodeling$and$Canopy$Height………………………………………..…………………………..$49$ CHAPTER!4:!Discussion………………………………………………………………………………………..…!49! 4.1 Influence$of$Locomotor$Strategy$on$Fracture$Frequency………………………………..$50$ 4.2 Influence$of$Locomotor$Strategy$on$Fracture$Deformity$and$Remodeling……....$51$ 4.3 Influence$of$Body$Size$on$Fracture$Frequency……………………………………………....$52$ 4.4 Influence$of$Body$Size$on$Fracture$Deformity$and$Remodeling………….…………...$53$ 4.5 Influence$of$Height$of$Travel$on$Fracture$Deformity$and$Remodeling……….........$54$ 4.6 Implications$for$Hominoid$Evolution$and$the$Last$Common$Ancestor……...….....$55$ 4.7 Future$Research……........................................................................................................................$57$ CHAPTER!5:!Conclusions…………………………………………………………………………………………!57! PART!2:!Internal!Bone!Geometry! CHAPTER!1:!Introduction……………………………………………………………………………………..…!59! 1.1 Changes$in$Morphology$Caused$by$Fracture………..……………………………………...…$59$ 1.2 Hypotheses……………………………………………………………………………………………….…$60$ 1.2.1 Locomotion$Hypotheses…………………………………………………………………………….…$60$
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