The$Nuances$of$Locomotor$Strategies$in$Suspensory$$(Apes):$$$ $

Locomotor$Costs$in$Terms$of$Skeletal$Injury$

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!

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$$geometry$associated$with$bone$fracture$and$bone$remodeling$in$suspensory$ apes.$$

To$obtain$the$first$goal,$fracture$frequency,$severity,$and$remodeling$are$examined$ in$limb$$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! ! !

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!

!

Copyright!by!

Jessica!Hughes!

2012!

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! iv! ! !

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!

!

!

For!my!grandfather,!Wayne!Burns,!!

who!taught!me!strength,!perseverance,!and!patience.!

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! 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.""

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! 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…………………………………………………………………………….…$60$

! ix! ! 1.2.1.a Terrestrial$Quadrupedal$Locomotion$will$be$Related$to$Smaller$Cross$Sectional$

Area$Than$Suspensory$Locomotion………………………………………………………………$60$

1.2.1.b Consistently$Used$Elements$will$show$the$Most$Difference$in$Cross$Sectional$

Area………………………………………………………………………………………………………….…$61$

1.2.2 Ecological$Hypotheses……………………………………………………………………………….…$61$

1.2.2.a Difference$in$Cross$Sectional$Area$will$be$Correlated$to$Body$Size……………….…$61$

1.3 Explanation$of$Predictions……………………………………………………………..…………..…$61$

CHAPTER!2:!Materials!and!Methods……………………………………………………………………..…!62!

2.1 Sample…………………………………………..…………..…………………………………………………62$

2.2 XZray$Computed$Tomography$(CT)$Scanning…..………..……………………………………62$

2.3 ImageJ$&$BoneJ$Analysis…..……………………………………………………………………………65$

2.4 Statistical$Analyses…..……………………………………………………………………………...……66$

$

CHAPTER!3:!Results…………………………………………………………………………………………………66!

3.1 Analysis$of$the$CSA$of$the$Control$Group$XZray$Computed$Tomography$(CT)$

Scanning…..……………………………………………………………………………..……………………67$

3.2 Comparison$of$Fractured$Elements$and$Their$Unaffected$Counterparts$by$

Genus……………………………………...……………………………………………………………………67$

3.3 Comparison$of$Fractured$Elements$and$Their$Unaffected$Counterparts$by$

Element………………………………………………………………………………………………..………68$

$

CHAPTER!4:!Discussion………………………………………………………………………………………..…!68!

! x! ! 4.1 Analysis$of$the$CrossZSectional$Area$of$the$Control$Group………….………………...…68$

4.2 Comparison$of$Fractured$Elements$and$Their$Unaffected$Counterparts$by$

Genus…………………………………………………………………...………………………………………69$

4.3 Comparison$of$Fractured$Elements$and$Their$Unaffected$Counterparts$by$

Element………………………………………………………………………………………………………..69$

4.4 Further$Research……………………………………………………….…………………………………70$

CHAPTER!5:!Conclusions…………………………………………………………………………………………!71!

REFERENCES……………………………………………………………………………………….………………………$72$

!

!

! xi! ! LIST!OF!TABLES!

PART!1:!Bone!Fractures!

Table$2.1:$$ The$14$Elements$of$the$ForeZ$and$HindZlimb.………………………..……………....…..28$

Table$2.2:$$ Survey$of$$skeletons$examined.…………………………………………………….28$

Table$2.3:$$ The$6$Measurements$Taken$From$Each$Element.………………………………….…..30$

Table$2.4:$$ Deformity$Scale$Rubric.…………………………………………….…………………...…..…….33$

Table$2.5:$$ Remodeling$Scale$Rubric.…………………………………………….……………...……..…….34$

Table$3.1:$$ Comparison$of$Fracture$Frequencies.……………………….………………………...…….42$

Table$3.2:$$ Comparison$of$Fracture$Frequencies$by$Element.…………….…………..……..…….42$

Table$3.3:$$ Fractured$Element$Side.…………………………..……….………………………………..…….42$

PART!2:!Internal!Bone!Geometry!

Table$2.1:$$ Specimens$CTZScanned.…………………………………………………………..……………….64$

Table$3.1:$$ Results$of$Paired$TZTests$of$CSA$of$the$Test$Group$by$Genus…………….……….68$

Table$3.2:$$ Results$of$Paired$TZTests$of$CSA$of$the$Test$Group$by$Element………..…..…….68!

!

!

!xii! ! LIST!OF!FIGURES!

PART!1:!Bone!Fractures!

Figure$1.1:$ Hominoid$Cladogram…………………………………………………………………………..…….3$

Figure$1.2:$$ Arboreality$profiles$for$Pan,$Pongo,$Hylobates,$and$Papio………..….………………8$

Figure$1.3:$ Gibbon$Locomotor$Mode……………………………………………………………..……..……...9$

Figure$1.4:$ Orangutan$Locomotor$Mode.………………….…………………………………………..…….10$

Figure$1.5:$ Chimpanzee$Locomotor$Modes.…………………………………………………..……..…….11$

Figure$1.6:$ Baboon$Locomotor$Mode.………………….………………………..……………………..…….12$

Figure$1.7:$ Responses$to$bone$loading.……………..……………………………..…………………..…….19$

Figure$1.8:$ Diagram$of$loading$modes$acting$upon$a$long$bone.………………………………….20$

Figure$1.9:$ The$StressZstrain$Curve$for$Bone$in$Compression$and$in$Tension.………...…...23$

Figure$1.10:$ $The$Bone$Remodeling$Cycle.………………………………………………………………..….25$

Figure$2.1:$$ $The$relationship$between$the$log$of$the$recorded$body$weight$from$ collection$records$and$the$log$of$the$geometric$mean$for$Papio,$Pan,$and$

Pongo…………………………………….…………………………………………….…………………………….…..…….37$

Figure$2.2:$ $The$relationship$between$recorded$body$weight$from$collection$records$and$ the$standardized$log$of$the$geometric$mean$for$Papio,$Pan,$Pongo,$and$

Hylobates.…………………………………………….………………………………..…………………………..………...38$

!xiii! ! $

Figure$3.1:$$ $A$fractured$left$$of$an$orangutan.…………………………….…………...…….43$

Figure$3.2:$ $Number$of$fractured$elements$in$each$remodeling$category$for$each$ genus.……………………….…………………………………………………………………………..………………..…….44$

Figure$3.3:$$ Number$of$fractured$elements$in$each$deformation$category$for$each$ genus.……………………….………………………………………………………………………………..…………..…….44$

Figure$3.5:$$ The$relationship$between$fracture$frequency$and$the$standardized$log$$ of$the$geometric$mean.……………………….…….…………..……………………………………….………..…….46$

Figure$3.6:$$ Distribution$of$the$degree$of$deformation$with$respect$to$body$ size…..……………………….……………………………………………………………………………….…………..…….47$

Figure$3.7:$$$ Distribution$of$the$degree$of$remodeling$with$respect$to$body$ size…..……………………….……………………………………………………………………………….…………..…….49$

PART!2:!Internal!Bone!Geometry!

Figure$2.1:$ Cross$section$of$the$diaphysis$of$a$long$bone.……………………………….……..…….65$

Figure$2.2:$$ CT$scans$slides$of$the$cross$section$of$the$left$and$right$femur$of$Papio$P52$ from$the$University$of$Texas$at$Austin.……………………………………………………….…………....…….65$

Figure$2.3:$$ 3ZDemensional$rendering$of$the$right$femur$of$Papio$P52$from$the$University$ of$Texas$at$Austin.……………………………………………………………….………………………………….…….66$

Figure$4.1:$$ Sample$CT$scans$slides$of$the$left$and$right$humerus$of$an$orangutan$that$are$ color$coded$and$prepared$for$the$calculation$of$humeral$torsion…………………………………….71$

!xiv! ! PART!1:!Bone!Fractures!

CHAPTER!1:!Introduction!

Primate$locomotor$costs$are$often$assessed$in$terms$of$energy$expenditure$(Hunt,$

1991;$Fleagle,$1999;$Pontzer$and$Wrangham,$2004;$Thorpe,$2005;$Thorpe$et$al.,$2006;$

Crompton$et$al.,$2010;$Hanna$and$Schmitt,$2011).$However,$factors$other$than$energy$ expenditure$can$act$as$evolutionary$pressures$on$locomotor$adaptations$and$behaviors$

(Thorpe,$2005;$Jarrell,$2011).$Injury$may$be$a$significant$cost,$in$that$a$severely$injured$ animal$may$be$unable$to$secure$enough$food$to$maintain$activities,$avoid$predation,$or$find$ mates$(Thorpe$et$al.,$2006).$Thus,$safety$is$as$likely$as$energetics$to$be$the$impetus$of$ natural$selection$and$both$have$the$potential$to$impact$reproductive$fitness$(Pontzer$and$

Wrangham,$2004;$Thorpe,$2005;$Thorpe$et$al.,$2006).$Primates$in$general,$because$of$their$ arboreal$habitats,$may$be$more$vulnerable$to$skeletal$injury$than$many$other$mammals.$

Schultz$(1944)$in$studying$skeletal$pathologies$among$gibbons,$suggested$that$apes$in$ particular$engage$to$varying$degrees$in$highZrisk$locomotor$strategies$(Schultz,$1944).$$$

The$arboreal$milieu$that$comprises$a$forest$canopy$is$navigationally$challenging$ because$preferred$food$sources$such$as$fruits$are$commonly$located$on$slender$and$flexible$ branches.$Branch$compliancy$makes$$transfer$from$one$tree$to$another$particularly$difficult$ for$large$bodied$apes$(Thorpe,$2005).$Thus,$arboreal$feeding$and$travel$increase$the$ likelihood$of$falls$for$arboreal$apes.$The$relationship$between$arboreal$falls$and$bone$ fractures$has$been$documented$for$Pan,$Hylobates,$and$Papio$(Lovell,$1991;$Jurmain,$1997;$

Carter,$et$al,$2008).$Moreover,$injuries$associated$with$falls$are$considered$a$leading$cause$ of$long$bone$fractures$among$primates$(Lovell,$1991;$Jurmain,$1997;$Carter,$et$al,$2008).$

! 1! ! For$the$suspensory$apes,$evolutionary$pressures$have$shaped$locomotor$adaptations$ related$to$exploiting$small$branch$substrates.$$

Extant$apes$relative$to$most$other$living$primates$are$large$in$body$size$and$ therefore$have$a$low$branch$to$body$size$ratio$that$increases$the$risk$of$branch$failure$ under$loading$(Rodman,$1984;$Fleagle,$1999;$Jarrell,$2011).$Balancing$a$large$body$with$a$ high$center$of$gravity$over$a$narrow$branch$is$biomechanically$challenging$as$small$ displacements$of$the$center$of$mass$lead$to$high$destabilizing$moments.$Below$branch$ suspension$allows$apes$of$large$body$size$to$utilize$small$branches.$However$the$inherent$ risk$of$supporting$a$large$body$on$a$small$substrate$is$still$present.$Below$branch$ suspension$presents$its$own$host$of$risk$factors.$Suspensory$locomotion$in$the$wild$often$ occurs$across$multiple$supports$of$varying$size,$stability,$and$compliance$increasing$the$ risk$of$substrate$failure$(Rose,$1973;$Thorpe,$2005).$During$arboreal$locomotion$the$ displacement$of$branches$upon$contact$increases$the$risk$that$an$individual$will$lose$ contact$with$the$support$causing$a$fall$(Rose,$1973;$Thorpe,$2005).$$Given$their$propensity$ for$armZswing$feeding$and$travelling,$suspensory$apes$may$be$particularly$vulnerable$$to$ falls$associated$with$loss$of$substrate$contact$$because$they$are$often$supported$by$$only$ one$point$of$contact$between$hand$and$branch.$If$they$loose$contact$with$the$support$they$ fall$away$from$it,$as$opposed$to$towards$the$support$in$above$branch$locomotion$and$are$ less$likely$to$recover$their$stability.$Thus,$because$apes$have$a$relatively$large$body$mass$ compared$to$other$primates,$and$because$larger$animals$must$absorb$more$high$impact$ energy$upon$falling$(Radasch,$1999;$Jarrell,$2011),$falls$are$more$likely$to$have$more$severe$ consequences$for$apes.$$

! 2! ! In$this$thesis$research$I$investigated$long$bone$fractures$in$museum$collections$of$ three$genera$of$suspensory$apes,$Hylobates,$Pongo,$and$Pan,$in$order$to$identify$whether$ varying$locomotor$repertoires$manifest$with$equal$or$differential$patterns$of$limb$injury.$$

In$addition$to$quantifying$the$frequency$of$long$bone$fractures$among$these$primate$taxa,$I$ examined$the$deformation$and$remodeling$of$bones$associated$with$fracture$injury.$CrossZ sectional$geometry$of$affected$long$bones$and$their$corresponding$elements$was$assessed$ for$differential$bone$deposition$due$to$changes$in$loading$patterns$associated$with$injury.$$

1.1 Suspensory*Locomotion*and*Hominoid*Ecology*

Lesser$apes,$great$apes,$and$ humans,$whether$extinct$or$extant,$ are$classified$within$the$primate$ superfamily$Hominoidea$(Jauch$et$ al.,$1992)(Figure$1.1).$Extant$ Least Common Ancestor?* hominoids$(gibbons,$orangutans,$ ! gorillas,$chimpanzees,$bonobos$and$ Figure!1.1:!Hominoid!Cladogram.!Hominoids!include!the! lesser!apes!(siamangs!and!gibbons),!great!apes!(orangutans,! humans)$are$far$less$diverse$than$ gorillas!and!chimpanzees),!and!humans.!Most!Miocene!apes! were!evolutionary!dead!ends.!But!some!Miocene!ape,! the$extinct$hominoid$species$of$the$ discovered!or!yet!to!be!discovered,!was!the!last!common! ancestor!to!the!extant!hominoids!(Begun!and!Gurche,!2006).! Miocene$epoch$(Begun,$2006;$MoyàZ Asterisks!(*)!denote!extinct!primates.!(Image!modified!from! Montgomery!et!al.!2010)! Solà$et$al.,$2009;$Begun,$2010;$

McNulty,$2010;$Begun,$2012),$a$period$extending$from$23.0$to$5.3$million$years$ago$

(International$Commission$on$Stratigraphy,$2010).$Nearly$40$genera$of$Miocene$fossil$apes$ are$known$from$localities$across$the$Old$World$(Begun,$2006;$Begun,$2007;$Begun,$2010)$

! 3! ! and$their$number$is$eight$times$that$of$extant$ape$genera$(Begun,$2006).$Although$the$fossil$ record$of$MidZMiocene$apes$is$relatively$rich,$reconstructing$the$full$evolutionary$history$of$ hominoids$is$problematic.$The$Miocene$fossil$record$for$apes$is$sporadic$throughout$the$ near$20$my$epoch$and$predominantly$consists$of$isolated$jaws$and$teeth,$some$of$which$ remain$difficult$to$assign$taxonomically$(Pilbeam,$1979;$Begun,$1996;$McNulty,$2010).$

Statistical$predictions$based$on$the$fossil$record$suggest$that$no$more$than$7%$of$all$ primate$species$that$ever$existed$are$known$from$fossils$(Tavaré$et$al.,$2002).$Living$ hominoids$are$one$of$the$least$represented$groups$of$mammals$in$relationship$to$their$past$ diversity$(Pilbeam,$1979;$McNulty,$2010).$*

Derived$traits$for$extant$hominoids$include$absence$of$an$external$tail,$frequent$ semiZupright$and$upright$postures,$relatively$short$trunks,$enhanced$grasping$capabilities,$ large$brains$relative$to$body$size$and$flexible$foreZlimbs$with$highly$mobile$wrists$

(McNulty,$2010).$The$majority$of$these$derived$anatomical$traits$result$in$semiZupright$and$ upright$postures$and$enhanced$grasping$capabilities$that$facilitate$suspensory$behavior,$ the$main$locomotor$and$postural$mode$among$the$extant$hominoids.$$$$

One$of$the$earliest$known$fossil$hominoids$with$suspensory$traits$is$Morotopithecus$ bishopi,$a$large$bodied,$35Z45$kg$ape$from$Uganda$dating$to$the$Lower$Miocene$(20.6$ million$years$ago)$(MacLatchy$and$Pilbeam,$1999).$Based$on$its$ovate$glenoid$fossa$and$ vertebrae$with$caudally$directed$spinous$processes$and$perpendicular$transverse$ processes,$Morotopithecus$is$described$by$MacLatchy$and$colleagues$as$a$highly$arboreal$ species$that$relied$on$vertical$and$cautious$foreZlimbZdominated$climbing$and$facultative$ suspension$with$some$retained$quadrupedal$behaviors$(MacLatchy$et$al.,$2000).$The$fossil$

! 4! ! record$indicates$that$by$the$MidZMiocence$(16$to$12$million$years$ago)$hominoids$ presented$morphological$features$consistent$with$habitual$suspensory$locomotion,$ including$full$circumduction$at$the$,$a$broad$trunk$(Gebo$et$al.,$1997;$Thorpe$et$al.,$

2006),$a$$positioned$more$dorsally$than$earlier$hominoids$such$as$Morotopithecus$

(Thorpe$et$al.,$2006),$a$wristZantebrachial$joint$character$complex$and$an$extended$ulnar$ styloid$process$that$allowed$for$increased$adduction$and$supination$when$climbing$and$ suspending$(MoyàZSolà$et$al.,$2004).$These$characteristics$are$shared$with$extant$ hominoids.$

During$the$middle$Miocene$in$Europe,$some$15$million$years$ago,$the$fossil$genus$

Dryopithecus$emerged.$This$genus$may$have$given$rise$to$African$apes$(Begun,$2006)$

(Figure$1.1).$$exhibits$features$that$are$more$specialized$than$those$in$earlier$ apes,$including$longer$$and$large,$powerful$hands$and$fingers,$which$are$ characteristics$of$living$suspensory$apes$(Begun$1994;$McNulty,$2010).$Oreopithecus,$from$ the$late$Miocene,$approximately$7$million$years$ago,$presents$unique$skeletal$features$ along$with$the$typical$long$arms$and$large,$powerful$hands$and$fingers$characteristic$of$ suspensory$apes$(McNulty,$2010).$The$pubis$does$not$resemble$that$of$apes,$but$closely$ resembles$the$pubis$of$the$hominin$Australopithecus$afarensis.$The$foot$of$Oreopithecus$ differs$from$specialized$climbers,$showing$a$change$in$the$direction$of$leverage,$causing$the$ foot$to$be$more$stiff$and$capable$of$supporting$the$body$during$bipedal$locomotion$(Köhler( and$MoyáZSolá̀,$1997).$$Köhler'and'MoyáZSolá̀$(1997)$have$interpreted$the$unique$bipedal$ foot$and$pelvis$of$Oreopithecus$as$wellZadapted$for$bipedal$locomotion.$They$assert$that$

Oreopithecus$engaged$in$$while$feeding$and$may$have$shuffled$bipedally$ between$food$resources.$Compellingly,$the$ecological$scenarios$that$have$been$suggested$

! 5! ! for$the$bipedal$evolution$of$Oreopithecus,$population$isolation$and$selective$pressure$ focusing$on$energy$efficient$feeding$behaviors,$are$similar$to$some$proposed$for$the$origins$ of$human$bipedal$postures$(e.g.,$Jolly$1970;$McNulty,$2010).$Although$the$strength$of$ evidence$for$bipedalism$in$Oreopithecus$has$been$questioned,$there$is$little$doubt$regarding$ the$suspensory$adaptations$in$this$Miocene$ape$(Begun,$2007).$Studying$the$locomotor$ strategies,$adaptations,$and$ecology$of$suspensory$apes$may$provide$greater$depth$of$ insight$into$the$locomotor$behaviors$of$these$early$apes,$including$the$hominoid$last$ common$ancestor.$

Although$the$fossil$record$for$apes$is$extremely$sparse$from$the$late$Middle$

Miocene),$this$modest$record$suggests$that$more$recent$hominoid$taxa$retained$suspensory$ characteristics$through$time$(McNulty,$2010).$Moreover,$extant$apes,$like$their$Miocene$ predecessors,$vary$in$the$mode$of$suspensory$behaviors$in$which$they$engage.$For$ instance,$smallZbodied$gibbons$(extant$Hylobates)$are$almost$exclusively$arboreal$while$the$ large$bodied$gorillas$(extant$Gorilla)$are$predominately$terrestrial.$Even$with$the$ incomplete$fossil$record$from$the$Late$Miocene,$when$the$last$common$ancestor$of$the$ hominoid$clade$was$present,$using$a$bottomZup$approach$and$studying$the$impact$of$injury$ on$extant$apes$gives$insight$into$the$impact$of$similar$injuries$for$our$Miocene$ancestors$

(McNulty,$2010).*

1.2 Limb*Fracture*in*Suspensory*Primates*

It$is$difficult$to$say$what$fitness$costs,$in$terms$of$survival$and$reproductive$success,$ wild$primates$incur$as$a$result$of$fractured$bones$(Bulstrode$et$al.,$1986).$Falls$are$likely$to$ be$rapid,$shortZterm$events.$Nevertheless,$falls$among$adult$suspensory$apes$are$well$

! 6! ! documented$suggesting$that$falls$and$associated$injuries$may$be$relatively$frequent$

(Goodall,$1986;$Lovell,$1990;$Jurmain,$1997;$Carter$et$al.,$2008).$$Although$injured,$ individuals$with$fractured$bones$must$continue$to$rely$to$some$extent$on$compromised$ limbs$to$support$their$bodies$during$feeding$and$traveling$in$order$to$survive.$As$such,$ injured$wild$primates$may$contend$with$severe$anatomical$consequences$including$ reduced$limb$length,$loss$of$muscle$mechanical$advantage,$and$limb$atrophy,$all$of$which$ may$perturb$normal$patterns$of$locomotor$and$feeding$behaviors$further$disadvantaging$ individuals$who$already$incur$increased$energetic$cost$associated$with$the$physiological$ processes$of$injury$repair$that$follows$bone$fracturing.$$$

To$better$understand$the$incidence$and$severity$of$bone$fracture$among$wild$ suspensory$apes,$I$investigated$long$bone$fractures$in$three$wild$caught$genera,$Hylobates,$

Pongo$and$Pan.$The$primary$suspensory$strategies$differ$for$these$species$and$include$ brachiation,$quadrumanus$climbing,$and$$swing/knuckleZwalking,$respectively.$I$ focused$on$these$genera$in$order$to$determine$whether$varying$locomotor$repertoires$ manifest$with$equal$or$differential$patterns$of$limb$injury.$$The$genus$Papio$(baboons),$a$ relatively$large$bodied$terrestrial$quadrupedal$,$was$also$examined$in$order$to$ compare$effects$of$suspensory$and$terrestrial$modes$on$fractures.$Because$baboons$(Papio)$ often$feed$and$travel$on$the$ground$(Johnson$et$al.,$2012),$I$expected$them$to$exhibit$fewer$ fractures$than$suspensory$apes.$Assessment$of$the$relationships$between$fracture$ frequency$and$severity$for$terrestrial$and$arboreal$primates$should$provide$insight$into$the$ degree$of$increased$risk$associated$with$arboreal$locomotion.$$In$addition$to$quantifying$ the$frequency$of$long$bone$fractures$among$these$four$primate$genera,$I$also$examined$the$

! 7! ! extent$of$repair$and$remodeling$of$fractured$limb$bones$in$order$to$identify$relationships$ between$fracture$repair,$locomotor$strategies,$and$body$size.$

Terrestrial$environments$present$largely$continuous,$uniform$routes$with$less$ variation$in$substrate$stability$than$arboreal$environments$(Garber,$2007).$Arboreal$ milieus$present$a$greater$number$of$discontinuities$and$less$predictable$stability$among$ substrates$of$widely$varying$dimensions$and$stiffness$than$terrestrial$habitats.$Therefore,$ the$risk$of$injury$due$to$falls$is$likely$to$be$greater$for$arboreal$primates.$Evidence$of$ impact$trauma$in$ape$skeletons$(Schultz,$1969;$Jurmain,$1997;$Lovell,$1990)$along$with$ documented$observations$of$ape$falls$(Goodall,$1986)$draw$attention$to$the$risk$of$serious$ injury,$even$death$from$arboreal$falls$(Thorpe$et$al.,$2009).$The$suspensory$genera$ examined$in$this$study$are$expected$to$have$different$risk$factors$for$falls$and$injuries$ associated$with$their$locomotor$strategies,$ Arboriality profiles for each genus ecological$variables,$and$body$size.$$

Pan 1.2.1 Suspensory*Locomotion*and*Risk*of*

Injury* Pongo

Hylobates $The$genus$Hylobates$(gibbons$and$

siamangs)$moves$about$and$feeds$primarily$in$the$ Papio middle$and$upper$levels$of$the$canopy$in$Southeast$ 0 % 20 % 40 % 60 % 80 % 100 %

Percent of

Asian$rainforests$(Fleagle,$1999),$only$infrequently$ Figure!1.2:!Arboreality!profiles!for!Pan,!Pongo,! Hylobates,!and!Papio.!(modified!from!Jarrell,! descending$to$the$ground$(Vereecke$et$al.,$2006).$ 2011*)! *Sources:!Pan!(Hunt,!1992;!Rodman,!1984);! Gibbons$are$the$most$suspensory$of$the$extant$ (Pongo!(Rodman,!1984);!Hylobates(Cannon!and! Leighton,!1994;!Islam!and!Feeroz,!1992;! apes,$typically$spending$greater$than$99%$of$their$ Vereecke!et!al.,!2006);!Papio!(Hunt,!1992;!Rose,! 1977;!Dunbar!and!Dunbar,!1974;!Napier!and! Napier,!1967)! ! 8! ! time$in$trees$at$heights$above$25$meters$(Cannon$and$Leighton,$1994;$Islam$and$Feeroz,$

1992;$Jarrell,$2011)(Figure$1.2).$They$move$principally$by$brachiation,$a$specialized$mode$ of$arm$swinging,$which$is$so$rapid$that$at$times$neither$foreZlimb$contacts$the$substrate,$ introducing$a$true$flight$phase$(Michilsens$et$al.,$2009).$Gibbons$also$occasionally$engage$in$ slow$quadrumanus$climbing,$a$form$of$semiZsuspensory$fourZlimb$travel,$especially$when$ feeding$(Garber,$2007).$$

Gibbons$specialize$on$a$diet$of$ripe$fruit$and$new$ leaves$(McConkey$et$al.,$1999).$Fruit$occurs$in$widely$ scattered$clumps$throughout$the$forest,$and$hangs$high$in$ the$canopy$near$the$terminal$ends$of$branches$(Fleagle,$

1999).$To$meet$nutritional$needs,$gibbons$must$forage$

over$a$relatively$large$area$in$order$to$access$stands$of$ Figure!1.3:!Gibbon!Locomotor! Mode.!A!gibbon!in!a!suspensory! fruit.$Gibbon$foraging$involves$bridging$and$leaping$ posture!at!the!terminal!end!of!a! branch.!(Photo!courtesy!of!J.! behaviors$among$terminal$branches,$increasing$the$ Milsteen)! likelihood$of$substrate$failure$under$loading$as$well$as$fracture$injury$from$arboreal$falls$

(Figure$1.3).$Speedy$richochetal$brachiation$may$also$lead$to$more$frequent$misjudgment$ in$substrate$choice$and$result$in$more$falls.$$$

The$genus$Pongo$(orangutans)$is$the$largest$habitually$arboreal$mammal.$Among$ the$suspensory$apes,$it$is$second$only$to$Hylobates$in$its$degree$of$arboreal$travel$(Fleagle,$

1999).$This$genus$spends$nearly$90%$of$its$time$in$the$arboreal$environment$(Rodman,$

1984).$Adult$females$(mean$mass$35.8$kg),$which$are$considerably$smaller$than$adult$ males,$are$almost$entirely$arboreal.$The$larger$adult$males$(mass$range$60$to$90kg),$more$

! 9! ! frequently$come$to$the$ground$to$travel$between$trees$(Rodman,$1984;$Fleagle,$1999).$

Orangutans$typically$travel$and$feed$in$the$middle$and$upper$levels$of$the$Southeast$Asian$ forest$canopy$(Thorpe$et$al,$2008),$spending$approximately$72%$of$their$time$at$heights$ between$10$and$20$meters$(Thorpe$and$Crompton,$2005;$Jarrell,$2011).$$

Like$gibbons,$orangutans$primarily$subsist$on$ fruit$and$young$leaves,$and$their$large$body$size$and$ metabolic$requirements$require$significant$foraging$ hours$in$the$unstable$terminal$ends$of$branches$high$in$ the$canopy$(Cant,$1992).$Their$tendency$to$cross$gaps$ on$unstable$branches$puts$orangutans$at$risk$for$an$ injuryZinducing$fall$(Figure$1.4).$This$risk$of$falling$due$ to$substrate$failure$may$be$substantially$higher$for$ orangutans$because$of$their$heavy$mass$when$ Figure!1.4:!Orangutan! Locomotor!Mode.!Female! compared$to$smaller$arboreal$apes.$$ orangutan!in!a!suspensory! posture!with!her!offspring.! Pan$(chimpanzees$and$bonobos)$are$the$least$arboreal$of$the$suspensory$apes$(Photo!courtesy!of!Arkive)!! examined$in$this$study,$and$frequently$travels$terrestrially.$However,$because$chimpanzees$ and$bonobos$feed$primarily$on$fruit,$nuts,$and$leaves$(Tweheyo$et$al.,$2003;$Stanford$and$

Nkurunungi,$2003),$they$spend$much$of$their$foraging$time$in$trees,$where$they$encounter$ many$of$the$same$falling$risks$as$gibbons$and$orangutans$(Cant,$1992)$(Figure$1.5).$

Chimpanzees$usually$occupy$the$lower$levels$of$the$forest$woodland$canopy$at$heights$ below$11$meters$(Jarrell,$2011),$where$they$engage$in$a$mixture$of$suspensory$and$ quadrupedal$locomotion$(Carlson$et$al.,$2006).$They$use$a$variety$of$suspensory$and$seated$

!10! ! feeding$postures$(Fleagle,$1999).$When$traveling$between$wooded$areas,$chimpanzees$ locomote$quadrupedally$using$a$specialized$form$of$terrestrial$locomotion$described$as$ knuckleZwalking,$which$is$also$characteristic$of$gorillas$(Rose,$1973).$During$knuckleZ walking$the$hands$contact$the$ground$via$the$dorsal$side$of$the$intermediate$phalanges$ while$the$feet$contact$the$ground$heal$to$toe$(Jarrell,$2011).$Pan$is$the$least$arboreal$of$the$ suspensory$apes,$spending$on$average$only$about$55%$of$its$time$in$the$arboreal$ environment,$which$is$considerably$less$than$gibbons$and$orangutans$$(Rodman,$1984,$

Hunt,$1992;$Jarrell,$2011).$Still,$their$moderately$large$body$size$may$increase$the$ likelihood$of$falling$due$to$branch$failure$while$feeding$arboreally.$Nevertheless,$their$close$ proximity$to$the$ground$may$decrease$the$probability$of$fracture$injury$when$compared$to$ the$more$arboreal$gibbons$and$orangutans.$$

Figure!1.5:!Chimpanzee!Locomotor!Modes.!On!the!left,!a!chimpanzee!hangs!in!a!suspensory!posture! near!the!terminal!end!of!a!branch.!To!the!right!a!chimpanzee!is!knuckle]walking!on!the!ground.!!(Photo! courtesy!of!Arkive)!! ! $Baboons$(Genus$Papio)$are$quadrupedal$monkeys$that$primarily$locomote$ terrestrially$(Figure$1.6).$Baboons$are$omnivorous,$consuming$a$wide$variety$of$foods$ including$fruits,$stems,$tubers,$leaves,$seeds,$insects,$mushrooms,$bark,$gums,$and$soil$

!11! ! (Johnson$et$al.,$2012).$They$are$well$adapted$to$ savannas$and$their$varied$diet$permits$them$to$ forage$chiefly$on$the$ground$(Eisenberg$et$al.,$1972;$

Higham$et$al.,$2009).$Though$baboons$may$seek$the$ safety$of$rock$outcroppings$and$low$trees$for$ Figure!1.6:!Baboon!Locomotor! sleeping,$they$do$not$travel$at$heights$above$5$ Mode.!A!baboon!locomoting! terrestrially!with!its!infant!(Photo! meters$(Jarrell,$2011).$Thus,$they$are$far$less$likely$ courtesy!of!J.J.!Lopinot).! ! to$succumb$to$incur$injury$due$to$falls$than$any$of$the$suspensory$apes$described$in$this$ study.$$

To$summarize,$the$three$genera$of$suspensory$apes$in$this$study$spend$55%Z99%$of$ their$combined$travel,$resting,$and$feeding$time$among$arboreal$substrates$(Figure$1.2).$$

Because$the$fruits$and$leaves$preferred$by$apes$grow$in$clusters$at$the$terminal$ends$of$ branches,$much$of$this$time$is$spent$on$dangerously$small$branches.$These$substrates$differ$ markedly$in$size$and$stiffness.$As$canopy$height$increases,$branch$diameter$decreases$and$ branch$compliance$increases$(Thorpe,$2005).$Moreover,$at$a$greater$distance$from$the$core$ of$the$tree,$branches$taper,$increasing$compliance$and$providing$less$stable$support$for$the$ suspensory$apes$as$they$feed$or$cross$gaps$(Sussman,$1991;$Cant,$1992).$Canopy$gaps$and$ the$jumbled$distribution$of$the$terminal$branches$that$approach$these$gaps$increase$the$ amount$of$energy$required$for$apes$to$safely$bridge$between$them$(Cant,$1992;$Thorpe$et$ al.,$2006;$Thorpe$et$al.,$2009).$$

Navigating$thin$and$terminal$supporting$branches$in$the$most$productive$areas$of$ fruiting$trees$may$be$the$key$selection$pressure$for$the$evolution$of$suspensory$behaviors$

!12! ! in$primates$(Hunt,$1992).$Unlike$terrestrial$environments$that$typically$provide$a$uniform$ and$stable$substrate,$arboreal$environments$are$more$challenging.$Because$arboreal$ substrates$vary$in$size$and$stiffness,$with$substantial$gaps$and$discontinuities$among$them,$ navigating$among$them$is$complex$(Garber,$2007).$Thus,$arboreal$travel$compounded$by$ large$body$mass$may$increase$risk$of$injury$from$falls,$including$the$risk$of$bone$fracture$ injury.$$

1.2.2 Safety*Features*

Evolution$likely$favors$behaviors$and$anatomical$adaptations$that$limit,$but$may$not$ eliminate,$the$risk$of$injury$from$falls$related$to$suspensory$locomotion.$Although$gibbon$ postural$and$locomotor$anatomy$is$broadly$similar$to$that$of$other$great$apes,$several$ gibbon$traits$appear$to$reduce$risks$associated$with$their$highZspeed$arm$swing$ brachiation.$Among$apes,$gibbons$possess$the$longest$foreZlimbs$relative$to$both$humeral$ and$body$size$(Michilsens$et$al.,$2009).$Their$phalanges$are$long,$slender$and$curved$$

(Napier,$2005).$Nonetheless,$the$hands$and$feet$of$gibbons$are$well$muscled$and$relatively$ strong$(Midlo,$1934;$Napier$2005),$allowing$secure$and$precise$grasp$of$a$variety$of$ substrates.$Furthermore,$the$gibbon$shoulder$has$a$globular$humeral$head,$greatly$reduced$ tubercles,$and$a$cranially$directed$glenoid$fossa$that$allows$full$360°$shoulder$ circumduction,$greater$than$any$other$ape$(Gebo$et$al.,$1997).$The$cranially$directed$ glenoid$fossa$positions$the$foreZlimb$more$directly$in$line$with$the$center$of$gravity$during$ suspension$(Midlo,$1934;$Gebo$et$al.,$1997;$Fleagle,$1999).$At$the$wrist,$the$ulnar$styloid$is$ reduced$(the$shortest$among$apes)$allowing$greater$rotation$of$the$hand$at$the$wrist$

(Midlo,$1934;$Fleagle,$1999).$These$traits,$in$combination$with$their$large$range$of$motion,$

!13! ! may$allow$gibbons$enhanced$control$and$ability$to$grasp$substrates$during$highZspeed$ locomotion,$thereby$reducing$the$risk$of$falling.*

Orangutans$may$have$the$highest$risk$of$branch$failure$due$in$large$part$to$their$ extreme$body$size$(Thorpe,$2008).$Like$other$suspensory$primates,$orangutans$have$long$ foreZlimbs$with$elongated,$hookZlike$hands$(Midlo,$1934;$Fleagle,$1999),$curved$digits,$and$ a$short$pollex$(Midlo,$1934;$Thorpe,$2008).$Their$extremely$mobile$hindZlimbs$have$ dexterous$feet$with$curved$digits$and$a$shortened$hallux$(Midlo,$1934;$Thorpe,$2008).$

Orangutans$engage$often$in$quadrumanus$scrambling$as$a$primary$locomotor$strategy,$ dispersing$body$weight$across$multiple$substrates$through$use$of$all$four$limbs$(Cartmill$ and$Milton,$1977).$Orangutans$primarily$feed$in$suspensory$postures$and$employ$their$ long$reach$to$manipulate$branches$bringing$food$closer$to$them,$thus$avoiding$unsound$ terminal$ends$of$the$branches$within$the$high$canopy$(Cant,$1987).$Adult$males,$twice$the$ body$size$of$females,$will$occasionally$travel$to$the$ground$rather$than$risk$bridging$ arboreal$gaps$(Cant,$1987).$The$specialized$behaviors$of$orangutans$coupled$with$ anatomical$adaptations$greatly$enhance$safety$and$stability$in$the$trees,$but$do$not$ eliminate$the$risk$of$falling$or$the$repercussions$of$serious$injury.$$$

Chimpanzees$are$caught$in$an$evolutionary$and$energetic$tradeoff$(Pontzer$and$

Wrangham,$2004).$The$competing$demands$of$terrestrial$and$arboreal$locomotion$have$ resulted$in$behavioral$and$anatomical$adaptations$that$are$not$as$finitely$focused$on$ suspension.$They$have$grasping$hands$and$feet$that$are$helpful$when$anchoring$to$arboreal$ substrates$and$moderately$curved$digits$that$help$enhance$branch$contact,$but$these$ adaptations$characterize$all$suspensory$apes$and$are$less$extreme$in$chimpanzees$than$in$

!14! ! orangutans$or$gibbons$(Midlo,$1934;$Hunt,$1992).$Chimpanzees$are$moderately$adapted$to$ climbing$and$suspensory$behavior,$but$their$propensity$to$move$quadrupedally$through$ arboreal$substrates$and$to$spend$considerable$time$locomoting$terrestrially$probably$ confers$some$measure$of$safety$to$chimpanzee$locomotion.$Yet,$because$they$are$less$ specialized$with$respect$to$suspensory$locomotion,$compared$to$orangutans$and$gibbons,$ chimpanzees$may$have$a$greater$risk$of$falling$when$they$do$travel$within$the$trees.$$$

Finally,$when$quadrupedal$baboons$travel$in$trees,$they$do$so$at$heights$no$greater$ than$a$few$meters$(Jarrell,$2011).$Thus,$baboons$are$less$likely$than$the$suspensory$apes$to$ incur$fractures$to$their$long$bones.$$$

1.3 Hypotheses*

Although$all$apes$primarily$use$their$foreZlimbs$to$swing$through$the$forest$canopy,$ variation$in$body$size,$nuanced$differences$in$locomotor$strategy,$and$a$range$of$ecological$ factors$(e.g.,$substrate$availability)$likely$make$the$risk$of$injury$from$falls$highly$variable$ across$suspensory$groups.$Until$recently,$physiological$and$anatomical$evidence$of$injury$ and$recovery$had$not$been$systematically$investigated$with$respect$to$locomotor$modes$ among$primates.$However,$Heather$Jerrell’s$recent$study$of$22$arboreal$primate$taxa$ suggests$that$suspensory$primates$incur$a$greater$number$of$fractures$than$quadrupedal$ primates$but,$body$size$is$a$significant$factor$in$fracture$incidence$and$has$a$greater$effect$ on$fracture$frequency$than$locomotor$mode$(Jarrell,$2011).$Nonetheless,$the$relationship$ between$bone$fracture$and$the$varied$modes$of$suspensory$behavior$within$apes$that$ characterize$gibbons,$orangutans$and$chimpanzees$remains$unexplored.$In$this$thesis,$I$ investigate$parameters$of$suspensory$primate$locomotion$to$further$understand$why$

!15! ! fractures$occur$more$often$among$suspensory$primates$and$how$their$locomotor$patterns,$ ecological$preferences,$and$body$sizes$affect$fractures$and$remodeling.$To$this$end,$I$tested$ four$related$major$hypotheses.$$

1.3.1 Locomotion*Hypotheses**

Because$locomotor$strategies$among$gibbons,$orangutans,$chimpanzees$

(suspensory$apes)$and$baboons$(terrestrial,$quadrupedal$monkeys)$differ,$rate$and$ severity$of$fracture$will$also$differ,$where$severity$is$assessed$through$the$levels$of$ deformity$and$remodeling$apparent$in$the$fractured$elements.$$$

1.3.1.a Fracture*Occurrence*and*Severity*of*Fractures*will*be*Lowest*in*

Quadrupedal*Primates*

The$three$suspensory$apes$will$show$a$greater$percentage$of$limb$bone$fractures$ than$the$quadrupedal$baboons.*

1.3.1.b Fracture*Occurrence*and*Severity*will*be*Related*to*Suspensory*Behavior*

Among$suspensory$apes,$the$brachiating$gibbons$will$have$the$highest$occurrence$of$ fracture$as$well$as$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,$the$terrestrial$quadrupedal$baboons$will$have$the$lowest$fracture$frequency$and$ severity.$$

1.3.2 Ecological*Hypotheses***

Ecological$factors,$especially$body$size,$substrate$height,$and$substrate$stability,$will$ correlate$with$fracture$rate$and$severity.$

1.3.2.a Fracture*Occurrence*and*Severity*will*Increase*with*Increasing*Body*Size*

!16! ! Fractures$will$be$more$prevalent$in$species$with$larger$bodies.$

1.3.2.b Fracture*Occurrence*and*Severity*will*be*Highest*for*Animals*Foraging*

(Traveling*and*Feeding)*Higher*in*the*Canopy*

Fracture$rate$and$severity$will$be$greatest$in$species$that$travel$on$substrates$higher$ in$the$forest$canopy.$

1.4 Explanation*of*Predictions*

Falling$is$a$significant$hazard$of$brachiation$(Usherwood$et$al,$2003).$According$to$

Schultz$(1944),$the$higher$peak$forces$inherent$in$doubleZpendulum$brachiation$may$ increase$the$likelihood$of$branch$failure.$Also,$the$consequences$of$small$error,$such$as$ undershooting$the$intended$substrate$during$richochetal$brachiation,$can$result$in$a$ complete$miss,$a$subsequent$fall,$and$the$likelihood$of$injury$or$death$(Usherwood$and$

Bertram,$2003).$Given$the$doubleZpendulum$model,$I$predicted$that$true$brachiators$

(gibbons),$would$have$a$higher$rate$of$fracture$and$fracture$severity$than$the$other$apes$ due$to$their$habit$of$moving$rapidly$through$high$canopy.$$Navigating$this$part$of$the$forest$ may$require$travel$on$less$reliable$and$more$compliant$substrates$(Thorpe$et$al,$2008).$If$ the$inconsistent$substrate$quality$and$highZspeed$“flight$phase”$locomotion$of$gibbons$ leads$to$more$falls,$then$this$should$be$evident$among$osteological$specimens$available$for$ study.$$$$$

Because$orangutans$move$slowly$and$cautiously,$I$predicted$that$orangutans,$would$ have$a$high$rate$of$fracture/severity$as$well,$but$fracture$occurrence$will$be$lower$than$that$ of$brachiators.$Finally,$I$predicted$that$chimpanzees,$because$they$are$less$arboreal$than$ gibbons$and$orangutans,$are$less$prone$to$falling$from$heights$and,$therefore,$will$have$the$

!17! ! lowest$fracture$frequency$as$well$as$the$least$severe$fractures$among$apes$(Rodman,$1984,$

Hunt,$1992).$

To$test$these$hypotheses,$I$looked$for$correlations$between$locomotor$style$and$ fracture$frequency$and$severity,$between$preferred$height$of$substrates$and$fracture$ frequency$and$severity,$and$between$body$size$and$fracture$frequency$and$severity.$

1.5 Biomechanics*of*Locomotor*Support*in*Suspensory*Primates*

In$biomechanics,$kinetic$studies$examine$the$exchange$of$force$between$biological$ systems$and$the$environment$(Radasch,$1999;$Jarrell,$2011).$Force$is$equal$to$mass$ multiplied$by$acceleration.$When$force$is$applied$to$bone$it$is$referred$to$as$loading$or$ stress$(force$over$area).$A$bone’s$response$to$stress$and$deformation$is$dependent$on$the$ structural$and$material$compositions$of$the$bone$and$the$direction$and$magnitude$of$force$ applied.$

1.5.1 Bone*Composition*

The$vertebrate$skeleton$is$comprised$of$two$distinct$bone$tissues$that$differ$with$ respect$to$density$and$organization.$Cortical$or$compact$bone$consists$of$dense,$tightly$ packed$osteons,$units$of$mineralized$bone$in$which$living$bone$cells$are$essentially$trapped$ and$serviced$by$Haversion$capillaries$(Zoetis$et$al.,$2003,$Ralston,$2009).$The$outer$layer$of$ long$bones$and$the$entirety$of$bone$shafts$(diaphyses)$are$made$of$cortical$bone$(Ralston,$

2009).$Cortical$bone$mass$is$a$major$factor$in$body$mass,$and,$in$humans,$compact$bone$ accounts$for$80%$of$total$body$mass$(Zoetis$et$al.,$2003,$Ralston,$2009).$Unlike$dense$ cortical$bone,$trabecular$or$cancellous$bone$is$organized$into$a$latticeZlike$network$of$bony$ spicules$surrounded$by$fluidZfilled$spaces$that$house$bone$marrow,$essentially$bathing$the$

!18! ! bone$tissue$in$nutrients$(Langdon,$2005).$$The$epiphyses$(end$plates)$and$metaphyses$

(intervening$bone$between$endplate$and$diaphyseal$shaft)$contain$trabecular$tissue.$

Cortical$bone$provides$the$main$structure$of$each$skeletal$element,$while$trabecular$bone$ provides$increased$resistance$to$directional$force.$Both$cortical$and$trabecular$bone$are$ made$of$the$same$proteins$and$minerals$and$are$deposited$by$the$same$processes$$(Ralston,$

2009).$These$are$described$below.$$

Three$cell$types$build$and$maintain$ bone:$osteoblasts,$osteoclasts,$and$ osteocytes$(KleinZNulend$et$al.,$2003).$

Osteoblasts$create$bone$by$laying$down$a$ calciumZphosphate$matrix.$Osteoclasts$in$ turn$resorb$bone$by$secreting$an$acid$that$ demineralizes$the$bone$and$employing$an$ enzyme$that$dissolves$the$original$bone$ matrix$(Teitelbaum,$2000).$Osteocytes$are$ Figure!1.7:!Responses!to!bone!loading.!(Pearson!and! Lieberman!et!al.,!2004)! mature$osteoblasts$enveloped,$and$thus$ entrapped,$by$hardened$bone$matrix.$They$lie$within$hollow$lacunae$inside$osteonal$ matrices$and$connect$and$communicate$with$each$other$via$filopodial$extensions$that$ course$through$small$channels$called$canaliculi$(KleinZNulend$et$al.,$2003).$Osteocytes$ detect$mechanical$stimuli,$such$as$internal$muscular$force$and$external$impact$force$

(Currey,$1984;$KleinZNulend,$2003;$Safadi$and$Khurana,$2010).$It$is$probable$that$ osteocytes$use$mechanical$stimuli$to$trigger$events$such$as$remodeling$by$releasing$

!19! ! chemical$signals$to$osteoblasts$and$osteoclasts$(Mullender$and$Huiskes,$1995;$KleinZ

Nulend,$2003;$Safadi$and$Khurana,$2010)(Figure$1.7).$$

1.5.2 Modes*of*Loading*

$Body$movement,$for$example$locomotion,$subjects$the$skeleton$to$five$modes$of$ mechanical$loading:$compression,$tension,$shear,$torsion,$and$bending$(Figure$1.8).$Loading$ may$be$linear$or$angular.$Tension,$compression,$and$shear$are$linear$modes$of$loading,$ while$torsion$and$bending$are$angular$modes$(Swartz,$1993).$Bones$respond$according$to$ the$mode,$direction,$and$magnitude$of$the$applied$load$(Burstein$et$al.,$1972).$

Figure!1.8:!Diagram!of!loading!modes!acting!upon!a!long!bone!(in!this! case!the!humerus!of!a!feline)(Swartz,!2009).!The!dashed!line! represents!the!neutral!axis!running!through!the!center!of!the! diaphysis.!! $

Tensile$forces$produce$elongation$deformation.$In$contrast,$compressive$forces$ produce$shortening$deformation.$When$subjected$to$bending,$both$tension$and$ compression$affect$the$bone$but$at$different$locations.$$Compression$shortens$the$concave$

!20! ! side$around$the$neutral$axis$of$the$bone,$while$tension$lengthens$the$convex$side$around$ the$neutral$axis,$with$the$greatest$stress$applied$to$the$plane$of$bending$(Swartz,$1993).$$

For$example,$bending$along$a$long$bone$produces$a$slight$gradient$of$stress$extending$from$ maximum$compression$(shortening)$on$one$side$of$the$neutral$axis$to$maximum$tension$

(lengthening)$on$the$other$side$of$the$neutral$axis.$Midway$between$the$two$maxima$lies$ the$neutral$zone$of$the$crossZsection$(Pearson$and$Lieberman,$2004).$$At$this$neutral$plane$ stress$is$absent.$Stress$generated$in$bending$depends$not$only$on$the$magnitude$of$bending$ force$but$also$on$the$bending$moment.$Shear$loading$occurs$when$opposing$forces$distort$a$ structure$as$though$layers$of$the$material$are$sliding$in$opposite$direction$of$each$other.$

Twisting$or$torsion$involves$a$rotational$moment$applied$about$the$long$axis$of$a$bone$and$ causes$shearing$forces$as$well,$but$between$concentric$layers.$During$movement,$as$in$ locomotor$travel,$bones$often$concurrently$experience$more$than$one$type$of$loading$ mode.$Bending$is$the$most$common$complex$loading$mode$for$bones$during$locomotion$

(Swartz,$1993)$and$puts$the$bones$under$compression$and$tension$(Mercer,$2006).$

Long$bones$are$essentially$hollow$tubes$of$layered$cortical$bone.$Unlike$solid$rods,$ these$tubes$provide$greater$resistance$to$bending.$The$majority$of$bone’s$mass$is$ distributed$in$the$cortical$bone$walls$of$the$tube$farthest$from$the$neutral$axis,$where$the$ moment$of$inertial$resistance$is$high,$thereby$increasing$resistance$to$load$failure.$

Excessive$stress$and$strain$under$any$of$the$modes$of$loading$will$lead$to$bone$failure$in$ the$form$of$a$fracture.$$$

1.5.3 Stress*and*Strain*

!21! ! Bone$has$a$predictable$reaction$to$loading$that$can$be$represented$by$a$stressZstrain$ curve$(Figure$1.9).$Tension$and$compression$are$the$most$frequent$loading$modes$incurred$ by$animals$in$motion.$When$a$force$is$applied$to$bone$tissue$during$loading,$there$is$a$ moderate$amount$of$elastic$response$(Burstein$et$al.,$1972).$Bone$absorbs$force$and$ deforms$slightly$(represented$by$the$area$under$the$“elastic$region”).$If$stress$remains$in$ the$elastic$region,$the$removal$of$the$stress$will$allow$the$bone$to$return$to$its$original$ shape.$Increases$in$force$will$cause$the$bone$to$deform$or$break.$If$the$stress$remains$in$the$ plastic$region$of$the$stressZstrain$curve,$the$bone$will$deform,$but$when$the$stress$is$ removed,$it$will$be$unable$to$return$to$its$exact$original$shape.$It$will$be$slightly$altered$

(Burstein$et$al.,$1972).$Fractures$are$the$result$of$loads$that$exceed$the$bone’s$elastic$and$ plastic$regions,$reaching$the$fracture$point,$and$causing$failure$(Burstein$et$al.,$1972;$

Swartz,$1993;$Mercer$et$al.,$2005).$

!22! ! Figure!1.9:!The!Stress3strain!Curve!for!Bone!in!Compression!(left)!is!graphical!representation!of!compression!applied!to!bone!causing!deformation!and!eventual!failure! (modified!from!Swartz,!1993).!The!Stress3strain!Curve!for!Bone!in!Tension!(right)!is!a!graphical!representation!of!tension!applied!to!bone!causing!deformation!and! eventual!failure!(modified!from!Mercer!et!al.,!2005).!The!graphs!appear!very!similar!because!the!process!of!deformation!due!to!tension!and!compression!are!identical.! The!major!difference!is!the!slope!of!the!line!to!the!point!of!yielding.!The!steeper!slope!represented!in!the!Compression!Curve!(left)!shows!that!more!force!is!required! to!reach!the!yielding!point!in!compression!than!in!tension.!! !

!23! ! Falls,&particularly&those&from&an&extreme&height,&generate&high&magnitude&forces.&

High&impact&loading&combined&with&large&body&mass&suggest&that&suspensory&apes&are& probably&exposed&to&greater&injury&risk,&including&bone&fracture,&than&are&smaller&bodied& and&terrestrial&primates.&Upon&impact&with&the&ground&or&another&flat&substrate,& compression&is&likely&to&be&the&type&of&force&absorbed&by&the&bone.&This&is&especially&true&if& an&individual&sustains&a&vertical&fall&feet&first.&However,&when&an&individual&falls,&it&is&likely& to&try&to&reach&out&and&attempt&to&catch&hold&of&nearby&supports.&If&a&foreAlimb&or&hindAlimb& strikes&a&branch&perpendicularly,&then&this&limb&will&likely&absorb&a&large&bending&or& shearing&force&through&a&small&point&of&impact,&concentrating&force&over&a&small&area& resulting&in&high&bone&stress.&Because&mass&and&acceleration&determine&force,&highAspeed& locomotion,&like&that&of&gibbons&during&richochetal&brachiation,&generates&high&force&that& must&be&absorbed&during&the&impact&collision&of&a&fall.&Larger&body&size&will&also&increase& the&impact&force&incurred&during&falls.&A&higher&magnitude&of&force&absorbed&during&a&fall& increases&the&likelihood&of&reaching&the&fracture&point&of&bone&causing&failure.&Differential& locomotor&strategy,&anatomy,&and&ecology&among&primates&affect&the&level&of&fracture&risk&&& during&daily&travel&and&feeding.&!

1.6 Bone!Repair&

& According&to&Wolff’s&law&(Wolff,&1986),&changes&in&bone&form&or&function&cause& corresponding&changes&in&the&internal&and&external&architecture&of&bone&(Pearson&and&

Lieberman,&2004).&&In&principle,&Wolff’s&law&implies&that&when&a&bone&is&fractured,& osteocytes&respond&to&this&mechanical&stimuli&and&release&chemical&signals&that&stimulate& the&reparation&of&the&failed&element&through&a&remodeling&process&(Currey,&1984;&KleinA

Nulend&et&al.,&2003;&Safadi&and&Khurana,&2010).&During&fracture&remodeling,&osteoclasts&

!24! ! resorb&damaged&bone&and& osteoblasts&lay&down&a&matrix& of&woven&bone&as&a&scaffold&or& temporary&patching&of&the& affected&area&(Ralston,&2009)&

(Figure&1.10).&Using&this& scaffold,&or&callous,&osteoclasts& Figure!1.10:!The!Bone!Remodeling!Cycle!(Ralston,!2009)! and&osteoblasts&resorb&and&deposit&bone,&respectively,&in&order&to&return&the&bone&to&its& natural&shape&and&restore&any&compromised&function.&

&Ideally,&a&fractured&bone&will&return&to&its&original&shape&when&remodeling&is& complete,&thus&restoring&the&original&muscle&support,&mechanical&advantage,&and& functionality&of&the&preAaffected&element.&Unfortunately,&this&is¬&always&the&case,&as& sometimes&the&fracture&is&too&severe&to&heal&properly.&Also,&skeletal&maturation&has&an& adverse&effect&on&remodeling,&and&juveniles,&at&least&among&humans,&are&likely&to&heal&more& quickly&and&with&fewer&lasting&effects&(e.g.&decreased&muscle&mechanical&advantage&and& decreased&functionality)&than&adults&(Hendrix,&2002).&In&practice,&this&means&that&juveniles& who&suffer&fractures&are&more&likely&to&have&more&successful&restoration&of&functionality& than&adults.&&

There&is&no&information&on&the&amount&of&time&it&takes&for&bone&to&remodel&in&wild& apes.&However,&the&forensic&literature&for&humans&gives&some&insight&into&the&process.&The& remodeling&period&is&temporally&variable,&and&largely&depends&on&the&severity&of&the&injury& and&the&age&and&health&of&the&individual&(Ortner&and&Putschar,&1981;&Burns,&1999).&

!25! ! Regardless&of&the&time&required,&the&sixAstep&sequence&of&bone&repair&is&consistent&among& species&(Burns,&1999).&First,&a&blood&clot&forms&within&hours&of&the&initial&injury,&flooding& the&area&with&cells&to&begin&the&remodeling&process&and&fight&infection.&Second,&within&a&few& days,&networks&of&vessels&bridge&the&ends&of&the&broken&bone&to&provide&a&pathway&for& nutrients&and&cells&essential&for&the&remodeling&process.&In&the&third&step,&osteogenic&cells& are&infused&into&the&affected&area&through&the&vessel&network.&They&differentiate&into&the& osteoclasts&and&osteoblasts&needed&to&build&bone&(Ralston,&2009).&This&continues& throughout&the&healing&process.&During&step&four,&osteoblasts&build&a&matrix&called&the&soft& callous&onto&which&minerals&can&be&deposited&to&bolster&the&damaged&bone.&This&soft& callous&may&take&weeks&to&assemble.&&

During&step&five,&a&bony&callous&is&formed&through&the&continued&deposition&of& minerals&within&the&soft&callous.&This&process&takes&1A2&months.&The&bony&callous&helps&to& stabilize&the&bone§ions&for&remodeling.&In&the&sixth&and&final&step,&osteoclasts&and& osteoblasts&remodel&the&callous&into&lamellar&bone.&The&bony&callous&becomes&more&smooth& and&dense&but&can&often&remain&visible&in&spite&of&continued&remodeling.&It&can&take&many& years&for&a&bone&to&fully&remodel&after&fracture.&Numerous&factors&may&slow&bone&repair& including&advanced&age,&poor&nutrition,&and&disease.&Infection&may&fully&disrupt&the& remodeling&process&and&lead&to&persistent&malformation&for&the&remainder&of&an& individual’s&life&(Burns,&1999).&&During&the&repair&period,&the&mechanical&function&of&bone&is& reduced&(Ortner&and&Putschar,&1981)&leaving&the&animal&vulnerable&by&limiting&locomotion& and&feeding&behaviors,&as&well&as&increasing&energetic&costs.&&

!26! ! Given&the&suspensory&locomotor&patterns&of&apes&and&the&possible&risk&of&injury& associated&with&them,&I&expected&that&fractures&of&the&limbs&occur&with&relative&frequency.&I& also&anticipated&that&an&injured&animal&might&rely&more&often&on&unaffected&limbs&with& greater&loading&magnitudes&to&compensate&for&the&disruption&of&function&to&a&fractured& limb.&If&this&is&the&case,&then&nonAfractured&limbs&may&also&become&modified&through&new& loading®imes.&

CHAPTER(2:(Materials(and(Methods&

2.1 Sample!

Skeletal&collections&of&three&genera&of&suspensory&apes,&Hylobates,&Pongo&and&Pan,& among&whom&locomotor&strategies&differ,&were&examined&in&order&to&identify&whether& varying&locomotor&repertoires&manifest&with&equal&or&differential&patterns&of&limb&injury.&

Although&Gorilla&exhibits&some&suspensory&behaviors,&it&is&the&most&terrestrial&of&the&extant& apes&and&has&been&excluded&from&this&study&due&to&its&low°ree&of&adult&arboreality.&The& genus&Papio,&a&terrestrial&quadruped,&was&also&studied&to&compare&suspensory&and& terrestrial&locomotor&modes.&Study&specimens&were&selected&based&on&the&availability&of& appropriate&sample&sizes&and&the&preservation&of&the&samples.&Inclusion&required&the& presence&of&the&14&elements&of&the&foreA&and&hindAlimb&(Table&2.1),&good&condition&of&the& bones&(complete,¬&broken&from&handling,&disarticulated&if&possible,&etc.),&and&absence&of& tendinous&and&cartilaginous&tissue.&Because&captivity&is&likely&to&affect&locomotor&behaviors& differently&than&a&natural&habitat,&and&captive&management&provides&medical&intervention& when&severe&fracture&injury&occurs,&only&wild&animals&were&examined&in&this&study.&&

&

&

!27! ! &&

The&extent&to&which&injury&may&bias&the&study&sample&is&uncertain.&Although&injured& animals&may&be&more&watchful&and&cautious&in&predation&avoidance&than&uninjured&animals&

(Schultz,&1944),&injury&may&nonetheless&increase&an&animal’s&likelihood&of&being&captured& or&shot&for&collection&if&the&injury&and&repair&phase&reduce&mobility&and&speed.&This&could& inflate&the&percentage&of&injured&individuals&within&a&skeletal&collection&with&respect&to&the& parent&population&(Randall,&1944).&Because&of&the&uncertainty&of&the&effects&of&injury&on& propensity&for&capture,&this&study&assumes&that&the&sample&is&representative&of&the&wild& population,&but&I&acknowledge&that&some&sample&biases&may&be&present.&&

One&hundred&and&fortyAone&specimens&representing&four&primate&genera&were& examine&and&analyzed.&The&sample&includes&gibbons&(Hylobates4spp.),&orangutans&(Pongo4 spp.),4chimpanzees&(Pan4troglodytes),4and&baboons&(Papio4cynocephalus)&obtained&from& three&skeletal&collections&(Table&2.2).&The&majority&of&the&animals&were&wild&shot&with&the&

!28! ! exception&of&some&of&the&baboons&at&the&University&of&Texas,&Austin.&These&individuals&were& wild&captured&and&then&euthanized.&&

2.2 &Visual!Assessment!of!Fracture!Severity!and!Bone!Deformation!

My&inventory&for&each&specimen&included&an&account&of&the&presence&or&absence&of& the&long&bones&of&the&foreAlimb&and&hindAlimb&(,&humeri,&radii,&ulnae,&femora,&tibiae,& and&fibulae)&as&well&as&any&record&of&age,&sex,&and&body&mass&found&within&collection& records.&!

& Paired&left&and&right&long&bones&were&assessed&for&evidence&of&fracture&based&on&the& methods&used&in¤t&forensic&contexts&as&outlined&by&Burns&(1999)&and&Byers&(2002).&

Photographs&were&taken&of&fractureAaffected&bones&from&the&ventral,&dorsal,&medial,&and& lateral&perspectives.&The&corresponding&unaffected&bone&was&also&photographed&from&the& ventral,&dorsal,&medial,&and&lateral&perspectives.&Bones&unaffected&by&fracture&were& recorded,&measured,&and&photographed&as&a&group&but&no&further&assessment&of&their& condition&was&recorded.&&

& A&digital&caliper&(Mitutoyo&500A171&needle&point&digital&caliper&accurate&to&the& nearest&0.01&mm)&was&used&to&take&measurements&of&limb&symmetry&from&the&long&bones.&A& total&of&six&measurements&were&taken&from&each&element&of&each&specimen&(Table&2.3).&The& maximum&length&of&each&bone&was&measured&using&an&osteometric&board&or&a&digital& caliper&depending&on&the&length&of&the&bone.&The&widest&points&of&the&proximal&and&distal& long&bone&ends&served&as&landmarks&to&determine&maximum&breadths.&Shaft&diameters& were&measured&at&25%,&50%,&and&75%&of&total&bone&length.&&

!29! ! &

& Where&evidence&of&a&fracture&injury&was&found,&the&fracture&and&associated&bony& response&were&examined&and&measured&as&follows.&The&proximalAdistal&length&of&the& fracture&site&was&measured&at&the&longest&point&of&the&fracture.&The&medialAlateral&length&of& the&fracture&site&was&measured&at&the&largest&point&of&the&fracture&site.&Any&spurs&or&other& superfluous&bony&structures&were&measured&in&length&and&height&of&projection&from&the& surface&of&the&bone.&These&measurements&were&needed&to&compare&fractured&and& remodeled®ions&of&the&injured&bone&to&the&corresponding&bone&on&the&unaffected&side.&

& Because&severe&displacement&fractures&may&reduce&otherwise&healthy&limb&length,& the&paired&unaffected&limb&bone&served&as&a&baseline&measure&of&bone&length&to&determine& the&amount&of&limb&shortening&from&injury&in&the&fractured&element.&&In&order&to&compare& limb&length&reduction&among&taxa&of&varying&body&size,&the&percent&difference&between& paired&elements&when&one&was&fractured&and&the&other&intact.&&

& Since&body&mass&was¬&known&for&all&individuals,&a&proxy&for&body&mass&was& obtained&using&a&specimenAspecific&geometric&mean&calculated&from&a&series&of& measurements&taken&on&each&individual&within&a&genus&(see&Section&2.3).&

!30! ! Multiple&specimens&presented&periAmortem&and/or&postAmortem&fractures.&Because& these&injuries&were&sustained&near&the&time&of&death,&they&may&be&artifacts&of&specimen&field& collection&rather&than&the&result&of&natural&behaviors.&Thus,&specimens&with&periA&or&postA mortem&fracturing&were&omitted&from&the&study.&Fractures&considered&periAmortem&or& postAmortem&were&those&showing&no&signs&of&remodeling.&Most&of&these&fractures&were&also& directly&associated&with&bullet&trauma.&Pathologies&that&might&be&related&to&joint&disease& served&as&additional&omission&criteria,&and&specimens&exhibiting&pathologies&were&excluded& based&on&comparisons&to&human&pathology&described&in&Burns&(1999)&and&Byers&(2002).&&&

2.3 Statistical!Analyses!

With&respect&to&the&prevalence&of&fractures,&I&generated&three&indices.&&First,&to& determine&the&fracture&frequency&of&injured&individuals&within&the&sample&pool&of&each& genus,&I&calculated&the&Specimen&Fracture&Frequency&(SFF)&variable.&To&calculate&the&SFF& variable,&the&number&of&individuals&with&at&least&one&fracture&was÷d&by&the&total& number&of&individuals&in&the&genus.&Second,&I&calculated&a&frequency&index&of&fractures& among&sampled&bones,&the&Element&Fracture&Frequency&(EFF).&The&EFF&was&calculated&as& the&number&of&fractured&elements&(bones)÷d&by&the&total&number&of&elements& examined.&Finally,&a&Cross&%&variable,&the&total&number&of&fractured&elements÷d&by& the&total&number&of&individuals&in&the&genus,&was&calculated.&The&Cross&%&was&calculated&to& account&for&individuals&having&more&than&one&fracture,&and&the&fact&that&some&specimens& were&incomplete&(therefore&the&element&number&may&be&different&than&the&expected&14& elements&per&specimen).&

!31! ! Deformation&and&remodeling&were&assessed&on&a&Severity&Scale&(1A5)&using¤t& forensic&methodology&outlined&by&Burns&(1999)&and&Byers&(2002).&The&severity&of& deformation&scale&is&based&on&deformity&types&described&by&Ortner&and&Putschar&(1981)&

(Table&2.4).&The&Remodeling&Scale&is&based&on&the&stages&of&bone&remodeling&listed&by&

Burns&(1999)(Table&2.5).

!32! ! Table&2.4:&Deformity&Scale&Rubric& & & Numerical* Observations*associated* Example* Example*Description* Value* with*levels*of*deformation.* No&evidence&of&fracture.&The& 1& bone&is&free&from&defect&and& N/A& N/A& appears&completely&intact.& Fracture&has¬&significantly& altered&the&shape&of&the&bone.& Papio&femur&exhibiting&small&callous& 2& A&small&callous&or&evidence&of& and&evidence&of&resorption.&& continued&bone&growth&may& & be&observed.& The&fracture&has&altered&the& shape&of&the&bone.&A&callous& may&be&observed.&A&slight& Pongo&humerus&exhibiting&a&slight& 3& change&in&the&angle&or&length& change&in&angle&and&length&of&the&bone& of&he&bone&may&be&observed.& & with&a&well&healed&callous.&& No&to&very&little&sign&of& infection.& The&fracture&has&altered&the& shape&of&the&bone,&the&bone& has&a&large&callous&with& Papio&femur&exhibiting&bone&spurs,&and& 4& evidence&of&infection.&The& a&change&in&the&angle&of&the&bone.& length&and/or&angle&of&the& & healed&bone&is&abnormal.& Small&spurs.& The&fracture&cannot&unite.& Large&callous&with&evidence&of& significant&infection.& Pongo&humerus&exhibiting&a&large& 5& Considerable&overlapping& callous&and&significant&overlapping.& bone&growth.&Large&spurs.& & Joint&fusion.&

!33! ! Table&2.5:&Remodeling&Scale&Rubric& & Numerical* Observations*associated*with* Example* Example*Description* Value* levels*of*healing.**

Bone&is&remodeled.&The&bone&may& & Pongo&humerus&showing& be&deformed,&but&shows&little&or& deformation,&but&a&smooth&remodel& 1& no&signs&of&active&architecture& with&little&evidence&of&continued& remodeling.& & remodeling.&& Bone&is&mostly&remodeled.&May&be& some&evidence&of&infection&or& Papio&femur&showing&bone&spurs& 2& resorption.&Bone&is&fully&fused&or& with&evidence&of&resorption.& separated.& & The&callous&is&fully&formed.&May& show&signs&of&infection.&The&bone& Pongo&humerus&showing&a&callous& 3& is&becoming&fused,&or&the&unused& & with&signs&of&infection.& bones&are&remodeling&over&ends.& Fracture&shows&evidence&of& resorption.&The&beginnings&of&a& bone&callous&are&forming.&The& Pongo&humerus&showing&a&callous& callous&may&connect&the&bones& 4& with&significant&overlap&and&signs&of& but&be&incomplete,&or&the&callous& infection.& may¬&have&connected&the& & fractured&area.&Infection&may&be& present.& Fracture&shows&no&signs&of& remodeling.&Ragged&edges.&No& Papio&femur&showing&a&complete& resorption&or&remodeling.& 5& disunion&between&the&femoral&head& Alternatively,&remodeling&has& & and&the&rest&of&the&bone.&& progressed&to&form&a&completely& alternate&bone&shape.&

!34! ! ! ! Fracture!frequencies!were!analyzed!statistically!based!on!morphological!data!

collected!directly!from!the!four!genera!as!well!as!behavioral!data!acquired!from!the!

literature.!All!statistical!tests!were!performed!using!R!statistical!software!(The!R!

Foundation!for!Statistical!Computing)!at!the!University!of!Cincinnati.!!

Many!of!the!specimens!in!the!osteological!collections!lack!recorded!body!weight.!I!

was!able!to!account!for!this!by!using!the!geometric!mean!(Mosimann,!1970;!Darroch!and!

Mosimann,!1985),!which!is!a!scaleOfree!numeric!marker!derived!from!linear!measurements!

taken!from!the!long!bones!of!each!specimen!(Whitcome,!2006).!In!this!sense,!the!geometric!

mean!variates!provide!a!unique!measure!of!overall!body!size!for!each!individual.!The!

G n formula! = χ1,χ2,χ3,⋅⋅⋅ χn was!used!to!find!the!geometric!mean!of!each!specimen!within!

each!genus,!where χ!represents!an!individual!linear!measurement.!The!calculated!

€geometric! mean!was!then!log!transformed!(log10)!to!account!for!the!nonOnormal!

distribution!of!body!sizes.!€ !

As!a!proxy!for!body!size,!the!log!of!the!geometric!mean!provides!a!fairly!accurate!

point!of!comparison!for!individual!body!size!in!humans!(Whitcome,!2006).!When!the!log!of!

the!recorded!body!weight!is!regressed!on!the!log!of!the!geometric!mean!for!Papio,!Pan,!and!

Pongo,!the!resulting!regression!lines!have!slopes!that!approach!isometry!(expected!

regression!slope!of!0.33)(Figure!2.1).!Therefore,!it!appears!that!the!log!of!the!geometric!

mean!provides!a!fairly!accurate!point!of!comparison!for!individual!body!size!in!Papio,!Pan,!

and!Pongo!(Figure!2.1).!Hylobates!lacked!sufficient!number!of!recorded!body!weights!to!

compare!to!the!geometric!means!calculated.!However,!when!all!genera!are!plotted!together!

the!relationships!between!geometric!mean!and!body!size!persists!(Figure!2.2).!Based!on!

!35! ! these!results,!log!geometric!mean!was!used!to!compare!Hylobates,!Papio,!Pan,!and!Pongo! with!a!good!degree!of!certainty.!

In!order!to!compare!geometric!means!among!genera!I!standardized!the!log!of!the!

logG − µ geometric!mean!for!each!genus!using!the!formula! σ !where!μ!is!the!mean!and!σ!is! the!standard!deviation!of!the!logged!geometric!mean!for!all!genera.! €

!36! ! Log Body Weight and Log of the Geometric Mean Log Body Weight and Log of the Geometric Mean Pan Papio

y=0.34634*x + 0.97551 y=0.31509*x + 0.88339 1.75 p=0.0372 1.45 p=5.55e-13 ! r=0.963 r=0.937726 Hylobates Hylobates Pan Pan Papio Papio Pongo Pongo

! 1.40 1.70 1.35 1.65 Log Mean of the Geometric Log of Mean the Geometric Log 1.30 1.60

1.85 1.90 1.95 2.00 1.3 1.4 1.5 1.6 1.7 1.8

Log of Recorded Body Weight Log of Recorded Body Weight

Log Body Weight and Log of the Geometric Mean Pongo

y=0.25765*x + 0.92107 1.55 p=1.69e-06 r=0.7988481 Hylobates Pan Papio Pongo 1.50

Figure!2.1:!The!relationship!between!the!log!of!the!recorded!body!

1.45 weight!from!collection!records!and!the!log!of!the!geometric!mean! for!Papio!(top!left),!Pan'(top!right),!and!Pongo!(bottom!left).!All!

Log Mean of the Geometric Log three!show!that!there!is!a!direct!correlation!between!the!log!of!the! geometric!mean!and!body!weight.!! 1.40

1.8 1.9 2.0 2.1 2.2 2.3

Log of Recorded Body Weight !37! ! Log Body Weight and Log of the Geometric Mean

y=0.20264*x + 1.06266 p=1.38e-08 r=0.668 1.7 Hylobates Pan Papio Pongo 1.6 1.5 Log of Mean the Geometric Log 1.4 1.3

1.0 1.2 1.4 1.6 1.8 2.0 2.2

Log of Recorded Body Weight

Figure!2.2:!The!relationship!between!recorded!body!weight!from! collection!records!and!the!standardized!log!of!the!geometric!mean!for! Papio,!Pan,!Pongo,)and!Hylobates.!It!shows!that!there!is!a!direct! correlation!between!the!standardized!log!of!the!geometric!mean!and! body!weight.!! It#is,#unfortunately,#not#! possible#to#assess#the#canopy#height#at#which#each#individual# included#in#this#study#traveled.#Therefore,#canopy#heights#for#the#following#analyses#were# based#on#compiled#estimates#from#the#literature#for#each#genus#(Rose,#1977;#Fleagle,#1980;#

Gittins,#1983;#Hunt,#1991;#Hunt,#1992;#Islam#and#Feeroz,#1992;#Cannon#and#Leighton,#1994;#

Thorpe#and#Crompton,#2006;#Cheyne,#2010;#Jarrell,#2011)#

Several#generalized#linear#regression#models#(glm)#were#used#to#explore#the# relationships#between#the#dependent#variable#fracture,#and#the#independent#variables# body#size,#locomotor#strategy#(quadrupedalism,#quadrumanus#shuffling,#dual#terrestrial#

!38! ! and#suspensory#strategy,#high#speed#brachiation),#and#canopy#height#(<5m,#<11m,#10T20m,#

>25m).#The#level#of#significance#for#each#test#was#set#at#5%#(α#<#0.05).#For#models#with# statistically#significant#findings#the#correlation#coefficient#is#reported.#Generalized#linear# regression#models#were#used,#as#opposed#to#linear#regression#models,#because#they#are# more#suitable#for#presenceTabsence#data.#A#glm#can#accommodate#response#variables#with# distributions#that#are#nonTnormal#(Zuur,#et#al.,#2007).#

• A#glm#regressing#fractures#on#locomotor#modes#used#the#formula:#

glm(formula=Frac~Genus,#family#=#binomial),#where#genus#is#a#proxy#for#locomotor#

mode.#In#this#model,#the#quadruped#genus#Papio#was#the#control#group.##

• A#glm#regression#of#fractures#on#suspensory#locomotor#modes#used#the#formula:##

glm(formula=Fracture#~#Genus,#family#=#binomial),#where#genus#was#a#proxy#for#

locomotor#mode.#In#this#model,#the#genus#Pan'was#s#the#control#group.##

• A#glm#was#performed#that#regressed#fractures#on#body#size#using#the#formula#

glm(formula=Fracture#~#Standard#Log#Geometric#Mean,#family#=#binomial),#where#

standard#log#geometric#mean#represents#individual#body#weight.##

• A#glm#was#performed#that#regressed#fracture#frequency#on#preferred#canopy#height#

using#the#formula#glm(formula=Fracture#~#CH.Genus,#family#=#binomial).#In#this#

model,#the#genus#Papio'is#the#control#group.###

Several#linear#regression#models#(lm)#were#used#to#explore#the#relationships# between#the#dependent#variables#fracture#deformation#and#remodeling#and#the# independent#variables#body#size,#locomotor#strategy,#and#canopy#height.#The#level#of# significance#was#set#at#5%#(α#<#0.05).#A#linear#regression#model#was#performed#that#

!39! ! regressed#fracture#deformation#on#suspensory#locomotor#modes#using#the#formula# lm(formula=Deformation#~#Genus),#where#genus#is#a#proxy#for#locomotor#mode#and#Papio# is#the#control#group.##

• A#linear#regression#model#was#performed#that#regressed#fracture#deformation#on#

body#size#using#the#formula#lm(formula=Deformation#~#Standard#Log#Geometric#

Mean),#where#standard#log#geometric#mean#represents#individual#body#weight.##

• A#linear#regression#model#was#performed#that#regressed#fracture#deformation#on#

suspensory#locomotor#modes#using#the#formula#lm(formula=Deformation#~#Canopy#

Height).#

• A#linear#regression#model#was#performed#that#regressed#fracture#remodeling#on#

suspensory#locomotor#modes#using#the#formula#lm(formula=Remodeling#~#Genus),#

where#genus#is#a#proxy#for#locomotor#mode.##

• A#linear#regression#model#was#performed#that#regressed#fracture#remodeling#on#

body#size#using#the#formula#lm(formula=Remodeling~#Standard#Log#Geometric#

Mean),#where#Standard#Log#Geometric#mean#represents#individual#body#weight.##

• A#linear#regression#model#was#performed#that#regressed#fracture#remodeling#on#

suspensory#locomotor#modes#using#the#formula#lm(formula=Remodeling#~#Canopy#

Height).##

CHAPTER(3:(Results(

3.1 Descriptive*Statistics*

3.1.1 Fracture*Frequencies*

!40! ! ## Fractures#were#identified#in#all#four#of#the#study#genera.##Of#the#141#individuals# examined#(pooled#sample),#47#fractured#elements#were#present#among#37#individuals#

(Table#3.1).#The#highest#frequency#of#fracture#was#found#in#Pongo#(41.2%)#when#comparing#

Cross#%#(total#number#of#fractured#elements#/#total#number#of#individuals).#Pan#had#the# fewest#(28.6%).#When#SFF#was#considered#(number#of#individuals#with#at#least#one# fracture#/#total#number#of#individuals),#again#Pongo'exhibited#the#highest#frequency#

(32.4%)#and#Pan#the#least#(22.9%).#Papio#(32.4%#Cross#%#and#29.4%#SFF)#unexpectedly# exhibited#more#fractures#than#both#Pan#and#Hylobates#(31.6%#Cross#%#and#21.1%#SFF),#but# fewer#than#Pongo.##

When#element#type#was#considered,#at#least#one#incidence#of#fracture#was#observed# for#each#of#the#seven#paired#elements#(Table#3.2).##Among#pooled#genera,#the##had# the#highest#fracture#frequency#at#4.9%.#The#humerus#and#femur#evinced#the#second#highest# fracture#frequencies#at#3.1%#for#both#elements.#Pongo'presented#a#marked#number#of#the# clavicle#breaks#(41.6%)#and#humerus#breaks#(62.5%).#However,#the#distribution#varied# among#genera.#Some#genera#did#not#exhibit#fractures#for#one#or#more#element#pairs.#

!41! ! !!!

!42! ! 3.1.2 Remodeling**

Nearly'90'%'of'the'observed'fractures'(38'out'of'47)'were'either'well'remodeled'or' remodeled'satisfactorily'(ranked'1'and'2,'respectively'on'the'Remodeling'Scale),'leaving'

10%'of'fractures'partially'remodeled'or'not'well'remodeled'(ranked'3'and'4,'respectively' on'the'Remodeling'Scale).'Only'two'fractures'(4%,'ranked'5'on'the'Remodeling'Scale)' showed'disunion'and'little'evidence'of'remodeling'(Table'3.2).''

3.1.3 Deformation*

'Over'a'third'of'the'fractures'(18'out'of'47)'ranked'4'and'5'on'the'Deformation'Scale,' showing'significant'evidence'of'an'alteration'of'the'shape'of'the'bone'(Figure'

3.1)(Figure3.3).'At'the'genus'level,'72%'of'observed'fractures'among'Pongo'had'(10'out'of'

14)'that'are'ranked'4'and'5'on'the'Deformation'Scale.'Papio'at'36%'and'Hylobates3at'33%'

(4'out'of'11,'and'4'out'of'12,'respectively)3had'considerably'fewer'fractures'with'severe' deformation,'while'Pan3altogether3lacked'any'fractures'that'would'be'ranked'in'the'severe' deformation'categories'altogether.'''

Figure!3.1:!A!fractured!left!humerus!of!an!orangutan!showing!considerable!deformation,! ranked!5!on!the!Deformation!Scale!and!3!on!the!Remodeling!Scale,!including!overlap!and!a! large!callous!on!the!distal!shaft.!!

!43! ! Fracture Remodeling by Genus Fracture Deformation by Genus T=20 T=18 T=6 T=1 T=2 T=0 T=13 T=16 T=8 T=10 20

15 3 7 1 15 6 2 5 Genus 10 Genus 2 12 Hylobates 12 Hylobates 10 Pan 10 Pan 10 Count Count 5 11 Papio 5 11 Papio 14 Pongo 6 14 Pongo 47 Specimens 47 Specimens 4 7 5 T=Total 5 T=Total 3 1 5 2 3 4 4 2 4 4 3 2 2 1 1 0 0

1 2 3 4 5 1 2 3 4 5 Remodeling Scale Deformation Scale

Figure!3.2:!Number!of!fractured!elements!in!each!remodeling!category!for! Figure!3.3:!Number!of!fractured!elements!in!each!deformation!category!for! each!genus.!The!numbers!within!the!columns!represent!the!number!of! each!genus.!The!numbers!within!the!columns!represent!the!number!of! fractures!represented!in!each!genus!for!the!remodeling!rating.!! fractures!represented!in!each!genus!for!the!deformation!rating.!! ! !

!

!44! ! 3.2 Locomotion(and(Ecology(

3.2.1 Comparison(Between(Quadrupedal(and(Suspensory(Locomotor(Modes(

Generalized*linear*regression*models*indicate*that*locomotor*modes*(quadrupedal* and*suspensory)*used*during*travel*do*not*have*a*significant*effect*on*the*fracture* frequency.*Relative*to*the*control*group*(Papio)*locomotor*modes*of*Hylobates*(p=0.77),*

Pan*(p=0.45),*and*Pongo*(p=0.67)*do*not*result*in*increased*fracture*frequency.*

3.2.2 Locomotor(Comparison(Among(Suspensory(Apes*

Although*Pongo*has*the*highest*SFF*(32.4%),*GLM*results*comparing*the*locomotor* modes*of*suspensory*apes*indicate*that*Hylobates*(p=0.69)*and*Pongo*(p=0.46)*do*not*have* significantly*higher*fracture*frequencies*than*Pan.*In*fact,*Hylobates3and*Pan3have*nearly* identical*SFF*percentages*(21.1%*and*22.9%,*respectively).**

3.2.3 Body(size*

As*predicted,*generalized*linear*regression*models*indicate*that*there*is*a*positive* relationship*between*body*size*and*limb*fracture*frequency*among*the*four*genera*Papio,3

Pan,3Pongo,3and3Hylobates.*As*the*standard*log*of*the*geometric*mean*increases,*the* likelihood*of*discovering*a*fracture*in*the*foreQlimb*and*hindQlimb*significantly*increases*

(p=0.02,*Correlation*Coefficient*=0.49)*(Figure*3.5).**

(

(

!45! ! Figure!3.5:!The!relationship!between!fracture!frequency!and! the!standardized!log!of!the!geometric!mean.!The!curve!shows! that!as!body!mass!increases!the!likelihood!of!fracture!also! increases.!! ! (

3.2.4 Canopy(height(

My*constructed*generalized*linear*regression*model*indicates*that*fracture* frequency*is*not*dependent*on*the*height*at*which*individuals*prefer*to*travel*The* preferred*canopy*height*of*Hylobates*(p=0.75),*Pan3(p=0.45),*Pongo*(p=0.67)*do*not* significantly*affect*fracture*frequencies*relative*to*Papio.*(

3.3 Deformation(and(Remodeling(

3.3.1 Deformation(and(Locomotor(Modes(

!46! ! As*predicted,*the*linear*regression*models*indicate*that*Pan’s*locomotor*strategies* result*in*a*significantly*low*rate*of*deformation*(p=0.03,*Correlation*Coefficient*=*Q0.96).*

The*locomotor*strategies*exhibited*by*Hylobates3(p=*0.78)*and*Pongo*(p=0.11)*showed*no* relationship*to*deformation.*

3.3.2 Deformation(and(Body(Size(

Although*fracture*frequency*is*significantly*related*to*body*size,*the*General*Linear*

Model*results*indicate*that*there*is*not*a*significant*relationship*between*body*size*and* deformation*among*the*four*test*groups*Papio,3Pan,3Pongo,3and,3Hylobates3(p=0.24)(Figure*

3.6).**

Body Size and Deformation

Hylobates 2.0 Pan Papio Pongo 1.5 1.0 0.5 0.0 -0.5 Standardized Log Geometric Mean Geometric Log Standardized -1.0 -1.5

1 2 3 4 5

Deformation Scale

Figure!3.6:!Distribution!of!the!degree!of!deformation!with! respect!to!body!size.! !

!47! ! 3.3.3 Deformation(and(Canopy(Height(

*The*lm*results*indicate*that*the*preferred*canopy*heights*for*Hylobates3(p=*0.78)* and*Pongo*(p=0.11)*are*not*related*to*deformation.*However,*Pan’s*preferred*canopy* height,*as*predicted,*correlates*with*a*decrease*in*the*degree*of*deformation*(p=0.03,*

Correlation*Coefficient*=*Q0.96).*

3.3.4 Remodeling(and(Locomotor(Modes(

The*lm*results*show*that*Pan’s*locomotor*strategies*are*significantly*related*to* greater*evidence*of*remodeling*(p=0.02,*Correlation*Coefficient*=*Q.097,).*However,*the* locomotor*strategies*exhibited*by*Hylobates3(p=*0.88)*and*Pongo*(p=0.07)*showed*no* relationship*to*remodeling.**

3.3.5 Remodeling(and(Body(Size(

Similar*to*the*models*for*deformation,*the*linear*regression*model*shows*that*there* is*not*a*significant*relationship*between*body*size*and*remodeling*among*the*test*groups*

Papio,3Pan,3Pongo,3and,3Hylobates3(p=0.21)(Figure*3.7).**

*

*

*

*

!48! ! Body Size and Remodeling 2.0 1.5 1.0 0.5 0.0 -0.5 Standardized Log Geometric Mean Geometric Log Standardized Hylobates Pan Papio

-1.0 Pongo -1.5

1 2 3 4 5

Remodeling Scale

Figure!3.7:!!Distribution!of!the!degree!of!remodeling!with! respect!to!body!size.! * !

3.3.6 Remodeling(and(Canopy(Height(

Pan’s*preferred*canopy*height*for*travel*is*correlated*to*increased*propensity*for* greater*remodeling*(p=0.02,*Correlation*Coefficient*=*Q0.97),*but*the*preferred*canopy* height*of*Hylobates3(p=*0.88)*and*Pongo*(p=0.07)*showed*no*relationship*to*remodeling.**

CHAPTER(4:(Discussion(

Analyses*of*skeletal*collections*yielded*three*statistically*significant*findings*in* support*of*my*hypotheses.*First,*there*is*a*positive*relationship*between*body*size*and* fracture*frequency*for*Hylobates,3Papio,3Pan,3and,3Pongo,3(p=0.02,*Correlation*Coefficient*=*Q

!49! ! 0.21).*As*size*increases*so*too*does*the*likelihood*of*foreQlimb*and*hindQlimb*fracture*

(Figure).*Thus,*individuals*of*larger*body*size*appear*to*be*more*vulnerable*to*risk*of* fracture*injury,*and*larger*suspensory*apes*incur*more*fractures*than*smaller*suspensory* apes.*Second,*the*semiQterrestrial*locomotor*strategy*and*preferred*low*canopy*height*of*

Pan,*the*least*arboreal*of*the*suspensory*apes*examined*here,*result*in*a*low*rate*of* deformation*(p=0.03,*Correlation*Coefficient*=*Q0.96).*Therefore,*chimpanzees*appear*to* incur*lower*severity*fractures*than*their*more*suspensory*conspecifics.*Third,*Pan’s* locomotor*and*canopy*preferences*increase*their*propensity*for*bone*remodeling*after* injury*(p=0.02,*Correlation*Coefficient*=*Q.097).*This*suggests*that*in*addition*to*sustaining* less*severe*injury,*chimpanzees*achieve*greater*bone*remodeling*than*the*more* suspensory*apes.*I*discuss*the*significance*of*each*of*these*points*below.**

4.1 Influence(of(Locomotor(Strategy(on(Fracture(Frequency(

The*analysis*of*the*relationship*between*locomotor*strategy*and*fracture*frequency* resulted*in*models*that*lacked*significance,*providing*no*support*for*my*prediction*that* highQrisk*behaviors,*such*as*rapidQspeed*brachiation,*would*be*associated*with*fracture* frequency*among*suspensory*primates.*Heather*Jarrell’s*(2011)*study*showed*that* suspensory*apes,*especially*Pongo3and*Hylobates,*do*have*more*fractures*that*can*be* attributed*to*falls*than*other*primates,*and*that*this*is*probably*due*to*their*locomotor* strategies.*However,*when*comparing*suspensory*apes*to*one*another,*the*nuances*of* locomotor*strategies*seem*to*have*little*effect*on*fracture*frequency.**

These*results*suggest*that*adaptations*related*to*locomotor*safety*during* locomotion*are*effective.*Although*each*of*the*three*suspensory*genera*engages*in*

!50! ! somewhat*different*locomotor*behaviors,*each*is*well*suited*anatomically*and*behaviorally* to*its*preferred*locomotor*mode.*Thorpe*and*Crompton’s*(2006)*research*supports*this* hypothesis*by*signifying*that*Pongo*locomotor*adaptations*are*consistent*with*safety*as* well*as*energetics.*Pontzer*and*Wrangham*(2004)*state*that*nonQenergetic*factors,*such*as* safety,*may*be*responsible*for*maintaining*energetically*costly*climbing*adaptations.*(

4.2 Influence(of(Locomotor(Strategy(on(Fracture(Deformity(and(Remodeling(

I*predicted*that*the*locomotor*modes*of*Hylobates*and*Pongo*would*result*in* increased*deformity*and*remodeling*compared*to*Pan.3I*surmised*that*the*highQspeed* richochetal*brachiation*of*Hylobates*and*the*tendency*of*both*Hylobates3and*Pongo*to*travel* on*small*branches*would*increase*the*likelihood*of*severe*fracture*including*increased* deformity*and*thereby*difficult*remodeling.*Although*the*models*show*that*Hylobates*and*

Pongo*locomotor*strategies*are*not*significant*predictors*of*deformity*and*remodeling,* there*is*a*significant*negative*relationship*with*deformity*and*remodeling*for*Pan3(p=0.03,*

Correlation*Coefficient*=*Q0.96).*This*means*that*utilizing*a*dual*locomotor*repertoire*that* includes*terrestrial*quadrupedalism*as*well*as*suspensory*arm*swinging*may*be*beneficial* for*fracture*recovery,*as*dependence*on*the*effected*limb*is*not*necessarily*essential.**

When*carrying*a*load,*chimpanzees*often*utilize*a*tripedal*gait*(Watson*et*al.,*2011).*

Use*of*a*tripedal*gait*could*also*allow*for*less*frequent*use*of*a*fractured*limb*during* healing*allowing*for*quicker*and*more*complete*remodeling.*It*is*also*possible*that*small* amounts*of*compressive*loading*on*fracture*injuries*may*augment*the*healing*process,* stimulating*bone*repair*and*maintaining*continuity*at*the*fracture*site.*Conversely,* continued*suspensory*behaviors*may*retard*healing*as*tensile*loading*associated*with* suspension*lengthens*bone.**

!51! ! Pongo,*though*fully*capable*of*traveling*terrestrially*when*needed,*does*not*employ* the*same*dual*locomotion*strategy*as*Pan.*Even*when*injured,*orangutans*are*unlikely*to* descend*from*the*high*canopy.*Because*they*are*so*large*in*body*size,*the*energy*required* to*consistently*move*from*the*ground*to*the*canopy*would*be*costly.*Therefore,*orangutans* may*remain*high*in*the*canopy,*utilizing*their*typical*quadrumanous*mode*of*locomotion.**

Although*baboons*locomote*terrestrially*using*a*quadrupedal*gait,*the*results*of*this* study*do*not*suggest*an*effect*on*deformation*or*remodeling*of*fractures.*This*may*be*a* product*of*baboon*behavior*and*social*interactions.*Like*chimpanzees,*baboons*are*known* to*use*tripedal*feeding*postures,*however,*tripedal*locomotion*is*infrequent*and*is*usually* slow*(Rose,*1977).*Aggressive*behavior*in*baboons*is*pervasive*(MacCormick*et*al.*2012),* and*the*ability*to*locomote*quickly*is*important*for*avoiding*injury.*Thus,*using*an*injured* limb*in*order*to*continue*locomoting*at*a*quicker*pace*and*avoid*further*injuries*may*be*a* more*pressing*issue*than*allowing*for*the*remodeling*of*a*previous*injury.**

4.3 Influence(of(Body(Size(on(Fracture(Frequency(

*For*all*three*genera*of*suspensory*apes,*especially*Pongo,*body*size*more*than*any* other*variable*appears**the*influence**fracture*frequency.**Model*results*show*a*significant* positive*relationship*between*body*size*and*fracture*frequency.*This*result*is*in*agreement* with*my*prediction*that*large*bodied*orangutans*incur*a*higher*injury*cost*with*respect*to* fracture*frequency*than*smaller*bodied*apes.**Although*orangutans*engage*in*slow* quadrumanus*climbing*and*bridging,*they*incur*a*higher*injury*cost*with*respect*to* fracture*frequency*than*less*cautious*apes,*particularly*gibbons,*who*also*travel*within*the* high*forest*canopy.*Thus,*the*anatomical*disadvantage*of*large*body*size*does*not*appear*to*

!52! ! be*fully*abated*by*the*cautionary*behavior*exhibited*through*quadrumanous*locomotor* strategy.**

Pongo3is*the*largest*living*arboreal*primate*and*is*arguably*the*largest*fully* suspensory*primate*known*among*extant*and*extinct*primate*taxa.*Scaling*laws*for*body* size*are*allometric*(Pritchard,*1993),*and*as*body*size*increases,*the*skeleton*increases*in* mass*at*a*greater*rate*to*support*the*loads*resulting*from*cubic*increase*in*body*volume.*

Whether*or*not*orangutans*fall*more*often*than*other*suspensory*primates*is*unclear.*

However,*even*with*the*increased*bone*mass*that*corresponds*with*their*larger*body*size,* orangutans*still*sustain*severe*fractures*due*to*the*impact*forces*caused*by*their*large* body*mass.*This*suggests*that*evolution*favors*safety*in*routine*loading*environments*as* opposed*to*safety*from*catastrophic*events.**

Given*the*relationship*between*body*size*and*fracture*frequency*for*Pongo,*it*is* surprising*that*Pan*does*not*have*a*similar*higher*incidence*of*severe*fracture.*Pan’s3dual* locomotor*behavior*of*arboreal*suspension*and*terrestrial*knuckleQwalking*and*their* ecological*interactions*may*well*abrogate*the*relationship*between*body*size*and*increased* severe*fracture*frequency.**

4.4 Influence(of(Body(Size(on(Fracture(Deformity(and(Remodeling(

Although*body*size*has*a*positive*relationship*with*fracture*rate,*body*size*is*not* significantly*related*to*fracture*deformity3(p=0.24,*Correlation*Coefficient=*Q0.21)*or* fracture*remodeling*(p=0.24,*Correlation*Coefficient=*Q0.21).*Surprisingly,*there*is*no* indication*that*deformities*are*more*common*or*more*severe**in*large*animals*for*whom* higher*impact*forces*would*be*expected.*Additionally,*remodeling*rates*show*no*

!53! ! association*with*body*size.*Rather*remodeling*rates*appear*to*be*consistent*across* suspensory*primates.*The*remodeling*rates*for*Papio*are*consistent*with*those*of* suspensory*primates*with*respect*to*size*as*well.*It*appears*that*the*degree*of*remodeling* may*be*consistent*with*respect*to*body*size*in*primates.***

4.5 Influence(of(Height(of(Travel(on(Fracture(Deformity(and(Remodeling(

Contrary*to*predictions,*the*hylobatid*and*pongid*preferences*for*feeding*and* traveling*in*the*high*canopy*have*no*significant*relationship*with*deformity*or*remodeling.*

However,*the*preferred*lower*substrate*height*for*Pan*is*negatively*related*to*deformity* and*remodeling.*It*is*possible*that*the*ability*to*compensate*for*a*fracture*both*in*feeding* and*locomotion*may*be*easier*for*chimpanzees*because*they*habitually*travel** quadrupedally*on*the*ground*where*either*tripedal*or*bipedal**use*of*their*unaffected*limbs* may*reduce*active*loading*and*increase*healing*of*the*injured*limb.*.**(

By*traveling*quadrupedally,*an*animal*can*disperse*force*across*three*limbs*and* remain*stable*while*locomoting.*This*allows*the*animal*to*discontinue*regular*use*of*an* injured*limb*until*some*level*of*remodeling*is*complete.*For*the*ape*genera*examined*in* this*study,*this*behavioral*option*is*limited*to*the*terrestrial*knuckleQwalking*Pan.*Both* tension*and*compression,*to*varying*degrees,*can*cause*disruption*in*remodeling* processes.*In*humans,*there*is*some*evidence*that*the*weight*of*the*shoulder*in*resting* position*is*a*sufficient*tension*to*cause*disunion*in*clavicle*fractures*that*are*allowed*to* heal*without*operative*management*(Preston*and*Egol,*2009).**It*is*possible*that*slight* compression*may*facilitate*healing,*as*opposed*to*tension,*in*instances*of*fracture*at* different*locations*on*the*foreQlimb*and*hindQlimb.*However,*excessive**compression*may** shorten**the*fractured*element.*KnuckleQwalking*allows**Pan*the*opportunity*to*better*

!54! ! control*the*magnitude*of**load**applied*to*a*fractured*element,*permitting*an*injured* individual*to*discontinue*regular*use*of*the*injured*limb.*Both*behaviors*may*foster* proclivity*for*effective*remodeling.**

* Thus*it*appears*that*body*size*influences*fracture*frequency*among*suspensory* apes,*with*the*larger*bodied*animals*incurring*more*fractures.*Also,*knuckleQ walking/terrestrial*travel*among*apes*is*a*factor*in*deformation*and*remodeling.*

Terrestrial*bouts*may*reduce*the*degree*of*deformation*among*apes*while*increasing*the* degree*of*remodeling,*with*the*caveat*that*terrestriality*alone*is*not*a*single*influence.*

Baboons*are*the*most*terrestrial*genus*in*my*study,*yet*the*fracture*percentages*observed* within*the*sample*are*higher*(29.4%)*than*those*in*chimpanzees*(22.9%)*and*gibbons*

(21.1%).*Baboons*may*incur*higher*risk*of*injury*from*intragroup*conflict*and*predation* avoidance*(Eisenberg*et*al.,*1972).*These*differences*may*be*ultimately*tied*to*the*social* and*mating*systems*characteristic*of*baboons.**

4.6 Implications(for(Hominoid(Evolution(and(the(Last(Common(Ancestor(

Suspensory*adaptations*first*appeared*in*the*MidQMiocene*apes*and*this*new* strategy*was*distinct*as*earlier*apes*(e.g.,*Proconsul)*were*quadrupedal*(McNulty,*2010).*

There*are*benefits*and*costs*associated*with*suspensory*locomotor*strategies.*Suspensory* adaptations*and*behaviors*allow*larger*bodied*animals*to*access*the*plentiful*resources* found*in*the*small*branch*setting.**Extant*apes*share*adaptations*with*extinct*MidQMiocene* apes*for*suspensory*locomotion*(Begun*1994;*Gebbo,*1997;*MacLatchy*et*al.,*2000;*MoyáQ

Solá*2004;*McNulty,*2010).*However,*there*are*limits*to*the*benefit*of*suspensory* locomotion.*Pongo’s*extreme*body*size*might*exceed*the*safety*boundary*afforded*by*the* suspensory*strategy*thereby*prompting*the*greater*occurrence*of*fractures.*It*is*telling*that*

!55! ! adult*Gorillas,*the*only*primate*larger*than*Pongo,3do*not*frequent*the*arboreal* environment.*It*is*probable*their*extreme*body*size*makes*frequent*arboreal*travel* dangerous.*

Despite*the*sparse*fossil*record*known*from*the*Late*Miocene,*when*the*last* common*ancestor*of*the*hominoid*clade*was*present,*the*study*of*the*nature*of*injury*on* extant*apes*provides*insight*into*the*impact*of*fracture*injuries*among*Miocene*ape* ancestors*(McNulty,*2010).*Although*humans*most*likely*diverged*from*a*chimpanzeeQlike* ancestor*(Begun,*1994),*it*is*difficult*to*tell*just*how*chimpanzeeQlike*our*last*common* ancestor*really*was*(McNulty,*2010).*It*is*possible*that*the*last*common*ancestor*of*the*

HomoQPan*clade*used*more*frequent*suspensory*behaviors*than*extant*chimpanzees,* perhaps*resembling*the*quadrumanous*strategy*adopted*by*orangutans.*However,*the* quadramanus*strategy*utilized*by*Pongo*appears*to*be*a*more*ancestral*strategy,*similar*to* that*employed*by*most*Miocene*apes*(McNulty,*2010).*Pan*and*Gorilla*depart*from*this* possible*ancestral*strategy,*frequenting*the*ground*more*often*and*relying*on*low*canopy* substrates,*thereby*incurring*fewer*severe*fracture*injuries*with*lower*costs,*including*low* degrees*of*deformation*and*high*levels*of*remodeling.*It*is*possible*that*this*more* terrestrial*strategy*and*the*decreased*injury*costs*associated*with*it*was*a*catalyst*for*a* shift*in*evolutionary*pressure*toward*the*most*extreme*terrestrial*ape,*humans.*As*we* learn*more**about*ape*evolution,*particularly*the*adaptive*florescence*of*hominoid* locomotor*strategies*within*the*Miocene**(Begun,*1994;*McNulty,*2010),*the**selective* pressures*that*shaped*the*biology*of*our*hominoid*ancestors*so*important*for* understanding*the*processes*and*circumstances*that*lead*to*human*origins*will*be*better* understood.**

!56! ! 4.7 Future(Research(

* Future*research*emerging*from*this*study*will*focus*on*delineating*the*effects*of* locomotor*strategy*and*canopy*height.*Because*the*most*suspensory*apes*feed*high*in*the* canopy*and*the*least*suspensory*feed*nearer*to*the*ground,*it*is*difficult*to*tease*apart*the* independent*effects*of*locomotor*strategy*and*preferred*canopy*height*on*suspensory* related*injury.**Carefully*estimated*fall*heights*for*each*individual*would*likely*have*better* predictive*value*than*average*canopy*height,*based*on*the*results*of*this*study.**Direct* association*of***behavioral*events*and*fracture*incidence*would*be*ideal*,*although*this*is,*of* course,*very*difficult*(if*not*impossible)*to*achieve.*Although*the*likelihood*of*observing* falls*among*wild*primates*is*slim,*following*apes*with*fractured*limbs*particularly* chimpanzees,*bonobos,*and*gorillas*may*be*possible*yielding*observations*of**their*(injury* modified)*travel*bout*strategy*as*a**realistic*alternative.*Given*the*intense*research*on* chimpanzees*and*bonobos*currently*conducted*at*multiple*field*sites*(e.g.,*Ngogo*and*

Kibale*National*Park,*Gombe*National*Park*in*Tanzania,*and*the*Tchimpounga*Chimpanzee*

Rehabilitation*Center*in*the*Republic*of*Congo)*comparing*past*locomotor*bout*behavior*to* bouts*postQinjury*may*make*it*possible*to*further*examine*how*suspensory*apes*cope*with* injury*through*behavior*modification.**

* Additionally,*the*inclusion*of*humans*in*future*study*would*provide*more*insight* into*the*evolution*of*the*hominines*from*the*last*common*ancestor,*as*well*as*the*origins*of* bipedalism.*The*examination*and*comparison*of*early*human*injuries*with*those*of*apes* may*also*provide*insight*into*the*emergence*of*purposeful*injury*treatment*practices.*

CHAPTER(5:(Conclusions(

!57! ! The*results*of*this*study*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*exhibited*by*Pan*have*a*negative*relationship* with*deformity*and*remodeling.*Such*strategies*may*provide*an*evolutionary*advantage,*as* fractures*that*are*incurred*by*Pan*are*less*likely*to*be*highly*deformed*and*are*more*likely* to*have*better*remodeling*results.*The*examination*of*fracture*frequency*and*severity*in* modern*apes*helps*to*emphasize*the*importance*of*injury*incurred*by*falling*as*a*selective* pressure*during*the*evolution*of*the*hominoid*clade.*In*future*studies,*the*increased* delineation*between*locomotor*strategy*and*travel*height,*as*well*as*the*inclusion*of*early* hominins*will*provide*increased*insight*into*the*evolutionary*pressures*faced*by*the*last* common*hominoid*ancestor*as*well*as*early*humans.*

!58! ! PART(2:(Internal(Bone(Geometry(

CHAPTER(1:(Introduction(

1.1 Changes(in(Morphology(Caused(by(fracture(

Morphological*changes*in*bones*often*occur*as*a*result*of*injury.*Decades*ago*

Adolph*Schultz*examined*changes*in*bone*morphology*caused*by*fracture*(Schultz,*1939,*

1944,*1956).*Although*small*in*sample*size,*his*1939*study*comparing*13*healed*long* bones,*from*the*genus*Hylobates,*with*their*nonQinjured/intact*counterparts,*identified* mean*shortening*of*4Q5%*(Schultz,*1939).*Although*his*sample*size*was*small,*this*study* was*influential,*and*his*results*guided*the*questions*I*ask*in*Part*2*of*my*thesis.**

In*Part313of*my*thesis,*I*categorized*changes*in*the*morphology*of*broken*bones* using*the*deformity*scale*(Table*2.4).*As*Wolff’s*law*implies,*(described*in*Part1,*section*

2.3),*limb*loading*causes*mechanical*adaptations*in*the*skeleton*to*strengthen*and*remodel* bone*in*accordance*to*loading*regimes*(Lieberman*et*al,*2004).*Skeletal*fractures*have*the* potential*to*drastically*alter*the*loading*environment*of*limb*bones.*Injury*induced* asymmetry*in*long*bone*length,*like*that*reported*by*Schultz*(1939),*may*alter*postural* and*locomotor*behavior,*thereby*disrupting*routine*kinematics.*How*animals*contending* with*an*injury*modify*behavior*is*unknown,*but*examining*bone*geometry*in*fractured*and* unfractured*limb*bones*may*elucidate*changes*that*reflect*injuryQinduced*changes*in* locomotor*strategy.*It*is*unlikely*that*changes*in*loading*patterns*are*limited*to*just*the* fractured*element.*Instead,*such*changes*should*also*affect*the*corresponding*element*as* compensations*are*made*to*continue*effective*locomotion.**

*

!59! ! The*crossQsectional*geometry*of*a*limb*bone*shaft*may*change*as*a*result*of* modification*to*mechanical*loading*on*long*bones*(Ruff,*2002;*Lieberman*et*al.,*2004;*

O’Neil*and*Ruff,*2004;*Pearson*and*Lieberman,*2004;*Main*and*Biewener,*2007).*Frost’s*

(2003)*mechanostat*theory*exPands*on*Wolff’s*law*by*explaining*the*mechanism*through* which*change*in*loading*regimes*can*bring*about*changes*in*bone*structure.*The*bones*use* a*feedback*loop*to*stimulate*bone*remodeling.*When*strain*thresholds*are*reached,*bone* remodeling*is*initiated*(Frost,*2003).*Increased*bone*deposition*reduces*strain*caused*by* increased*loading.*Conversely,*decreased*loading*and*decreased*strain*lead*to*resorption*of* bone*(Jarrell,*2011).*The*objective*of*Part*2*of*my*thesis*is*to*test*bone*response*to* differential*loading*patterns*caused*by*injury.*3

1.2 Hypotheses(

I*predicted*that*analysis*of*bone*crossQsectional*area*between*paired*limbs*would* show*evidence*of*change*in*morphology*due*to*differential*loading*patterns*when*one*limb* is*affected*by*fracture.3

1.2.1 Locomotion(Hypotheses((

Because*locomotor*strategies*among*gibbons,*orangutans,*chimpanzees*

(suspensory*apes)*and*baboons*(terrestrial,*quadrupedal*primate)*differ,*cross*sectional* area*between*fracture*affected*and*unaffected*limbs*will*differ*as*a*result*of*differential* use.***

1.2.1.a Terrestrial(Quadrupedal(Locomotion(will(be(Related(to(Smaller(Cross(

Sectional(Area(Than(Suspensory(Locomotion(

!60! ! Animals*that*frequently*use*terrestrial*quadrupedal*locomotion,*baboons*and* chimpanzees,*will*show*smaller*differences*in*CSA*when*affected*by*fracture*than*those* that*are*suspensory.*

1.2.1.b Consistently(Used(Elements(will(show(the(Most(Difference(in(Cross(Sectional(

Area(

Elements*that*are*consistently*used*in*the*preferred*locomotor*strategy*will*show* the*most*difference*in*crossQsectional*area.*The*difference*in*CSA*of*the*fractureQaffected* foreQlimbs*of*highly*suspensory*animals,*gibbons*and*orangutans,*will*be*greater*than*that* of*the*more*terrestrial*Chimpanzees*and*baboons.*

1.2.2 Ecological(Hypothesis(((

1.2.2.a Difference(in(Cross(Sectional(Area(will(be(Correlated(to(Body(Size(

Body*size,*positively*correlated*with*fracture*severity,*will*have*an*impact*on*the* difference*in*crossQsectional*area*between*fractured*limbs*and*their*corresponding* element.*The*greater*the*body*size*of*the*animal*the*greater*difference*in*CSA*between* fractureQaffected*and*unaffected*limbs.**

1.3 Explanation(of(Predictions(

I*predicted*that*there*would*be*a*difference*in*crossQsectional*area*of*fractured* elements*and*their*corresponding*parts.*These*differences*will*be*greatest*for*elements* that*are*frequently*used*for*locomotion.*For*example,*in*animals*that*primarily*use*their* front*limbs*for*locomotion,*the*difference*in*crossQsectional*area*will*be*greater*if*the*

!61! ! affected*limb*is*a*humerus*than*if*it*is*a*femur.*In*animals*that*are*frequently*quadrupedal,* the*difference*will*be*less*significant.**

I*predicted*greater*difference*in*CSA*between*fractureQaffected*and*unaffected*limbs* in*animals*of*larger*body*mass.*The*increased*severity*of*fractures*associated*with*body* size*could*mean*that*differential*loading*patterns*will*be*utilized*more*frequently*and*for*a* longer*period*before*function*has*returned*to*the*limb,*if*the*limb*regains*function.*The* differential*loading*could*cause*bone*remodeling*in*response*to*change*in*mechanical* stimuli.**

CHAPTER(2:(Materials(and(Methods(

2.1 Sample(

The*sample*consists*of*fractured*elements*and*their*corresponding*unaffected* element.*The*elements*were*selected*from*the*141*specimens*analyzed*in*Part31*of*this* project.*Only*fractured*elements*with*corresponding*unfractured*elements*were*chosen*for* study.**

2.2 XKray(Computed(Tomography((CT)(Scanning(

The*fractured*elements*and*their*corresponding*unfractured*elements*were* scanned*using*3Qdementional*XQray*computed*tomography3(CT)*scanning.*I*used*the*CT* scanning*facilities*located*at*the*University*of*Texas,*Austin*(UTCT)*to*scan*skeletal* elements*housed*at*this*university.*UTCT*utilizes*an*Xradia*MicroXCT*and*the*ACTIS* microfocal*subsystem.*I*used*the*Smithsonian*CT*laboratory*facility*(NMNH*CT)*to*collect* data*from*specimens*at*the*National*Museum*of*Natural*History.*The*CT*scanning*facilities* at*Case*Western*Hospital*(CASE)*were*used*to*examine*specimens*from*the*Cleveland*

!62! ! Museum*of*Natural*History.*Both*NMNH*CT*and*CASE*utilize*The*SOMATOM*Emotion*6* multiQslice*spiral*whole*body*Computed*Tomography*system.*CrossQsection*images*were* taken*at*2mm*intervals*through*the*entirety*of*the*length*of*the*bones*from*the*sample*of* fractured*elements*and*their*corresponding*elements*(Table*2.1).

!63! ! * !64! ! 2.3 ImageJ(&(BoneJ(Analysis(

CrossQsectional*area*(A)*was*used*to* determine*the*total*bone*deposited*in*the*areas* scanned,*indicating*the*bone’s*resistance*to*axial* compression*and*tension*(Lieberman*et*al.,*

2004).*Comparing*these*measurements*against* corresponding*scans*for*the*opposite*side*bone* Figure!2.1:!Cross!section!of!the!diaphysis! of!a!long!bone!(left).!Cross!section!of!the! from*the*same*individual*allows*for*evaluation*of* diaphysis!of!a!long!bone!with!the!cross! sectional!centroid!indicated!with!a!black! the*distribution*of*bone*density*between*the*two* point!(right).!(Modified!from!Cooper!et!al.,! 2007)! sides*(Figure*2.1).*If*an*animal*compensated*for* an*injury*by*relying*on*its*nonQinjured*side,*then*differences*in*bone*thickness,*area,*or* distribution*should*be*evident.*The*crossQsectional*area*was*calculated*using*the*BoneJ* plugQin*for*ImageJ*image*processing*and*analysis*software*(Doube*et*al.,*2010;*Rasband,*

2012).**Although*it*would*be*ideal*to*take*measurements*from*the*neutral*axis*of*each* bone,*it*would*not*be*possible*to*calculate*the*neutral*axis*of*the*samples*through*nonQ invasive*observation*(Pearson*and*

Lieberman,*2004).*The*neutral*axis*does* not*typically*run*through*the*crossQ sectional*centroid*of*most*bones,*but*for* the*sake*of*consistency,*the*crossQsectional* centroid*was*used*as*the*basis*for*all* Figure!2.2:!CT!scans!slides!of!the!cross!section!of!the! left!and!right!femur!of!Papio&P52!from!the!University! measurements*performed*in*BoneJ*(Figure* of!Texas!at!Austin.! 2.2).**

!65! ! CrossQsectional*area*measurements*were*taken*from* the*CT*scan*slides*that*most*closely*corresponded*with*the* points*on*each*bone*associated*with*25%,*50%,*and*75%*of*the* total*element*length*(Figure*2.3).*The*margin*of*error*for*image* measurements*was*less*than*or*equal*to*2*mm.**Measurements* were*taken*from*elements*affected*by*fracture*and*their* corresponding*unaffected*elements*and*paired*for*analysis.*I* only*included*slides*that*were*not*directly*affected*by*fracture.*

Images*that*revealed*large*callouses*and*spurs*were*not* included*nor*were*their*counterparts,*as*such*deformities* Figure!2.3:!3RDemensional! could*skew*the*results*in*favor*of*the*fractured*element.** rendering!of!the!right!femur!of! Papio&P52!from!the!University!of! In*order*to*control*for*any*possible*differences*between* Texas!at!Austin!marked!at!the! slides!that!are!25%,!50%,!and! left*and*right*elements*on*uninjured*animals,*I*examined*pairs* 75%!of!the!total!length!of!the! bone.!! from*five*individuals*with*complete*skeletons*that*showed*no* evidence*of*healed*fractures*or*bone*remodeling.*This*control*group*included*two* specimens*from*Hylobates3and*Pan3and*one*Pongo*specimen*(5*total*individuals).**

2.4 Statistical(Analyses(

PairedQt*tests*were*performed*using*R*statistical*software*(The*R*Foundation*for*

Statistical*Computing)*to*compare*measurements*of*CSA*for*the*broken*elements*and*their*

∑d t = n(∑d 2) − (∑d)2 unbroken*corresponding*elements*using*the*formula* n −1 .*Significance* was*set*at*a=0.05.* € CHAPTER(3:(Results(

!66! ! 3.1 Analysis(of(the(CSA(of(the(Control(group(

I*used*a*pairedQt*test*to*compare*measurements*of*CSA,*of*the*unbroken*left*and* unbroken*right*clavicles,*humeri,*ulna,*radii,*fermura,*tibiae,*and*fibulae*of*the*control* group.*The*left*side*is*significantly*larger*than*the*right*side*(t=4.02,*DF=*98,*p=0.0001),* with*a*difference*of*3.73*mm*between*mean*lengths*(95%*confidence*interval:*1.89*–*5.57* mm).*

When*testing*the*foreQlimb*and*hindQlimb*CSA*of*the*control*group*independently,* results*are*similar.*A*pairedQt*test*comparing*the*CSA*of*the*unbroken*left*and*unbroken* right*clavicles,*humeri,*ulna,*and*radii*of*the*control*group*shows*a*significantly*larger*left* side*than*the*right*(t=3.23,*DF=*62,*p=0.001)*with*a*difference*of*3.26*mm*in*mean*values*

(95%*confidence*interval:*1.24545*–*5.28313*mm).*Similarly,*a*pairedQt*test*comparing*the*

CSA*of*the*unbroken*left*and*unbroken*right*femora,*tibiae,*and*fibulae*of*the*control*group* shows*significantly*larger*left*side*than*the*right*(t=3.23,*DF=62*,*p=0.02)*with*a*difference* of*4.55*mm*in*mean*values*(95%*confidence*interval:*0.79–*8.31*mm).**

3.2 Comparison(of(Fractured(Elements(and(Their(Unaffected(Counterparts(by(

Genus(

When*comparing*the*CSA*measurements*using*paired*tQtests,*I*found*that*only*Pan* shows*a*significant*difference*in*mean*values*of*fractured*and*unfractured*elements.*(t=Q

2.23,*DF=*21,*p=0.04;*95%*confidence*interval:*Q11.55*to*Q0.41*mm).*This*indicates*that*the* fractured*elements*of*Pan*have*a*smaller*CSA*(Q5.98mm)*than*the*unfractured*elements.*All* other*tests*revealed*no*significant*difference*in*CSA*(Table*3.1).**

!67! ! *(

3.3 Comparison(of(Fractured(Elements(and(Their(Unaffected(Counterparts(by(

Element(

**When*comparing*the*CSA*measurements*using*paired*tQtests*by*element,*I*found* that*only*the*clavicles*show*a*significant*difference*(Q15.88*mm)*in*mean*value*of*fractured* and*unfractured*elements*(t=Q3.10,*DF=*23,*p=0.01;*95%*confidence*interval:*Q26.48*to*Q

5.27*mm).*This*indicates*that*the*fractured*clavicles*have*a*smaller*CSA*than*the* unfractured*elements.*All*other*tests*revealed*no*significant*difference*in*CSA*(Table*3.2).*

CHAPTER(4:(Discussion(

4.1 Analysis(of(the(CrossKSectional(Area(of(the(Control(Group(

The*analysis*of*the*crossQsectional*area*of*the*control*group*indicates*a*statistically* significant*difference*in*CSA*for*the*left*and*right*side*of*the*body.*The*bones*of*the*left*side*

!68! ! have*a*larger*mean*crossQsectional*area*than*those*on*the*right.*Although*findings*are* statistically*significant,*I*lack*confidence*that*these*results*are*biologically*meaningful.*The* margin*of*error*for*measurement*is*2*mm.*Given*a*difference*of*3.73*mm,*it*is*possible*that* the*outcome*is*the*result*of*measurement*error.*The*small*sample*size,*exclusion*of*the* genus*Papio,*and*the*measurement*margin*of*error*suggests*that*the*results*have*false* significance*due*to*sampling*insufficiencies.*Unfortunately,*due*to*the*cost*of*the*CTQ scanning*process,*this*was*the*largest*control*sample*obtainable*for*this*study.**

4.2 Comparison(of(Fractured(Elements(and(Their(Unaffected(counterparts(by(

Genus(

Pan*is*the*only*genus*with*a*significant*difference*in*CSA*between*fractured*and* unfractured*element.*Statistical*analysis*showed*that*the*mean*difference*in*CSA*between* fractured*and*unfractured*elements*in*Pan*was*5.98*mm*(p=0.04),*with*the*fractured* elements*smaller*than*the*unfractured*elements.*The*bone*geometry*difference*exclusive*to*

Pan*may*in*part*be*explained*by*the*findings*obtained*in*Part313of*this*thesis.*The*findings* show*that*the*locomotor*strategy*of*chimpanzees*has*a*negative*effect*on*deformation*and* remodeling.**That*is,*fractures*in*Pan*are*less*severe*and*remodeling*extent*is*greater*than* in*other*apes.*By*engaging*a*dual*locomotor*repertoire*of*terrestrial*quadrupedalism*and* suspensory*arm*swinging*chimpanzees*have*the*anatomical*and*behavioral*flexibility*to* exploit*modified*loading*patterns*on*their*limbs.*Therefore,*it*is*possible*that*temporary* disuse*and*lack*of*mechanical*loading*of*a*limb*due*to*fracture*injury*could*lead*to* resorption*of*bone,*decreasing*the*CSA.**

4.3 Comparison(of(Fractured(Elements(and(Their(Unaffected(Counterparts(by(

Element(

!69! ! Among*the*limb*elements,*only*the*clavicle*showed*a*significant*difference*in*mean* value*of*CSA*between*fractured*and*unfractured*elements.*Statistical*analysis*indicates*that* the*mean*difference*in*CSA*between*fractured*and*unfractured*clavicles*was*15.88*mm.*

Although*the*finding*is*statistically*significant*(p=0.01),*I*am*not*confident*that*this*finding* is*biologically*meaningful.*Subsequent*review*of*the*CT*slides*and*bony*landmarks*used*to* quantify*area*revealed*that*the*acute*uQshaped*angle*of*the*clavicular*bodies*might*have*led* to*measurement*error*skewing*the*results.*This*possible*error*would*have*been* exacerbated*in*measurement*of*clavicles*that*were*highly*deformed.*Thus,*possible* measuring*insufficiencies*reduce*overall*confidence*in*the*statistical*result.(

4.4 Further(Research(

Future*research*will*build*upon,*and*expand*the*results*of*this*successful* preliminary*study.*A*larger*control*group*will*be*essential*for*further*research,*and*the*CTQ scan*data*from*these*healthy*individuals*will*provide*a*wealth*of*data*for*future*projects.*

Following*apes*with*injuries,*among*them*chimpanzees,*bonobos,*and*gorillas,*and* observing*their*injury*associated*(possibly*new)*travel*bout*strategies*would*provide* insight*on*the*differential*use*of*fractured*limbs*that*may*be*associated*with*smaller*CSA*in* fractured*elements.**

Additional*anatomical*measurements*could*also*provide*evidence*for*a*decrease*in* mechanical*advantage*in*injured*limbs.*For*example,*humeral*torsion*could*be*compared* between*humeri*affected*by*injury*and*their*corresponding*unaffected*humeri*using*the* same*CTQscans*that*were*used*to*extract*the*crossQsectional*data.*By*demarcating*bony* landmarks*and*overlaying*the*slides,*humeral*torsion*could*be*calculated*by*finding*the* angle*created*by*the*intersection*of*the*bony*markers*(Figure*4.1).**

!70! ! Figure!4.1:!Sample!CT!scan!slides!of!the!left!and!right!humerus!of!an! orangutan!that!are!color!coded!and!prepared!for!the!calculation!of! humeral!torsion.! (

CHAPTER(5:(Conclusions(

( The*results*of*this*study*demonstrate*that*Pan*to*the*exclusion*of*the*other*apes* examined*here*has*a*lower*mean*CSA*for*fractured*elements*than*unfractured*elements.*

This*difference*in*bone*geometry*could*be*related3the*chimpanzee’s*ability*to*engage*in*the* dual*locomotor*behaviors*of*suspensory*locomotion*and*knuckleQwalking,*that*promote* reduction*in*body*mass*and*impact*load*on*the*injured*limb.**

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