212 Received 23May2014; Accepted12November2014 *Author ([email protected]) for correspondence HaverfordPhysics Department, College, Haverford, PA 19041, USA. and Platt,2014).Here,wereport usingheadcamvideotoexplore Zamani, 2014)andpeafowldetecting modelpredators(Yorzinski explore thevisualstrategiesusedbyfalconschasingprey(Kane and recorded bycamerasmountedontheheadsofbirds(headcams) to tools (Rutzetal.,2007).Recentstudieshaveusedthestable video 2009), interactwithconspecifics(Takahashi etal.,2004)anduse for example,howtheymovethroughtheirenvironment(BBC, received byorganisms inthe field,revealingnewinformationabout, Troscianko, 2013)nowmakeitpossibletomeasurethevisualcues 2012; Martin,2012).Animal-bornevideomethods(Rutz and and thedynamicsofitsbehavioralresponses(Fernández-Juricic, organism’s locomotorandperceptualcapabilities,itssensory cues biomechanical andsensoryecologyapproachthatconsiders the Many problemsinthestudyofanimalbehaviorrequireanintegrated gentilis, Looming,Antipredatorbehavior, Startleeffect Northern Goshawk,Visual guidance,Sensoryecology, Accipiter KEY WORDS:Pursuit–evasion,Predator–prey, Avian vision, Goshawk ( Video filmedbyacameramountedontheheadofNorthern Suzanne AmadorKane*,AndrewH.FultonandLeeJ.Rosenthal pursuit andprey-evasionstrategies When hawksattack:animal-bornevideostudiesofgoshawk RESEARCH ARTICLE © 2015.PublishedbyTheCompanyofBiologistsLtd|JournalExperimentalBiology(2015)218,212-222doi:10.1242/jeb.108597 INTRODUCTION ABSTRACT interception. some preydeimatic‘startle’ displaysmayexploittau-based concise reviewofpursuit–evasioninbiology, andconjecturethat interception strategy. We interprettheseresults inthecontextofa image alsosuggestedthatthegoshawkusedatau-based tactic foundbypreviousstudies.Thedynamicsoftheprey’s looming sensory basisforthesurprisingfrequencyandeffectiveness ofthis caused thegoshawktolosevisualfixationonprey, supportinga prey’s evasivetacticsindicatedthatonlysharpsidewaysturns showed themusingcurvingnon-CATD trajectories.Analysisofthe then turningrapidlytoattackbyclassicalpursuit;inafewcases,it goshawks interceptingpreyusingatrajectoryconsistentwithCATD, filmed fromthegroundgavesimilarresults.Inmostcases,itshowed suggesting thatthegoshawkusedfinite-feedbacksteering.Video cases, weobservedoscillationsinthevisualfixonprey, maintained alongthehorizontalthanverticaldirection.Insome direction (CATD) formovingprey. Visual fixationwasbetter prey, luresorperches,andusuallyusingconstantabsolutetarget prey ataconstantvisualangle,usingclassicalpursuitforstationary pursuit strategy. Thegoshawkflewtointercepttargetsbyfixingthe mathematical pursuitmodelswasusedtodeterminethegoshawk’s of novelimageanalysismethodsandnumericalsimulations visual guidancetopursuepreyandlandonperches.A combination Accipiter gentilis ) wasusedtostudyhowtheraptor strategy iscalled constantabsolutetarget direction (CATD) because criterion canbeappliedduring each constantvelocityinterval.This (Nahin, 2012).Ifthepreymaneuvers infrequently, thenthe CB This iscalledtheconstantbearing decreasingrange(CB)criterion the predatormaintainsitsbearingangleat: along v Northern Goshawk, for thefirsttimepursuit–evasionandlandingbehaviorin for apredatormovingatconstantvelocity, headcam video,weconsiderthebasicgeometryofimages Before reviewingpursuit–evasionstrategiesandtheirappearanceon goshawk visualfixation. We alsostudiedhoweffective prey-evasiontactics wereatthwarting ground providedcomplementaryinformationonspatialtrajectories. and pursuitstrategiestheraptorused,whilevideofilmedfrom methods thatenabledustodeterminewhichspecificvisualguidance video wasinterpretedusingnewopticalflow-basedimageanalysis environments (SebestaandBaillieul,2012).Inthisstudy, headcam context becauseitcanmaneuverathighspeedthroughcluttered Srinivasan, 2011), andthegoshawkisofspecialinterestinthis and collisionavoidance(MischiatiKrishnaprasad,2012; models haveinspiredroboticalgorithmsforswarming,following 1).Biologicallyderived goshawk), alarge diurnalraptor(Fig. constant v pointing frompredatortoprey, thebearingangle, and Mark,1975),itisusefultodefinethebaselinevector, prey’s estimatedfuturelocation(CollettandLand,1978;Lanchester 2010) andchasingslowprey(KalkoSchnitzler, 1998). beetles (Gilbert,1997)andbatsfollowingconspecifics(Chiu et al., (Zhang etal.,1990),flies(Land,1993;Trischler etal.,2010), when thepreymoves(Fig. center ofmotion(Fig. the prey(Nahin,2012)soprey’s imageremainsstationaryatthe pursuit (CP),inwhichthepredator’s velocityalwayspointstoward center ofmotion,whichisequivalenttobeingonacollisioncourse. γ the prey’s projectedvelocityrelative tothelocalopticalflow. For angles. We candefineanangle, vertical cameraangles( this figure;theprey’s positionis describedusinghorizontaland Possible imagesofmovingandstationarypreyarealsoshownin from thepredator’s centerofmotion(LeeandKalmus,1980). Pursuit–evasion inbiology =0 deg,thepreymovesoppositetoopticalflowtoward p , andtheangle To explaininterception,in which thepredatormovestoward The time-optimalpursuitstrategyforstationarypreyisclassical p Fg 2A).Theresultingopticalflow fieldradiatesoutward (Fig. v e and |v p β | ≥ betweenpreyvelocity |v Accipiter gentilis e |sinβ

2A). However, ingeneralCP isinefficient ϕ θ o andχ = , time-optimalinterceptionispossibleif sin

2B). CP hasbeenobservedforbees ) thatmapontothegoshawkvisual − 1 γ , tocharacterizetheorientationof ⎝ ⎜ ⎛ v|sin |v e v| |v p (Linnaeus 1758)(hereafter, β ⎠ ⎟ ⎞ v .(1) e v and p , withitsheadaxis ϕ R , between (Fig. 2C). For R and R ,

The Journal of Experimental Biology (CATD inFig. laws likeproportional navigation(PN)(Shaw, 1985).High-gain fixed targets (Osorioetal.,1990). at constantvelocity(Shima,2007), asobservedforfliestracking predator trajectoriesevenforprey thatremainmotionlessormove CATD reducestoclassicalpursuit–evasion(CPE)(Fig. instantaneous valueof keep theprey’s imageatconstant visual angle(determinedbythe al., 2006).ThepredatorcanimplementCATD bymaneuveringto indicated bytheangle ϕ RESEARCH ARTICLE directly awayfromthepredator( CATD reducestoCP. Forclassical evasion, i.e.thepreyflees compensate. Forstationaryprey(|v the predator’s controlsignal,stimulatingittoaccelerate prey visualanglefor Fig. course aremet:constantpreyvisualangleand CATD canbedemonstrated iftworequirementsforacollision trajectories isadefinitivetestforCATD. Inpredatorheadcamvideo, ways. Theconstantorientationof al., 2005;StankowichandBlumstein,2005). on atangentialapproachorcollisioncourse(Fernández-Juricic et data aremixedonwhetherpreyrespondmorestronglytopredators field maybeaby-productofitssensoryimplementation,given that However, camouflageofthepredator’s motionontheprey’s visual motion cueislooming(retinalexpansion)(Reddyetal.,2007). perceives nopreymotiononitsvisualfieldandviceversa;the only Krishnaprasad, 2006;Reddyetal.,2006)becausethepredator Warren, 2004).CATD isamotioncamouflagestrategy(Justhand bats (Ghoseetal.,2006;Ghose2009)andhumans(Fajen variesbutR These strategiescanbeimplemented byfeedback-basedsteering Proof ofCATD can bedeterminedfromempiricaldatainseveral CATD isusedbydragonflies(Combesetal.,2012;Olberg, 2012), Z Z χ τ=I/ θ Δt γ β Z v ϕ ϕ v a v Nproportionalnavigation T s R PN O deviatedpursuit I classicalpursuit–evasion f classicalpursuit τ̇ constantbearingdecreasingrange DP CPE constantabsolutetarget direction CP CB CATD List of symbolsand abbreviations List of p e o p min p 2A). Deviatedpursuit(DP)isthe moregeneralcaseofconstant ̇ goshawk–target distance(m) time whengoshawkassumesimpactposture(s) image verticalangle(deg) optimal bearingangle(deg) image horizontalangle(deg) simulation timestep(s) prey velocityangleonimage(deg) baseline–prey velocityangle(deg) Z minimum predator velocity(m prey velocity(m relative goshawk–target speed(m tau (s) bearing angle(deg) relative goshawk–target linearacceleration(m on-screen trajectoryarclength(pixels) baseline vector(m) prey size(m) prey imagesize(pixels) focal length(pixels) tau-dot 2A). Deviationsin when goshawkassumesimpactposture(m) has aconstantorientationintheEarthframe,as Z α inFig.2D.(Ghoseetal.,2006;Reddy ϕ≠ϕ (m) ϕ ο ) forfixedpredatorheadorientation s ο −1 and ) s −1 ) β γ≠ ϕ 0deg),Eqn =0 fromthe e R deg, soitresultsincurved |=0), Eqn in 3Dpredatorandprey s −1 ) ϕ ο γ 1 givesϕ 0deg(CATD in =0 set pointserveas 1 givesϕ s −2 )

2E). ο ο =0, and =0 and headcam video(EarthRangers,2011). Gannetsmake underwater, consistentwithCP, inground(Katzir, 1994)and kingfishers compensateforrefractiontoaimdirectlyattheir prey reported observingbirdsusinginterceptiontocatchprey. Diving context. A fewfieldstudies(Angell,1969;Curio,1976)have we surveyedtheliteratureforevidencenotinterpretedin this trajectory qualitativelysimilartothoseseenforCP andDP. a setpoint(Fig. velocity andvisualanglesontheheadcamimagecanoscillateabout Depending onthefeedbackconstantandpreymotion,prey’s (Ghose etal.,2006;Land,1993;SrinivasanandZhang,2004). with atimedelaybetweenevasivemaneuversandpredatorresponses et al.,2007),andbatsinsectsusefinitefeedbackimplementations feedback ispronetoinstabilitiesduesensorimotordelays(Reddy impact posture.[Typical goshawkwingspan98–115 how thebirdpitchesupward,extendsitsfeetandsometimesrollsslightlyin glove,showing hood withintegralvideocameralandingonthefalconer’s Fig. al. proposedthat thesebirdsmightpursueprey usingDP attheir interception point(FuxandEilam, 2009). 2008), butgazealternatelytoward movingvolesandaprospective 2008) andflydirectlytoward stationaryprey(IlanyandEilam, view salientobjectsatthecenter oftheirvisualfield(Ohayonetal., to theforwarddirection(Watanabe andTakahashi, 2013).Barnowls borne videoofpenguinspursuingkrillshowsthepreyimage close suitable for3Dtracking(Machovsky-Capuskaetal.,2012).Animal- propulsion thatlikelyusevisualguidance,leavingbubble trails consistent withCP aswellunderwaterchaseswithactive credit: RobertMusters. showing itsorientationpitcheddownwardrelativetotheheadaxis.Image Reynolds, 1997).](B)Goshawkwearingthehead-camera(headcam) As fewstudiesofpursuitstrategieshavebeenconductedforbirds, Because falconsarebifoveatelike otherdiurnalraptors,Tucker et

1. Goshawkwithhead-camera. B A The JournalofExperimentalBiology(2015)doi:10.1242/jeb.108597

2F), orPNcanresultinagraduallyarcingpredator (A) NorthernGoshawkwearingthe

cm (Squiresand V -shaped dives 213

The Journal of Experimental Biology 214 RESEARCH ARTICLE along thefaceofatalldam(Ponitzetal.,2014).Thisworkshowed aerodynamics ofperegrinefalconsstoopingtowardstationary lures 3.A recent articleusedhigh-speed3Dvideotostudythe Fig. able toconfirmCATD inonlyafewcases,suchasthatshown background (thesky)andconstantlymaneuveringprey, sowewere tracking wasusuallynotpossiblebecauseofthefeatureless with CATD butnotDP atapreferredfovealangle.Opticalflow between chasesandchangedwhenthepreymaneuvered,consistent (Kane andZamani,2014);thefixationanglesvariedsignificantly prey ataconstantvisualanglewithintheforwardbinocularrange determine thatfalconspursuingflyingbirdsmostoftenfixedthe to models(Tucker etal.,2000).We haveusedheadcamvideoto they reportedforstoopingfalconswerenotcomparedquantitatively deep foveal45 orientation ofthehorizontalandverticalcameravisualangles( Fig. of R is shownasabluearrow. red curve).Thebaselinevector, trajectory(graycurve)canoscillatearoundtheoptimalbearingangle(CB, navigation (PN)inwhichthepredator’s follows: (B)CP;(C)thegeometryforconstantbearing(CB)criterionusedinCATD; (D)CATD;implementations ofproportional (E)CPE;(F)finite-feedback pursuit (CP)andarabbittrackedbyconstantabsolutetargetdirection(CATD; arrows) withrespecttothelocalopticalflowfield.Labelsindicatearabbitnottracked(NT)byinterceptionstrategies( velocity. Theintersectionofthedashedlinesindicatescentermotionat(0

2. Schematicillustrationofheadcamimagesandtrajectoriesforvariouspursuit–evasionstrategies. relative tothefixedEarthframe.DisadaptedfromGhoseetal.(Ghoseal.,2006);FShaw(Shaw, 1985). D χ A v

deg visualangle;however, thecurvingtrajectories p (t v 3 p ) γ=0 (t v p 2 ϕ(t (t )

v 1 CATD deg 3 ) ϕ(t e v NT ) , preyvelocity; α e ϕ(t 2 (t ) α 3 1 ) v ) e CP (t θ 2 α v ) e (t 1 ) v p , constantpredatorvelocity; EF v e B v θ e , χ ). Blackarrowsindicatetheopticalflowduetoself-motionofpredatoratconstant ϕ , bearinganglebetween ϕ=0 ϕ=0 γ 0deg).Earth-frametrajectoriesforeachpursuitstrategyaredepictedas =0

deg, 0 2004). Studiesofowlsattackingsimulatedpreyshowed that proposed asanadaptiveresponsetointerception(EdutandEilam, behavior observedforrodentsunderattackbybarnowlshas been relevant predatorpursuitstrategies.Forexample,theevasive the birdsusedanyspecificvisualstrategies(Sheltonetal.,2014). in complextandemflightswithconspecificsfoundnoevidencethat high-speed stereometric3Dvideostudyofcliff swallowsengaged binocular visualfielduntilshortlybeforeimpact.Bycontrast,a strategies, thefalconpresumablywouldseeitspreyinupper Thus, althoughthisstudydidnotanalyzeforvisualorpursuit path thatleveledout(andinonecaseswervedslightly)nearimpact. and flewrelativelydirectlytowardthepreyalonganinclinedglide that falconskepttheirheadsorientedclosetotheforwarddirection v

deg deg p The antipredatorresponseofpreyhaspresumablybeenshapedby v deg). Anangle, p R Lorrain. indicate initialpositions.Imagecredit:EddydeMolandFrancois object trackedinblue),confirminguseofCATD. Solidcircles constant centerofmotion(indicatedbyadistantbackground wearing theheadcamflewatconstantvelocity, asshownbythe was interceptedbyasecondfalcon(upperleft). (red tracks)thatwasfixedataconstantvisualanglebeforeit Fig. The JournalofExperimentalBiology(2015)doi:10.1242/jeb.108597

.Headcamimagefilmedbyafalconpursuingcrow 3. R and v γ , definestheorientationofprey’s velocity(red p ; β v , anglebetween C e (A) Schematicheadcamimage,showingthe v p deg),apheasanttrackedbyclassical γ≠0 v CB p ϕ v e and R PN v e β ; α , theconstantangle The falcon R ,

The Journal of Experimental Biology ≤ (Tislerics, 2000),whichevadepredatorsbyfleeingatspeedsof extents greaterthanthecurrent goshawk huntsinthefieldhave unpredictablelocationsandspatial video isusefulforfilming staged encounterswithlures,but maneuvering ofagoshawkorrecord itsprey’s motion.Stereometric 2001) andrapidturns;Europeanrabbits( Goshawk speedshavebeenestimatedat30 found tousethesamehuntingbehaviorsaswildbirds(Fox,1981). 2006; Rutz,2006).Goshawksraisedandtrainedforfalconrywere Reported huntingsuccessratesrangefrom5%to>30%(Kenward, is alsoknownforpersistentchasesthroughdensebrushorforests. rapidly pursuingpreyinacontour-hugging tailchase.Thegoshawk include foragingbysoaringoverhead,thenstoopingonprey, and perch andthensilentlyswoopsdownuponprey. Othertactics and-wait predator, thegoshawkusuallyforagesfromanelevated Kenward, 1978;SquiresandReynolds,1997).A shortdurationsit- mammals inforestedandopenhabitats(Fox,1995;Kenward,2006; by theelusiveNorthernGoshawkasithuntsbirdsandsmall Several fieldstudieshaveidentifiedthemostcommontacticsused guidance (Shifferman andEilam,2004). sideways evasionmayalsofunctiontofrustratepredatorvisual 2011; Sheltonetal.,2014;Warrick etal.,2002).Thissuggeststhat low-radius high-g limitations duetofixedwingaerodynamics,whilebirdsachieve actual ormodelraptors.Thetheoreticalmodelsalsoassumed Lima, 1993;LimaandBednekoff, 2011; Lindetal.,2002)fleeing multiple birdspecies(Devereuxetal.,2008;Kullberg etal.,2000; compared withdodgingbyrodents(IlanyandEilam,2008) capture rateandhighobservedfrequencyofsidewaysevasion a purelylocomotivemechanismcannotexplaintheextremelylow Rosén, 2001;Howland,1974;vandenHoutetal.,2009).However, predator maneuverabilityandresponsetime(Hedenström offs hasbeenexplainedtheoreticallyastakingadvantageoflimited Eilam, 2004).Preyevasionbydodging,swervingandsteeptake- than classicalevasion(IlanyandEilam,2008;Shifferman and toward thepredator),andthatbothweresignificantlymoreeffective sideways evasionwasfarmoreeffective thandodging(turning RESEARCH ARTICLE 31±2 foveal angleof16±1 that oftheRed-tailedHawk(Lord,1956):aloweracuityshallow and Rosenfield-Wessels, 1975)witharetinalgeometrysimilarto objects (O’Rourkeetal.,2010).Goshawkeyesarebifoveate(Fite 2013a). Asaconsequence,theyuseheadmotiontotracksalient Dial, 2000),rapidaccelerationto which typicallyescapeusingsteeptake-off angles(Tobalske and necked Pheasants( al., 2007)thatweestimateat (O’Rourke etal.,2010)]andalimitedrangeofeyemotion(Jones binocular region[measuredat35±1 attacks (Kenward,1978;Rutz,2006;Widen, 1989). stoops (Alerstam,1987),and10–15 (Theriault etal., 2014).Therefore,forthisstudy wemadeuseof rate ( decision-making inflocks(Flack etal.,2013),butitscurrentlogging V (jinking) andsharpsidewaysturns(DriverHumphries,1988). Goshawk huntingbehavior andvision 16 -formation flocking(Portugaletal.,2014)andhierarchical This studyconsiderstwocommontypesofgoshawkprey:Ring- Diurnal raptorshavefrontallyorientedeyeswithaforward GPS hasenabledstudiesofmanyaspectsbirdflight,including m deg, bothdefinedrelativetotheforwardheadaxis. ≤

s 10 − 1 Hz) andaccuracy( (Garland, 1983),dodging,erraticzigzagswerving Phasianus colchicus turns usingavarietyofmaneuvers(Rosetal.,

deg andahigheracuitydeepfoveaangleof ≥ 0.25 ≤ ±3 ≤

m 19 ≤ deg forthegoshawk(Buck, m) cannotresolvetherapid

18 s

deg inotherraptorspecies − m ) (GiudiceandRatti,2001), 1 m 3 for levelflightandgliding

reconstruction volumes s − Oryctolagus cuniculus m 1

(Giudice andRatti, s − 1 for highaltitude ) for threetypicalpursuitsafterliveprey. Foreachvideo,we Supplementary materialTable within pheasant) (successrate:6%perpreyand8%pursuit),came 0.53–8.4 prey. Thepreypursuitshada meandurationof4.3±3.2 swoops fromperchesusuallyfollowedbypoweredflightafterthe tactics aswildgoshawks:threestoopsbegunfrommid-airand13 fled shortlybeforeinterception.Thegoshawkusedthesamehunting showed movingpreywhilefivestationarypheasantsthat made twosuccessivepursuitsafterthesameprey. Elevenpursuits chase begunwiththegoshawkatrest;inthreecases, and 10landingsonperches.Distinctpursuitsweredefinedasa and sixrabbitpursuits,threepursuitsafterbird-shapedfalconrylures We recordedandanalyzed29totalheadcamsequences:10pheasant live, wildprey. field duringforaging,flyingtowardperchesandlures,hunting headcam andgroundvideoofgoshawksflownforfalconryinthe at theprey’s centerofmasspointalongitsvelocity, and (C)arunningrabbit(R3)tracked byCATD. InBandC,magentaarrows optical flowwasnottrackedbecause thebackgroundchangedtooquickly; (A) stationarypheasant(P4a);(B)a movingpheasanttrackedbyCP (P7); Table pursuits correspondingtotheselabels aregiveninsupplementarymaterial and opticalflow(whitelinescircles) ofthreepursuits. Fig. optical flow( RESULTS i.4A–C showsvideoimageswithtracksindicatingpreymotion Fig.

4. Headcamimageswithtargettracks(magentacirclesandlines)

S1. Solidcirclesindicatethefirstposition inthetimesequence: C ≤ B A 2.1 s). Thegoshawksuccessfullycapturedonlyoneprey(a γ The JournalofExperimentalBiology(2015)doi:10.1242/jeb.108597 =0 deg).Imagecredit: RobertMusters. m ofinterceptingitspreyineightotherpursuits.

S1 givesfurtherdetails. v e , andoppositethe local Details of

s (range: 215

The Journal of Experimental Biology θ for detailsoftheimageanalysisandsimulations).Plotsmeasured 5A;seeMaterialsandmethods comparison withmeasureddata(Fig. stationary prey, luresandperchesCATD topursuemovingprey targets in25of28pursuits:itusedCP whenflyingtowardall angles. Instead,thegoshawkusedinterceptionwhenflyingtoward from mid-airoraperch(cf.Fig. of motionwhenthegoshawkflewtowarditstarget startingeither ~2 for prey, movingobjects(prey, thefalconer, etc.)weretrackedvia retinal fixationareaatthecenterofitsvisualfield;duringsearches goshawk visuallytrackedsalientobjects(prey, lure,perch,etc.)ina landing. Whilesearchingforpreyandbeforeflyingtoitstarget, the was visibleoncamerainalmostallcasesbeforeeachpursuitor data). (supplementary materialFigsS1–S5showplotsofallmeasured either theshallow(16±1 targets duringsearching,pursuitsandlandingsdidnotagreewith CATD wereusedtoproduceplotsof from camerageometryand goshawk–target speed,v section explainshowthegoshawk–target distance, in whichthebackgroundwastooerratic.TheMaterialsandmethods 216 RESEARCH ARTICLE flow wasmeasuredforallbutonevideoofamovingprey(Fig. (moving targets only)andimagesize, measured thetarget’s horizontalandverticalvisualangles(

θ (deg) χ (deg) Z (m) γ (deg) θ (deg) χ (deg) Z (m) θ (deg) χ (deg) Z (m) , The mainheadcamfindingsareasfollows.goshawk’s target The visualangleusedbythegoshawktoviewpreyandother χ Hz headsaccades.Theretinalfixationareaagreedwiththecenter –10 –10 –20 –20 –10 –20 –10 , 10 10 20 20 10 10 20 10 0 0 0 1 2 0 0 0 0 γ 0 0 0 5 andZ EF CD AB 07 05 02 0 –0.25 –0.50 –0.75 15–. 050 –0.5 –1.0 –1.5 versus timeareshownforfivepursuitsinFig. 10–0.5 –1.0 , andlinearacceleration, deg) ordeep(31±2 I . ComputersimulationsofCP and 0

2A andFig. θ Time (s) I , versustime.Theoptical θ (deg) χ (deg) Z (m) γ (deg) θ (deg) χ (deg) Z (m) θ (deg) χ (deg) Z (m) , χ –10 –10 100 –20 –10 –5 10 15 10 10 10 20 10 10 20 30 and 0 5 0 5 0 5 –0.8 0 0 0 0 0 0 0 deg) goshawkfoveal 15–. 050 –0.5 –1.0 –1.5 Z a 4A). , werecomputed versus timefor 06–. 020 –0.2 –0.4 –0.6 2– 0 –1 –2 Z , relative θ

, 5B–F χ

4B) ), γ the measured the approximategoshawkwingbeatperiod(Pennycuicketal.,1994); constant apartfromsaw-toothoscillationswithperiod0.2 jinking rabbit(Fig. pheasant’s erraticmotion(Fig. pheasant’s imageat pursuing aflying,jinkingpheasant,thegoshawkfixed could beseentomaneuverrelativethebackground,e.g.in goshawk hadtomaneuverachieveCATD, asinallcasestheprey CATD whenθ moving prey, fivetracksagreed withCPE(thespecialcasefor collision courseandprovidingstrongsupportforCATD. For supplementary materialFigs constant the goshawkviewedmovingpreyat merely constantvisualangle(DP).Ineightpursuitsofmovingprey, local opticalflow. Thisallowed ustoconfirmCATD, asopposedto flow, wecouldmeasuretheprey velocityangle, new imageanalysismethod:bytrackingboththepreyandoptical provided aviewofpreyandbackgroundthatallowedustouse pursuits ofmovingprey(Fig. supplementary materialFigs measured valuesillustratesthisagreement(Fig. data for at thecenterofmotion.A comparisonofthecomputer-simulated CP perches) wasconsistentwithconstantvelocitymotiontheprey the opticalflowforflighttowardstationarytargets (prey, luresor in eightof11 pursuits.Fig. θ θ valuethatchangedwhenthepreymaneuvered(Fig. , χ The JournalofExperimentalBiology(2015)doi:10.1242/jeb.108597 andZ on screenrelativetotheopticalflow. distance and supplementary materialTable pursuits andlandings(labelsdetailsgivenin and lines).Time series datafrommeasuredvideotracksof using CP (blacksquaresandline)CATD (graycircles goshawk vieweditstargetbeforeflight. γ (F) amovingrabbit(R3).Dashedlines: stationary pheasant(P4a),(E)amoving(P7)and (C) landingonaperch(L7);andpursuitsafter(D) series ofvisualangles( angles andpreydistances. Fig. θ 0deg;θ =0 versustimewasincloseagreementwithcomputer ≈ 0

5. Simulatedandmeasuredheadcampursuitvisual

deg) andthreewithCATD for θ versus timeinFig.

4C), thegoshawkmaintained =1.1±1.4 versustime:theaverage γ

definestheorientationofprey'svelocity 4A isatypicalvideoimageshowingthat

S1–S3). Samplevideoimagesfrom deg andγ≈0

S4, S5),provingtheywereona

4C) showhowheadcamvideo 4B, Fig. θ , χ γ ) andpredator–preydistances, ≈

0

(A) Computer-simulatedtime 5A withthecorresponding S1). (B)Pursuingalure(LR1);

deg andanapproximately

deg (CPE)inspiteofthe 5E). Whilepursuinga θ valueatwhichthe Z γ versustime: is goshawk–target γ , relativetothe γ≈0 deg.The θ≠0

deg andθ

s equalto

5B–D;

5E,F; Z ,

The Journal of Experimental Biology and thisresultedingreater Thus, sidewaysevasionwaseffective atthwartingvisualfixation sideways trajectory(supplementarymaterialFig. maintained (supplementary materialFig. initially stationaryandusedsidewaysevasionshortlybeforeimpact (supplementary materialFig. the preyevadedsuccessfullybymakingalarge sidewaysswerve only oneofdodging(Z ~0.2 one bound(0.2–0.3 fix thepreysuccessfully. Rabbits wereabletomakeamajorturnin frequently maneuveredevenwhenthegoshawkmanagedtovisually visualized separatelyrelativetothebackground,showingthatprey distance cases ofpreyfleeingdirectlyaway(minimumgoshawk–prey interception (supplementarymaterialTable material Fig. feedback-based interceptionmechanism(Fig. their optimalvaluesasthegoshawkmaneuvered,expectedfora data showedevidenceofoneormoreoscillationsin look forevidenceoffeedback-basedinterception.Infivecasesthese relative topreymotioninthegoshawkstudyalsopermittedus simulations ofCATD (cf.Fig. RESEARCH ARTICLE motion tolowerverticalvisualangles( visual angle,thoughcenteredhorizontally. However, thetarget’s motion andthetarget wereoff-screen atalarge positivevertical head tilteddownwardrelativetoitsvelocity, asboththecenterof flying fromaperch,thegoshawkapparentlyinitiallyflewwithits (supplementary materialFig. on thetarget wasnotmaintainedascloselyintheverticaldirection tactics inthissmallsample. brush. Theplotsofaveragehorizontalangle, object whileperchedandpursuedpreyvigorously, oftenthrough sequences inwhichthegoshawkalternatelyobservedastationary (Fig. impact ( so abruptthatwewereabletomeasurethetimeanddistancebefore Fig. simulations (cf.Fig. with the is explainedbythegoshawkassumingimpactposture,consistent orientation wasstablewithinmeasurementerror. Opticalflow slopes equaltozerowithinerrorbars,indicatingthattheheadcam Z Prey wereobservedtousevarioustacticssuccessfullyevade While thegoshawkfixeditstargets horizontally, visualfixation p (m) Fig. 0 1 2 3 4 S1, Fig. s. Thesedataalsoshowedthat 6A); forliveprey, thechangesin LR1 6B showsthefixationangleversustimeforthreevideo AB T Z

LR2 p min χ and versustimebehaviorpredictedbyourcomputer θ

=3±3 LR3

S2). Forlurepursuitsandlandings,thedropinχ constantbutnot S4C–E, Fig. Z

L1 L2L3 p ) atwhichthegoshawkassumedimpactposture m), eightofsidewaysevasion(Z

s), whilepheasantscouldturnortake-off in 5A with5B,C,Fandsupplementary material Track min

L4 L5L6L7L8 S5A,D,E). Z =1.4 min

S4A, Fig.

S3, Fig.

values onaveragethanotherevasion γ≈0 S3). Inthreecases,thegoshawk m). Motionofthepreycouldbe

5A,F). Tracking ofopticalflow γ

deg (DP)asthepreyflewona diverged from0 χ S4C,E, Fig. χ S5D) orwhenthepreywas weremoregradual. <0

L9 L10

deg) justbeforeimpact S1). Therewereseven

5E,F; supplementary 0 0.2 0.4 0.6 θ

S4B, Fig. versustimehad min S5A,E). When T p (s) deg onlywhen =9±11 θ andγ

θ (deg) S5B,C). m) and –20 –10 about 10 20 0 was 0 100 groundspeeds forflightstowardstationaryprey(10–18 targets wasanalyzedtomeasuretherangeofaveragegoshawk centripetal accelerationduringturns.Headcamvideoofstationary acceleration forstationarytargets only;wecouldnotdetermine 3.9±1.6 Netherlands MeteorologicalInstitute),withmeanvaluesof Wind speeddatawereretrievedfromanearbyweatherstation(Royal the frame rateperiod(1/30 relative speedontimescalesthatwerelongcomparedwiththevideo visually fixitsmaneuveringprey, itmanagedtoachieveaconstant result meansthatwhilethegoshawkwasalwaysmaneuveredto as well10outof11 (91%)pursuitsaftermovingprey. Thelast relative speedin71%(12of17)flightstowardstationarytargets, top speed.Thegoshawk’s Z previous dataindicatingbothpreyspeciescanmatchthegoshawk’s Fig. attack thepreyfrombehind(Fig. goshawk initiallymaintainedconstant of swervingtoonesidebeforeimpact(Fig. immediately beforeimpactwereconsistentwiththegoshawk’s habit The target image’s occasionalsmallhorizontaldeviations [cf. fig. head duringforwardmotiononlyinfrequentlyandbysmallamounts tracking alsoallowedustodeterminethatthegoshawkturnedits lower rangesforflightstowardstationarylures(7–16 perches (5–13 pursuit inwhichthegoshawkinitiallyflewwithitsvelocityoriented showsstillimagesandon-screentrajectoriesfora 7 repeatedly. Fig. then convertedtoatailchasewhileitattackedtheprey, often goshawk initiallyflewtoreachtheprey’s immediatevicinityand strategies, andifso,howtheywereimplemented.Ingeneral,the goshawk andpreytrajectorieswereconsistentwithdifferent pursuit to computetheeffectiveness ofdifferent evasivetactics. were selectedtoshowsuccessfulcapturessotheycouldnotbeused the sametacticsingroundandheadcamvideo,videos visibility orcameraangle.Althoughthepreyevadedcaptureusing be determinedmostofthetime,whileremainderhadpoorprey (58 of86)thevideos,goshawk’s andprey’s trajectoriescould to pursue,attackandcapturefleeingrabbitspheasants.In67% the groundthatshowedgoshawksflyingfromfalconer’s glove analyzed anarchiveofvideosfilmedusingasinglevideocameraon relative tomovingpreyrangedfrom013 goshawks indicatedtheheadcamdidnotinterferewithflight.Speed Measured valuesforv We examinedthegroundvideoforevidenceofwhether To studythepursuittrajectoriesofbothgoshawkandprey, we Z S3).

200 300 data agreedwithconstantlineardecelerationbeforeimpact. 4C andfig. m Time (s)

s − The JournalofExperimentalBiology(2015)doi:10.1242/jeb.108597 1 and range1.5–6.7

m

s −

400 500 1 3C inLeeandKalmus(LeeKalmus,1980)]. ). Theagreementwithspeedsreportedforwild

s). In29%offlightstowardstationarytargets, and versus timewasconsistentwithconstant a gave goshawkgroundspeedandlinear

600 m

s − 1

. and T Distance fromtarget( headcam stabilitydata. Fig. squares) andtime( fixation angle Dashed line:meanvalueof began toassumeimpactposture. squares) atwhichthegoshawk each timeseries. Dashed lines:averagevaluesfor plotted overthemeasuredrange. color symbols)versustime, objects forthreevideos(different 5D; supplementarymaterial

6. Impactpostureand Z p . (B)Average horizontal 1A). Intwopursuits,the while maneuveringto

m

s − θ 1 ofstationary , consistentwith T

p m ms , open Z p

s , solid − (A) 1 −1 ), with Z ) and p 217

The Journal of Experimental Biology 218 RESEARCH ARTICLE the samedirection(Fig. and thetwoanimalsmovedwiththeirvelocitiesinapproximately the goshawkflewslightlyaboveandimmediatelybehindrabbit plane approximatelyorthogonaltothecameraaxis,itshowedthat final pursuitcouldbeidentifiedasCPEbecauseittookplaceina and its3Dtrajectoryinterceptedthatoftheprey(Fig. trajectory ontheimagewasaverticalline,italwaysfacedforward, interception coursewiththerabbit:aftertake-off, thegoshawk’s the goshawkinitiallyflewwithitshorizontalbearingonaCATD downward andoutofthescreen.Inthiscase,itisunambiguousthat Fig. changed directionbyjinking (supplementarymaterial interception course,sometimes correctingcoursewhentherabbit on atrajectoryconsistent with aCATD piece-wise linear 1.5±0.8 goshawk andpreyin20typical pursuitswithmeanduration at thesametime. position ofthepreyon-screenandtheir3Dtrajectoriesintersected when thegoshawk’s bearingpointedtowardtheextrapolatedfuture could onlybedemonstratedforconstantpredatorandpreyvelocities the goshawkflewtowardprey. Similarly, supportforCATD tracks onvideo,theirplotsof predator andpreyvelocitieswhenthegoshawkhadparallel Fig. prey didnotusedirectevasion(Fig. ground videosshowedthegoshawksusingCP initiallywhenthe toward theprey’s extrapolatedfutureposition).Infact,noneofthe current location)orwithinterception(forwhichitmustorient consistent withCP (whichrequiresittoorienttowardtheprey’s linear on-screen.We alsocouldtellwhetherthegoshawk’s posewas the lastrequirementrulesoutacceleratedmotionthatonlyappears thus presentedastrongargument formotionatconstantvelocity, as of linearon-screentrajectory, linear constant directionandwhenitchangeddirection.Thecombination apparent directionofitsmotionon-screen,whetheritmovedina dependence of velocity, whichrequiresbothalinearon-screentrajectoryand determine whethertheanimal’s motion wasconsistentwithconstant screen trajectoryand information abouteachanimal’s motion. Bymeasuringboththeon- In spiteofthis,wecoulddetermineconsiderablerelevant AB Using theseideas,wemeasured tracksandarclengthsforthe Most videoswerenotfilmedeitherhead-onorinorthogonalview. S6A,C,E). Infour cases,theentirechasewas also CPE.In12 S6A,D). ProofofCPEcouldbeascertainedforconstant y (pixels) s. In16ofthetrackedpursuits, thegoshawksinitiallyflew C s versus time.Fromitspose,wecoulddeterminethe s

(arc lengthalongthetrajectory)wecould 7B,C). s versus timehadthesameslope,and s versus timeandconstantpose x (pixels)

7A; supplementarymaterial

7A,C). The (supplementary materialFig. toward itstarget atanapproximatelyconstantbearingangle point ofastationarytarget, whichconfirmedthatthegoshawkflies pursuits, whichcouldcorrespondtoDP, PNornosinglestrategy. moved atconstantvelocity, wecannotfurtherdescribethese for allfourandCATD forthreeofthepursuitswhererabbit (supplementary materialFig. into afinalpursuitthatapproximatedtangenttotheprey’s motion the goshawk’s trajectoryconstantly curvedasitmadeabankedturn ending inattackandeventualcapture.Intheremainingfourvideos, ≤90 immediately turnedin0.2–0.4 cases, whenitcameclosetointerceptingtheprey, thegoshawk about visualfixation thatthegoshawkquickly resolvedvia the preyfleddirectlyorjinked, this resultedinonlysmallvariations or classicalevasionplusjinking, andonlyrarelybydodging.When sometimes turnedtheirheads,apparently tofoveateprey. fovea. Thegoshawkdidnot foveatetargets, while falcons occasionally turnedtheirheads inflight,likelytousetheirdeep more gradually),didnotviewpreyatthecenterofmotion, and over longertimes(possiblybecausethefalcon’s preymaneuvered compared withthegoshawk,falconsfixedtheirpreyvisually species wereobservedtofixpreyvisuallyanduseinterception, our twoheadcamstudies(KaneandZamani,2014).While both (McCormack etal.,2013),itisinterestingtocompareresults from falcons andgoshawksarenowclassifiedinseparateorders goshawks, withsomepursuitsusingundeterminedstrategies. As recorded bygroundvideosupportedthefrequentuseofCATD by for horizontalthanverticalvisualangles.Thepursuittrajectories bats, thegoshawkmaintainedcriterionforCATD moreclosely pursued movingpreyusingCATD inthemajorityofcases;alsolike maintained thepreyatconstantvisualangleduringpursuitsand (Ghose etal.,2006),theheadcamdatashowedgoshawk landing onperches.Likedragonflies(Combesetal.,2012)andbats chickens (Moinardetal.,2005)andpigeons(Green1992) stationary prey, luresandperches,similartoresultsfoundfor for barnowls(FuxandEilam,2009).ItusedCP whenflyingtoward fixed itstarget atthecenterofitsvisualfield,aspreviouslyfound While searchingforpreyorbeforeflyingtoaperch,thegoshawk DISCUSSION Finally, wealsoanalyzedfourvideosfilmedfromthevantage The preyinthisstudywereobserved tofleebysidewaysevasion deg inordertofollowthepreyahigh-speedCPEtailchase The JournalofExperimentalBiology(2015)doi:10.1242/jeb.108597 credit: DavidandAdamBurn. arrows indicatetheirdirectionsandstartingpositions.Image video. Circlesshoweachanimal’s positionevery0.4 mass. (C)Goshawk(red)andrabbit(black)tracksfromthis and black(rabbit)arrowsstartingateachanimal’s centerof Their approximatedirectionsareindicatedbyred(goshawk) intercept therabbit,then(B)turningtopursueitviaCPE. after therabbitwasflushed,showinggoshawkflyingto pursuing andattackingarabbit. Fig.

7. Video filmedfromthegroundofagoshawk

S7) (seeBuck,2013b).

S6B,D,F). ApartfromrulingoutCP

s (onetotwowingbeats)through (A) Stillimageshortly

s and

The Journal of Experimental Biology constant tau-dot, studies haveshownthathummingbirdsandpigeonsmaintain provide aquantitativemeasureofpreyloomingdynamics.Previous To studyitsapproachtocollision,weusedthetaufunction range consistentwithvaluesreportedbyGoslow(Goslow, 1971). captures andlandingsattimesdistancesthatlaywithinanarrow Shifferman andEilam,2004). in determiningthesuccessofprey-evasionmaneuvers(Eilam,2005; reinforce theargument thatvisualperceptionplaysasignificantrole evasion comparedwithclassicalplusjinking.Theseresults goshawk didnotapproachpreyascloselywhentheyusedsideways visual angleduringpursuits.Ourheadcamdataalsoshowedthatthe goshawk toleratedlessvariationinthehorizontalthanvertical deviation in wingbeat period.Bydefinition,sidewaysevasioncausesthegreatest goshawks werecapableofexecutinglarge angleturnsinasingle horizontal visualangle,eventhoughthegroundvideoshowed evasion ledtoalarge, rapidlossofvisualfixationalongthe horizontal visualangle.Bycontrast,abrupt,large-angle sideways goshawk managedtokeepthepreyatapproximatelyconstant maneuvering. Evenwhenthepreywasnotfixedvisually, the RESEARCH ARTICLE to flushoutinsectprey(Arbanas,2006;Jab by spreadingandpivotingitsconspicuouslypatternedwingstail For example,thepaintedredstarthasbeenshowntomimiclooming evolved behaviortoexploitthiswidespreadresponselooming. (Sun andFrost,1998;Wang andFrost,1992).Someanimalshave and timetocollision,isindependentofbinoculardepthcues Vincent, 1995).Thisreactionisduetoneuronssensitivelooming 2007), frogs(Yamamoto etal.,2003)andhumans(Regan including birds(Schiff, 1965),fish(Dill,1974),crabs(Olivaetal., control signal. so thegoshawkmustregulateitsmotionusingloomingcuesasa by flyingatconstantvelocitywhenthepreyconstantlymaneuvers, used atau-basedinterceptionstrategy:itcannotachieve interception (Leeetal.,1993).Thisshowsthatthegoshawkalso equivalent tothegoshawkmaintainingconstant toward stationarytargets and91%ofpursuitslivepreyis 1992). Thelinearityofour Green, 1990)andbatsuseacoustictautointerceptprey(Leeetal., 1981), hawksusetau-relatedcuestoinitiatelanding(Daviesand flow cuesforstreamliningpriortowaterimpact(LeeandReddish, 1993; Leeetal.,1991).Plunge-divinggannetsusetau-basedoptical detection bythe predator)(Ruxtonetal.,2004). Theappearanceof non-exclusive hypotheses(e.g. last-minute displaysalsodeterearly on thesehypotheses(Ruxtonet al.,2004). the paintedredstart,andlittleempirical testinghasbeenperformed However, many ofthesedisplaysareverysimilartothoseusedby or deflectingattacktothedisplayed bodypart(Ruxtonetal.,2004). confusing thepredatorbydisruptingasearchimage(Bond,2007), larger tointimidatethepredator (CooperandStankowich,2010), (Edmunds, 1974).Previouslyproposedfunctionsincludeappearing wings, tailsorruffs, inflating bodyparts,orerectingfeathersfur abruptly larger insizejustbefore attackbyspreadingconspicuous behind manyother‘startleeffect’ displays inwhichpreyappear the responsetoloomingmightexplaincognitivemechanism 1996). We hypothesize thatsensoryexploitation(Stevens,2013)of move radiallytosimulatefleeing(NationalGeographic,2007; Hunt, two circularphotophoreschangediameteranditslightedarm tips 2000) andthevampiresquidusesanantipredatordisplayinwhich The goshawkwasfoundtoassumeimpactpostureforlure Looming objectselicitareflexiveescaperesponseinmanytaxa, Tests ofthisconjecturemustdistinguishamongothermutually γ andhorizontalvisualangle,soitisrelevantthatthe τ ̇ ≈ 1, duringaerialdockingandlanding(Leeetal., Z versus timedatafor59%offlights ł o ń ski andStrausfeld, τ ̇ ≈ 1 beforeprey τ ̇ ≈ 1 simply τ = I / I ̇ to (Jabł relationship betweencontrastandloomingfoundinsometaxa variable effective tau-dot,withcontrastmanipulationsprobingthe predator’s responsetopresentationscorrespondingnaturaland Stevens etal.,2008).Experimentscouldassessinsteadthe on theeffect ofdifferent patterns(Ingalls,1993;Sargent, 1990; that werestaticorsimplifiedtheactualdynamicswhilefocusing collision scenarios.Previousexperimentshaveusedpresentations fields couldbemodeledtocomparetheirtau-dotvalueswith these displays(Brooke,1998;Sargent, 1990)onpredatorvisual visual guidance (Ballerinietal.,2008;Mischiati andKrishnaprasad, flocking modelshavehadtorely onuntestedassumptionsabout pursuing insectsacaseofspecial interest(Schuler, 1990).As wind anddifferences betweenpreyspecies(Fox,1995),with birds effect ofhunger(withinhumanelimits),variationduetoterrain or studying predationofstationary versusmovingpreyorlures,the 1980). Infuturework,itwillbe importanttoaddresstheseissuesby territorial defense,catchingalure,socialplay, etc.)(Treleaven, hunger levelandthepursuit’s purpose(e.g.huntingforfood, et al.,2012). integrated empiricalstudiesofpredatorandpreybehavior(Combes Leonard, 2010;Wei et al.,2009),highlightingtheimportanceof the assumedpredatorandpreybehaviors(Nolfi,2012;Pais and modeling studieshavefoundthattheoptimalstrategydepends on targeting andcapturetechniques (Fox,1995).Pursuit–evasion pursuits endingbycollidingwithprey, andonlygraduallydevelop object playandpractice.Northerngoshawksbeginwithinefficient juveniles developskillsthroughsocialplay, preytransferbyparents, Although huntingbehaviorisinnateinraptors(Bustamante,1999), goshawks andfalconsneednotapplyineverycircumstance. Ghose etal.,2006).Consequently, wecautionthatthesefindingsfor fiddler crabs(LandandLayne,1995)bats(Chiuetal.,2010; strategies fordifferent scenarios,includingflies(Land,1993), 2012). away fromtheirforwarddirection(Limaetal.,2014;Martin collide withman-madeobjectsbecausetheyoftenfocusattention zero visualangles,thissupportsthehypothesisthatthesebirdsmay was unproblematic.Asbothspeciesfrequentlyfixedpreyatnon- through theunobstructedsky, soviewingthepreyatalateralangle the falconsinourpreviousstudy(KaneandZamani,2014)flew swerving toavoidabranchwhilepursuingpheasant.)Bycontrast, avoidance. (Inonepursuit,weobservedthegoshawkrapidly where itscentralbinocularfieldcanprocessdepthcuesforobstacle goshawk’s habitofpursuingpreythrough denseforestandbrush, 2008). CATD followedbyCPEalsoseemswell-suitedtothe for bats(KalkoandSchnitzler, 1998)andowls(Hausmannetal., accurately asitattacksfrombehind,astrategypreviouslyreported Interception followedbyCPEallowsthegoshawktomaneuver to subdueandkillpreywiththeirtalons(SustaitaHertel,2010). falcons, whichoftenkillonimpact,goshawkstypicallyneedtime but allowsonlyabrieftimewindowforcapture.Unlikestooping moving prey, interceptionlets thegoshawkreachitspreyquickly, CP bestpreservestheelementofsurprise,facilitatingcapture.For vicinity andthenkillit.Forstationaryprey, rapidinterceptionvia must solveseveraldistinctproblems:findprey, reachitsimmediate duration andmetaboliccostofdifferent flightbehaviors.Thisraptor premium oncapturesuccessrateaswellsearchstrategy, pursuit consider thatthisraptoreatslarge, infrequentmeals,placingahigh optimal foragingtheory(StephensandKrebs,1986),onemust The pursuitstrategyemployedbybirdsmayalsorelatetotheir Other taxahavebeenfoundtousedifferent pursuit–evasion In comparingthegoshawk’s observedhuntingbehaviorwith o ń ski, 1999;Landwehretal.,2013). The JournalofExperimentalBiology(2015)doi:10.1242/jeb.108597 219

The Journal of Experimental Biology polynomial leastsquaresfitsto effect, thecamerawasmountedpitcheddownwardsuchthat goshawk’s upwardpitchingbeforeimpact(Goslow, 1971).To offset this impact duetothemountingofcameraabovebodyaxisand relative toopticalflow. Thetarget imagesweredisplaceddownwardbefore pursuits. Theprey’s motionandposeonscreenwasusedtodetermine in mostcasesandthatthegoshawkdidnotuseheadsaccadesduring Relative goshawk–target speed, collision time(time=0 linear fitstothe accuracy forobjectsimaged f 3 Burn, DaleMewsvideos;www.dalemews.com) filmedoveraperiodof Northampton, MA,USA).Allerrorbarsares.d. analysis andotherdatawerecarriedoutinOrigin8.6(OriginLab, uncertainty inpreyspecies’ sizeandpose(systematic).Allfitting,statistical calculated fromuncertaintyinmeasured estimated poseangles.Target distances, from averagepreybodydimensionscorrectedforperspectiveusing corresponded to0 center ofmotionconfirmedthat changes inperspective.Usingopticalflowduringflighttodeterminethe background objects,becauseautomatedmethodscannotaccommodatelarge Zamani, 2014).Opticalflowwasmeasuredmanuallybytracking mass) madebyRobertMusters.Thecameraaxiswas converted intocameraangles( was usedtotracktarget imagecoordinatesinpixelsandhowthesewere previously howImageJ(NationalInstitutesofHealth,Bethesda,MD,USA) confirmed bythelevelhorizonandopticalflow. We havedescribed 2007), apartfromsomerollbeforeimpactorduringshortrapidturns,as processing becausethegoshawkmaintainedheadnystagmus(Jonesetal., CI) abovetheeyes.Theheadcamvideowasstablewithoutdeshakepost- mounted inafiberglass hood(totalheadcam+mass=20 and glidedinastraight line.Changesin simulated goshawk wasallowedtomaneuverwithout limitsonacceleration ~0.01 220 RESEARCH ARTICLE Huizhou, China)(29.97 the ARRIVEguidelines(NC3Rs2010). Haverford CollegeInstitutionalAnimalCareandUseCommitteefollowing hunting innaturalenvironments.Allexperimentswereapprovedbythe Mews, UK).Allpreywerewildanimalsencounteredbytheraptorsduring video, allgoshawkswereraisedbyaparentandflownforfalconry(Dale by masterfalconerRobertMustersinherthirdhuntingseason.Forground (female, 1.30 Netherlands, on6 Field recordingwiththeheadcamtookplacenearTwenthe, The stereometric video(Theriaultetal.,2014)tracking. rapidly improvingGPS(Pettitetal.,2013)andhigh-speed field forfurtherinvestigationusingheadcamsincombinationwith eye placementandmotions(Martin,2014).Thispresentsawide (Shelton etal.,2014)andinbirdswithotherretinalspecializations, non-predation scenarios,suchasflyingorflockingwithconspecifics 2012), thereismuchtolearnfromthestudyofvisualguidancein (CATD). Goshawkandrelativegoshawk–prey speeds(v for stationaryprey(CP)ormoving andintermittentlymaneuveringprey using theimagetracksofstationary nearbybackgroundobjects. measured usingImageJand,whennecessary, correctedforsmallcamerapan dogs orferrets.Goshawkandpreytracksonthevideoimages were that showedseveralgoshawkspursuingrabbitsandpheasantsflushed by v MATERIALS ANDMETHODS

e is thecamerafocallength(pixels)and years usingvariousconsumercamcorders(25 =10 Ground videoswereobtainedfromanonlinearchive(A.Burnand D. Target size, Headcam videowasrecordedusingmodel808camcorders(Toplanter, Computer-simulated headcamimageswere createdusingPython2.7code s; 2 m

s − h recordingtime;fieldofview:52 1 ) andinitial

kg, 2.5 O , wasmeasureddirectlyforpostsandluresdetermined Z

deg inthegoshawk’s verticalvisualfield(Fig. days (December2012toJanuary2013).Thegoshawk versus timedatawereusedtodeterminetheprojected years old)wasraisedincaptivitybyaparentandflown

frames s); otherwise,theoriginfortimewasarbitrary. Z values weretakenfrommeasured values.The ≤ 15 s θ − θ≈0 , 1 Z deg off-axis). WhenZcouldbemeasured, v ; 1280×720pixelresolution;shutterspeed χ , andacceleration, versus time;errorbarsin ) indeg(±0.3

deg agreedwiththeforwarddirection Z χ I duetoperspective changesasthe , werefoundfrom:Z=Of/Iwhere is theimagesize(pixels)( I

deg horizontal,31 and

frames

f deg; 95%CI)(Kaneand values (statistical),and s a − h 1 , werefoundfrom =2.4±0.5 ; 720×1280pixels) p

=15 g, v

deg vertical) ≤ and 1.5% body

m

1B). χ≈15 cm (95%

s a ≤ − 1 2.7% were deg and γ Dill, eeex .L,FrádzJrcc . rb,J .adWitnhm M.J. Whittingham, and J.R. Krebs, E., Fernández-Juricic, C.L., Devereux, ais .N .adGen P. R. Green, and M.N.O. Davies, E. Curio, T. Stankowich, and J.D. Jr Crall, W. E., Cooper, and J.M. Iwasaki, D. E., Rundle, S.A., Combes, M.F. Land, and T. S. Collett, 66 Koshland IntegratedNaturalSciencesCenterofHaverfordCollege. Hughes MedicalInstituteandaSpecialProjectsawardfromtheMarionE. This researchwasfundedbyagranttoHaverfordCollegefromtheHoward with A.H.F. andwrotethesimulationcodewithL.J.R. S.A.K. conceivedoftheprojectandwrotepaper, performedthevideoanalysis The authorsdeclarenocompetingfinancialinterests. made bytwoanonymousreviewers. headcam imageanalysis.Finally, weappreciatethemanyhelpfulsuggestions correspondence withGrahamTaylor thatresultedinseveralnewideasfor Musters, DavidBurn,JackHubleyandRobertGiroux,fromemail their videos.We benefittedgreatlyfromadviceonfalconryfalconersRobert headcam, andDavidAdamBurnforpermissiontoreproduceimagesfrom We wishtothankRobertMustersforflyingShintathegoshawkwhilesheworea time step, flicker fusionfrequencies(Fox,1995;Jonesetal.,2007)setthesimulation (camera–body axisdistance)usingmeasuredtimescales.Typical avian goshawk assumedimpactpostureweremodeledbylinearlyincreasing http://jeb.biologists.org/lookup/suppl/doi:10.1242/jeb.108597/-/DC1 Supplementary materialavailableonlineat hu . ed,P . in . rsnpaa,P .adMs,C.F. Moss, and P. S. Krishnaprasad, W., Xian, P. V., Reddy, C., Chiu, alrn,M,Cbbo . adle,R,Cvga . ibn,E,Gadn,I., Giardina, E., Cisbani, A., Cavagna, R., Candelier, N., Cabibbo, M., Ballerini, L. Arbanas, Angell, T. T. Alerstam, Supplementary material Funding Author contributions Competing interests Acknowledgements References EarthRangers rvr .M n upre,D.A. Humphries, and P. M. Driver, utmne J. Bustamante, uk L. Buck, L. Buck, roe M.DeL. Brooke, BBC od A.B. Bond, vulgaris Habitat affects escapebehaviourandalarmcallingincommon starlings hawk butnotinpigeons. approaching animalaffects decisionstoattackorescape. dragonflies andtheirprey. biomechanics andecologythroughpredator-preyinteractions:flightperformance of 1284. Comp. Physiol. paired bigbrownbats, Effects ofcompetitivepreycaptureonflightbehaviorandsonarbeampatternin peregrinus Rangers Foundation. escape. 1396. Johannesburg:BirdLifeSouthAfrica. Ornithological Congress fledging dependenceperiodofraptors.In Gold, (BirdsinSlowMotion) Motion) eot,V,Olni . aii . rccii .etal. evidence fromafieldstudy. A. Procaccini, G., Parisi, animal collectivebehaviordependsontopologicalratherthanmetricdistance: A., Orlandi, V., Lecomte, Library. IthacaNY: CornellLabofOrnithology. Available at:www.macaulaylibrary.org Bird Unpredictability in wadingbirds. and apostaticselection. Goshawk (AnimalCamera) ms (Potts,1984). L. M. (2009). 8 , 225-241. (1976). . Newtownmountkennedy, CountyWicklow, Ireland. (2013a). . Ibis (2013b). (1974). Escaperesponseofzebra Anim. Behav. (1969). A studyoftheferruginoushawk:adultandbroodbehavior. Δ (2006). (2007). Theevolutionofcolorpolymorphism:crypticitysearchingimages, and thegoshawk (1987). Radarobservationsofthestoopperegrinefalcon t Flying withtheFastestBirdsonPlanet:PeregrineFalconand The JournalofExperimentalBiology(2015)doi:10.1242/jeb.108597 =11 150 (2011). (1999). Ecologicalfactorsaffecting huntingbehaviourduringthepost- The EthologyofPredation . Oxford:ClarendonPress. 125 (1998). Ecologicalfactorsinfluencingtheoccurrenceof‘flashmarks’ Funct. Ecol. , 191-198. ohw MEGsakC nHa elTm (BirdsinSlow Goshawk BM8E-GoshawkCUonHeadRealTime Goshawk Slow-MotionPouncingonPreyShotwithPhantomHD ms, andthegoshawk’s reactionslaggedpreymotionby Painted Redstart(Myioboruspictus), , 191-204. Kingfisher Diving-Feeding 22, 711-722. Eptesicus fuscus Annu. Rev. Ecol.Evol.Syst. , Durban(ed.N.J.AdamsandR.H.Slotow),pp.1381- Naturwissenschaften J. Exp.Biol. . London:BBC. Proc. Natl.Acad.Sci.USA . Newtownmountkennedy, CountyWicklow, Ireland. (1978). Howhoverfliescomputeinterceptioncourses. 12, 339-346. Accipiter gentilis (1990). Opticflow-fieldvariablestriggerlandingin 215 (1988). . J.Exp.Biol. (2010). Preyorpredator?Bodysizeofan . Berlin:Springer. , 903-913. Danio Proceedings ofthe22ndInternational . Ibis 77, 142-144. , Vol. 2014. Woodbridge, ON:Earth Protean Behaviour. TheBiologyof ( 129 Brachydanio rerio 38, 489-514. 213 , 267-273. 105 ML Video 464938.Macaulay , 3348-3356. , 1232-1237. (2008). Interactionruling Behav. Ecol. ) 1.Stimulusfor (2012). Linking 21, 1278- Sturnus (2008). (2010). Living Falco J. h

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