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Page 1: A computer vision for animal ecology...computer vision can be used to study animal camouflage (Tankus & Yeshurun, 2009) and biomimicry (Yang, Wang, Liang, & Møller, 2016). For example,

J Anim Ecol. 2018;87:533–545. wileyonlinelibrary.com/journal/jane  | 533© 2017 The Author. Journal of Animal Ecology © 2017 British Ecological Society

Received:11April2017  |  Accepted:17October2017DOI:10.1111/1365-2656.12780

R E V I E W

A computer vision for animal ecology

Ben G. Weinstein

DepartmentofFisheriesandWildlife,MarineMammalInstitute,OregonStateUniversity,Newport,OR,USA

CorrespondenceBenG.WeinsteinEmail:[email protected]

HandlingEditor:LauraPrugh

Abstract1. Acentralgoalofanimalecologyistoobservespeciesinthenaturalworld.Thecostandchallengeofdatacollectionoftenlimitthebreadthandscopeofeco-logical study.Ecologistsoftenuse imagecapture tobolsterdata collection intime and space. However, the ability to process these images remains abottleneck.

2. Computervisioncangreatlyincreasetheefficiency,repeatabilityandaccuracyofimage review. Computer vision uses image features, such as colour, shape andtexturetoinferimagecontent.

3. Iprovideabriefprimeronecologicalcomputervisiontooutlineitsgoals,toolsandapplicationstoanimalecology.

4. I reviewed187existingapplicationsofcomputervisionanddividedarticles intoecologicaldescription,countingandidentitytasks.

5. Idiscussrecommendationsforenhancingthecollaborationbetweenecologistsandcomputer scientists and highlight areas for future growth of automated imageanalysis.

K E Y W O R D S

automation,cameratraps,ecologicalmonitoring,images,unmannedaerialvehicles

1  | INTRODUCTION

Observing biodiversity can be expensive, logistically difficult andtime-consuming.Manyanimalsarerare,secretiveandinhabitremoteareas. Animal presence and behaviour may vary over broad spatialand temporal scales, anddependon importantbut infrequentlyob-servedevents,suchasbreeding,predationormortality.Directobser-vationof these events can be disruptive towildlife, andpotentiallydangerous to observers.To reduce cost, labour and logistics of ob-servation,ecologistsareincreasinglyturningtogreaterautomationtolocate, countand identifyorganisms innaturalenvironments (Pimmetal., 2015). While image capture has greatly increased sampling,our ability to analyse images remains a bottleneck in turning thesedataintoinformationonanimalpresence,abundanceandbehaviour.Computervisioncanincreasethebreadth,durationandrepeatabilityofimage-basedecologicalstudiesthroughautomatedimageanalysis(Delletal.,2014;Kühl&Burghardt,2013;Pennekamp&Schtickzelle,

2013).Computervision is a formof image-based computer sciencethatusespixelvaluestoinferimagecontent(LeCun,Bengio,&Hinton,2015).Theatomicunitofdata in computervision is an imagepixelthat represents colour in the visible spectrum. Pixels are arrangedintogroupssuchthatpixelproximity,orientationandsimilaritycreatea group identity. Pixelvalues, and the resulting group identity,maychange among images to create a sequence of objects. By creatingrulesforthepixelcharacteristics,relationshipsandchangesthroughtime, computervisionalgorithmscan replace laborioushand-reviewofecologicalimages.

Thegrowthinecologicalimagedataisfuelledbyitseconomy,ef-ficiencyand scalability (Bowley,Andes,Ellis-Felege,&Desell, 2017;Dell etal., 2014). Massive repositories of image data are availablefor ecological analysis, uploaded from field-based cameras (Giraldo-Zuluaga,Gomez,Salazar,&Diaz-Pulido,2017;Swansonetal.,2015;Zhang,He,Cao,&Cao,2016)orcapturedbycitizenscientists(Deselletal., 2013;Joly etal., 2014). For example, researchgradedatasets

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from iNaturalist (675,000 images of 5,000 species,VanHorn etal.,2017) and Zooniverse (1.2million images of 40 species; Swansonetal.,2015),highlightthegrowthinhigh-qualityimagescapturedbyresearchersandthepublic.However,imagedatacollectionhasgreatlyoutpacedimageanalysistools.Whileahumanmaybebetteratfind-inganimals in time-lapsevideo (Weinstein,2015),orhaveagreaterknowledgeofbirdidentification(Bergetal.,2014),whenconfrontedwith100,000images,itisdifficulttofindthetime,organizationandconcentrationtovalidateeachimagemanually.Myaimistodescribetheongoingworkinutilizingcomputervisionforanimalecology,pro-videabriefdescriptionoftheconceptsthatunitecomputervisional-gorithms, and describe areas for collaboration and growthwith thecomputervisioncommunity.

2  | APPLICATIONS OF COMPUTER VISION TO ANIMAL ECOLOGY

Ecological computer vision has grown out ofmultiple disciplines,with contributions from computer science (Branson, Van Horn,Belongie,&Perona,2014),astronomy(Arzoumanian,Holmberg,&Norman,2005)andremotesensing(LaRue,Stapleton,&Anderson,2016).This article covers applicationsof computer vision to find,count and study animals in natural landscapes using images col-lected in the human visual spectrum.Applications from specimenmorphometrics, microscopy (Pennekamp & Schtickzelle, 2013)andanimaltracking in laboratorysettingsarereviewedelsewhere(Dell etal., 2014; Robie, Seagraves, Egnor, & Branson, 2017). Tofindarticles,IusedWebofSciencetosearchfor“ComputerVisionAND(EcologyORAnimals),”yielding284articles.Ithenperformedthreeadditionalsearchesforarticlesusingimageanalysistools,butlacking the computer vision label: “Automated species measure-mentAND images” (n=103), “Automated speciesdetectionANDimages” (n=126) and “Automated species identificationAND im-ages”(n=196).Finally,Ireviewedthefirst200resultsfromGoogleScholarfor“ComputerVisionANDecology”publishedsince2000.For all searches, articles were included based on the followingcriteria.

1. The article described a peer-reviewed application of computervision. Articles introducing hardware for image capture, or re-viewing existing applications, were excluded.

2. Thearticlewasaimedatansweringanecologicalquestion,broadlydefinedas the identity,demographyandbehaviourofanimals innatural environments using images collected in human visualspectrum.

3. Theapplicationusedanautomatedorsemi-automatedimageanal-ysis algorithm. Articles using manual review of images wereexcluded.

Thissearchandfilteringcriteriaresultedin187articles,withconsis-tentgrowthincomputervisionapplicationsovertime(Figure1).Thesearticlesusedavarietyofopensourcetoolstoaidimageanalysis(Table1).

Iorganizedarticlesaroundthreecommontasksforecologicalcomputervision:description,countingandidentification(Figure2).Fromtheper-spectiveofimage-basedcomputervision,descriptionisthequantifica-tionofthecoloration,patterningandrelativesizeofanimalsandtheirimmediatesurroundingenvironment.Countingisthedetectionandenu-merationofanimalswithinanimage.Identityistheclassificationofanindividualorspeciesbasedonitsappearance.Foreachofthesetasks,mygoalistohelpecologistsgraspthecurrentpossibilityforimageau-tomationbyintroducingbasicterminology,applicationsandhighlightingacasestudy.

3  | DESCRIPTION

Ecologistoftenseektounderstandanimalappearanceandtheir re-lationshiptothesurroundingenvironmentusingdigitalobservations.Thesecretivenatureofmanyanimalsmakesdirectdescriptiondisrup-tiveandpotentiallydangeroustoboththeorganismandresearcher.Computer vision algorithms have greatly increased the ability tonon-invasively measure organisms through image analysis (n=56).Toascertainthesize,positionandspectralcharacteristicsofecologi-calobjects in images,computervisiontoolsuse imagefeatures (seeBox1)tofindimportantpixelswithinandamongimages.Imagefea-turesareoftenareasofhighturnoverinpixelvalues,causedbyedgesofobjectsofinterest.Forexample,tocorrectlyoutlineaflyingbird,algorithmsmight look for theareaswhere thewings intersectwiththesky(Atanbori,Duan,Murray,Appiah,&Dickinson,2016).Imagefeatureshavebeenprimarilyusedtostudytheevolutionaryecologyof animal coloration (Stoddard, Kilner, & Town, 2014), shape (Lavyetal.,2015)andpatterning(Levy,Lerner,&Shashar,2014).Comparedto human review, computer vision provides amore consistentwaytoscoreanimalappearanceacross imagesbyusingnon-RBGcolourspaces, such asHSVorYChCr,which are less sensitive to changesin illumination and other image artefacts (Kühl & Burghardt, 2013;Troscianko,Skelhorn,&Stevens,2017).Bycomparingimagefeatures,computer vision can be used to study animal camouflage (Tankus& Yeshurun, 2009) and biomimicry (Yang, Wang, Liang, & Møller,2016).Forexample,Stoddardetal.(2016)developededgedetectionalgorithms toevaluate the relative camouflageofnesting shorebirdspeciesascomparedtotheirnestingsubstrate(Figure3b).

Imagefeaturescanalsobeusedtomeasuresizeinbothspecimensand free-living animals (Olsen &Westneat, 2015). Based onmulti-ple images frompairs of cameras, computervision tools have beenusedtodescribeanimalsizeandshape,suchasinwhales(Howland,Macfarlane, & Tyack, 2012), and coral (Jones, Cantin, Berkelmans,Sinclair, & Negri, 2008; Naumann, Niggl, Laforsch, Glaser, &Wild,2009).Thenextfrontierfor image-basedecologicaldescription is in3Dreconstructionofmorphologyandmovement (Haggag,Abobakr,Hossny,&Nahavandi,2016;Lavyetal.,2015).Three-dimensionalim-aginghasrecentlybeenusedtotrackanimalbehaviourwithinlargein-doorenclosures(e.g.Barnardetal.,2016),andapplyingthesetoolstoanimalsinnaturallandscapesisandevelopingareaofresearch(Robieetal.,2017).

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F IGURE  1 Thegrowthincomputervisionapplicationsovertime(n=187).Fromtheperspectiveofimage-basedcomputervision,descriptionisthequantificationofimagefeaturestodescribecoloration,patterningandrelativesizeofanimalsandtheirsurroundinghabitat.Countingisthedetectionandenumerationofanimalswithinanimage.Identityistheclassificationofanindividualorspeciesbasedonitsappearance

TABLE  1 Commonlyusedtoolsforcomputervisionapplicationtoecology

Name Reference Task Comments

OpenCV Bradski(2000) Description,Counting,Identity

Sourcelibraryforcomputervisionalgorithmsinpython/java/C++

ImageJ Abràmoffetal.(2004) Description,Counting Segmentationandthresholding

BISQUE Kvilekvaletal.(2009) Description,Counting Alsoservesasahostingplatformforimageanalysistools

AgisoftPhotoscan – Description Commercialsoftwarefor3Dmodelreconstructionfromimages

StereoMorph OlsenandWestneat(2015) Description Rpackagefor3dreconstructionandimagecalibration

NaturePatternMatch Stoddardetal.(2014) Description Comparingfeaturesamongecologicalimages

MotionMeerkat Weinstein(2015) Counting Backgroundsubtractionforanimaldetectioninvideosandimages.

GoogleCloudAPI – Identity ClassificationofimagecontentusingCloudVisionAPI,deeplearningsourcelibraryusingTensorFlow

Merlin VanHornetal.(2015) Identity BirdidentificationappforiPhoneandAndroid

Wildbook Cralletal.(2013) Identity Individualidentificationanddatamanagementtools

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3.1 | Case study: High- resolution mapping of penguin colonies using structure- through- motion

To map habitat suitability, ecologists often use remotely sensed en-vironmentalvariablesasaproxy for theenvironmentalconditionsen-counteredbyanimals.Whiletraditionalremotesensingcapturescoarse

changesinhabitatquality,animalsexperiencetheenvironmentatfine-scales,inthreedimensions,andfromalandscapeperspective.McDowalland Lynch (2017) generated ultra-fine scale (<1cm)maps of penguincoloniesbystitchingtogetherthousandsofoverlappingimagesusingatechniquecalledstructure-from-motion.Theresultingthree-dimensionalsurfaceallowedfine-scalemappingofGentoopenguin(Pygoscelis papua)

F IGURE  2 Thenumberofecologicalcomputervisionarticles(n=187)foreachfocaltaxaandcomputervisiontask.Fromtheperspectiveofimage-basedcomputervision,descriptionisthequantificationofimagefeaturestodescribecoloration,patterningandrelativesizeofanimalsandtheirsurroundinghabitat.Countingisthedetectionandenumerationofanimalswithinanimage.Identityistheclassificationofanindividualorspeciesbasedonitsappearance

Box 1 Glossary of key computer vision terms for ecological image analysis

Description

Features:Pixelpropertiesbasedonthecolour,texture,orrelationshiptosurroundingpixels.

Colour space:Numericsystemusedtodescribethespectralinformationcontainedinpixelvalues.

Edges:Imagelocationswithabruptchangesinpixelvalues,alsoknownas‘corners’.Oftenusedtofindcorrespondingpointsbetweenimages.

Structure-from-motion:Approachforreconstructingthe3Dstructureofastationaryobjectbasedonstitchingtogetherimagestakenfrommultipleangles.

Optical flow:Theidentificationofanalogouspixelsamongimages,usedtotrackobjectorcameramovement.

Counting

Segmentation:Theprocessofpartitioningimagesintolabelledregions.

Contours:Curvedlineswhichencompassconnectedpixelswithsimilarcolour,intensityortexture.

Blobs:Groupsofconnectedpixelswithafixedidentityorlabel.

Image morphology:Imageprocessingtoolsformanipulatingpixelsbasedonthevaluesofthesurroundingpixels.Forexample,‘opening’reducesnoiseintheforegroundbyremovingweaklyconnectedpixels.

Background subtraction:Theremovalofirrelevantcontentestimatedfrommultipleframesofvideo.Subtractingthestaticportionsoftheframefromthecurrentimageyieldstheestimatedforegroundobjects.

Identity

Labelled training data:Imageswithknownobjectsofintereststhatcanbeusedtotrainmachinelearningclassifiers.

Unsupervised classification:Multidimensionalclusteringalgorithmstodividepixelsintoanapriorinumberofgroupsbasedonimagefeatures.

Neural-network or ‘deep learning’:Ahierarchicalmachinelearningclassifierthatusestrainingdatatocategorizeimagecontentwithoutapriorispecificationofimagefeatures.

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nests andcapturedvariation in slopeandaspect thatmayhavebeenmissedbycoarsersatellite-basedremotesensing(Figure3a).

4  | COUNTING

While remotely placed cameras provide a low-cost alternative tohumanobservers,theamountofdatageneratedbyfieldstudiescanbeoverwhelming.Thepotentiallyhighcostofimagereviewandstor-agemeansthatfindingtheanimalsofinterestwithinlargebatchesofimages can improve the speed and efficiency of biodiversitymoni-toring.Evenmotion triggeredcamera trapssuffer frommany false-positive images due to wind and moving vegetation. In computervision,findingnovelobjectswithinseriesofimagescanbeachievedusingbackgroundsubtraction,whichdistinguishessedentaryobjects,suchastreesandclouds,frommovingobjects,suchasanimals,withinvideosorgroupsofimages(PriceTacketal.,2016;Ren,Han,&He,2013;Weinstein,2015) (Figure4a).Abackgroundmodel is created

bycomputinganexpectedimagebasedonthepreviouspixelvalues(Stauffer&Grimson,1999).Theforegroundmodeldescribesthenon-backgroundpixelsasafunctionofthedifferencebetweentheprevi-ousbackgroundmodelandthecurrentframe(Figure4a;Christiansen,Nielsen, Steen, Jørgensen, & Karstoft, 2016; Sobral & Vacavant,2014).Thebackgroundmodelchangesovertimebasedonnewpixelvalues, thereby reducing false positives from shifts in illuminationandexternalmovement,suchaswind,wavesorcamerashake.Onceimages have been divided into foreground and background pixels(knownassegmentation),objectsarepartitionedintodiscretegroups,withconnectedsetsofpixelscorrespondingtoindividualorganisms.

Ifound55articlesthatusedaformofbackgroundsubtractiontode-tectandcountanimals,primarilyformammals(n=24)andbirds(n=22).Thesestudiesreporthighaccuracyinremovingemptyframes,buttherewerepersistentchallengesinreducingfalsepositivesfromstrongwindandotherextraneousmovementinheterogeneousenvironments(PriceTacketal.2016).Tailoringdetectionalgorithmsto individual taxacangreatly improve accuracy, for example, Zeppelzauer (2013) reported

F IGURE  3 Applicationsofcomputervisiontodescribingecologicalobjects.(1)FromMcDowallandLynch(2017),athree-dimensionalmapofthePortLockroypenguincolonywascreatedbyoverlayinghundredsofindividualphotographs(1a)todescribethelocationofGentoopenguin(Pygoscelis papua)nests(1b).Flagsdenoteoccupiedpenguinnestsidentifiedintheimages.Thesurfacewasturnedintodigitalelevationmap(1c)tomeasuretherelativepositiveandhabitatchoicebyindividualpenguinsfornestsiteselection.(2)FromStoddardetal.(2016),snowyplover(Charadrius nivosus)nestclutch(2a)segmentedintoeggandbackgroundregions(2b),edgedetectionwasusedtoquantifyedges(2c),inordertocalculatethedegreeofeggcamouflagecomparedtothebackgroundsubstrate(2d).SeeAcknowledgementsforcreditsandpermissions [Colourfigurecanbeviewedatwileyonlinelibrary.com]

(a) (b) (c)

(a) (b) (c) (d)

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>95% accuracy in detectingAfrican elephants (Loxodonta cyclotis) bybuildingacolourmodelfromtrainingdata.State-of-the-artapproaches(Renetal.,2013;Zhangetal.,2016)canbothidentifyimagesofinterest,aswellasdefinewherewithinanimageananimaloccurs.Thisisacrucialfirststepincroppingphotostoanalysespeciesidentity(seebelow).

New computer vision tools have opened new avenues for imagedatacollection.Automatedcountdatahavebeentakenfromtime-lapsevideo (Steen&Ski, 2014), camera traps (Matuska,Hudec,Kamencay,Benco,&Zachariasova,2014),uploadedbycitizenscientists (Kosmalaetal.,2016)andcapturedfromairbornesensors(vanAndeletal.,2015).In particular, automateddetection algorithms are increasingly used tofind large animalswithin remotely sensed imagery captured by high-resolutioncommercial satellites (Barber-Meyer,Kooyman,&Ponganis,2007)andunmannedaerialvehicles(Hodgson,Kelly,&Peel,2013;Liu,Chen,&Wen,2015;vanAndel etal., 2015).Commercial satellite im-ageryofferswidespatialcoverageatsub-metre resolution,but is lim-ited by atmospheric conditions, temporal coverage and high cost. Tofindanimalswithinthisimagery,studieshaveusedpixel-basedanalysis(Fretwell,Staniland,&Forcada,2014), imagedifferencing(LaRueetal.,2015)andsupervisedclassificationusingmachinelearning(Yangetal.,2014).Severalapplicationsfocusonaggregationsofindividualsincolo-nialbreedingsitesduetotheirlargespatialsizeanddistinctvisualsigna-tureonthesurroundingenvironment(Barber-Meyeretal.,2007;Lynch,White,Black,&Naveen,2012).WhileresultsfromSouthernrightwhales(Eubalaena australis)(Fretwelletal.,2014),polarbears(Ursus maritimus)(LaRueetal.,2015),andsavannaungulates(Yangetal.,2014)highlightthepromiseof this technology,considerableautomation isneeded to

reduce the laborious handvalidation of images at scale (LaRue etal.,2016).

Incomparison to satellite-based imagery,unmannedaerialvehicleshavetheadvantagesofgreatertemporalflexibilityandlowcost(Seymour,Dale,Hammill,Halpin,&Johnston,2017).Thetrade-offisthedecreasedspatial extent limited by flight time and legal restrictions (Crutsinger,Short,&Sollenberger,2016).UAVshavebeensuccessfullyusedtocountwaterbirdpopulations,duetothebirds’openhabitatandcolonialbreed-ingstrategy (Descamps,Béchet,Descombes,Arnaud,&Zerubia,2011;Groom, Krag Petersen, Anderson, & Fox, 2011). Chabot and Francis(2016)reportedthatautomatedcountsofwaterbirdswerewithin3%–5%ofhumancountsacross16applications.RecentimprovementsofUAV-basedcountingincludeutilizinghyperspectraldata(Beijboometal.,2016;Witharana&Lynch,2016),pixel-shapemodelling (Liuetal.,2015)andcombiningbackgroundsubtractionwithmachinelearning(Torneyetal.,2016)(Figure4b).Recenteffortstocountanimalsusedeeplearningneu-ralnetworksarepromising,butrequiretensofthousandsoftrainingim-agesgatheredbyhumanannotation(Bowleyetal.,2017).

4.1 | Case study: Counting hummingbird–plant interactions using background subtraction

Topredict therules thatdeterminethe interactionsamongspecies,ecologistsoftenusethefrequencyofinteractionsasaproxyforfit-ness effects (Bartomeus etal., 2016). To determine the number ofvisitsbetweenbirdsandflowers,WeinsteinandGraham(2017)usedtime-lapse cameras to filmmultiple days of flower visitation.Using

F IGURE  4 Applicationsofcomputervisiontodetectingandcountingecologicalobjects.(a)Backgroundsubtractionofvideoframesyieldsthedesiredmotionobject(Weinstein,2015)basedonchangesinpastpixelvalues.(b)CountingwildebeestfromimagerycapturedbyunmannedaerialvehicleinTanzania(Torneyetal.,2016).Theleftpanelarecorrectidentificationsofwildebeest,therightpanelarefalsepositivescausedbyaflockofjuvenileostrich.SeeAcknowledgementsforcreditsandpermission[Colourfigurecanbeviewedatwileyonlinelibrary.com]

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background subtraction algorithms, theywere able to process over8,000hr of hummingbird visitation videos (Weinstein, 2015). Thisvideo-based strategy allowed sampling at much greater temporalextents, and thereforeminimized thepotential foroverlooking rareinteractions.Fromthesedata,theauthorsmodelledspeciesinterac-tionsbasedonmorphologicalsimilarityandflowerabundancetotestpredictionsofoptimalforagingtheory(Weinstein&Graham,2017).

5  | IDENTITY

Ecologistsoftenneedtoinventorythediversityoftaxaorthenumberofindividualsofagivenspeciesinageographicarea.Thestrongre-lationshipbetweensamplingdurationandobservedspeciesrichnessmeans that data collection can often be expensive and logistically

challenging.Image-basedanimalclassificationhasthepotentialtore-ducecosts,allowgreatergeographiccoverageandcauselessdistur-bancetopotentiallysensitiveecosystems.

For individual-level identification, computervision algorithms useimagesofknownindividualstomatchnewimagesbasedonthesimilar-ityofphenotypicpatterns(Figure5a).Bymatchingtheimagefeaturesamongimages,matchingalgorithmsscorethe likelihoodthattwoim-agesareofthesameindividual.Foranimalswithuniquemarkings,thiscanbea low-costalternative toexpensive trappingand taggingpro-grams.Thisapproachwaspioneeredforfluke identification inmarinemammals (Adams,Speakman,Zolman,&Schwacke,2006;Beekmans,Whitehead, Huele, Steiner, & Steenbeek, 2005; Gilman, Hupman,Stockin,&Pawley,2016)andhassincebeenappliedonawiderangeoftaxa,fromzebras(Equus grevyi)(Crall,Stewart,Berger-Wolf,Rubenstein,& Sundaresan, 2013), to elephants (L. cyclotis) (Ardovini, Cinque, &

F IGURE  5 Applicationofcomputervisiontopredictingindividualandspeciesidentity:(a)Matchingalgorithmsscorethesimilarityofphotographedzebrastoalibraryofknownimagestotrackindividualsovertime(Cralletal.2013).(b)FromMarburgandBigham(2016),adeeplearningclassifieristrainedonastarfishspeciesclassbasedontrainingdataoflabelledimages.Theclassifieristhenusedtopredicttestingdatatoevaluatetheaccuracyoftheapproach.Inthisexample,thetrainingandtestingdataareseparateobjectswithinthesameimageframebasedonboundingboxesthatdistinguishanimalsfromtheimagebackground.SeeAcknowledgementsforimagecreditsandpermissions[Colourfigurecanbeviewedatwileyonlinelibrary.com]

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Sangineto, 2008), and box turtles (Terrapene carolina) (Cross, Lipps,Sapak,Tobin,&Root,2014).Thesemethodsareeffectiveinidentifyinganimalswithcomplexmarkings,suchasgiraffes(Giraffa camelopardalis)(Bolger,Morrison,Vance,Lee,&Farid,2012),whalesharks(Rhincodon typus)(Arzoumanianetal.,2005)andcatfish(Rineloricaria aequalicuspis)(Dala-Corte,Moschetta,&Becker,2016),and range fromcompletelyautomated(Town,Marshall,&Sethasathien,2013),toinvolvinghumanfeedback duringmatching (Duyck etal., 2015). Crall etal. (2013) re-portedaccuracyratesrangingfrom95%forGrey’szebras(E. grevyi)to100%forjaguars(Panthera onca)usingtheHotSpotteralgorithm,whichcanbeaccessedthroughtheWildbookwebplatform.

Automatedspeciesidentificationisrapidlydevelopingfieldwithanex-plosionofnewapproachesandpromisingresults(Figure5b).Whileinitialattemptsfocusedontraditionalmachinelearningwithanaprioridivisionofimagefeatures(e.g.Blanc,Lingrand,&Precioso,2014;Lytleetal.,2010),the accuracy of these approacheswas generally low (>70%).However,recentadvancesusingnewdeeplearningmodelshavegreatlyimprovedmodel performance across a wide variety of animal taxa, from coral(Beijboometal.,2016)to largemammals (Gomez,Diez,Salazar,&Diaz,2016) (Table2).Themajorityofapplications I reviewedhadaparticulargeographicfocus,forexampletherodentcommunityoftheMojavedes-ert(Wilberetal.,2013).Thenextstageisageneraltestofmachinelearn-ingmodelsacrosssystemstofindtheoptimalnumberoftrainingimages,modelparametersandtherequiredspectraldiversityofpotentialclassesthatleadstoincreasedpredictiveperformance(VanHornetal.,2015).

5.1 | Case study: Merlin, a bird identification app powered by deep learning neural networks

The Merlin project demonstrates the potential for revolutionarychangeinecologicalidentification(Farnsworthetal.,2013).Merlin

is the joint project from Visipedia and the Cornell Laboratory ofOrnithology to identify600commonNorthAmericanbirdspecies(VanHornetal.,2015).The identificationalgorithmusesGoogle’sTensorFlowdeep learningplatform,aswellascitizensciencedatafromeBirdtogeneratepotentialspecieslistsgivenauser’slocation(Bransonetal.,2010).WhileMerlinisprimarilygearedtowardsciti-zenscientists,pairingthistechnologywiththegrowingnumberofpublicallyaccessiblephotos(e.g.iNaturalist.org)promisestobolsterobservationsofrareandcrypticspeciesforbiodiversitymonitoring.

6  | COLLABORATION WITH COMPUTER VISION RESEARCHERS

Thecombinationofhigh-qualitydata,appliedusecasesandinterestingproblemswillleadtoproductivecollaborationsamongecologistsandcomputervisionresearchers.Whilecomputervisiontoolsarebecom-ingmoreaccessibletoecologists,state-of-the-artsolutionswillbenefitfromcollaborationwiththecomputervisioncommunity.Findingandmaintainingthesecollaborationscanbedifficultgiventhedifferenceinterminologyandaimsofecologistsvs.computerscienceresearchers.Isuggesthighlightingthreeareasofpotentialmutualinterest:

1. Ecology has intriguing and challenging technical problems. Thenatural world is complex and heterogeneous. Changes in illu-mination and backgrounds make animal detection difficult.Changes in organism appearance and shape are challenging forclassification algorithms. Ecologists should emphasize the gen-erality of their proposed problem, and frame collaborations asa potential area for development of new algorithms, ratherthan as an applied example.

ReferenceTraining images Taxa

Species or classes

Average accuracy (%)

Wilberetal.(2013) 5,362 Mammals,Reptiles 7 76.4

Yuetal.(2013) 22,533 Mammals 18 83.8

Chen,Han,He,Kays,&Forrester(2014)

9,530 RainforestMammals

19 38.3

Hernández-Sernaetal.(2014)

1,800 Fish,Butterflies 32 92.87

92 11 93.25

Atanborietal.(2016) – Birds 7 89.0

Bergetal.(2014) Avg.of200perspecies

Birds 500 66.6

Beijboometal.(2016) 28,400 Coral 10 88.9

Marburg&Bigham(2016) 8,586 Benthicinverte-bratesandfish

10 89.0

Gomezetal.(2016) 14,346 Savannaanimals 26 88.9

Qin,Li,Liang,Peng,&Zhang(2016)

22,370 Fish 23 98.6

Villonetal.(2016) 1,400 Fish 8 65.8

Sunetal.(2017) 9,160 Fish 15 77.27

Fengetal.(2016) 4,530 Moths 50 53.12

TABLE  2 Evaluationstatisticsforrecentcomputervisionapplicationstopredictingspecies-levelidentity.Articlesshownonlyincludeapplicationstomorethanfivespeciesandquantifiedtheclassificationaccuracyusingatestingdataset.Accuracyisonlyreportedforthebestperformingmodelineachpaper.Articlesareorderedbypublicationdate

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2. Ecologists can improvecomputervisionalgorithmsbyprovidingbiological context (Berg etal., 2014). Ecological rules that mayseemtobecommonsense,suchas“thereshouldnotbefishonland,”requireneuralnetworkstoidentifybothobjectsinanimage(“fish”),scenecontext(“land”)andtherelationshipbetweenimagefeatures.Onewaytoovercomethiswouldbetocumbersomelytrainanalgorithmwiththousandsofimagesoflandwithoutfish.Ecologyprovidesamorestraightforwardandeffectivemethodbyusingimagemetadata,suchastimeorlocation,toassistinimageclassification.Forexample,combiningimagelocationwithexpertvettedspeciesregionalchecklistsmightshowthatonlyafewspe-cies with a given coloration occur in given location. Similarly,imagecontextcanassistfuturepredictions.Forexample,ifanal-gorithmidentifiesawildebeestinanaerialimage,itmaybemorelikelytoalsofindzebras(Swansonetal.,2015).Finally,ecologicalcontextcanreducetheburdenofgatheringtrainingdatabyex-ploitingtheinherentconservationofbodyplansamonganimalstocreatehierarchicallabels.Ratherthanthinkingofallpotentialin-dividualcategories(e.g.blackbear,grizzlybear,polarbear,etc.),hierarchical labellingexploits theconnectionsamonganimals tocreatenestedcategories(e.g.Ursus).Tree-basedclassificationap-proacheshavebeeneffective inotherareasofcomputervision,

andfitsnaturallywiththestudyofevolutionarytaxonomy(Favret&Sieracki,2016).

3. Ecologistsarecollectingvastamountsoflabelleddata.Computervision applications, and especially deep learning approaches, re-quire significant training and testing data. High-quality datasetsaredifficulttofind,andalackoflabelleddataisamajorobstacleincomputer vision research (Belongie&Perona, 2016;Berg etal.,2010;Gomezetal.,2016).Packagingimagedatasetsandmakingthempubliclyavailablewill raiseawarenessof theopportunitiesforecologicalcollaboration.

7  | FUTURE GROWTH

Thefutureofecologicalcomputervisionwillcombinenewalgorithms,data and collaborations to study animals in natural environments.The rise of neural networks as the central tool in image classifica-tion(Gomezetal.,2016;LeCunetal.,2015),backgroundsubtraction(Christiansenetal.,2016)andimagedescription(Mohanty,Hughes,&Salathé,2016) is akeydevelopment thatwithbringnewoppor-tunitiesforecologicalcomputervision(Figure6).Untilrecently,thegrowthofthesetoolshasbeenslowedbyalackofaccesstocutting

F IGURE  6 Overviewofaneuralnetworkformachinelearningprediction:(a)Pixelconvolutionscreatecombinationsofinputpredictorsbydownsamplingandpoolingimagefeatures,(b)agenericdeeplearningstructure,inputdatapassesthroughhiddenlayers,callednodes,tocreatepathwaysfrompredictorstoprediction.Theactivationscoreateachofthesenodesisusedtoestimatemodelweights.Incurrentdeeplearningapplications,therewillbemanyhiddenlayersofnodestocreatecombinationsofinputpredictors[Colourfigurecanbeviewedatwileyonlinelibrary.com]

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edgealgorithms.TherecentunveilingoftheGoogleCloudMachineLearningplatformcouldbeaquantumleapinaccessforecologists.Releasedin2016,GooglegivesusersaccesstoawebservicetoretrainmodelsusingGoogle’spopularTensorFlowsoftware.TensorFlowisacomputationalgraphalgorithmthatrepresentsmathematicalopera-tionsasnodesandstoresdatainmultidimensionalarrays.Ratherthanbuildingamodelfromscratchforeachapplication,userscanretrainpre-builtmodelstoaddnewimageclasses.Knownastransferlearn-ing,thisapproachusesthestrengthsoftheunderlyingarchitecture,butaddsflexibilityforspecializedproblems.Thisgreatlyreducesthetimeandexpertiseneededtoimplementimageanalysissolutions.

Apersistentchallengeincomputervisionapplicationsiscollectingsufficientlabelleddata(Bergetal.,2010).Newdatacollectionoppor-tunities through datamining (Zhang, Korayem, Crandall, & Lebuhn,2012)andcitizenscientistswillbroadenthepotentialsourcesof la-belled ecological data (Swanson, Kosmala, Lintott, & Packer, 2016).Thenaturalexcitement forplantsandanimalsmeansthatgatheringfurtherlabelleddataispossiblethroughonlinecitizenscientistefforts(VanHornetal.,2015).Inparticular,projectsontheZooniverse,iNat-uralistandWildlife@homewebplatformsprovideawayofengagingimportantusercommunities(Deselletal.,2013;Kosmalaetal.,2016).Thenextstepisintegratingcitizenscientistsasapartofgreaterau-tomation, ratherasanalternative toautomation.Knownas “humanin loop”approaches,thisstrategycan learndirectlyfromhumanan-notations to provide feedback and recommendation for future datalabelling(Bransonetal.,2010;Reda,Mateevitsi,&Offord,2013).Thiswillcombinetheexpertiseandexcitementfromcitizenscientists,withthegreaterstandardizationofautomation.

ACKNOWLEDGEMENTS

Iwouldliketothankmanyresearchersfortheircontributionstothisreview: JasonParham (Figure5a), andAaronMarburg (Figure5b)contributedunpublishedfigures.FiguresfromTorneyetal.(2016)andStoddardetal. (2016)wereusedunderthePlosOneCreativeCommons License. Thanks to Shanis Barnard, DrewWeber,WillPearse, Margaret Kosmala, Tanya Berger-Wolf, Chuck Stewart,J. J. Valletta and Oscar Beijboom for their helpful input. Themanuscript was improved by the assistance of two anonymousreviewers.Themetadata for the reviewed filesaswell as the re-sults of each of the fourWeb of Science searches are providedin theSupporting Information.Theauthordeclaresnoconflictof interest.

DATA ACCESSIBILITY

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.b700h(Weinstein,2017).

ORCID

Ben G. Weinstein http://orcid.org/0000-0002-2176-7935

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SUPPORTING INFORMATIONAdditional Supporting Information may be found online in thesupportinginformationtabforthisarticle.

How to cite this article:WeinsteinBG.Acomputervisionforanimalecology.J Anim Ecol. 2018;87:533–545. https://doi.org/10.1111/1365-2656.12780


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