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Lauren M. Robinson Alexander Weiss Editors Nonhuman Primate Welfare From History, Science, and Ethics to Practice Nonhuman Primate Welfare Lauren M. Robinson (cid:129) Alexander Weiss Editors Nonhuman Primate Welfare From History, Science, and Ethics to Practice Editors LaurenM.Robinson AlexanderWeiss WolfScienceCenter SchoolofPhilosophy,Psychologyand UniversityofVeterinaryMedicineVienna LanguageSciences,DepartmentofPsychology Vienna,Austria UniversityofEdinburgh Edinburgh,UK LanguageResearchCenter GeorgiaStateUniversity KyotoUniversity,WildlifeResearchCenter Atlanta,GA,USA Kyoto,Japan ISBN978-3-030-82707-6 ISBN978-3-030-82708-3 (eBook) https://doi.org/10.1007/978-3-030-82708-3 #SpringerNatureSwitzerlandAG2023 Thisworkissubjecttocopyright.AllrightsarereservedbythePublisher,whetherthewholeorpartofthe materialisconcerned,specificallytherightsoftranslation,reprinting,reuseofillustrations,recitation, broadcasting,reproductiononmicrofilmsorinanyotherphysicalway,andtransmissionorinformation storageandretrieval,electronicadaptation,computersoftware,orbysimilarordissimilarmethodology nowknownorhereafterdeveloped. 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Theregisteredcompanyaddressis:Gewerbestrasse11,6330Cham,Switzerland To Charlie and Danny —Alexander Weiss To Imogene, Sammie, and Terri —Lauren M. Robinson Preface Bothanimalsandcaretakersarelikelytobenefitfrompositivefeedbackfromoneanother. Engagingininteractionsthatarepleasantforbothcaretakersandtheanimalsarelikelyto createabetterworkenvironmentforcaretakersandtohelpinstillpositiveattitudesregarding theanimalstheycarefor.1 —CorriD.Waitt(1975–2014) ThisbookoriginatedinaphotocontestthatwasheldbySpringerandthatthefirst editorhadenteredinto.DuringconversationswithSpringerthattookplaceafterthe contestwasover,itemergedthataneditedbookonnonhumanprimatewelfarewas lackingfromtheircollection.SoonaftertheseconversationswithSpringer,thefirst editorcontactedpotentialauthorsandfoundthattherewereenoughpeoplewillingto contributechapters.Aproposalwaswritten,andSpringeracceptedtheproposal. Thetopicofanimal welfare isbroad andcutsacrossdisciplines. Therefore,two goalsguidedourchoiceofauthorsandareastocover.Thefirstgoalwastoprovidea resource for people who work with nonhuman primates. As such, we sought out a widerangeofexpertswhocouldwriteabouttopicsrelatedtothewelfareofprimates indifferentsettings,suchasinlaboratories,zoos,andsanctuaries,andprimatesfrom different backgrounds, including those kept as pets or used in the entertainment industry.Thesecond,related,goalwastoprovidearesourceforpeoplewhoguideor shapepolicyon,orengenderdebatesabout,theproperuseandcareofprimates(note thatwefullyexpectthatthesetwoaudienceswilloverlap!).Totheseends,wesought out chapters from philosophers, ethicists, legal scholars, and both advocates and adversariesoftheuseofnonhumanprimatesinresearch.Finally,insupportofthese goals, we recruited authors whose chapters would provide historical overviews for these other chaptersandtried tofind authors willing to write about the situation in countries other than the USA, member nations of the European Union, and other countriesinEurope,suchastheUK.Wehopethatthereadersofthisbook,including thosethatwedidnotmention,andespeciallystudents,willagreethatwehavebeen modestlysuccessfulinachievingourgoals. 1TakenfromWaittC.etal.(2002).Theeffectsofcaretaker-primaterelationshipsonprimatesinthe laboratory.JApplAnimWelfSci5(4),309–319.https://doi.org/10.1207/S15327604JAWS0504_05 vii viii Preface Ofcourse,aswithTop10lists,weexpectthatopinionswilldifferwithregardto what we did and did not include in this book. In particular, we expect that some chapters and/or their authors will raise some readers’ hackles. We therefore feel compelledtoexplainourreasonsfor including these chaptersand/orinvitingthese authors.Wedecidedearlyonthatthereadersofthisbookwouldbebestservedifwe providedabroadrangeofviewpointsandsowegavealloftheauthorsthefreedom topresenttheirviewsandsteppedinonlytoprovideguidanceandfeedbacksothat theirchaptersarethebestrepresentationsofthoseviews.Wethinkthatreaders,upon closerconsideration,willagreethatthepotentialfortheseuncensoredviewstospark debatewillengagenon-expertsandultimatelybenefitcaptivenonhumanprimates. A few notes of thanks are in order. This book could not have been completed without the contributions of the authors. Their hard work and patience are much appreciated. We also gratefully acknowledge the assistance from the editors at Springer. They were always on hand to answer our questions. In addition, a considerableportionofAlex’sworkonthebookandchapterwascompletedduring a Visiting Professorship at the Kyoto University Wildlife Research Center. He thanks his hosts, and especially Professor Miho Inoue-Murayama, for their help andformakingthiswonderfulopportunitypossible. Sincehumansbegantokeepprimatesincaptivity,humanshavemadevaststrides in understanding their cognitive abilities, social bonds, and personalities. We hope that the science, practice, information, and wisdom presented in this book will go some way in ensuring that, whether they are in our care or not, these evolutionary cousinsofourswillleadgoodlives. Finally,apersonalnoteontheepigraph.CorriWaittwasanAmericanwhohad cometotheUKin1998tostudyprimatebehaviorandwelfareattheUniversityof Stirling.CorriandI(AW)wereintroducedbyamutualfriend,andCorriwasoneof thefirstpeopleoutsideofEdinburghthatImetafterImovedtotheUKin2005. EverysooftenCorrihadanearlymorningflighttocatch.Ontheseoccasions,she wouldaskifshecouldstayinthesparebedroominmyflaton11JohnstonTerrace, where I lived at the time. I was always happy to have her over. On most of those visits,westayedinmysittingroom,fromwhichonecanseeEdinburghCastle,and wewouldchat.Iwoulddrinkteawithlemonandsugar,andIdonotrecallwhether shejoinedmeornot(itisfunnyandtragichowminordetailssuchasthesefadeso quickly, especially as they are what we end up treasuring). Corri was terrific company.IlearnedalotaboutlifeintheUKandmanyotherthings.Ialsolearned thatshewasbrightandwarmandhadaterrificsenseofhumorandthatshewaskind, sweet,anddedicatedtobeingdecenttoeverybody,humanandnonhumanalike. Corrilostherlifetoanaggressiveformofcancerin2014.Everybodywhoknew her, including some of the contributors to this book, knows what a loss her death was.IdidnothaveCorriinmindwhenIagreedtoco-editthisbook,butifshewas alive,IwouldhaveinvitedCorritocontributeachapter.Unfortunately,thatwasnot Preface ix tobe.AllIcandonowistohopethatthisisthebookthatCorriwouldhaveenjoyed readingandthat,bysharingthesememories,Iamkeepingherspiritalive. Vienna,Austria LaurenM.Robinson Kyoto,Japan AlexanderWeiss Contents PartI HistoryofNonhumanPrimatesinCaptivityandPrimateWelfare inDifferentSettings TheHistoryofPrimatesinZoos. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 GeoffHosey TheHistoryofChimpanzeesinBiomedicalResearch. . . . . . . . . . . . . . . 31 PatriciaV.Turner UsingPrimatesinCaptivity:Research,Conservation,and Education. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57 MarkJ.Prescott TheWelfareofPrimatesinZoos. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79 KathyR.BakerandHollyL.Farmer WelfareofPrimatesinLaboratories:OpportunitiesforRefinement. . . . 97 HannahM.Buchanan-Smith,LouTasker,HayleyAsh, andMelanieL.Graham TheWelfareofPrimatesKeptasPetsandEntertainers. . . . . . . . . . . . . 121 RachelHevesi PrimatesUnderHumanCareinDevelopingCountries:Examples FromLatinAmerica. . . . . . . . . . .. . . . . . . . . . . . .. . . . . . . . . . . . . .. . 145 R.G.Ferreira,C.Ruiz-Miranda,S.Sita,S.Sánchez-López,A.Pissinatti, S.Corte,L.Jerusalinsky,P.G.Wagner,andC.Maas PartII AssessingNonhumanPrimateWelfare UsingBehaviortoAssessPrimateWelfare. . . . . . . . . . . . . . . . . . . . . . . 171 CorrineK.LutzandKateC.Baker CognitiveBiasTasks:ANewSetofApproachestoAssess WelfareinNonhumanPrimates. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207 EmilyJ.BethellandDanaPfefferle xxii xii Contents PhysiologicalMeasuresofWelfare. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231 JohnP.Capitanio,JessicaVandeleest,andDarcyL.Hannibal QuestionnairesandTheirUseinPrimateWelfare. . . . . . . . . . . . . . . . . 255 MariekeCassiaGartner PartIII NonhumanPrimateHousingandHusbandry MeetingCognitive,Behavioral,andSocialNeedsofPrimates inCaptivity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 267 CatherineF.Talbot,LisaA.Reamer,SusanP.Lambeth, StevenJ.Schapiro,andSarahF.Brosnan PrimateBreedingColonies:ColonyManagementandWelfare. . . . . . . 307 JamesC.HaandAdrienneF.Sussman CommonHusbandry,Housing,andAnimalCarePractices. . . . . . . . . . 323 KristineColeman,GregoryTimmel,KammProngay,andKateC.Baker HousingandHusbandryforPrimatesinZoos. . . . . . . . . . . . . . . . . . . . 355 H.L.Farmer,K.R.Baker,andF.Cabana HumaneEndpointsandEndofLifeinPrimatesUsedin Laboratories. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 375 SarahWolfensohn PartIV IndividualDifferences,Application,andImprovement ofNonhumanPrimateWelfare PrimatePersonalityandWelfare. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 395 LaurenM.RobinsonandAlexanderWeiss Sociality,Health,andWelfareinNonhumanPrimates. . . . . . . . . . . . . . 413 BrianneA.Beisner,DarcyL.Hannibal,JessicaJ.Vandeleest, andBrendaMcCowan ResearchBenefitsofImprovingWelfareinCaptivePrimates. . . . . . . . . 445 StevenJ.SchapiroandJannHau Enrichment.. . . .. . . .. . . .. . . .. . . . .. . . .. . . .. . . .. . . .. . . .. . . .. 463 CaralynKemp ChallengingCognitiveEnrichment:ExamplesfromCaringforthe ChimpanzeesintheKumamotoSanctuary,JapanandBossou, Guinea. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 501 NarukiMorimura,SatoshiHirata,andTetsuroMatsuzawa TrainingResearchPrimates. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 529 MollieBloomsmith,JainePerlman,AndreaFranklin,andAllisonL.Martin