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Fascinating Life Sciences Jin-Hua Li · Lixing Sun Peter M. Kappeler Editors The Behavioral Ecology of the Tibetan Macaque Fascinating Life Sciences Thisinterdisciplinaryseriesbringstogetherthemostessentialandcaptivatingtopics in the life sciences. They range from the plant sciences to zoology, from the microbiome to macrobiome, and from basic biology to biotechnology. The series not only highlights fascinating research; it also discusses major challenges associ- ated with the life sciences and related disciplines and outlines future research directions. Individual volumes provide in-depth information, are richly illustrated withphotographs,illustrations,andmaps,andfeaturesuggestionsforfurtherreading orglossarieswhereappropriate. Interested researchers in all areas of the life sciences, as well as biology enthu- siasts, will find the series’ interdisciplinary focus and highly readable volumes especiallyappealing. Moreinformationaboutthisseriesathttp://www.springer.com/series/15408 (cid:129) (cid:129) Jin-Hua Li Lixing Sun Peter M. Kappeler Editors The Behavioral Ecology of the Tibetan Macaque Editors Jin-HuaLi LixingSun SchoolofResources DepartmentofBiologicalSciences,Primate andEnvironmentalEngineering BehaviorandEcologyProgram AnhuiUniversity CentralWashingtonUniversity Hefei,Anhui,China Ellensburg,WA,USA InternationalCollaborativeResearch CenterforHuangshanBiodiversity andTibetanMacaqueBehavioralEcology Anhui,China SchoolofLifeSciences HefeiNormalUniversity Hefei,Anhui,China PeterM.Kappeler BehavioralEcologyandSociobiology Unit,GermanPrimateCenter LeibnizInstituteforPrimateResearch Göttingen,Germany DepartmentofAnthropology/Sociobiology UniversityofGöttingen Göttingen,Germany ISSN2509-6745 ISSN2509-6753 (electronic) FascinatingLifeSciences ISBN978-3-030-27919-6 ISBN978-3-030-27920-2 (eBook) https://doi.org/10.1007/978-3-030-27920-2 Thisbookisanopenaccesspublication. ©TheEditor(s)(ifapplicable)andTheAuthor(s)2020 OpenAccessThisbookislicensedunderthetermsoftheCreativeCommonsAttribution4.0International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any mediumor format, as long as you give appropriate credit to the originalauthor(s)andthesource,providealinktotheCreativeCommonslicenceandindicateifchanges weremade. Theimagesorotherthirdpartymaterialinthisbookareincludedinthebook’sCreativeCommonslicence, unlessindicatedotherwiseinacreditlinetothematerial.Ifmaterialisnotincludedinthebook’sCreative Commonslicenceandyourintendeduseisnotpermittedbystatutoryregulationorexceedsthepermitted use,youwillneedtoobtainpermissiondirectlyfromthecopyrightholder. Theuseofgeneraldescriptivenames,registerednames,trademarks,servicemarks,etc.inthispublication doesnotimply,evenintheabsenceofaspecificstatement,thatsuchnamesareexemptfromtherelevant protectivelawsandregulationsandthereforefreeforgeneraluse. Thepublisher,theauthors,andtheeditorsaresafetoassumethattheadviceandinformationinthisbook arebelievedtobetrueandaccurateatthedateofpublication.Neitherthepublishernortheauthorsorthe editorsgiveawarranty,expressedorimplied,withrespecttothematerialcontainedhereinorforany errorsoromissionsthatmayhavebeenmade.Thepublisherremainsneutralwithregardtojurisdictional claimsinpublishedmapsandinstitutionalaffiliations. ThisSpringerimprintispublishedbytheregisteredcompanySpringerNatureSwitzerlandAG. Theregisteredcompanyaddressis:Gewerbestrasse11,6330Cham,Switzerland Their [Tibetan macaques’] flat, broad, bearded faces provide perhaps the most humanlike countenance I have ever seen in a monkey.... Apart from chimpanzees, I had never seen primate males so intensely involved with each other. In chimpanzees, too, males are at the same time rivals and friends, and I would argue the same for human males. —Frans de Waal, The Ape and the Sushi Master (2001) Foreword MysterysurroundedTibetanmacaquesforalongtime,evenforexperts.Thespecies wasnotidentifieduntilthelastthirdofthenineteenthcentury,andnothingmorethan itsgeographicdistributionandexternalcharacterswereknownforthenexthundred years. It was long referred to as Père David’s macaque, a rather odd name in reference to the French missionary and naturalist Father Armand David, who first collected the species.Moreover, the currentname, Tibetan macaque, ismisleading sincethespeciesistypicallyfoundineast-centralChinaandnotwithinthebound- ariesofTibet.ThisisduetothefactthatPèreDavidinitiallylocatedthespeciesata placeclosetotheSino-Tibetanborderofhistime. Wehadtowaituntilthe1980stoseeMountEmeiandMountHuangshancometo lightontheprimatologymap.ThisiswhereQikunZhaoandZiyunDengfromthe KunmingInstituteofZoologyandQishanWangandJinhuaLifromAnhuiUniver- sity began to study the behavior and life history of Tibetan macaques, definitively adding anewdimensiontothemacaquelandscape.Istill havethereprintsoftheir publications in my bibliography, some written in Chinese. The works of Hideshi Ogawa,CarolBerman,andanewgenerationofprimatologistssoonfollowed.Now appears this multi-authored volume entirely devoted to the Tibetan macaque. This combinedeffortof two dozen scientiststoreview40 years ofresearch andpresent newfindingsaboutasinglespeciesshouldbeviewedasacelebrationofthespecies. It frees Tibetan macaques from the purgatory of scientific papers scattered across various journals and collections to join the small club of primate species that are honoredwiththisattention.Manypeoplewouldconsiderthatbrownmonkeyslike Tibetanmacaquesalllooksimilar.Althoughtheydonothavetheimmediatevisual appealofmorebrightlycoloredprimates,brownmonkeyshavedifferentbutequally attractiveassets.Withtheirfierygazeandprominentbeards,Tibetanmacaquesare no exception, and their adaptations and behaviors attract a great deal of research interest. As scientists we are expected to test hypotheses and theories. Some of the contributors tothis bookdoso,addressing broad issues suchascooperativestrate- gies,socialdynamics,collectivedecisions,feedingecology,andpathogentransmis- sion. They use Tibetan macaques as a model to investigate mainstream research vii viii Foreword questionsinthefieldofbehavioralecologyandevolution.Everyanimalspecieshas its singularities, however, and deserves to be studied for itself. This is why other contributors seek to identify what makes Tibetan macaques special, investigating patternssuchassocialplay,calltypes,orthefascinating“bridging”interactionsin which infants play a role as buffers to reduce tension between adults. Science generally values the testing of general theories more than the humble seeking of whatgivesaspeciesitsowntouch.Intheend,however,bothoftheseapproachesare necessary. Years ago, I was struggling to rank the different species of macaque accordingtotheirlevelsofsocialtolerance.Quantitativemeasureswereavailablein a limited number of species and I had to rely on qualitative data for others. I remember asking Qikun Zhao about the behaviors particular to Tibetan macaques at a conference held in Japan in 1996. I was trying to guess their social style, i.e., theirowntouch.Thisresultedinatentativescalingofmacaquespecieswhichwould later be amended when quantitative data became available in Tibetan macaques. It shouldbeemphasizedthatthestoryisfarfromover.Asdiscussedinthebook,why and to what extent the different behavioral traits constituting social styles may covaryduringtheevolutionaryprocessstillremainstobeelucidated.Iamdelighted toseehowthestudyoftheparticularmeetsthegeneralbyyieldingnewperspectives andhypothesestobetested. Astheeditorspointout,thisbookshouldnotbeconsideredanend,butrathera beginning.ThishighlightingofresearchintoTibetanmacaqueshasthepotentialto strengthen Chinese primatology and favor its development at the national and internationallevel.Itmay inturnhelptheTibetanmacaques.Likeotherspeciesof non-humanprimates,theirpopulationsarethreatenedbythelossandfragmentation oftheirhabitat.Admiring,knowledge,andconservationshouldgohandinhandto savethefutureofthisuniquespecies. UniversityofStrasbourg,Strasbourg BernardThierry France Preface This book is mainly based on research papers presented in a spirited international primatology symposium held in the scenic area of Mt. Huangshan, China, in the summerof2017.Thechaptersweregroupedintofourlogicalparts.PartIconsistsof asinglechapter,whichoffersabriefintroductiontorecentdevelopmentsinChinese primatologyandashorthistoryofresearchontheprimatesofChinaingeneraland theTibetanmacaqueinparticular. Part II contains seven chapters (Chaps. 2–8) focusing on social behavior and socialdynamicsinTibetanmacaques.InChap.2,Jin-HuaLiandPeterM.Kappeler provide a comprehensive review of three decades of field research in Tibetan macaques at the Valley of Monkeys, highlighting the significance of this species asamodel for understandingbroader questions inprimate behaviorandevolution. LixingSun,Dong-PoXia,andJin-HuaLifollowupinChap.3byintroducinganew way to analyze the dynamics of macaque social hierarchy from a social mobility perspective with new insights unveiled through comparing Tibetan macaques with Japanese macaques. In Chap. 4, Dong-Po Xia, Paul A. Garber, Cédric Sueur, and Jin-HuaLilookintotheinternalbehavioralmechanismspromotinggroupstabilityin Tibetanmacaquefromabehavioralexchangeandbiologicalmarketpointofview.In Chap. 5, Xi Wang, Claudia Fichtel, Lixing Sun, and Jin-Hua Li investigate how Tibetanmacaquesmake collectivedecisions during group movements.InChap.6, JessicaA.Mayhew,JakeA.Funkhouser,andKaitlinR.Wrightexplorethesignif- icance of play behavior in the development of social cognition in juvenile Tibetan macaques.ThischapterisfollowedbySofiaK.Blue’sanalysisofvocalcommuni- cationinChap.7,whichgeneratesinsightsfromcomparingTibetanmacaqueswith other macaque species.In Chap. 8, Krishna N.Balasubramaniam, Hideshi Ogawa, Jin-HuaLi,ConsuelIonica,andCarolM.Bermanofferacomprehensivereviewof Tibetanmacaque’ssocialstructure,withinsightsfromtheirpreviousworkonsocial styles, comparative studies with other macaque species, and male–male social tolerance. PartIIIcontainstwohighlyfocusedstudiesaboutritualizedbehaviorofTibetan macaques with the implication about how culture evolves. In Chap. 9, Grant J. Clifton, Lori K. Sheeran, R. Steven Wagner, Jake A. Funkhouser, and Jin-Hua ix x Preface Li examine how infants are used for the regularly observed behavior of bridging between adult females. This is further pursued in Chap. 10, where Hideshi Ogawa compares bridging behavior in two populations of Macaca assamensis, which are then compared with Tibetan macaques to explore the evolutionary origins of this highlyritualizedbehavior. Part IV is composed of four chapters, focusing on how Tibetan macaques live with microbes, parasites, and diseases. In Chap. 11, Binghua Sun, Michael A. Huffman, and Jin-Hua Li take us into the microbial world inside the gut of Tibetan macaques and show how microbes adapt to the social behavior of the species. Then, Michael A. Huffman, Binghua Sun, and Jin-Hua Li present data in Chap. 12 to test the hypothesis that the diet of Tibetan macaques may incorporate self-medicativeaspectstobettersurviveintheirenvironment,apropositionthathas never been examined in this species before. Broadening the scope in Chap. 13, KrishnaN.Balasubramaniam,CédricSueur,MichaelA.Huffman,andAndrewJ.J. MacIntoshreviewpreviousworkoninfectiousagentsathuman–macaqueinterfaces andofferseveralkeyfuturedirectionsforresearchinthisarea. Many recent discoveries in primatology involve technological advancements in research,whichisthecontentofPartIV.Inasinglechapter(Chap.14),YongZhu andPaulA.Garber explorethegreatpotentialofthehighfieldMRItechnologyin the study of primate behavior and cognition. While promising, this new imaging technologyhasseveralobviouslimitationsatpresent. Allinall,thecontributorsofthisvolumeexamineabroadrangeoftopicsabout the behavioral ecology of the Tibetan macaque. Although data are still far from adequateandsomeconclusionsaretentative,wehopethisvolumewillhelpremove theTibetanmacaquefromthelistoflittleknownprimatespecies.Weexpectthatthe information presented here can stimulate further comparative study of behavioral, ecological,andevolutionaryquestionsaboutmacaquesandotherprimatesandhope that this contribution will facilitate the integration of Chinese primatology into the mainstreamfield. Hefei,Anhui,China Jin-HuaLi Ellensburg,WA,USA LixingSun Göttingen,Germany PeterM.Kappeler

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