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resource(th ecolony )[9 ].B ycont rast, vulturineguinea fowl(Acrylliumvulturinum ) move cohesivelyin groupsthat arestable acrosssea sons(intermedia televel),and groups roostand movepreferentially with othergro ups(upperlev el),butthere pro- ductiveunits withinthe group(lower level)can change fromoneseaso ntothe next [10 ].Thus, stability isnotnecessar ily equallydistri butedacrosslevels,and birds maypr ovideanidealsetofs pecie sto developadee pe runderstandingof how typesofmult ile velsocieties(Figure1

AlthoughGruet eret al.[1]definedt he

lowerlev elasthecore unit ,thismi ghtmis - representsocietie swheremembership in thesoc ietyisclearest at intermediate (e.g.,groupso fvulturineg uineaf owl)or higher(e. g.,coloniesofs lender-billed gulls)leve ls.Studiesfrom birdscanalso allowsocia lversusnon socialdrivers of nestednesstobedise ntangl ed. Whilemul- tilevelsoc ietiescanemergefrom social preferences,seemingly identicalpatt erns can arisefrom spatialand resource-driven processes.Simplystudy ingpatternso f socialstru cturearisingat largerecological scaleswillun doubtedly uncovercommu- nitys ubstructuringdrivenbyresourc e distribution andhabitat configuration [11

Forex ample,songbirds canmaintaincon-

sistentcommu nitystructure,attw ospatial scales,that issufficientlystabl etomaintain experimentallyinducedloca ltraditions acrossgene rations[12 ]. However,suc h communitystructur earisesthrougha combinationofindividu aldif ferencesin microhabitatpreferences (lowerlevel),and habitatgeomet ryrestricting themovement of individualsacrossthe woodland(upper level)[11 ].Th isexam plehighlightsho w studiesinbirds canhelpreveal mecha- nismstha tgenerat epatternsofsoci al structurethatar econsiste ntwiththo se from multilevelsocieties,even tothepoint of exhibitingsomeof thesameseemingly adaptivebehavio ursasmultilevelsocie ties (localtradit ions),butwithoutanysocia l preferencestakingpl aceathigherl evels.Weh opethatth eworko fGrueteret al.[1] will inspireresearch onmultilevel societ ies in birds.Much canbe gainedby expanding existingeviden ceofcomplexandnes ted avianso cietiesintothe multilevelsoci ety framework.Whenimplementing thisframe- work,s tudieswillneed toexplicitly consider the numberof levels,theirs tabilityandc ohe- sion,and the mechanismsun derlyingthe emergenceand/or maintenanceof each level.Indoin gso ,studieson birds willhelp withdev elopingabettermechanisticun- derstanding ofmultilevels ocieties,a nd whether, regardlessofthedrivers,indi- viduals canre apbene fitsfrom living in a nestedpopulation structure,such as informationtransmiss ion.1 Max PlanckInstitute ofAnimalBehav iour,Depa rtmentof

Germany

2

Departmentof Biology, UniversityofKonst anz,

3 Centrefor theAdvanc edStud yofCollecti veBehaviour,

Germany

4

These authorscontributed equally

*Correspondence:dpapageorgiou@ab.mpg.de(D. Papageorgiou)and dfarine@ab.mpg.de (D.R. Farine).

Twitter:@DanP apageorgiou(D.Papageorgiou)and

@DamienFarine(D.Farin e).https://doi.org/10.1016/j.tree.2020.10.008© 2020Else vierLtd.Allrights reserved.

References

1.Grueter,C.C. et al.(2020)Mult ilevelorganisation ofanimal

sociality.TrendsEcol .Evol.9, 834-847 2. Riehl,C. (2013 )Evolutionaryro utestonon-kincoope rative breedinginbirds. Proc.R.Soc.BBiol.Sci.280,20 132245 3. Stacho,M.et al.(2020)Acor tex- likecanonicalcir cuitin the avianforebrain. Science369, eabc5534 4. Henry, L.et al.(2015)Dialec tsinanimals: evidence, devel- opmentandp otential functions.Anim.Beha v.Cogn.2,

132-155

5. Ferreira,A.C.et al.(2020)How tomakeme thod ologica l decisionswhe ninferring socialnetworks.Ecol.Evol .17,

9132-9143

6. Brandl,H.B. et al.(2019)Wildze bra finchestha tnest

synchronously havelong-term stablesocial ties.J. Anim. Ecol.Publishedonline August12,2019. https://doi.org/

10.1111/1365-2656.13082

7.Francesiaz,C.et al.(2017)Familiarity drives social

philopatryina no bligatecolo nialbreederwith weak interannualbr eeding-sitefidelity.Anim.B ehav.124,

125-133

8.

Bell,H. L.andFor d,H.A.(198 6)Acompari sono f

the socialorgan izationofthreesyntopicspecieso f Australianthornbill,Acanthiza.Behav.Ecol .Sociobiol.

19,381 -392

9. Painter,J.N. et al.(2000) Complexsocia lorganizationre- flectsg eneticstructure andrelatednessi nthecooperativelybreeding bellminer,Manorinamelan ophrys.

Mol. Ecol.9, 1339-1347

10. Papageorgiou,D.et al.(2019)The multil evelsocietyofa small-brainedbird.Curr. Biol.29, R1120-R1121 11. He,

P.etal.(2019)Th erol eofhabitat configurationin

shaping socialstructure: agap instudies ofanimal social complexity.Behav.Ecol .Sociobiol.73, 9 12. Aplin,L.M.et al.(2015)Expe rimentallyinducedinnovations lead topersi stentcultureviaconf ormityin wildbirds.

Nature518,538 -541

Letter

On Multifaceted

Definitions ofMultilevel

Societies: Responseto

PapageorgiouandF arine

Cyril C.Gruet er,

1,2,3,

XiaoguangQi,

4

DietmarZinne r,

5,6

Thore Bergman,

7,8

Ming Li,

9,10

Zuofu Xiang,

11

PingfenZhu,

9

Alex Miller,

1

MichaelKrüt zen,

12

Julia Fischer,

5,13

DanielI. Rubenstein,

14

T.N.C.Vidya ,

15

BaoguoLi,

4,10

Maurício Cantor,

16,17,18,19,20,21

and LarissaSwedell

22,23,24,25

Papageorgiouand Farine [1

], intheir com- ment onour re centsynthesisofanimal multilevelsocieties [2 ],provide several examplesofnest edn essinaviansocial systemsandcal lfora fullerinc orpora tion of birdsi ntoourtheoretical framework.

Wef ocusedmainlyonma mmalsto con-

struct ourp roposedframeworkbe cause multilevelsocietiesa rebest knownfrom thista xonomicgroup.Pap ageorgiouand

Farine[ 1

] pointout several birdspecies thatform neste dsocialarrangements andargue that,bydivingdeeply into examplesfrombir ds,the remaybevaria- tions infor mthatmeetour criteriafor a multilevelsociety:a soc ials ystemwith a stablecore leveland atleast onerecog- nizable upperlevel.Papageorgiouand

Farine[1

] raisetwoqu estio ns:(i)whether theope rationaldefinitionofmu lti levelsoci- etiessho uldberelaxe dtoacco mmodateTrends inEcology &E volution Trendsin Ecology &Evolution,Janu ary2021, Vol.36,No.1 17 birdsp eciesthatshowmor estabilit yat higherleve lsofsociety ;and( ii)whether societieswith multipl etiersresulting solely fromha bitatpreferencesins teadofsocial preferencessh ouldbeclassified asmulti- levelsoci eties.

PapageorgiouandFarine [1

] arguethato ur criteriashoul dberelaxedto includ e social stabilitya tanyleve lofa nestedsociety andthat theco reunitd oesnotnec essarily needto bethe lowest level. However,we maintainthat:(i )encompassi ngever ysoci- ety withadem onst rablemodularstructure would invalidatetheinclus ionc riteriawe developedfor distinguis hingmultilevel societiesfromo thertypeso fsystems withdetectablesubstr ucture;a nd(ii)a more permissivede finitionwoul dhamper efforts inident ifyingthe eco-evolutionary driversofm ulti levelsocietiessensu stricto. Moreover,maint ainingthisdis- tinctionbetw eenmultilevel societieswith at leastt woconsistentlevels andsocie- tieswithasinglestablelevelcombined withot herunstable associations(assee n in severalbirdtaxa )iscr ucialbecau seevo- lutionaryproce ssessuchasinformation flowa nddisea setransmissionareexpected to differbetwee nthesetypesof societies.

Thatsa id,wearen otop posedt othei dea

that themost stablelevels canbehighe r levelsrat herthanthe core unit.Societie s withsta bleintermedi ateandupperlevels, yet unstablelowerle vels(asexem plified by vulturineguinea fowlAcrylliumvultur inum

3]),c ouldconstitu temultilevelsociet ies,as

we originallyacknowled ged[2 ]. Infact ,in our discussionof themultilevela lliances ys- tem ofthe Shark Baybottl enosedolphi ns (Tursiopssp.)wepo in tedoutthatth issys- temde viatesfromourde finitioninth atthe highlyco hesiveandstableun its(se cond- orderallian ces)occuratale velabovethe coreuni t.Accord ingtoourframework, however,asociet yw ithunstablecor e units,nointe rme diatelevel,andcleares t membershipatahighe rleve lw ouldnot representamulti level societybutin steada systemwithato misticfission-fusion dynamics.This isex empli fied bythe north - ern muriqui(Brachyteleshypoxan thus), whichexh ibitsflexibleassoci ationpatterns at basallevels butcohes ivenessat the upperlevel,bothspatiallyandtempo rally[ 4].

Papageorgiouand Fari ne[1

]shortlistfive possibleaviancandidatesformultilevelso- cieties. Butwhichonesactuallyfitourdefini- tion? Beyondvulturineguinea fowls,bell miners (Manorinamelan ophrys) maybe a goodfit, asdiscret esocialorganization manifests itselfon atleast threelevel s[ 5

Two additionalspeciesapp earto'tick the

boxes'. Inspec tacledparrotlets( Forpus conspicillatus), monogamouspairsare em- bedded withinputative lystablegroups, which thenform flocks [6 ]. Thisdo esap- pear tobe amultilev elsoc iety,butmore data onass ociationpatte rnsareprobably needed torule outalternat ives.In white- frontedbee-e aters(Meropsbullo ckoides), thereisa nint ermedi atesocialtierbetween thebr eedingpairandth elargerco lony[ 7 which couldqualif ytheirsoc ietyasmulti- level.Careful screeningof thelite rature will likelyrevealsim ilarsyste msinhitherto neglected taxa.

The secondmajor questionraisedby

PapageorgiouandFar ine[1

]pertainsto whether thede finition ofmultilevel socie- tiess houldincludestru cturedsocieties brought aboutby sharedspatialprefe r- enceso rotherecologica lopportunities (e.g.,p referencesforcertainsleeping andfo ragingsites)inst eadofsocial prefer- ences.Insom ecases itisnotk nownto whatde greetheformatio nofa distinct level ise cologicallyinducedor theresult of individualexpressionsof socialprefer- ence. Fors omespecies, westilldonot know exactlywhere the socialglue endsand habitat-inducedoverlapbegins (i.e.,atw hich spatialscale sthesocial processesare paramo unt).Whilecore (andint ermediate)levelsareundoubtedly genuinesocial groupingstha tcrystallizeforreproductivepurposesand socialsupport, weshould beopen tothe idea that as sort- mentintoupper-levelgroupingsisnotexclu- sivelydriv enbysocial prefer encesbutmay alsoinvolveecologicallydrivenmechanisms.

Apexlev elsinpartic ular oftenrepresent

aggregationsofind ividuals resultingentirely froman exter nalfactor(e.g., themagnetic effectsth atlocalized resourcesexerton socialuni ts,asisthe case with rare safe sleepingsites intheclassic example of thetr ooplevelin hamadryasba boon s[ 8]), whichare verydif ferent froma'group' ofindividuals in whichthepresence and identifyof conspecifics matter.L ack of individualization,however,doesno t preclude thepo ssibilitythatindividuals derive benefits frombeing associated withth eapexg roupinglev el(e.g.,'safety in numbers').

Becausewe cannotalwaysa scertain

whetheraparticu lar levelofamultilevel societyi ssoc iallyorecologicallydriven, this shouldnot be adecisivefactor in classifying asociety as multilevelor not.

In ourv iew,thecr itical criteriaare:(i)consis-

tency ofindividual membershipin eachlevel over time,and (ii)spatio-temporal cohesi on of thecore anduppe rlevel s.Animportan t goal forfuture research istoquantifythe relativecontri butionsofsocialproce sses and ecologicalfactors in shapingadditional levelsin animal societies.Thiswil lrequire fine-graineddata onhow animals move relativeto eachothe rand, ideally,onhow they mayp erceiveeachotherasi ndividuals and membersof distinct sociallevels.

It wouldalso beinteres tingto compare

theco nsistencyofgroupingsth atar epur- portedlysocially versusecological lydriven.

Papageorgiouand Farine[ 1

] arguethat studiesfrom birdscan allowsocia lvers us non-socialdriversofn estedsociallev els to be disentangled.Whilewe agreetha ta broaderpersp ectiveisuseful,iti snot clear to ushow birdsare inany way more suitabletha nmammalsfordist inguishing the driversofsoc ialleve ls,particularlyas few ofthe irexamplesare unambiguously

Trends inEcology &E volution

18Trendsin Ecology &Evolution,Janua ry2021, Vol.36,No.1

multilevel.Clearly, muchfurtherworkis neededand data frommammal s,birds, and othertaxa willbecrucia lin enrichi ng and refiningour un derstandingoftheevolu- tionaryprocesse sresponsiblefor theemer- genceand maintena nceofthisintrig uing social system. 1 SchoolofHuma nSc iences,Th eUniversityofWest ernAustrali a,

Perth,WA60 09,Aust ralia

2 Centrefor Evolutionary Biology,School ofBiologicalScien ces, The UniversityofWeste rnAust ralia,Perth,WA 6009,Australia 3 InternationalCentre ofBiodiversity andPrima teConservation,

Dali University,Dali,Yunna n67100 3,China

4 ShaanxiKey Laboratory forAnimalCons ervation, Collegeof Life Sciences,Northwest University,Xi'an, 710069,China 5 CognitiveEtholo gyLaboratory,German PrimateCenter(DPZ), 6

Germany

7 Departmentof Psychology, Universityof Michigan,AnnArbor,

MI, USA

8 Departmentof Ecology andEvolutionary Biology, Universityof

Michigan,Ann Arbor, MI,USA

9 CAS KeyLabor atoryofAnimal Ecology andConservation Biology,Inst ituteofZoology, Chaoyang District,Beijing 100101, China 10

Center forE xcellenceinAnimalE volutionand

Genetics, ChineseAcademy ofSciences, Kunming

650223,Chi na

11 Collegeof LifeScie nceand Technology,Cent ralSouth Universityof Forestry andTechnology,Changs ha,Hunan

410004,Chin a

12 Departmentof Anthropology ,UniversityofZurich, 8057,

Zürich,Swit zerland

13 Departmentfor Primate Cognition,Geo rg-August-University 14 Departmentof Ecology andEvolutionary Biology, Princeton

University,Princeton, NJ,USA

15 Evolutionaryand Organismal BiologyUnit,Jawa harlalNehru Centrefor Advanced Scientific Research(JNCASR), Jakkur,

Bengaluru56006 4,India

16

Departmentfor theEcology ofAnima lSocieties, Max

PlanckIn stituteofAnimal Behavior, Konstanz,7 8464,

Germany

17 Centrefor theAdva ncedStud yofCollective Behaviour,

Universityof Konstanz, Konstanz,78464, Germany

18 Departmentof Biology, UniversityofKonst anz,Konstanz,

78464,Germa ny

19 DepartamentodeEcol ogiae Zoologia,Universidade Federal de SantaCatarina, Florianópolis,88048 -970,Brazil 20 Centrode Estudos doMar,Universid adeFede raldo Paraná,

Pontaldo Paraná, 83255-000,Brazil

21

Schoolof Animal, PlantandEnvironment alScien ces,

Universityof theWitwat ersrand, Johannesburg,2000,South

Africa

22
Departmentof Anthropology ,QueensCollege,City University of NewYork, Flushing, NY,USA 23
New YorkConso rtiuminEvolutionar yPrima tology,NewYork,

NY, USA

24

Anthropology,Biology andPsychologyProg rams,CUNY

GraduateCent er,365Fifth Avenue, NewYork,NY,USA

25

Departmentof Archaeolog y,UniversityofCapeTown ,

Rondebosch,7701, CapeTown, SouthAfr ica

*Correspondence:cyril.grueter@uwa.edu.au(C.C. Grueter).

© 2020Elsevi erLtd.Allright srese rved.

References

1. Papageorgiou,D. andFarine, D.(2020) Multilevelsocieties

in birds.TrendsEcol .EvolPublishedonl ineOctober 29, 2. Grueter, C.C.et al.(2020) Multilevelorganisatio nofanimal sociality.TrendsEcol .Evol.35, 834-847 3. Papageorgiou,D.et al.(2019)Them ulti levelsocietyofa small-brainedbird.Curr. Biol.29, R1120-R1121 4. Strier,K.B. et al.(1993)De mographyandsocialstru ctureofon e groupof muriqu is(

Brachytelesarachnoides ).Int.J .Pri matol.14,

513
-526 5. Painter,J.N.et al.(2000)Comple xsocialor ganizationreflectsge- neticstruc tureandrelated nessinth ecooperativelybreedingb el l miner,Manorinamelano phrys.Mol.E col.9, 1339-1347 6. Wanker,R. et al.(1998)Disc riminationofdifferentsoci al compan- ionsins pec tacledparrotlets(Forpusconspic illatus):evi dencefor individualvoc alrecognition.Behav. Ecol.S ociobiol.43, 197-202 7. Hegner,R.E. et al.(1982)Spati alorganization ofthewhite- frontedbee -eater.Nature298, 264-266 8. Kummer,H.(196 8) SocialOrga nizationofHamadryasBa- boons:AFieldStud y, TheUniversityo fChica goPress

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