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CarnivoranEcology
CarnivoranEcology TheEvolutionandFunctionof Communities
StevenW.Buskirk ProfessorEmeritus,UniversityofWyoming
GreatClarendonStreet,Oxford,OX26DP, UnitedKingdom
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Preface
Thisbookarosefrommyseveraldecadesofinterest inandresearchoncarnivorans.Likemanyyoung peoplewithnaturalisttendencies,Iwasparticularlyintriguedbymyearlyencounterswithwild carnivorans—theirrarity,elusiveness,andimplicit threattomywell-being.Ivividlyrecallseeingmy firstbeartrackonasolobackpackingtripinthe SierraNevadaofCalifornia,followedbyasleeplessnightspentcontemplatingmyfate.Irecallthe horrorofmyoldersisterwhenIaskedhertostop ourparents’carsothatIcouldretrievearoad-killed domesticcatandadditsskulltomycollection.In thesummersofmycollegeyears,workingasatour guideinMountMcKinley(nowDenali)National Park,Alaska,Iobservedregularinteractionsinvolvingwolves,caribou,brownbears,moose,redfoxes, andotherspecies.Someoftheseobservationswere dramaticandphotogenic,butcuriousaswell.Why did150-kgbrownbearsinvestsomucheffortto capture200-ggroundsquirrels?Whydidwolves givebirthinthesamedensfordecadesonend, eventhoughtheywerewellknownandprone tohumandisturbance?Whywerecoyotesdeathly afraidofbeinganywherenearwolves,whilered foxesmerelystayedoutoftheirgrasp?
MyPhDresearchandsubsequentfaculty appointmentinZoologyandPhysiologyatthe UniversityofWyominggavemeopportunities topursuethesekindsofquestions.Whilemost carnivoranresearchofthattimegravitatedto intraspecificandpredator–preyinteractions, myinterestsrangedmorewidely.Myresearch addressedvariousmechanismsbywhichcarnivoransmightbelimited:thermalenergetics, allometry,toothmorphology,fastingendurance, geneticvariability,andinterspecificcompetition. Ilearnedthatpredator–preyinteractionswere
asmallpartofourgrowingunderstandingof whatlimitsthedistributionsandabundancesof carnivorans.
Duringthoseearlyyears,Idependedonthestandardacademicreferencesoftheday:journalarticles,monographs,bookchapters,theses,dissertations,andR.F.Ewer’s(1973) Thecarnivores.Ewer’s monographwasthedefinitivesourceforcarnivoranbiology—especiallypaleontologyandbehavior. Writingthecurrentaccountnearlyfiftyyearson, Ibenefittedfromawealthofhigh-qualitymaterial facilitatedbytherevolutioninpublishing—aproliferationofjournaltitles,manyofthemopenaccess, expandedopportunitiesforscientistsindevelopingcountriestopublishtheirwork,andmanymore womenworkingandpublishingasscientists.The periodsince2000hasofferedunprecedentedopportunitiestowriteabooksuchasthis,andthepandemicof2020–22gavemyisolationandfocusnew purpose.
Whatqualifiesmetowriteabookaboutallcarnivorans?Iamnotthemostprolificauthorofcarnivoranpapers,northeonewiththebroadestgeographicexperience.Othershavespentmoretime inthefield,oraremorequantitativethanI.However,myinterestsextendinmultipledirections, allofwhichrelatetohowcarnivoranssucceedor failinthewild.Iamasintriguedbyanswersto bigecologicalquestionsasbysolutionstospecific conservationproblems.Iamassatisfiedbyunderstandingofsomeecologicalpuzzleasbywatching alargecarnivorestalkanungulate.Iappreciatenew discoveriesinnaturalhistoryasmuchasIdostudiesoffunctionalgenomics.Ialsovaluethosewho studycarnivoransandsharetheirfindingswithscientistsandthepublic.Thisgroupoverlapsstrongly withthosecommittedtoassuringthepresenceand
importanceofcarnivoransinfuturecommunities. Thisbookisreallyabout,for,andtheresultof theworkofcarnivoranbiologists,conservationists, andnaturalists,bothprofessionalandamateur.It isabouttheirpassion.Lastofall,hopefullyitisa motivationforotherstofollowintheirtracks.
StevenW.Buskirk
ProfessorEmeritus,UniversityofWyoming December10,2022 SilverCity,NewMexico,US
Referencescited
Ewer,R.F.(1973). Thecarnivores.Ithaca:CornellUniversity Press.
Acknowledgments
Manypeoplesupportedandaidedmeinwriting thisbook.MywifeBethencouragedmeatevery stageandtoleratedmanyinterruptionstoourroutinesothatIcouldspendtimewriting.ClosecolleaguesDennisKnightandCarlosMartinezdelRio werereliablediscussantsandsourcesofencouragementearlyintheconceptionandearlywriting phases.HannahSeaseproducedallgraphicarts work,keepingpacewithmyrequeststhroughout hergraduatestudiesingraphicarts.
TheWilliamRobertsonCoeLibraryattheUniversityofWyomingprovidedoutstandingsupport,fillingscoresofrequestsformaterials,andtheJ.Cloyd MillerLibraryatWesternNewMexicoUniversity providedadditionalassistance.Myacademichome, theDepartmentofZoologyandPhysiologyatthe UniversityofWyoming,providedofficespaceand othersupportformostofdurationoftheproject.
Ibenefittedfromreviewsbyoverthirtyscientists,eightofthemcommissionedbyOxfordUniversityPress,andotherssolicitedbyme,who generouslyreviewedchaptersorshortersections: BenjaminAllen,RudyBoonstra,JeffBowman, JosephBump,EmilianoDonadio,JacobGoheen, HenryHarlow,DennisKnight,SergeLariviere, PaulLeberg,JasonLillegraven,CarlosMartinez delRio,SterlingMiller,RobertNaiman,Richard Ostfeld,JonathanPauli,JamesD.Rose,Oswald Schmitz,JohnSchoen,Qian-QuanSun,Blaire
VanValkenburgh,LarsWerdelin,andAndrzej Zalewski.Collectively,thereviewerscorrected errorsoffact,identifiedimportantomissions,providedmorepertinentormorerecentreferences, andimprovedtheorganizationandpresentation. Withouttheirhelptheprojectwouldnothavebeen possible.
Theillustrationsstrengthenthenarrative throughout,andsomeofthefinestartworkand photographywerecontributedgratisorlicensed atreducedrates.IparticularlythankJustinBinfet, DarinCroft,WaltonFord,StanGehrt,DonGutoski, EsperanzaIranzo,JeffreyKerby,JanetKessler, DéboraKloster,SusanMcConnell,ChrisMills, LarissaNituch,VelizarSimeonovski,Alejandro Travaini,JuanZanón,thePhilmontScoutRanch, andKasminGallery.AlthoughIhavetriedto selectphotostakenundernaturalconditions,I cannotassurethatnonewasstagedorinsomeway contrived.
ThestaffofOxfordPressweremostsupportiveandencouraging.IanSterlingwasimmediately receptivewhenIapproachedhimwithmyproposal,andconsistentlyimprovedmypresentation aswellasmyunderstandingsofhowthebookcould bemademostuseful.CharlieBathprovidedexcellentsuggestionsondraftchapters,andKatieLakina shepherdedtheprojectthroughtheeditorialand productionprocesses.
2.6.1Scansorialecomorph
2.6.2Dog-likeecomorph
2.6.3Cat-likeecomorph
2.6.4Scavengerecomorph
2.6.5Semi-fossorialecomorph
3.3Earlycarnivorans
4.1.1Solublecarbohydrates
4.2Dietaryrequirements
4.8.1Generalpatterns
5.1.2Chemosense
5.1.3Hearing
5.1.4Electromagneticradiation
5.1.5Geomagnetic
5.2Brainmorphology
5.2.1Brainsize
5.2.2Brainregionalsize
6.3.3Trophictransmissionandpreybehaviors
6.4Scavengingandaccesstocarrion
6.5Directeffectsonplantlifecycles
7.2.2Interferencecompetition
7.2.3Influencesoninterference
7.2.4Mesopredatorrelease
7.2.5Demographiceffectsofinterference
7.2.6Coexistenceorinterference?
7.2.7Abioticfactorsandinterference
7.2.8Humaninfluenceoninterference
7.3Domesticdogsascompetitorswithwildcarnivorans
7.4Carnivorans:apex,meso-,andother
8.1Whoeatswhom?
8.2Docarnivoranslimitpreyabundance?
8.2.1Bottom-upvs.top-downeffectsonherbivores
8.3Trophicdiversityandlimitingeffects
8.4Howherbivoresavoidpredation
8.4.1Antipredatorstructures
8.4.2Antipredatorchemicals
8.4.3Inducedpredatordefenses
8.5Physiologicalanddemographicresponsestorisk
8.6Carnivoransandpreypopulationcycles
8.7“Prudent”and“wasteful”predators
8.8Apparentcompetition
9.2Trophiccascades
Introductionto CarnivoranEcology
OrderCarnivorarepresentsoneofthemostspeciesrich,phenotypicallydiverse,widelydistributed, andecologicallyinfluentialmammalianlineages. Itsextantmembersliveonallcontinentsandin alloceansandrangefromvole-sized(c.30g) tolargerthanarhinoceros(c.4,000kg).They eatdiversefoodsincludingleaves,fruits,insects, honey,marineinvertebrates,andmammalslarger thanthemselves.Somespecieslivebelowground forweeksatatime,afewlivemostlyinthe forestcanopy,andothersliveatseaformonths onend.Manyarewildernessdwellers,waryof humansandtheiractivities,whilesomenondomesticspeciesthriveinmajorcities,largely dependentonhumansforfood,shelter,orprotectionfromlarger,wildercarnivorans.NoothermammalianorderapproachesCarnivorainthebreadth ofadaptivesuitesshownandecologicalniches occupied.
Humanshavealwaysbeenkeenlyinterestedin carnivorans.Ourhomininancestorswerepreyed onbycarnivoransandcompetedwiththemfor food.Bothspecieshuntedthesamepreyanddrove eachotherawayfrompreycarcasses(Figure 1.1) (Espigares etal.,2013).Paleolithichumansconvertedapotentialcompetitor,thewolf,toapartner. Theresultantdogwasthefirstdomesticatedanimal, andbecameessentialtohumanlives,providinga foodsource,vigilanceagainstintruders,transport ofpossessions,andassistanceinhuntingandherding(Figure 1.2).Dogsbecamesoimportanttoearly humansthattheyarecreditedwithshapinghuman evolutionasmuchashumansshapedtheirs(Pierotti andFogg,2017).
Thelife-or-deathnatureofpredationelicitsstrong humanemotions—eitherthepredatoreatsand lives,orthepreyescapesandsurvives.These
emotionsarestrongerwhenweimagineourselves oranimalsweownasprey.Asaresult,wehavelong imbuedcarnivoranswithspiritualpowerstomatch theirimpressivephysicalabilities,andourancestorsrepresentedcarnivoransinsomeoftheearliest figurativeart(Figure 1.3)(HartandSussman,2008; Azéma,2015).Today,wecontinuetousecarnivoranstosymbolizewildness,ferocity,andindependenceinvisualandliteraryarts.Everypocketand foldofmosthumancultures—languages,parables, spiritualbeliefs,andsymbols—isrichwithcarnivoranreferences.
1.1 “Carnivoran”vs.“carnivorous”
Theterms“mammalianpredator,”“mammalian carnivore,”and“carnivoran”arenotpreciselysynonymous.Predatorsareanimalsthatkillandconsumemulticellularanimals(Taylor,1984),whether oneatatime,orfilteredfromwaterbythethousands.Eagles,dragonflies,andbluewhalesare predators.Bycontrast,acarnivoreconsumesthe fleshofanimals,whetheritkillsorscavengesit;vultures,snakes,andVenusflytrapsarecarnivores and carnivorous.Carnivorans,thesubjectofthisbook, areexclusivelymammalsinOrderCarnivora—a branchofthetreeoflife.Speciesintheorder maypursueandkillvertebrates,eattermitesexcavatedfromsoil,orsubsistentirelyonplantparts (Figure 1.4).“Hypercarnivore”sometimesindicates aspecieswithadietexceedingsomethresholdlevel ofvertebrateprey,typicallykilledratherthanscavenged.Mostmembersofthecatfamily,theFelidae, areconsideredhypercarnivores.Otherterms,such as“mesopredator,”“apexpredator,”and“keystone predator,”haveimprecisemeaningsthatIparseas theyariseinthebook.
Figure1.1 Thefirstcontactbetweenhumansandthesaber-toothed Smilodon inAmerica,interpretedbyVelizarSimeonovski.Carnivoranshave beencompetitorswithandpotentialpredatorsofhomininsfrombeforewebecamehumansthroughtotoday. Painting:©VelizarSimeonovski.
Figure1.2 Lions(right)depictedonthewallsofSalleduFondinChauvet-Pontd’ArcCave,France,datingto32,000–30,000yearsago.Thelions appeartobewatchingarhinocerosonadistantpanel.Carnivoransweresubjectsofsomeoftheearliestfigurativeart.Verticalscratchesinthe lowerrightandontherhinocerospaintingweremadebycavebearstrappedindeepchambers.
Photo:J.Clottesin Azéma(2015),CC4.0.
Asisoftenthecaseinbiology,thedefiningtraits oftheCarnivora—thetraitsheldbyallmembers ofthelineage,bothlivingandextinct—aredifficult tostatewithoutqualification.Traditionally,biologistshavecitedthepresenceofcheekteeththathave shearingfunctions,comprisingtheupperfourth premolar(P4)andlowerfirstmolar(M1).Allliving carnivoranshaveancestorswiththistrait.However, livinggenets,bears,andsealshavesecondarilylost theshearingfunctionofthoseteeth,andatleast onespecieshaslostthoseteethcompletely.Some prehistoriclinagesofothercarnivorousmammals hadshearingcheekteeth,buttheyoccupiedother positionsinthetoothrow,forexampleM1 andM2. Theywerenothomologoustomoderncarnassials, andthelineagesthatexhibitedthemhavenoliving descendants.Thefusedscaphoidandlunatecarpal bones(thescapholunate)aresometimesregardedas
definingthegroup,becauseallmodernspecieshave thattrait,butsomeearlycarnivoransdidnot.
Predatoryplacentalmammals—thosethatprimarilykillotheranimalsforfood—occurinseveral orders,includingshrewsandmoles(OrderSoricomorpha),bats(Chiroptera),whales(Cetacea),pangolins(Pholidota),andhairyanteaters(Pilosa).If webroadenourframeofreferencetoincludemarsupialpredators,severaladditionalordersmust beincludedasmammaliancarnivores.Evensome obligateherbivores,amongthemungulatesand rodents,preyonorscavengevertebratesopportunistically(Boonstra etal.,1990; Dudley etal.,2016). Finally,manyextinctnon-carnivoranlineageswere atleastpartiallycarnivorous.Clearly,OrderCarnivoraisnotuniqueamongmammalsinkillingand eatingvertebrates.Thisbookisaboutamammalian lineage,notaforagingstyleortrophicniche.
Figure1.3 RockartinnorthwesternSaudiArabiashowingdogsresemblingmodernCanaandogsassistingwithlionhunting.Variousglyphs fromthissiteincludetheearliestdepictionsofdogsonleashes,12,000–10,000yearsold.Theupperimageisshadedtoshowreliefthatisless visibleinthelower,unalteredimage.
Photo:Guagninetal.(2018,Figure10)bypermission.
Figure1.4 Venndiagramofthe relationshipsbetweencarnivory,herbivory, andOrderCarnivora.Herbivorousmammals overlapwiththeCarnivora,andthe Carnivoraoverlapwithcarnivorous mammals.Elephantsareherbivorous non-carnivoranmammals.Thegiantpanda isanherbivorouscarnivoran.Thebrown bearisanomnivorouscarnivoran,neither fullyherbivorousnorcarnivorous.Thetigeris acarnivorouscarnivoran,andthekiller whaleisacarnivorousnon-carnivoran mammal.InthisbookIuse“carnivorous”to denotediet,and“carnivoran”todenote phylogeny—inclusioninOrderCarnivora.
1.2 Thecarnivorans—whoandwhere?
Theapproximately287extantspeciesofcarnivoransareorganizedintofifteencurrentlyrecognized families(AppendixI)andoccuronallcontinents,if weincludesealsthathauloutonAntarcticbeaches. Thesenumberschangeaswelearnmoreabout howmammallineagesarerelated.Forexample,the neotropicalolinguitorecentlyhasbeenidentifiedas distinctfromotherolingos,andtheAfricangolden wolfwasjudgedaseparatespeciesfromthegolden jackal,(Gaubert etal.,2012; Helgen etal.,2013).On theotherhand,thelong-recognizedredwolfofeasternNorthAmericaisnowregardedasanancient hybridofthewolfandthecoyote,withuncertain endangeredspeciesstatus(vonHoldt etal.,2016,but see Hohenlohe etal.,2017).Attheleveloftaxonomicfamilies,theskunksandstinkbadgerswere groupedwithweaselsandottersintheMustelidae beforeFamilyMephitidaewasrecognizedaswarrantingrecognition(DragooandHoneycutt,1999). Witheachsuchdiscovery,ourknowledgeofcarnivoranclassificationbecomesmorereflectiveof evolutionaryhistory,asrevealedthroughgenetic andmorphologicalstudies.
Carnivoranspeciesaredistributedunevenly acrosslineagesandcontinents.FamilyMustelidaeholdssixtyspecies,whereastheNandiniidae, Ailuridae,andOdobenidaeholdasinglespecies each.TheFelidae,Canidae,andMustelidaeare
nearlycosmopolitan,foundonallcontinentsexcept AntarcticaandAustraliabeforehumanstransportedthem.Ontheotherhand,theeightspecies ofEupleridaeoccuronlyonMadagascarIsland, theircommonancestorhavingraftedtherefrom theAfricanmainlandaround20millionyearsago (Ma).Thethirty-threeextantspeciesofseals,sea lions,andwalrusmakeupthepinniped(earfoot) group—alineagecomprisingtwoorthreefamilies thatarosefromasingleaquaticancestor.“Fissiped” (splitfoot),ontheotherhand,denotestheremaining,mostlyterrestrial,non-pinnipedcarnivorans.
1.3 Thegrowthofknowledge
Before1900,understandingofcarnivoranecology (asopposedtonaturalhistory)waslimited,often basedonloreandconjecture.Muchofourknowledgeoftheirgenetics,behavior,andreproduction atthattimeresultedfromobservingdomesticcats, ferrets,anddogs,andfarmedminksandfoxes (Figure 1.5).Verylittlescientificknowledgeabout wildcarnivoransexisted,andmostinterestcenteredonthevalueoftheirfursorotherbody partsandthethreattheyposedtoagriculture.They weredifficulttostudydirectlybecauseoftheirlow densities,elusivebehaviors,andconstantpersecutionnearhumans.Wellintothetwentiethcentury, theleadingecologicalquestionsaboutcarnivorans
Herbivorous mammals Carnivora Carnivorous mammals
Elephant
Giant panda
Brown bear Tiger
Killer whale
dealtwithhowmanyungulates,waterfowl,and othervaluedvertebratestheykilledandhowtomitigatethoselosses(Leopold,1933).Inthelatetwentiethcentury,however,perspectivesshifted,tools improved,andecologicalresearchonthisgroup surged.Thenumberofscientificjournalarticles indexedbyWebofSciencewith“Carnivora”asa topicincreasedbyafactorofelevenfrom1992to 2016,comparedwithafactoroffourfor“mammal”andsixfor“Mammalia.”Newunderstandings ofcarnivoranbiology,especiallyecology,beganto unfoldinthe1960s,whencarnivoransgainedsignificanceinconservationissues,eitherasthreatened taxaorasagentsofendangermentofothertaxa orcommunities.Forexample,theseverecontractionindistributionandabundanceofthebrown bearinthecontiguousUnitedStatesfrom1850 to1950resultedingreatlyexpandedresearchin bearbiology,broadlycast.Of159scientificjournalarticleswiththetopics“grizzlybear + Yellowstone”indexedbyWebofScience,allbuttwowere publishedsubsequenttotheinitial1975listingof theYellowstonepopulationundertheEndangered SpeciesAct.Similarly,noarticlesindexedbyWeb ofSciencedealtwiththepopulationgeneticsofthe cheetahbeforethediscoveryby O’Brienandcolleagues(1983) thatcheetahsexhibitedlowgenetic variability.Thisfindinghadsuchstrongconservationimplicationsthat153subsequentarticles
reportedongenetictraitsofcheetahsrelatedto evolutionaryorecologicalprocesses.Geneticdepletioninothercarnivoranspeciesbecamearesearch focusaswell.
TheAmericanminkisanexampleofacarnivoranthathasstimulatedresearchasaresult ofthegreatecologicalharmitcauses.Introduced toEuropeandSouthAmericaduringthetwentiethcenturyforfurproduction,ittodayposes threatsonbothcontinents,spurringintensivestudy (BonesiandPalazon,2007; Crego etal.,2016).Over thepasttwenty-fiveyears,publishedstudieson theecologyofinvasiveAmericanminksoutside ofNorthAmericahavegreatlyoutnumberedthose conductedwithinthespecies’nativerange.
Thisexpansionofknowledgereflectsthat humansneedtoknowmuchmoreaboutcarnivoranecologythantheydidseventyyearsago. Forexample,publichealthplannersnowmust considerwhetherthemostrapidlyemerging infectiousdiseasesofhumansareinfluencedby thediversityandabundanceofwildcarnivorans (Section11.3.1)(Levi etal.,2012, Hofmeester etal., 2017).Thecurrentincidenceandseverityofsuch debilitatingzoonosesasavianandswineinfluenza, Lymedisease,andtick-borneencephalitismay bemediatedbythepresenceandabundanceof predators—manyofthemcarnivorans—thatkill intermediateoralternatehosts(Thulin etal.,2015).
Figure1.5 Farmedblack-phasered foxesatFrommFoxFarm,Wisconsin,US, intheearlytwentiethcentury.Knowledge ofcarnivoranreproductiveandnutritional physiologyduringthateracamelargely fromobservingdomesticatedandfarmed animals.
Photo:FrommHistoricalSociety.
EventheviralpandemicCOVID-19hasbeenlinked totransmissionoftheSARS-CoV-2virusamong variouswildanddomesticmammals—particularly carnivorans—andhumans.Thecarnivoransinclude domesticdogsandcats,captivetigers,andAmericanminks(VinodhKumar etal.,2020; Hammer etal.,2021).
Atthesametime,carnivoransarecredited withperformingvaluableecologicalservicesnot understooddecadesago.InChapter 6 Ishow thatbearsarerecognizedfortransportingmarinederivednutrientsinsalmoncarcassesfromspawningstreamstoneighboringforestsalongtheNorth PacificRim.Leopardsandpumasprotectsome plantsfromoverusebyherbivores.Fruit-eatingcarnivoranstransportseedsawayfromparentplants, insomecasesmoreeffectivelythanbirdsorherbivorousmammals.LeopardsinIndiaevenreceive creditforreducinghumanfatalitiesinflictedbyferal dogs,althoughleopardsthemselveskillasmall numberofhumans.Eachofthesefunctionsand serviceshasbeenrecognizedorbetterunderstood recently,contributingtoamuchricherandmore nuancedpictureofhowcarnivoransaffecthuman livesandwell-being.
1.4 Purposeandorganization ofthebook
Thisbookisintendedasatextforacollegecourse incommunityecologyorpredationecology,and asareferenceforstudents(academicorotherwise) ofecologywhohavesomebackgroundinbiologicalconceptsandvocabulary.Itemphasizesdocumented,mechanisticexplanationsfortheecologyof carnivoransandspeciestheyinteractwith.Importantly,Idonotreviewallbiologicalknowledgethat appliestotheCarnivora—onlythoseaspectsthat setcarnivoransapart;manyaspectsofcarnivoran biologyresemblethoseofothermammalianorders. Forexample,thevibrissaeofcarnivoransarewell developedandimportantfortactilesensation,but theprimaryresearchmodelforthisorganhasbeen thelaboratoryrat,notacarnivoran.Ananalogous situationexistsforgutfermentation—itisrareinthe Carnivoraandisbetterunderstoodfromstudiesof othermammalianorders.Tohelpwithvocabulary issues,Iprovideaglossaryoftechnicalterms.
Becauseofmyfocusoncommunityecology,the readerwillfindonlypassingmentionofsometopicscentraltocarnivoranbiologyinthepast.These includeintraspecificbehavioralinteractions:sociality,matingsystems,parentalcare,andterritoriality. Thesetopicswereattheforefrontofcarnivoranecologyduringthe1970s—theheydayofinterestinkin selection—buttheyareperipheraltocommunity interactions.Ecologicalsystemsarecomplex,with indistinctboundariesbetweencomponents.Predationrelatestocompetition,andcompetitionaffects populationgrowth.Populationdensityaffectsdispersal,which,inturn,drivescolonizationandbiogeography.Thiscomplexitymakesecologydifficult tocompartmentalize,andmychapterorganizationrequiresthereadertonavigatespecifictopics viatheindex,inadditiontothetableofcontents. Forexample,thereaderinterestedinpopulation biologywillfindcarnivoran-inducedchangesin preypopulationscoveredinChapter 8,butthe demographyofcarnivoransthemselvesistreatedin Chapter 10.Dentaladaptationsaremostlycovered inChapter 2,butsomeotheraspectsofdigestive morphologyfitbetterinChapter 4,thechapteron physiology.Theresponsesofpreyspeciestocarnivoranscanbebehavioral,physiological,demographic,orhaveuncertainmechanisms,andthese processesarecoveredinvarioussections,best locatedviatheindex.Chemicaldefensesagainst carnivoransbypreyandothercarnivorans,andby plantsagainstherbivores,aswellasdetoxification ofvenomsbycarnivorans,areeachtreatedseparately,insectionsbestlocatedintheindex.Habitat ecologyisatraditionalandhighlydiffusetopicthat permeateswildlifebiology.Scarcelyasectionofthis bookdoesnothavehabitataspects.However,no aspectofcarnivoranhabitatecologyseemsunique totheorder,soIfolddiscussionsofhabitatinwith others.
Thisaccountisbasedalmostentirelyonthepeerreviewedscientificliterature.Iusebothprimary andsecondarysources,relyingoncommunity-level analyses,meta-analyses,orreviewswherepossible. Ihavetriedtobecomparativethroughout,contrastingcarnivoranfamilieswitheachotherandcarnivoranswithothervertebratecarnivores,includingmarsupials,reptiles,andbirds.Ihavetended toprefermechanisticallybasedstudiestothose
basedonlyoncorrelativeresultsormodelingand havefavoredwidelyaccessiblepublicationstomore obscureones.
WhileIhavetriedtoenhancethegeographicand taxonomicdiversityofthecasestudiesthatIcited, Irecognizethattheliteratureisbiasedtowardstudiesfromdevelopedcountriesandonhigh-profile orendangeredcarnivorans.Therefore,mypresentationnodoubtincludesculturalbiasesthataffect thegeneralityofmyconclusions.Insomecases whereexamplessupportageneralizationandmultiplepublishedexamplesillustratethepoint,Ihave tendedtociteastudyfromaregionorecosystemthatislesswellrepresentedintheliterature, ratherthananequallyillustrativestudyfromNorth AmericaorwesternEurope.
Someunifyingthemesconnectthevariousfacets ofcarnivoranecology,andIreturntothemfrequently.Thesefactorsexplainmuchofthegreat diversityofformandfunctionacrosstheCarnivora, aswellasmanyofthedifferencesbetweencarnivoransandothermammalianorders.Themost importantarebodysize,metabolicrate,andtrophic level.Allometryisthestudyofbodysizeandits consequences,andthereaderwillnotetherecurringimportanceofallometryinmanyprocessesat physiologicalandcommunitylevels(Calder,1984). Metabolicrateisafunctionofbodysize,body temperature,andmitochondrialdensity,andhas strongexplanatorypowerincarnivoranecology. Trophicleveliscorrelatedwiththesefactors;carnivoransthateatlargemammalianpreyexemplify theconstraintsimposedandbenefitsconferredby highmetabolicrateandlargebodies—highforaging costsandmaintenancecosts—butfoodavailability thatismoreseasonallyconsistentthanforherbivoresorpredatorsofectotherms.Bywatchingfor therecurringmentionofbodysize,metabolicrate, andtrophiclevel,thereadercanappreciatehow muchcarnivorandiversityarisesfromonlyafew principles.
1.5 Contextincarnivoranecology
WhileIsearchforpatternincarnivoranecology, Imakescarcelyageneralizationaboutthisgroup withoutaqualificationorcaveat.Contingencies
havecausedthegrouptoradiateintoanastonishingrangeofphenotypes.Trophicnichedetermines dentition,digestiveprocess,andgutpassage.Sizeof preyspeciesaffectshuntingbehavior,frequencyof predationevents,andcompetitiveinteractionswith scavengers.Contextliesattheintellectualcoreof carnivoranecology,andIhaveembraceditfully. Conservationalsoisanappliedarenainwhich contextisall-important.Carnivoransarewidely regardedasoneofthemostthreatenedmammalian lineages,withseverechallengestospecies,subspecies,andpopulationsacrossEarth.Ontheother hand,carnivoransalsocauseorexacerbateconservationproblemsforotherspeciesthatarerare orthreatened.Furthercomplicatingthepicture, humanshavebenefitedsomecarnivoranspecies(or stoppedpersecutingthem),andothersarereoccupyingtheirformergeographicrangeswithorwithouthumanassistance.Carnivoreconservationdoes notmerelyrepresentasadlistofdecline,dysfunction,anddisappearance,butexamples—admittedly anomalous—ofrestorationandindependentrecovery.Ecologicalandsocio-economiccontextdeterminehowcarnivoransarefaringinthemodern world.Alltold,thebiologyoftheCarnivoraisan extraordinarilyrichsubdiscipline,fullofpattern, nuance,contingency,andrelevancetohumancultureandlivelihoods.
1.6 Nomenclature
Forthecurrentscientificnomenclatureofcarnivorans,IhavemodifiedWilsonandReeder(2005) toreflectrecenttaxonomicrevisions(AppendixI). Commonnamesaremoreproblematic,becauseall arelocalorregional,andusingonerequiresselectingfromamongthoseusedbyvariousindigenous groupsorcolonizingnations,orthenativetongue oftheoriginalnamingauthority.BecauseIwritein English,Idefaulttomylanguage,butIhavetried tousethecommonnameappliedmostgeographicallybroadlywherethespeciesoccurs.Forexample, Pumaconcolor occursfromPatagonia,SouthAmericatoYukonTerritory,NorthAmerica,withmany locallyusednamesoveritsrange.However,the commonnameappliedovermostofthegeographic rangeis“puma,”whichIusehere.
References
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Functionalmorphology
Functionalmorphologyconsidershoworgan-and tissue-levelstructureandcolorationarethebasis offunction.Atsmallerphysicalscales,“histology,”“cellstructure,”and“molecularbiology”are morecommonterms.HereIconsiderstructurewith directecologicalrelevance,importantforlocomotion,preyhandling,crypsis,communication,and reproduction.“Ecomorphology”isasynonym,and livingandfossilcarnivoransarewellrepresented assubjects.Thecarnivoran-specificliteratureon thissubjectfocusesmostlyonthreemorphological regions:theskull,theforelimbs,andthehindlimbs. Theskullissignificantbecauseofthegreatrange offunctionsitperformsandthespatialtrade-offs betweenthem.Theforelimbisimportantbecause itsstructurediffersacrosslocomotorandforaging styles:swimming,diggingthroughsoil,sprinting, andclimbingallleavestrongadaptivesignatures. Toalesserextent,thehindlimbalsoreflectsadaptationstolocomotormodes.
2.1 Theskull
Theskullisthebonystructurewiththemostcomplexdesigntrade-offsandconstraintsofanyvertebratebodypart.Incarnivoransitscomponents havekeyfunctionsindisplay-defense,preycapture, mastication,vision,hearing,balance,olfaction,cranialenervation,andendocrinefunction,aswellas housingthebrain.Thelargestbodyofworkdealing withskullmorphology—dentitionaside—concerns howtrophicspecializationaffectsnon-dentalskull features. Moore(2009,p.197)exploredhowthe ancestralcarnivoranjawjointdivergedintwotrajectoriesfordietaryspecializations.Thejawofmost carnivoransfeaturesadeepmandibularfossaon thetemporal(= “squamosal”)bonethatlimitsthe
lateralmotionofthemandible.Theshearingfunctionofthecarnassialsoccursononesideatatime, andthemandibleshiftstowardtheshearingside foranysinglebite.Moreherbivorouscarnivorans— thegiantpandaandspectacledbears—donothave shallowermandibularfossaeasmightbeexpected forthegreaterrangeofmotionrequiredforgrindingleavesandstems.Instead,theirfossaeareeven deeperthanthoseofmorepredaceouscarnivorans andthemandibleshiftslaterallyduringasinglebite toachievethegrindingeffect.Thischewingmotion differsfromthatfoundinallotherherbivorous mammals.
Theadaptivetrajectorytowardkillingpreylarger thanthepredatorrequiresfurthermodificationto theskull.Thisnicheisoccupiedbylargefelids, canids,someursids,andsomehyaenids.Canine teethmayseemremarkablyuniforminshapeacross extantcarnivorans,butinfactshowstrongmodificationforvariousroles.Thesinglemostbiomechanicallychallengingfunctionoftheskullandteethis applyingjawforcetothetipsofthecanineteeth whilehandlingstrugglinglargeprey(Penrose etal., 2020).However,thattaskdiffersacrosscarnivoranfamilies.Slender,sharpcaninesarefoundin taxa(e.g.felids)thatkillbyquickstabstothecervicalregion(dorsalspineorneckvessels).More robustcaninesoccurinpredatorsthattakelonger tokillpreythatstruggle,orthatconsumebony material.Canidstendtohavemorecurvedcanine teeth,plausiblytoholdstrugglingpreyforlonger times(Pollock etal.,2021),andnotonlymustthe canineteethbestout,butalsothejawadductor musclesandassociatedbonystructuresmustbe strengthened—otherwise,thebraincaseisvulnerable.Theseadductors,originatingfromthesagittalcrest,thenuchalcrest,andthezygomaticarch,
areespeciallypowerfulinpredatorsoflargeprey. Thesagittalcrestrunsantero-posteriorlyalongthe dorsalmidlineandisthesiteoforiginforthetemporalismuscle,thelargestjawadductor.Itinserts onthecoronoidprocessofthemandibleandcloses thejaw.Tallandmassivesagittalcrests,resembling thesailsofsailfish—arefoundinseveralcarnivoranlineages:pinnipeds,hyaenids,ursids,andsome mustelids.Themassetermuscle,anotherpowerful jawadductor,originatesfromthezygomaticarch andinsertsontothelateralmandible.Thenuchal crest,whichfollowsthedorso-posteriormarginof theoccipitalbone,isthesiteofinsertionofneck extensormusclesthatoriginatefromthecervical vertebrae,poweringheadmovementsusedinsubduinglargeprey.Amongcarnivoranpredatorsof largeprey,allofthesestructuresarelargerelativetothefloorofthebraincase(Penrose etal., 2016).
Thebonylabyrinthisacomplexstructurethat reflectsfeedingandnon-feedingforces.Encased inthetemporalbone,itcomprisesorgansofbalance(thesemicircularcanalswithampullae)and hearing(thecochlea).Whilenotfeedingstructures perse,thecanalsarekeytomaintainingequilibriumandspatialorientationbymeasuringangularaccelerationinthreeplanes.Itisthereforean importantsenseformammals,especiallycarnivorans,withactivelocomotorandforagingstyles. Thatis,theymuststabilizetheheadinorderto allowthebraintoprocessvisualinputswhilepursuingandsubduingprey.Schwabandcolleagues (2019)showedthatalldimensionsofthesemicircularcanalswerelargerinambushingcarnivorans thaninomnivoresorpouncehunters.Astrong phylogeneticsignalwasapparentaswell.Other skullfeaturesarecloselytiedtosensorymodalities (Section5.1.2).
2.1.1 Dentition
Muchstudyofmodernandprehistoricdietsof carnivoransandothercarnivorousmammalshas concernedpreyhandling(grippingandkilling) andmasticating.Basalcarnivoranshadtheprimitiveeutheriandentalformula—I3/I3,C1/C1,P4/P4, M3/M3—andteethinsomeofthesepositions evolvedmorequicklythaninothers.Alandmark incarnivorandentitionisthecarnassial(shearing)
pair:P4/M1.Thisfeatureallowsseveringofmuscle andconnectivetissue,sothatpartsoflargecarcassescanberemovedandeitherswallowedorconsumedawayfromthepreycarcass,therebyreducingconflict.TheearliestcarnivoranshadlessprominentcarnassialP4/M1 structuresthandomodern predaceousforms.Alldentalevolutioninvolved changesinsizeandshape,aswellassometooth loss;nocarnivoranlineageshowsanincreasein toothnumber.Incisorshaveundergonerelatively littlechangeinmorphologyornumber,andthe caninesareretainedeveninspeciesthatdonotuse themtohandleprey.Thisreflectsthedualfunctionsofcanines:preyhandlinganddisplay-defense. Aardwolves,bat-earedfoxes,andpandas—none ofthemprimarilypredatorsofvertebrates—have caninessimilarinshapeandonlyslightlysmaller tothoseofvertebrate-killingrelatives.Inatleast fivepredaceousmammalianlineages(twometatherian,threecarnivoran),canineteethbecamesoelongatedthattheyextendedoutsidetheoralcavity. Mostofthesetaxashowedthesaber-toothedcondition,usingcaninesforpreykilling,whereasthe oversizedcaninesofwalrusesfunctionprimarilyin displayanddefense.
Consistentwithadaptivechangestothecarnassialsthemselves,othertoothpositionsreflectthe importanceofkillinglargepreyvs.othertrophic strategies(Figure 2.1).Withspecializationonpredationandameatdietcamethereductioninsizeand numberofthepost-carnassialteeth(M1−3,M2−3).In felids,thebestextantexamples,premolarsP1−2 and P1−2 arelostaswell,becauseadietofanimalsofttissuerequireslittlemasticationbeforeswallowing— duodenallipasesandpeptidasesaresufficient toinitiatedigestion.Thesecondtrajectory—a trendtowardomnivory,frugivory,andfolivory— retainedthepost-carnassialsandmodifiedthem forgrinding,givingthemmulti-cusped,rounded (bunodont)shapes.Bunodontteethcrushinvertebrateexoskeletonsandshells(e.g.inthewalrus andotter),andcoarselygrindplantmaterial(e.g. inbears).Inthehighlycarnivorousspottedhyena, thepre-carnassialpremolarsareenlargedforbone crushing—importantforascavengeroflargeungulatecarcasses.Piscivorouspinnipedstendtoretain large,sharpcanines,buthavelostthepositionspecificfunctionsofancestralcheekteeth,includingthecarnassialpair(Box 2.1).Instead,theytend
Figure2.1 Lowerdentitionsoftheearliestandmoderncarnivorans,showingenlargement,reduction,andlossofcheekteethwithdiverging diets.A: Protictis (Viverravidae),aninsectivore-carnivoreofthePaleocene(M3 lost).B:Modernlion,astrictcarnivore(M2–3 lost).C:Redfox,an omnivore(M2 retained,bunodont,M3 vestigial).D:Giantpanda,anobligatefolivore(M2–3 bunodont).E:Aardwolf,anobligatetermitivore(M2–3 variablyvestigialorlost).F:Californiasealion,anobligatepiscivore(M2–3 lost,post-caninesreducedandhomodont).
M
Figure2.1 continued towardgeneralized,nearlyhomodontcheekteeth (Figure 2.1F),consistentwithswallowingfishwhole orseveringthemintolargepieces(KienleandBerta,
2016).Importantly,carnivorandentalspecializationshavetendedtobeirreversibleoverevolutionarytime;theydisappearvialineageextinction,
(f)
Box2.1Filter-feedingcarnivorans
Severalpinnipedshaveevolvedhighlyspecializedcheek teeththatfacilitatethefilteringofaquaticinvertebrates.The waterisgulpedintotheoralcavityandpharynx,thenejected pasttheprojectionsonthecheekteeth(Figure 2.2).Thetrait hasarisenseveraltimesinthephocidsandinbothfreshwaterandmarineforms.Itreachesitsmostextremeexpression
inthecrabeatersealoftheAntarcticOcean,whicheats almostentirelyfinger-sizedkrill.TheBaikalsealofRussia showsamoremoderateexpressionofthesametrait—it feedsheavilyonfreshwateramphipods(Watanabe etal., 2020).
Figure2.2 Thecheekteethofthefilter-feedingcrabeaterseal,showingdentalprojectionsthatfilterkrillfromseawater.
Photo:©TePapaTongarewaMuseumofNewZealand.
ratherthanbyrestoringlosttoothfunctions.This issimilartomammaliandentalevolutiongenerally,butcontrastswiththatofsquamatereptiles, inwhichmultipletoothcuspsarosetogrindvegetation.Insomelineages,thesecuspsdisappeared, andcheekteethrevertedtounicuspidformasdiets returnedtocarnivory(Lafuma etal.,2021).
2.2Post-cranialskeleton
Noothermammalianordermatchestherangeof morphologicaladaptationsforlocomotionandforagingobservedintheCarnivora.Severallocomotormodalitiesarerecognizable,andsomespecies exhibitmorethanone.Basalcarnivoranswere