ArticlePDF AvailableLiterature Review

Abstract

Because ungulates are important contributors to ecosystem function, understanding the "ecology of fear" could be important to the conservation of ecosystems. Although studying ungulate ecology of fear is common, knowledge from ungulate systems is highly contested among ecologists. Here, we review the available literature on the ecology of fear in ungulates to generalize our current knowledge and how we can leverage it for conservation. Four general focus areas emerged from the 275 papers included in our literature search (and some papers were included in multiple categories): behavioral responses to predation risk (79%), physiological responses to predation risk (15%), trophic cascades resulting from ungulate responses to predation risk (20%), and manipulation of predation risk (1%). Of papers focused on behavior, 75% were about movement and habitat selection. Studies were biased toward North America (53%), tended to be focused on elk (Cervus canadensis; 29%), and were dominated by gray wolves (40%) or humans (39%) as predators of interest. Emerging literature suggests that we can utilize predation risk for conservation with top-down (i.e., increasing predation risk) and bottom-up (i.e., manipulating landscape characteristics to increase risk or risk perception) approaches. It is less clear whether fear-related changes in physiology have population-level fitness consequences or cascading effects, which could be fruitful avenues for future research. Conflicting evidence of trait-mediated trophic cascades might be improved with better replication across systems and accounting for confounding effects of ungulate density. Improving our understanding of mechanisms modulating the nature of trophic cascades likely is most important to ensure desirable conservation outcomes. We recommend future work embrace the complexity of natural systems by attempting to link together the focal areas of study identified herein.
Ecology and Evolution. 2022;12:e8657.    
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https://doi.org/10.1002/ece3.8657
www.ecolevol.org
Received:27August2021 
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  Revised:31J anuar y2022 
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  Accepted :3Februa ry2022
DOI: 10.1002/ece 3.8 657
REVIEW ARTICLE
“Ecology of fear” in ungulates: Opportunities for improving
conservation
M. Colter Chitwood1| Carolina Baruzzi2,3 | Marcus A. Lashley2,4
Thisisanop enaccessarti cleundertheter msoftheCreativeCommonsAttributionL icense,whichpe rmitsuse,dis tribu tionandreprod uctioninanymed ium,
provide dtheoriginalwor kisproperlycited.
© 2022 The Author s. Ecolog y and EvolutionpublishedbyJohnWiley&S onsLtd.
1Depar tmentofNaturalResourceEcolog y
andManagement ,Oklah omaState
University,Still water,Okla homa,USA
2Depar tmentofWildlife,Fisheries,and
Aquaculture,MississippiStateU niversity,
Starkville,Mississippi,USA
3SchoolofForest ,Fisheries,and
Geomat icsSci ences,UniversityofFl orida ,
Gaines ville,Florida,USA
4Depar tmentofWildlifeEcolog yand
Conser vation,Unive rsit yofFlorida,
Gaines ville,Florida,USA
Correspondence
M.Colte rChitwood,De part ment
ofNatura lResourceEcolog yand
Managem ent,Oklahom aStateUniversity,
Stillwater,OK,USA .
Email:colter.chitwood@okst ate.edu
Abstract
Becauseungulatesareimportantcontributorstoecosystemfunction,understanding
the“ecologyoffear”couldbeimportanttotheconservationofecosystems.Although
studyingungulate ecology offear is common, knowledge from ungulatesystemsis
highly contested among ecologists. Here, we review the available literature on the
ecologyoffearinungulatestogeneralizeourcurrentknowledgeandhowwecanlev-
erageitforconservation.Fourgeneralfocusareasemergedfromthe275papersin-
cludedinourliteraturesearch(andsomepaperswereincludedinmultiplecategories):
behaviora l responses to predat ion risk (79%), physiologic al responses to pre dation
risk(15%),trophiccascadesresultingfromungulateresponsestopredationrisk(20%),
and manipulation of predation risk (1%).Of papers focused onbehavior, 75%were
about movementand habitatselection. Studies were biasedtoward North America
(53%),tendedtobefocusedonelk(Cervus canadensis;29%),andweredominatedby
graywolves(40%)orhumans(39%)aspredatorsofinterest.Emergingliteraturesug-
geststhatwecanutilizepredationriskforconservationwithtop-down(i.e.,increasing
predationrisk)andbottom-up(i.e.,manipulatinglandscapecharacteristicstoincrease
risk or risk pe rception) approache s. It is less clear whe ther fear-related changes in
physiology have population-level fitness consequences or cascading effects, which
couldbefruitfulavenuesforfutureresearch.Conflictingevidence oftrait-mediated
trophic cascadesmight be improved with better replicationacross systems andac-
counting for confounding effectsof ungulatedensity.Improvingour understanding
ofmechanismsmodulatingthenatureoftrophiccascadeslikelyismostimportantto
ensure desirable conservationoutcomes.Werecommend future work embrace the
complexityofnaturalsystemsbyattemptingtolinktogetherthefocalareasofstudy
identifiedherein.
KEYWORDS
antipredatorbehavior,predationrisk,predator,prey,trait-mediatedef fects,vigilance
TAXONOMY CLASSIFICATION
Behaviouralecology
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1 |  INTRODUC TION
The ecolo gy of fear was co nceptualize d by Brown et al. (1999) as
the “melding of the prey and predator's optimal behaviors with
theirpopulationandcommunity-levelconsequences.”The ecology
of fear conce pt synthes ized the two ap proaches t o predator–prey
interac tions (Hunter & Pr ice, 1992; Paine, 1980; Peck arsky et al. ,
2008;Polisetal.,2000):(1)predatorskillpreyforfood(Lima,1998;
Schmitz et al., 1997; Taylor, 1984); and (2) predators scare their
prey(Lima&Dill,1990;Peckarskyetal.,2008;Preisseretal.,20 05;
Schmitzetal.,2004;Trusselletal., 2006).These direct(i.e., lethal)
andindirect(i.e.,non-lethal,non-consumptive)effect sof predation
combinetoaffectpreyandtheirinteractionswiththebroaderfood
web,which can generateindirecteffec ts throughprocessesinand
across ecosystems (Hawlena & Schmitz, 2010a, 2010b; Hawlena
etal.,2012;Peckarskyetal.,2008;Schmit zetal.,2010;Teckentrup
etal.,2018).
Theecologyoffearhasgainedmomentuminrecentyears,hav-
ingbeenappliedtovariousterrestrialandaquaticsystems(Dudeck
etal.,2018;Michaudetal.,2016;Nunesetal.,2018).Aplethoraof
literaturehasfocusedonungulateresponsestopredationrisk,likely
becauseungulates andtheir vertebrate predators are oftencharis-
matic(e.g.,graywolves[Canis lupus]andelk[Cervus canadensis])and
thusgarnerthemostattentionfromabroadanddiverse audience,
particularly when set in well-known locations (e.g., Yellowstone
National Park, USA; African savannas). Moreover, ungulates are
widespread globally,important economically and ecologically,and
areoftensympatricwithlarge,apexpredatorsthatareofconserva-
tionconcern(i.e.,threatened,endangered,rare,reintroduced).Thus,
broad rev iew and under standing of t he state of res earch into the
ecologyoffearis warranted, particularlygiventheinterestinusing
theecologyoffearforconser vation(Gaynoretal.,2021).
Recently,researchershavebeguntosummarizeresearchtopics
related tothe ecology offear, including non-consumptive effects
ofpredation(Say-Sallazetal.,2019),theroleoflargecarnivoresin
restorationecology (Alston etal.,2019),methodologicalvariation
inchar ac te rizin gpred ationrisk(Mol let al.,2017),andimprovingin-
ferenceinst udiesofp redatio nrisk(Pr ughetal.,2019).I mp or tant ly,
these studies are highlighting shortcomings andbiases that could
affectconservationandmanagementdecisions.Forexample,Say-
Sallaz et al. (2019)highlighted astrongtaxonomicandgeographic
bias ass oci at edw it hre s ea r ch onn on-co nsu mpt iveef f ect sof pre da-
tioni nl ar geterres tr ialm am ma ls ,n ot in gt ha tgraywo lvesan dN or t h
America dominated the peer-reviewed literature. Likewise, they
determi ned that antipred ator behavioral r esponses of prey com -
prisedthemajorityoftheliteratureonnon-consumptiveeffectsof
predati on (Say-Sallaz et a l., 2019). Other recen t work highlighte d
atendencyamongresearcherstosimplifyotherwisecomplexsys-
tems by focus ing on one carn ivore and one ung ulate when mos t
systems b eing studied h ad multiple spe cies of carnivore s and/or
ungulates(Mont gomeryetal.,2019).St udydesignswit houtexper i-
mentalandlongitudinalcomponentslikelyoversimplifyresultsand
could bemisleadingortoogeneralto be appliedtoother systems
(Montgomery et al.,2019). Thoughthese reviews identify biases
that could af fect large mammal conser vation and management,
none of them summarized the myriad research topics and results
alreadypublishedonungulatesundertheecologyoffearconcept.
Toaddress biases,improvefuture studydesignsonpredationrisk,
andultimatelyimproveourunderstandingof how tousetheecol-
ogy of fear inconservation,wesought to compile and summarize
thecurrentbodyofworkfromwhichfuture studiescoulddevelop
increasinglycomplexquestionsintofeareffectsandtheirrelevance
toecology,evolution,conservation,andmanagement.
2 | METHODS
We conducte d a literature se arch for arti cles using the key words
“ungulate”and“ecologyoffear”or“landscapeoffear”inthesearch
engineGoogleScholar.Wepurposelykeptoursearchtermsgeneral
toallowresearchthemestoemergefromthepublishedrecord,and
weusedeachpaper'sliteraturecitedtosnowballsampleotherrele-
vantwork.Wenotedthatmoststudiesonungulatesandtheecology
offearfailtofullydisentangledirectandindirecteffect s(Peersetal.,
2018);however,wecontendstudiesrelatedtobehaviorandphysiol-
ogy are more well disentangled than those documenting other in-
direct e ffect s in ecosystem s. Thus, we consi dered the ar ticles we
found to be valuable research onthe ecology of fearinungulates,
withthecaveatthatthemechanismsbehindthoseeffects maynot
bedefinitiveinallarticlescited.Also,thoughwereferto“ungulates”
broadlythroughoutthispaper,ourfocuswasonungulatesforwhich
fear-basedpublishedworkappearedinoursearch.Thus,wedidnot
conductsearchesforspecificungulatespecies(commonorscientific
names)orgroups.Wesearchedforstudiesbetween1999(whenthe
ecologyoffearconceptwaspublished)andJuly2018.Additionally,
weestablished aG oogle ScholarAlertthatflaggedpapers indexed
on Googl e Scholar af ter our searc h and before we com pleted our
reviewofallthepapers.Thisapproachallowedustoincludeseveral
paperspublishedin2018a nd2 019,aftertheconclusionofourman-
ual search. Though many ungulate-focused predator–prey papers
before 1999 could also be nested under the ecology offear para-
digm,wechosetofocusonmorerecentliteraturewhereinterestin
the topic a mong acade mics has inc reased, as in dexed by citat ions
peryearofBrownetal.(1999;Figure1).
Aftersurveyingtheliterature,wegroupedpublicationsintofour
areasoffocus,withsomepublicationsf ittingundermult ipl ecatego -
ries.Theareasoffocuswerebehavioralresponsestopredationrisk,
physiologicalresponsestopredationrisk,trophiccascadesresulting
fromungulateresponsestopredationrisk,andmanipulationofpre-
dationrisk.Wedefinedabehavioralresponseasanyreactiveorpro-
active r esponse of ung ulates to pre dation risk s, includin g changes
at fine-scal e (e.g., vigilance) or br oad-scal e (e.g., habitat use). We
definedphysiologicalresponsesas any change inthephysiologyof
ungulatesas a result of predation risks, including changes in body
chemistry (e.g., stresshormones)or diseaserisk. Wedefined atro-
phiccascadeasoccurringwhenpredatorsalteredungulatebehavior,
   
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CHITWO OD eT al .
resultingintherelease ofplants from herbivory (Polisetal.,20 00);
thiscouldincludeanychangeintheplantcommunity(i.e.,plantdis-
tribut ion, abunda nce, or stru cture) resu lting from th e influence of
predationriskonungulates.Also,trophiccascadesincludedcascad-
ingef fectsofungulateresponsestopredation riskon otheranimal
taxaorecosystemprocesses.Wedefinedmanipulationofpredation
riskasanyactiontakenorthat could betaken byhumanstointen-
tionallycausefear(i.e.,increasingperceivedoractualpredationrisk
viatop-downorbottom- upmanagementappr oaches)toevokeade-
sirableecologicalconsequence.
3 | RESULTS AND DISCUSSION
Theliteraturesearchyielded275studiesrelevant totheecologyof
fear in ungulates (Appendix S1). While most paperscovered multi-
pletopics,themoststudiedareaoffocuswasbehavioralresponses
topredation risk (e.g., habit at selection,space use, vigilance; 79%;
n =216;Figure2a).Somestudieswerefocusedontrophiccascades
(20%;n =56),whilefewerfocusedon physiologicaleffects offear
(15%;n =41)and only three(1%)on manipulation ofpredation risk
for wildlifemanagement (Figure2a). More than half of the studies
tookplaceinNorthAmerica(53%;n =145;Figure2b),mainlyinthe
GreaterYellowstoneEcosystem(n =60;22%of all studies;41%of
NorthAmericanstudies). Fewer studies were conducted in Europe
(20%; n = 56), Sub-Sahar an Africa (16%; n = 45), and othe r world
regions (11%;n =29; Figure2b). Overall,81ungulatespecieswere
studiedsince thefear concept was first published, with studies of
elkcomprisingthelargest proportion(29%;n = 79;Figure 3a).The
majorityofresearchwasfocusedonjustafewpredators,dominated
bygraywolves(40%;n=111;Figure3b)andhumans(39%;n = 107;
Figure3b)thattogetheraccountedfor79%ofthestudies(n =218).
3.1  |  Behavioral responses to predation risk
Inthepresenceofpredators,prey generally alter theirbehaviorto
becomemoredifficulttocapture,detect,orencounter.Antipredator
behaviorsare acomplexsuite ofinnate andlearnedbehavioralre-
sponses, which can be individual or species-specific (Chamaillé-
Jammes et a l., 2014; Thurfjel l et al., 2017). They can b e affected
by predator s pecies and hab itat charac teristic s. For example, a m-
bush pred ators make animals m ore fearful of com plex vegetative
struc ture with poor vis ibility likely be cause of uncert ainty in the
FIGURE 1 Thenumberofcitationsperyear(accordingto
GoogleScholar)ofBrownetal.(1999),whoconceptualizedthe
ecologyoffear
20
40
60
80
100
2000 2005 2010 2015 2020
Year
Number of citations
FIGURE 2 Proportionofresearchpapersfocusedoneachoffourmajortopicareasofstudy(a)andpropor tionofresearchpapersby
geographicareaoffocus(b).Becausepaperscouldcovermultipletopics,proportionsinAdonotsumto1
0.4%
0.4%
0.4%
1%
3%
3%
3%
16%
20%
53%
Central Asia
North Africa
Oceania
South Asia
Latin America
Middle East
East Asia
Sub Saharan Africa
Europe
North America
0% 20%40% 60% 80%
1%
15%
20%
79%
Manipulation of Risk
Physiological Responses
Trophic Cascades
Behavioral Responses
0% 20%40% 60%80%
(a) (b)
4 of 15 
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   CHITWOOD eT al .
predator l ocation (Lone et a l., 2014), whereas curso rial predators
makeanimalsmorefearfulofareaswithhighvisibilityand poor es-
capability(Riginos&Grace, 2008;Ripple &Beschta,2003,2006a).
Additio nally, human ac tivities c an elicit fea rful res ponses in un gu-
lates and, in human-dominated landscapes, human presence and
activ ity can af fect ungu late behavior a nd predator–prey d ynamics
(Ciuti et al., 2012; Shannon et al.,2014).Humanhunting couldop-
pose adaptive responses to nat ural and sexual selection through
exploit ation-induced evolutionary change (Ciuti et al., 2012). We
separatedthestudiesofungulatebehaviorinresponsetopredation
risk (n = 216) into two subtopics: movement and habitat selection
(75%;n =161)andvigilanceandherding(32%;n =70).
3.1.1  |  Movementandhabitatselection
Habitatqualit yisimportantto howungulatesreducepredationrisk
(Bleicher,2017).Infact, animalscanmitigatepredation risk in vari-
ouswayssuchasreducing the time spent foraging, foraginginless
riskyareasoratlessriskytimes,orincreasingvigilancewhenforag-
ing in risk y places (Brow n, 1999; Gehr, Hofer, Ryser, et al., 2018).
Inthisway,animalsmovearound the landscape adjusting theirbe-
havior to accommodate spatiotemporal variation in predation risks
(Basilleetal.,2015).
Spatial avoidance is commonly reported in ungulates to reduce
predationrisk, but less workhasdocumentedtemporalchanges to
avoidrisk. Severalspecies suchas muledeer(Odocoileus hemionus;
Laundré,2010),elk(Bacon&Boyce,2016; Fortinetal.,2005), and
hartebeest (Alcelaphus buselaphus; Ng’we no et al., 2017) exhi bit a
negative relationship in spatial distribution with predation risk.
However, avoidance c an be mediated by r esource availab ility. For
example , hartebees t, plains zebra (Equus quagga), an d Grant's ga-
zelle (Nanger granti) prefer a reas with high g rass biomass t o areas
ofhighvisibilit yduringdroughts(Riginos,2015).Astudyofac tivit y
patternsinSundacloudedleopard(Neofelis diardi)showsthatinthe
absenceofcloudedleopards,beardedpigs(Sus barbatus)weremore
nocturnalthanwhenleopardswerepresent,perhapsindicatingthe
beardedpigs altertheir activity pattern to decrease predation risk
(Rosseta l. ,2013) .O nes tud yl ookedatro ed eer (Capreolus capreolus)
spatialandtemporalbehaviorreportingthatroedeeravoidareasof
highchronicpredationby Eurasian lynx (Lynx lynx)at nightbutnot
duringthedayinsummerbecauselynxactivityislowduetohuman
disturbanceduringtheday(Gehr,Hofer,Pewsner,etal.,2018).
Thedecisionofwhereandwhentoforageorseekcoveroccurs
across spatiotemporal scales (Lima & Dill, 1990) and even small
habitat changes can playan import antrole in prey habitat selec-
tion because they affect prey cost oflocomotion (Gallagher etal.,
2017). Altend orf et al. (2001) con cluded that mule de er respond
topredation risk from mountain lions (Puma concolor)by changing
their foraging decisions at the scales of vegetation types and spe-
cific featuresofthevegetationt ype such as edges.Atfiner scales,
many studies have documented behavioral responses to predation
riskrelatedtoforageselectionandquality.Forexample,bison(Bison
bison)reducedselectionofhigh-qualit yforagingsites(i.e.,siteswith
abundantCarex atherodes)aswolfriskincreasedinwinter(Fortin&
Fortin,2009).HamelandCôté(2007)repor tedthatfemalemountain
goat s(Oreamnos americanus)tradedoffforageabundance(andsome
forage quality) for safetycover.Similarly, some studies have linked
behavioraleffectsofpredationrisktofine-scalelandscapefeatures
and vegetative cover. For example, Nubian ibex (Capra nubiana)
FIGURE 3 Proportionofresearchpapersfocusedondifferentungulatetaxa(a)andproportionofresearchpapersfocusedondifferent
predatortaxa(b).Becausepaperscouldincludemultipleungulateandpredatortaxa,proportionsdonotsumto1
3%
4%
4%
5%
5%
5%
5%
5%
6%
11%
39%
40%
Lynx lynx
Acinonyx jubatus
Ursus americanus
Lycaon pictus
Panthera pardus
Ursus arctos
Crocuta crocuta
Canis latrans
Puma concolor
Panthera leo
Homo sapiens
Canis lupus
0% 10% 20% 30% 40%
3%
3%
3%
3%
3%
3%
4%
4%
4%
5%
6%
7%
7%
7%
7%
7%
8%
8%
29%
Alcelaphus buselaphus
Giraffa camelopardalis
Nanger granti
Taurotragus oryx
Phacochoerus africanus
Sus scrofa
Tragelaphus strepsiceros
Bison bison
Syncerus caffer
Connochaetes taurinus
Aepyceros melampus
Odocoileus hemionus
Rangifer tarandus
Alces alces
Capreolus capreolus
Cervus elaphus
Equus quagga
Odocoileus virginianus
Cervus canadensis
0% 10%20% 30%40%
62 other species of ungulates each comprise
less than 2% of research papers
19 other species of predators each comprise
less than 2% of research papers
(b)(a)
   
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  5 of 15
CHITWO OD eT al .
perceivedgreater risk of predation as their distance fromcliff and
slope edgesincreased, and theirperception of risk decreasedwith
vegetativecover (Iribarren& Kotler, 2012). Likewise, Kuijper et al.
(2013)lin kedco ar se woodydebristofine-sc al eriskef fectsonungu-
latesinthepresenceofwolves.
Movement,spaceuse,andhabitat selection also likely relateto
predatorhuntingmode.Forexample,astudyinSouthAfrica(Thaker
etal., 2011)using seven ungulates andfive largec arnivores deter-
minedthatmostof thesmallerprey species(e.g.,impala[Aepyceros
melampus])avoidedthespaceuseofallpredatorstoreduceprobabil-
ityofencounter.Concomitantly,largerspecies(e.g.,bluewildebeest
[Connochaetes taurinus])onlyavoidedareasofintensespaceuseby
lions(Panthera leo)andleopards(Panthera pardus).Theauthorscon-
cludedthatungulates usedasimplebehaviorrule:avoid areasused
bysit-and-pursuepredators(lionandleopard)butincreasewariness
inareasusedbycursorialpredators(e.g.,cheetah[Acinonyx jubatus]
and African wild dog [Lycaon pictus]).Similarly,otherstudiesusing
predator excrementatforaging areasmonitored withcamera traps
demonstrated red deer (Cervus elaphus) were not only app arently
able todiscernhunting modefromthe typeofexcrement present,
but also us ed different ant ipredator behavio rs to mitigate risk of
each thr eat (Wikenro s et al., 2015). Red de er spent less t ime for-
aging at sites whenthreatened by ambush-style predation riskbut
onlyadjustedvigilanceundercursorial-stylepredationrisk.Multiple
decision rulescombine to affect ungulatespace use (and otheran-
tipredator behaviors), especially in multi-predator systems where
predatorsdifferinhuntingmode(Thakeretal.,2011).
Some stu dies have repor ted weak eviden ce for behavior al re-
sponsestopredationrisk.Forexample,Nicholsonetal.(2014)found
littlesuppor tthatmoose(Alces alces)habitatusewasdependenton
predationriskfromwolves, thoughtheyacknowledged severalun-
derlyingexplanationsthatcouldhavebeenconfounding(i.e.,intense
harvestbyhumans, no time to adaptto recolonizingwolves, adap-
tation mayoccur atfiner scalesthanmeasured).Similarly,Samelius
et al. (2013) conc luded that recol onizing lynx (Lynx lynx) had lim-
itedef fect son habit atselectionofroedeer(Capreolus capreolus)in
Sweden.Theauthorssuggested theirresultsprovided evidencefor
the compl exity of prey r esponses to r isk and that suc h responses
li ke lywer eva ria ble bet w eenec osy s tem sa n dp red ato r–p reyco nst el-
lations(Sameliusetal.,2013).ResultsfromHernándezandL aundré
(2005) may support this premise,astheyconcludedthatpredation
pressurefrom reintroduced wolvesshiftedelkhabitatuse thereby
decreasingtheirdietqualitybutdidnotresultinasimilarchangein
spaceuseordietqualityofbison.Theweakevidenceforbehavioral
responsesto predation risk inthese studies, coupledwithdiffering
responsesofsympatricungulates,maybelinkedtopredatorhunting
mode(Thakeret al., 2011),antipredatorstrategiesoftheungulates
(Ebyetal.,2014),sizediscrepanciesbetweenpredatorandprey(Eby
etal., 2014),a lackofa response, or failure to detectitwith study
designorsamplesize.
One intere sting behavioral concept that relates to movement
and habit at select ion is the idea th at ungulates ar e using intragu -
ild intera ctions to me diate the land scape of fea r by concentrat ing
activity in proximity to humans as a shield to other predators
(Berger, 2007; Schmitz et al ., 2004). Beca use humans are preda-
tors of ungu lates, situat ions where hum ans are used as sh ields to
otherpredators representaninteresting twist, whereby ungulates
apparen tly perceive h umans as les s threatenin g than other p reda-
tors.Thus, ungulatesmayactuallyuseacarnivore'sfearofhumans
totheirownbenefit.For example, Berger(2007) documented syn-
chronyinmooseparturition,whichinvolvedchangesinmoosespace
usecommensuratewithcarnivorerecolonization.Mothersinareas
free of brown bears(Ursus arctos) and non-parous females did not
alterspaceuse,whilethosegivingbirthdidsonearertopavedroads
avoidedbybrownbears(Berger,2007).Similarly,muledeerfemales
appear tocompensateforgreaterexposuretopredationriskby in-
creasing theirac tivit yandherbivoryintensit yclosetoa remotebi-
ological field station, presumably because they could forage more
selectively in areas coyotes avoided due tohuman activit y (Waser
etal.,2014).Suchresultsindicatethatshift sinspaceuselikelyhave
occurredin other mammalian taxa in the presence of humans and
thatresearchersshould accountfor indirect anthropogeniceffects
on species distributions, behavior, and interactions (Berger,2007).
Fearofthehuman“superpredator”mayberelevantforlargecarni-
vores(Smithetal.,2017)andungulates(Crawfordetal.,2022)alike,
buttheextenttowhichsuchfearvariesacrosslandscapesandtaxa
isunknown.Forexample,predatorssuchascoyotesmayberesilient
tourbanization,andthus,initiateevenmorecomplexpredator–prey
interactionsinurbanareas(Jonesetal.,2016).
3.1.2  |  Vigilanceandherding
Vigilanceofpreyspeciesisoneoft hemoststudiedaspect sofan-
tipredatorbehaviorbecauseitisoneofthemostcommonadapta-
tio nsusedb yanimalsforeva lu atingpr ed at ionrisk an disre lativel y
easy to mea sure (Benois t et al., 2013). Time sp ent scanning f or
predatorsgenerallypreventsanimalsfromotheractivities(butsee
Périquetetal.,2012andBergvalletal.,2016),suchasforagingor
grooming,sothatanimalsmustcarefullytradebetweenreducing
riskandacquiringenergy (Creel,2018;Illius& Fitzgibbon,1994).
Theamountoftimeallocatedinvigilancedependsonriskpercep-
tion.Forinstance,Drögeetal.(2017)showthatAfricanungulates
(i.e.,ha rte be est ,plai nzeb ra,an do ribi[Ourebia oribi])increasevigi-
lancewhenclosetopredatorsinplaceswherepredatorencounter
probabi lity is high. V igilance als o depends on h erd size beca use
herdingungulates generallyrelyon group vigilancesothatindi-
viduals can spendless time scanningfor predators as groupsize
increases(Lima& Dill,1990). As such,herdsizeis also relatedto
riskperception.Forinstance,Molletal.(2016)repor tedthatherd
sizeinsever alAfricanun gu lates pe ciesdepends onpreda torhunt-
ing mode anddurationofpredation risk.However,vigilanceand
herd size are not alwaysdirectlyrelated,astheyalso dependon
other fa ctors affec ting individ ual risk such as rep roductive s ta-
tus(Lietal.,2012),sex(Barnieretal., 2016;Benoistetal.,2013),
offsp ring presen ce (Blanchar d et al., 2017; Lashley et a l., 2014),
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intraspecific competition (Biggerstaffetal.,2017;Fattorini etal.,
2018), habitat features (Pays et al., 2012), cover and visibility
(Iranzoetal .,20 18;Paysetal .,20 12 ),preyfora gi ng st rateg y( Cr eel
etal.,2014),andpredatorpresence(Iranzoetal.,2018).
We still do not fully understand the nuances of antipredator
behaviorslikevigilance andherding (Beauchamp, 2019).Forexam-
ple,Creel et al. (2008)determined that Gallatinelkweremore vig-
ilantthanNorthernRange elk despitelowerbackgroundriskin the
Gallatin C anyon. Ind eed, Le Sao ut et al. (2015) prov ided eviden ce
thatvigilancebehavior probably persists atsome level,evenin the
absence of predation risk. Pre sumably, the costs ass ociated with
overt vigilancearetoolow in some casesto generatestrong selec-
ti o npre s s u ref o rnon - v igil a ntp h e n ot ypes, p a r t icul a r l ygi v ent h e con-
sequencesofbeingunequippedtoavoidpredationinthefuture(Le
Saoutetal.,2015).Likewise,thelevelofriskmayinteractwithgroup
size to affec t vigilance re sponse in some c ases but not in oth ers,
andvigilancemayalsobeusedtomonitorconspecifics,especiallyin
low-risksituations(Beauchamp,2019).Olfactory andauditor ycues
areusedtoassessrelativerisk,buttheyarealsounderstudied(Lynch
et al., 2014). For example,the odor of wolves and lynx cancreate
fine-scal e risk facto rs for red dee r (Kuijper et al., 2 014;Wi kenros
etal.,2015). As noted earlier,reddeer apparentlydiscernbet ween
thepredatorhuntingmodebasedonodorsfromexcrement,adjust-
ingtheir antipredator strategyaccordingly(Wikenroset al., 2015).
However,ourunderstandingofhowolfac toryandauditor ycuesare
usedin avoiding predationriskisrudimentary,andweneedfurther
researchtoevaluatetheuseofolfactor ycuesindifferentspecies.
3.2  |  Physiological responses to predation risk
Ungulatesmustbalanceforageacquisitionandriskavoidance,which
necessitatesinterplaybetweenphysiologyandbehavior(McAr thur
etal.,2014).Ascantamountofresearchgoesevenfurther,likening
ungulatep hysiologic alre sp on se st opar as it is manddiseaseto th er e-
sponsesdocumentedunderfearofpredation.Behavior,asdiscussed
intheprevioussection,isaninterfacethatenablesungulatestouse
orleaveforage patches depending on theirphysiological tolerance
torisk (McArthuret al., 2014).By default,these behavioralchoices
inresponsetopredationriskca nberelatedtodietqualityandnutri-
tionalcosts,andwechosetoincludedietqualityandnutritioninthis
section,whilerecognizingthattheyaretopics arguably sortedinto
“behavior”aswell.Weseparatedstudies on ungulatephysiological
responsestopredationrisk(n =41)intotwosubtopics:dietquality
andnutrition(71%;n =29)andfitnessandphysiolog y(32%;n =13).
3.2.1  |  Dietqualityandnutrition
Behavioral responses adopted by prey species under threat of
predation induce import ant risk effects on the prey, especially
nutrit ionally-me diated risk eff ects. As p reviously ment ioned, prey
mayswitchtolowerqualityfoodpatchesifriskisdecreasedenough
towarrant the cost toforagingor ungulates mayreduce theirfood
intaketoincreasevigilance.Forexample,plainszebrasincloseprox-
imity tolions had a lower quality diet,indicating that adjustments
in behavio r when near lion s carry nu tritional cos ts (Barnie r et al.,
2014). White-t ailed deer (O. virginianus) switche d to an abundant
low-quality food (i.e.,oak Quercus spp.) in responsetostressfrom
coyotes(Cherry,Warren,et al., 2016).Similarly,predationpressure
fromreintroducedwolvesintheGreaterYellowstoneEcosystemin-
ducedshiftsinelkhabitatuse,whichloweredthequality oftheelk
diet(Hernández&Laundré,2005).However,nutritionally-mediated
riskeffectsarenotnecessarilyubiquitousinallpredator–preyrela-
tionships,asHernándezandLaundré(2005)alsoreportedthatbison
didnotdisplayasimilarchange inhabitatuseanddietaryqualityto
whattheyobservedinelk.
An emerg ing literature bas e also indicates th at predation risk
cancausephysiologicalchangesthataltertheperceivedrelativeim-
portanceofnutrients,which mayaffectdietarychoicesandhealth
(Hawlena & S chmitz, 2010b). Th is has been well de monstrated i n
an arth ropod syste m where spide rs change diet se lection of pr ey
by changing i ts physiologic al demands for c arbohydrates (B arton,
2010;Beckermanetal.,1997;McMahonetal.,2018;Rothleyetal.,
1997; Schmitz, 1998). Interestingly, similar results have been re-
portedinvertebratetaxa(Carmassietal.,2015;Clinchyetal.,2013;
Klingamanetal.,2016;Leaver&Daly,2003),butexamplesfromun-
gulateshavenot beenrepor ted.Althoughdemonstratingpredation
risk inducingphysiological changes that manifest in health and be-
haviorisinherentlydifficult,thisnewfrontierofmergingnutritional
ecologywithpredationrisktheoryhasthepotentialtoadvanceour
understandingoftheecologyoffear.
3.2.2  |  Fitnessandphysiology
Boonstra (2013) suggested that several ungulate species that
evolved with largepredatorsare adaptedtocoping with predation
pressureandthereforethey sufferfrom acutestress (i.e.,elevated
glucocor ticoidsblood levelfor minutestohours). Onthe contrary,
othermam ma ls pecie ssuc ha ss no ws hoehareorarct icgroun ds qu ir-
rel may suf fer from chronic s tress showing elev ated chronic (i.e.,
daystoweeks)glucocorticoidsbloodlevel,whichmayhavenegative
fitnessconsequences(Boonstra,2013),evenforfuturegenerations
(Sherif f et al., 2010). Some research investigating glucocorticoid
stresshormonesstudyingungulatesreportedsimilarpatterns(Creel
et al., 20 09; Le Saout e t al., 2016; Pecore lla et al., 2016; Pér iquet
etal.,2017;but seeZwijacz-Kozicaetal., 2013),but further inves-
tigationonungulatehormonalresponsetopredationanditsfitness
consequencesareneeded.Infact,predationhasbeenrelatedtode-
creased fecundity in hartebeest (Ng’weno et al., 2017)and white-
taileddeer(Cherr y,Morgan,etal.,2016,butseeMicheletal.,2020)
andcontrastingresultshavebeenreportedinelk(Creeletal.,2011;
Middleton et al., 2013). Predator-induced stress and selection of
low-qualityforagetoavoidpredationhavebeensuggestedtocause
decreas ed fecundity (C hristianson & Cre el, 2010; Ng’weno et al .,
   
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CHITWO OD eT al .
2017),butthespecificpathwaysthroughwhichpredationindirectly
affectindividualfitnessstillhavetobedefined.
3.3  |  Trophic cascades resulting from ungulate
responses to predation risk
Ungulatesrepresenttheintermediatetrophic level,potentiallylink-
ing apex predators to changes in plantcommunities. Thus, trophic
cascades are caused via behavioral adjustments and density re-
sponsesofungulatestopredationriskthat,inturn,affectthedistri-
butionsandrelativeabundancesofplantsandmayindirectlyaffect
other biota and ecological processes as well (Beschta & Ripple,
2009;Estesetal.,2011;Ripple&Beschta,2012;Ritchie&Johnson,
2009). Two type s of trophic ca scades have be en describ ed in the
literature: (1) density-mediated, and (2) trait-mediated (Werner &
Peacor,2003).Density-mediatedtrophic cascades occur asa result
ofungulatepopulationregulationbyapexpredators,whichrelease
palatable plant species fromherbivory.Trait-mediatedtrophiccas-
cadesresultfromungulateantipredatorbehaviorsinresponsetothe
perceptionofpredationrisksthatareinvokedbypredators(seepre-
vioussectionsonbehavior and physiology for examples ofspecific
traitmodifications).
Trait-mediatedtrophic cascades could releaseplantsfromher-
bivory d ue to spatial avoida nce or decrease s in foraging ra te due
topredatorpresence(Ripple etal.,2016).Studieson trait-mediated
trophic c ascades generally entail systems with a single prey and
predator,whichcreatesaknowledgegapregardingtrophiccascades
inmorediversepredatororpreycontexts(Flageletal.,2016;Ripple
et al., 2015). Many historical ecosystems had multiple predators
with each hunting mo de, making the behavioral decisions of the
ungulatemorecomplicatedandthe resulting trophic cascadepre-
sumablymorecomplex;thus,thetri-trophiccasc adegenerallystud-
iedmight not represent all complex situations (Norumetal.,2015;
Schmitz et al., 200 4; Thaker et al., 2011). For example, Ford et al.
(2015)repor tedthatthereintroductionofAfricanwilddogs(Lycaon
pictus)suppresseddikdik (Madoqua guentheri) populations but did
notresultintrophiccascadestotheplantcommunity,likelybecause
ofherbivorediversity inthesystem.Furthermore, surrogatepred-
ators, ei ther introduced o r invading, may or may not c ause trait-
mediated trophiccascadessimilar to that ofnative predators, even
iftheyhavethesamegeneralhuntingmode.Asanexample,coyotes
have recently expanded their range acrosseastern North America
(Hody&Kays,2018),andstudiesinthesoutheasternUnitedStates
haveimplicated themas an importantpredatorand primary cause
of sharp population declines of white-tailed deer in some areas
(Chitwo od et al., 2014; Chit wood, Lash ley,K ilgo, Moorma n, et al.,
2015; Chitwo od, Lashley, Kilgo, Pol lock, et al., 2015; Kil go et al.,
2012). Thoug h they are coursin g predators sim ilar to the primar y
historical predator(i.e., red wolf [Canis rufus]),recentliterature has
repor ted coyote selec tion agains t behavioral t raits of whit e-taile d
deer that h ad presuma bly evolved as an a daptive res ponse to red
wolves(Chitwoodetal.,2017).Moreover,coyotesaremoreresilient
thanwolves tourbanization,so they may exertgreater controlson
ungulate s in urbanized lands capes (Jones et a l., 2016). That said,
coyotescanhavecascadingeffectsonplantcommunitiesbyaltering
traitsofwhite-taileddeer(Cherry,Warren,etal.,2016).Considering
the rapidly changing climate and burgeoning human urbanization,
theex pec tati on sofpredator se xp andingranges intonewar ea sisre-
alis ticandt heeffe ct sofnewpredatorsandnewpredator–preycon-
texts may becomeanincreasingly impor tant areaof focus.Indeed,
trait-mediated trophiccascadescan be mediatedbyseveral poten-
tially interactingfactors, leading to debateonthe actual existence
ofthe trophic cascades. Many observations have been scrutinized
andcontrastingresultshave beenpresented (Creel&Christianson,
2009;Kauffmanetal.,2010),bringingintoquestionwhetherornot
trait-mediatedindirecteffectsareimportantpartsofecosystemsor
rather ju st the resul t of research fa iling to disent angle them f rom
density-mediatedmechanisms.
Predic ting the stren gth of trophi c cascades (i .e., how far they
reachacrosstaxaandecologicalprocesses,aswellasthemagnitude
of their ef fects) is com plicated bec ause a multit ude of factor s af-
fectsthis phenomenon(Schmitzet al., 200 4).ShurinandSeabloom
(2005)r epo r te dth es t re ngthofcascad eswasre lated to sizedis cr ep-
ancybetweenherbivoresandplants,whereaspredatorbodysizein
relation to the ungulatehadnoeffect.Contrastingly,DeLong et al.
(2015)reportedthatpredatorbodysizewasimportantindetermin-
ingthestrengthofresultanttrophiccascadesbecausethestrength
ofpredator-preyinteractionsgenerallyincreaseswithpredatorsize.
Also,predatordensitymightbeimportantinthestrengthofthere-
sultingtrophicc ascades.Forexample,BeschtaandR ipple(2010 )re-
po rte dt herei nt rod uc t io no fM exi canwolv es (C. lupus baileyi)didnot
resultinatrophiccascadeonaspeninArizona,perhapsbec ausethe
densityofwolveswastoolowrelativetoelkdensities(i.e.,3wolves
per100elk).
There are t hree ways trophic cascades are gener ally studied:
(1)p redator rem oval or exclusio n, (2) predato r reintrodu ction, an d
(3)ungulate exclusion(Sheltonet al.,2014).The first two methods
are fundamentally dif ferentin that predator removals are measur-
ing the tro phic cascad es leading to what is cons idered ecologi cal
degradation (Côté et a l., 2004), and predator reintroduc tions are
measuri ng trophic casc ades presum ed to be leading to e cological
restoration(Ripple&Beschta,2004).Thethirdapproach(i.e.,ungu-
lateexclusion)maystudytrophiccascadesfromeitherpointofview,
andthemethodsmaybepairedtoyieldstrongerinferences(Ford&
Goheen,2015).
3.3.1  |  Predatorremoval
Predator removal experiments have been conducted to measure
the cascadingeffects inmany systems dominated by avian, lizard,
and ant predators (Schmitz et al., 2000). However, large preda-
tor removal expe riments are more di fficult to co ntrol at the sc ale
needed to stud y ungulate sys tems. The wi despread e xtirpat ion of
apexpredatorshasgivenrisetoseveralopportunities,albeitusually
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with poor replication, to study how ungulates af fect ecosyste ms
without p redation risks (Ritchie et al., 2012). In systems with out
predators,ungulatepopulationsmayincreasesubstantially,degrad-
ingtheplantcommunityasaresultofintenseunimpededherbivory
(Côté et al., 20 04). Seve ral exampl es exist to cor roborate th is no-
tion.Bergeretal.(2001)foundthatthelossofgrizzlybearsandgray
wolvesledtothedegradationofriparianareasviadensity-mediated
moose herbivory,which erodedthe bird community in the Greater
Yellowstone Ecosystem. Ripple and Beschta (2006a) repor ted a
density-mediatedtrophiccascadelinkingincreasedhumanpresence
tocougardeclines,increasedmuledeerdensity,decreasedcotton-
wood regen eration, incr eased soil erosi on, and decreas ed aquatic
and terrestrial diversit y in Yellowstone National Park. Likewise,
Wallach et al.(2010) reported that predator control of dingoes (C.
lupus dingo)resultedinpopulationincreasesininvasive herbivores
anddecreases inbiodiversity.Finally,inareview,Estesetal.(2011)
detailedmanytrophiccascadesthroughdifferenttrophiclevelsand
ecologicalprocessesresultingfromtheextinctionofapexpredators,
includingalterationsofdiseasedynamics,wildfireonthelandscape,
carbonsequestrationpatterns,invasivespeciesinvasionsandpreva-
lence,andbiogeochemicalcycles.
Interestingly,recent evidence has indicated that ungulate den-
sitiesmayexceednutritionalcarryingcapacityfor decadeswithout
nutritionalfeedbackonthepopulation(LeSaoutetal.,2014).That
sameresearchalsohighlightsthedisparitybetweenstablestatesof
ungulatepopu la ti on sw it ha ndwitho ut pr edatorsan dhowdr as tica l-
ternativestablestatesinungulatepopulationsmayaffectecosystem
process es. The ext ensive herbi vory pres sure may result i n natural
selectionfavoringplantspecieswithheightenedherbivorydefenses
(Strauss &Agrawal, 1999) or induce plant defenses within species
(Stotzetal.,2000).However,top-downcontrolslikelywilllimitver-
teb ratep opulationstoalowerdensitythanb ot tom-upcontr ols,c re-
atingthedisparityinstablestatesoftenobser vedbetweenpredator
andpredator-freeenvironment s(Terborghetal.,20 01).
3.3.2  |  Predatoraddition
ThereintroductionofwolvestoYellowstoneNationalParkhaspro-
vided thestandard example of how fearaffects ungulates in ways
thatc ascadeto plant communities,dependentwildlifespecies,and
other ecological processe s (Beschta & Ripple, 2009; Estes et al.,
2011; Ripple & Be schta, 2006 b, 2012; Ritchie & John son, 2009).
Wecommonlythinkofthescenarioasrestoringecosystemfunction
because the predator rever ts ungulate populations and behavior
fromthealternativestablest atebacktothehistoricalstablestate.
These“naturalexperiments”providetheopportunitytoevaluatethe
resilien ce of an ecosyste m to the altern ative stabl e state bec ause
wecanobserve the recover yofecologicalprocesses.For example,
Ripple andBeschta(2003)monitored cottonwoodrecovery follow-
ing reintroduction of wolves and noted that riskier sites had taller
trees an d greater ann ual growth , and height w as signific antly cor-
related to gu lly depth, whic h is linked to escap ability or risk iness
of the area . Those areas we re most susce ptible to her bivory con-
sequences following the extirpation of wolvesbut also were more
resilient b ecause of a fas ter recovery ti me. The reintro duction of
pre dator smayprovisi ono there cosyste mser vicesthatarenotread-
ily anticipated. For example, wolves affect grazing by ungulates in
waysthatcascadestoalte re dmicr ob ialac tivityan dnutrient dy nam-
icsofgrasslands(Frank,2008).Rippleetal.(2014)reportedanother
examplewherewolfpresencemodulatedgrizzlybeardietindirectly
byaffecting fruit production through the regulationofelk density
andforagingbehavior.Eventhegeomorphologyofriversmaybeaf-
fectedbyherbivorydifferentlydependingonwhethertheungulates
areforagingundertheriskofpredation(Beschta&Ripple,2012).
3.3.3  |  Ungulateexclusion
Ungulate h erbivory c an have ecosystem w ide and long-te rm con-
sequences. For example, Nuttle et al. (2011) demonstrated in a
long-termungulateexclusionexperimentthathighwhite-taileddeer
densityatstand initiation resulted in century-long changes in eco-
system func tion, includingsimplifiedforest structureandcomposi-
tion,decreasedcanopy foliage density,decreased insect diversity,
and decreased bird diversity. Similarly, Shelton etal. (2014) used
ungulate exc losures to show t hat white-t ailed deer ha d cascadi ng
effects onplantcommunities in allforageclasses, whichindirectly
affectedsmall wildlife species. Ford et al. (2015)reportedthat the
recover yofwilddogsfo llowingreintroductioninKe nyalimitedden-
sities of dik dik but did nottrigger a trophic cascade,possibly be-
causeofthediversityofbrowsersoratimelaginindirectef fects.
3.4  |  Manipulation of predation risk
Recently,researchersandpractitionershavecometotherealization
thatmanagementstrategiescanpotentiallyusefearofpredationas
abasisformanagementdecisions(Cromsigtetal.,2013;Suracietal.,
2016).Indeed,humanshaveusedfeartodeterwildlifedamagesince
thedawnofagriculture.Forexample,theuseofascarecrowiscom-
monplaceandservesasavisualcuetowardoffdepredatingwildlife
incropfields.Likewise,farmershaverecommendedtheuseofhuman
hair asa scent cue to deter deerfrom gardens. These household
remediesfordepredationbyungulatesarerootedintheecologyof
fearconcept and provideclassicexamplesof howthelandscapeof
fearcanbemanipulatedasamanagementtool.Generally,theland-
scape offearcanbe managedbypassive(e.g.,predatorreintroduc-
tions)andactive(e.g.,hunting, predatorcues,habitatmanipulation)
means,withatop-downorbottom-upapproach.
3.4.1  |  Top-downapproaches
Berger et al. (2001) suggested the potential for usinghuman hunt-
ing to invoke the t rophic casc ades provide d by wolves to restor e
   
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CHITWO OD eT al .
ecosystemfunction.Cromsigt etal.(2013)embraced thisidea with
th ec on cep to f“ hu nti ng forfe ar,”w he ret he yprop ose du sin gh untin g
asatop-downapproachtomanagingundesiredeffectsofungulates.
Otherpotentialmethodssuchastrainingdomesticatedpredatorsto
deterprey (Atkinsetal., 2017)are being usedincreasinglytomiti-
gate human-wildlifeconflic ts, butthese likelyare less practical for
ungulates.An importantconsiderationwhen designing and study-
ing thesemanagement approaches ishow the natural apex preda-
tor of the system affects ungulatebehaviorand how the resulting
behaviorscascadetoothertrophiclevels.Thetrophic cascadesare
oftencontextdependentbecausethesameungulatesmayusedif-
feringmethodstoavoiddifferentpredators,differentungulatesmay
use diff erent strate gies to avoid the sam e predator, and dif ferent
environm ental contex t may make the sam e ungulate use di ffering
methodstoavoidthesamepredator(seeprevioussectionontrophic
cascades).Moreover,strategies of usinghumans to reestablish the
landscapeoffearmayonlyworkafteralagtimefortheungulateto
establishthatthepredatorisindeedathreat(LeSaoutetal.,2014).
Additionally,theymayhavelimitedeffectiveness(ornotworkatall)
if anthrop ogenic stim uli cause mis matched perce ption and be hav-
ioralresponsesinthe targetedanimals(Smith etal.,2021).Itisthis
contextdependencythatmaymakeusingatop-downapproachdif-
ficulttoapply,particularlyasecologicalobjectivesbecomenarrower.
3.4.2  |  Bottom-upapproaches
Fewstudieshavedirectlymeasuredthepotentialtoapplyabottom-
upapproachofmanagingungulateswithfear.However,severalex-
amples existfrom othertaxa. For example, Fernández-Juricic et al.
(2001) sug gested that u nderst anding anim al response s to humans
couldaidinthedesignofparkstodecreasestress-relatedfearfrom
human ac tivity. Alte rnatively, that s ame concept co uld be used to
cause an imals to behavioral ly avoid sensitive are as. For example,
Blackwell et al.(2013) proposed a frameworkto reduceavian col-
lisions withaircrafts by utilizing concepts in the ecology of fearto
guide habitat management surrounding landing strips on airports.
Clearly,vegetationstructureandcompositionandthedistributionof
coverandfoodsalsoaffectungulatebehavioratleastinpartbecause
thosefactorsaf fectpredationrisk.Becauselandmanagementprac-
tices ca n drastical ly alter the land scape chara cteristic s associated
with veget ation, using mana gement practi ces to augment troph ic
cascadesforpurposesofrestorationmaybepossible.Insupportof
thisnotion,Hebblewhiteetal.(2009)reportedthat loggingincom-
bination with fire increasedthe amountof forage biomass, but elk
avoidedtheseareasbecauseofincreasedpredationriskfromwolves
intheCa nadianRock ies .Th us,thedramaticchangeinplantcommu-
nitystructurealteredtheungulateperceptionofthearea'sriskiness,
whichcausedthemtoshif tbehaviortoavoidthoseareas.Similarly,
RiginosandGrace(2008)reportedthatvisualobstructionfromtree
densityincreasesfearinsomeungulates,whichcascadestotheforb
communit y in open are as. Contras tingly, Lashl ey,Chi twood, Kay s,
et al. (2015) demonstrated that white-tailed deer avoided areas
withpoorvisualobstruction,eventhoughthoseareasoftenhadthe
greatestavailablenutrition(Lashley,Chitwood,Harper,etal.,2015).
Inallofthose cases, perception of predation risk drovetheanimal
decisionsdespite foragepatchquality,but theantipredatorbehav-
iors of the u ngulate dict ated what lands cape chara cteristic s were
actuallyavoided.Landscape structure may drive theperception of
risk,meaningthatmanipulatinglandscape structuretodrivea de-
sirable trophic cascade could be possible, thoughmanylife-histor y
factorsoftheungulateinvolvedmayconfounddesirableoutcomes.
4 | CONCLUSIONS
Understanding ungulate ecology of fear and its system-wide ef-
fectswouldhelpustobetterinterpretungulateecology,improve
wildlifeconservationandmanagementprograms,andunderstand
communit y dynamics (Teckentrupet al., 2018). Ourreview dem-
onstratedthatmost studiesoftheecologyoffear canbelumped
into three c ategories of in quiry: be havioral resp onses to pred a-
tion risk , physiological re sponses to preda tion risk, and tro phic
cascades resulting from ungulate responses to predation risk.
A fourt h categor y,man ipulation of p redation ri sk, has bee n less
studiedbutnonethelessrepresentsaninterestingopportunityto
takeresearchresultsandincorporatethemintoconservationand
managementplanning(e.g.,Gaynor etal.,2021).Importantly,our
review suggeststhat collaboration across researchfoci (e.g., be-
havioral effectsonphysiologyandhowtheyscaleto population-
levelconsequences) presents an opportunity to design complex
research questions that have otherwise, more often than not,
beentreateddisparately.
OurreviewalsoconfirmsrecentworkbySay-Sallazetal.(2019),
who reported a biasinthe taxabeing studied andthe locations in
theworldinwhichtheyarestudied.Suchbiaspresentsaproblemon
multiplefronts.First,itappears thatcharismatictaxa and locations
or events (e. g., wolf reintrod uction to Yellowston e National Park )
dominatetheliterature,meaningotherpredator–preyrelationships
andsystemsarenotcontributingproportionallytoourscientificun-
derstandingoftheecolog yoffear.Second,manystudiesarelimited
intaxonomicscope,evenwhenmultiplepredatorandungulatespe-
ciesare availableatagivenstudy site,which ignoresthe complex-
ity associated withmany predator–prey systems(Moll et al.,2017;
Montgomery et al.,2019)andlikely limit sinference. Third,studies
on movement a nd habitat sel ection domi nated the topic s studied
under the ecologyof fearparadigm, but we do notbelieve habitat
selectionalonewillbeenoughtomechanisticallyexplainecologyof
fear.Manyradiotag-basedstudiesareobservationaloropportunistic
innature.Rigorousexperimentalandreplicatedstudiesarerequired
formechanisticunderstandingofhowfearscalestopopulation-level
processes(seePeersetal.,2018;Prughetal.,2019).
Ungulate responses to predationriskdependonenvironmental
features, life-histor y traits, and social structure (Ford & Goheen,
2015).However,themajorityof research into “ecologyof fear”fo-
cusesonelk.Additionalresearchonless-studiedungulates,coupled
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withpredatorswith differenthunting techniques,willbeimportant
to under standing th e effect s of fear on ungula tes. We know that
thetwotypesofpredationrisk,individuallyorcombined,mayhave
differenteffectsonungulateresponses(Creeletal.,2014,Wikenros
et al., 2015, but see Dröge et al., 2017). However, the majorit y of
researchfocusesoncursorialpredators,andlittleresearchevaluates
theeffectsofambushpredatorsortheeffectsofcursorialandam-
bushcombined.Moreover,interindividualvariationintraitssuchas
boldnessorshynessmightplayanimportantroleaffectingungulate
perceptionrisk(Bleicher,2017),buttheyarelargelyunstudiedinthe
ecologyoffearcontext.
Therelationshipofdiseaseandparasitismtotheecologyoffear
could haveimport antecological, economic, or human health con-
sequences, but the relationships between infection risk and fear
respons es are still la rgely unexpl ored (only 5 pape rs [<2%] in our
reviewwereexplicitlyconnectedtodiseaseorparasitism).Predators
may limit disease spread by reducing host densities or selecting
infected individuals (Packer et al., 2003), but they could simulta-
neouslyincreasetransmissionriskatlowerungulatedensitiesifun-
gulatesincreasegroupsizeinresponsetopredationrisk.Also,given
thathost–parasiteinteractionspotentiallyinfluencetheprevalence
ofvector-bornediseases,incorporatingindirecteffectsofparasites
onungulate hosts couldhaveimplications on mitigation of disease
risk (Al lan et al., 2010). Unders tanding how non- consumptive ef-
fectsof parasitismaffec thostpopulationdynamicsandpotentially
cascadethroughfoodwebsisimportant(Daversaetal.,2021).With
numerous zoonotic pathogens transmitted via parasites, how they
contributetotheecologyoffearcouldhaveimplicationsforhuman
healthandeconomies.
Duetothelackofreplicationanddifficultyofisolatingtrait-
mediated f rom density-me diated factors , there is contrast ing
evidence regarding trait-mediated trophic cascade effects on
communities, ungulate populations, and ungulate physiology.
Moreover, recent work highlighted concerns with sampling
design th at affected t he strengt h of a trophic cas cade in the
Greater YellowstoneEcosystem(Briceetal.,2022).Studies on
trait-mediated trophic cascades in particular suffer from the
taxonomic and regional biases mentioned previously because
they tendto be focused on cursorial predators in the Greater
Yellowstone Ecosystem, likely due to the natural experiment
provided by the reintroduction of wolves (Bleicher, 2017).
Meanwhil e, we know very litt le about trophic c ascades gen-
erated by am bush predators (M oll et al., 2016; Thaker et a l.,
2011;Wikenros et al.,2015). Overcoming such biasshould be
fundamental to increasing ourknowledgeoftrophicc ascades.
Iftheecologyoffearhas broad importance in causingtrophic
cascades, avoidingbiasshould be fundamentalto thestudy of
its effects as well asits application to conservation andman-
agement.Giventhat allofthestrategies wecurrentlyembrace
tomanipulatefearforconser vationpurposesarerootedinelic-
itingdes ir ablet ro ph iccas ca des ,t hi sm aybe th em ostimpo r tant
fo c ala reaf orf utur ere s ear c hif we a ret ou s eth eeco log y off ear
successfullyinconservation.
If the ecology of fear is a valuable ecological paradigm, we
must look beyond wolves and elk in North America and toward
studies that embr ace complexity i n research design (as noted by
Montgom ery et al., 2019, Prugh et al. , 2019, a nd Say-Salla z et al.,
2019). Though resu lts of studies h ighlighted here in often provide
conflictingdirectionalit yormagnitude ofef fect,theyprovidevalu-
ablebuildingblocksforimprovingfuturestudiesofecologyoffearin
ungulates.Thethreepredominateareasofresearchfocusweiden-
tified overlapwithoneanotherextensively; recognizingtheyoccur
inanincreasingly anthropogenicworld (Bergeretal., 2020) willbe
importanttoconsider.Someauthorshavearguedthatgiventheper-
vasiveeffectsofhumansonear th,quantifyinghumandisturbanceis
ahighpriorit yfor conservationandthat understanding the fitness
costs ofhumanactivities (e.g., hiking,hunting)is animportant area
forfutureresearchdespitethechallengeforfieldstudies(Ciutietal.,
2012,butseeSchuttleretal.,2017).Onlybyembr aci ng“m ess ypro-
jectio ns” (Berger et al ., 2020) will we be a ble to predic t how fear
might aff ect popula tion dynami cs and ecolo gical proce sses across
systems, accounting for multiple predators of varying sizes and
hunting m odes, with nu merous prey opt ions. We believe the c ur-
rentbodyofliteratureonecologyoffearcomesupshortonbroadly
explaining predator–prey dynamics in complex systems. However,
thesheernumberofpapersonthetopicdemonstrateclearinterest
amongecologists,makingfutureworkonecologyoffearthatmuch
more valuable ifit embraces complexity and expands beyond the
few species and systems that have driven the development of the
conceptthusfar.Theareasofresearchfocusidentifiedinthisreview
compriseafoundationforfutureresearch tolinkbehavior,physiol-
ogy,trophic cascades, and management alltogether as one,rather
thanthinkingofeachinavacuum.
ACKNOWLEDGEMENT
We thank the A ssociate Edit or and two ano nymous review ers for
thought fulcommentsthatimprovedthemanuscript.
CONFLICT OF INTEREST
Authorsdeclarenoconflictofinterest.
AUTHOR CONTRIBUTIONS
M. Colter Chitwood: Conceptualization (equal); Investigation
(equal);Methodolog y(equal);Writing–originaldraft(lead).Carolina
Baruzzi: Data curation (lead); Investigation (equal); Methodology
(equal); Visualization (lead); Writing – original draft (supporting).
Marcus A. Lashley:Conceptualization(equal);Investigation(equal);
Methodology(equal);Writing–originaldraft(supporting).
DATA AVAIL AB ILI T Y STAT E MEN T
DataareprovidedaspartofthemanuscriptandAppendixS1.
ORCID
M. Colter Chitwood https://orcid.org/0000-0001-7240-7430
Carolina Baruzzi https://orcid.org/0000-0003-1796-9355
Marcus A. Lashley https://orcid.org/0000-0002-1086-7754
   
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CHITWO OD eT al .
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How to cite this article:Chitwood,M.C.,Baruzzi,C.,&
Lashley,M.A.(2022).“Ecologyoffear”inungulates:
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