ArticlePDF AvailableLiterature Review


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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  Revised:31J anuar y2022 
  Accepted :3Februa ry2022
DOI: 10.1002/ece 3.8 657
“Ecology of fear” in ungulates: Opportunities for improving
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,
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
M.Colte rChitwood,De part ment
ofNatura lResourceEcolog yand
Managem ent,Oklahom aStateUniversity,
Stillwater,OK,USA .
studyingungulate ecology offear is common, knowledge from ungulatesystemsis
highly contested among ecologists. Here, we review the available literature on the
behaviora l responses to predat ion risk (79%), physiologic al responses to pre dation
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
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
ensure desirable conservationoutcomes.Werecommend future work embrace the
antipredatorbehavior,predationrisk,predator,prey,trait-mediatedef fects,vigilance
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   CHITWOOD eT al .
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. ,
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
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
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
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).
related tothe ecology offear, including non-consumptive effects
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
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 -
predati on (Say-Sallaz et a l., 2019). Other recen t work highlighte d
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-
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
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
We conducte d a literature se arch for arti cles using the key words
offearfailtofullydisentangledirectandindirecteffect s(Peersetal.,
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
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
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-
the topic a mong acade mics has inc reased, as in dexed by citat ions
areasoffocus,withsomepublicationsf ittingundermult ipl ecatego -
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-
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resultingintherelease ofplants from herbivory (Polisetal.,20 00);
tribut ion, abunda nce, or stru cture) resu lting from th e influence of
ingef fectsofungulateresponsestopredation riskon otheranimal
riskasanyactiontakenorthat could betaken byhumanstointen-
viatop-downorbottom- upmanagementappr oaches)toevokeade-
Theliteraturesearchyielded275studiesrelevant totheecologyof
fear in ungulates (Appendix S1). While most paperscovered multi-
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
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
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
2000 2005 2010 2015 2020
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
Central Asia
North Africa
South Asia
Latin America
Middle East
East Asia
Sub Saharan Africa
North America
0% 20%40% 60% 80%
Manipulation of Risk
Physiological Responses
Trophic Cascades
Behavioral Responses
0% 20%40% 60%80%
(a) (b)
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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
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
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
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
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)
highchronicpredationby Eurasian lynx (Lynx lynx)at nightbutnot
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
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
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
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%
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
  5 of 15
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-
Movement,spaceuse,andhabitat selection also likely relateto
etal., 2011)using seven ungulates andfive largec arnivores deter-
minedthatmostof thesmallerprey species(e.g.,impala[Aepyceros
[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
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
decision rulescombine to affect ungulatespace use (and otheran-
tipredator behaviors), especially in multi-predator systems where
Some stu dies have repor ted weak eviden ce for behavior al re-
littlesuppor tthatmoose(Alces alces)habitatusewasdependenton
predationriskfromwolves, thoughtheyacknowledged severalun-
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
responsesto predation risk inthese studies, coupledwithdiffering
mode(Thakeret al., 2011),antipredatorstrategiesoftheungulates
etal., 2014),a lackofa response, or failure to detectitwith study
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-
free of brown bears(Ursus arctos) and non-parous females did not
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).
3.1.2  |  Vigilanceandherding
Vigilanceofpreyspeciesisoneoft hemoststudiedaspect sofan-
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
riskandacquiringenergy (Creel,2018;Illius& Fitzgibbon,1994).
(i.e.,ha rte be est ,plai nzeb ra,an do ribi[Ourebia oribi])increasevigi-
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),
6 of 15 
   CHITWOOD eT al .
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
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-
size to affec t vigilance re sponse in some c ases but not in oth ers,
low-risksituations(Beauchamp,2019).Olfactory andauditor ycues
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
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
necessitatesinterplaybetweenphysiologyandbehavior(McAr thur
ungulatep hysiologic alre sp on se st opar as it is manddiseaseto th er e-
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-
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
towarrant the cost toforagingor ungulates mayreduce theirfood
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
ducedshiftsinelkhabitatuse,whichloweredthequality oftheelk
didnotdisplayasimilarchange inhabitatuseanddietaryqualityto
An emerg ing literature bas e also indicates th at predation risk
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,
1997; Schmitz, 1998). Interestingly, similar results have been re-
gulateshavenot beenrepor ted.Althoughdemonstratingpredation
risk inducingphysiological changes that manifest in health and be-
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.,
(Sherif f et al., 2010). Some research investigating glucocorticoid
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-
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)
Middleton et al., 2013). Predator-induced stress and selection of
decreas ed fecundity (C hristianson & Cre el, 2010; Ng’weno et al .,
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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-
other biota and ecological processes as well (Beschta & Ripple,
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
palatable plant species fromherbivory.Trait-mediatedtrophiccas-
vioussectionsonbehavior and physiology for examples ofspecific
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
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
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
have recently expanded their range acrosseastern North America
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
thanwolves tourbanization,so they may exertgreater controlson
ungulate s in urbanized lands capes (Jones et a l., 2016). That said,
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,
rather ju st the resul t of research fa iling to disent angle them f rom
Predic ting the stren gth of trophi c cascades (i .e., how far they
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-
relation to the ungulatehadnoeffect.Contrastingly,DeLong et al.
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
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
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
8 of 15 
   CHITWOOD eT al .
with poor replication, to study how ungulates af fect ecosyste ms
without p redation risks (Ritchie et al., 2012). In systems with out
(Côté et al., 20 04). Seve ral exampl es exist to cor roborate th is no-
moose herbivory,which erodedthe bird community in the Greater
Yellowstone Ecosystem. Ripple and Beschta (2006a) repor ted a
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)
Interestingly,recent evidence has indicated that ungulate den-
sitiesmayexceednutritionalcarryingcapacityfor decadeswithout
ungulatepopu la ti on sw it ha ndwitho ut pr edatorsan dhowdr as tica l-
process es. The ext ensive herbi vory pres sure may result i n natural
(Strauss &Agrawal, 1999) or induce plant defenses within species
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
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).
because the predator rever ts ungulate populations and behavior
fromthealternativestablest atebacktothehistoricalstablestate.
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-
byaffecting fruit production through the regulationofelk density
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
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
hair asa scent cue to deter deerfrom gardens. These household
fearconcept and provideclassicexamplesof howthelandscapeof
scape offearcanbe managedbypassive(e.g.,predatorreintroduc-
tions)andactive(e.g.,hunting, predatorcues,habitatmanipulation)
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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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
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
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
cascades).Moreover,strategies of usinghumans to reestablish the
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
3.4.2  |  Bottom-upapproaches
amples existfrom othertaxa. For example, Fernández-Juricic et al.
(2001) sug gested that u nderst anding anim al response s to humans
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.
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
thisnotion,Hebblewhiteetal.(2009)reportedthat loggingincom-
bination with fire increasedthe amountof forage biomass, but elk
intheCa nadianRock ies .Th us,thedramaticchangeinplantcommu-
whichcausedthemtoshif tbehaviortoavoidthoseareas.Similarly,
communit y in open are as. Contras tingly, Lashl ey,Chi twood, Kay s,
et al. (2015) demonstrated that white-tailed deer avoided areas
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
Understanding ungulate ecology of fear and its system-wide ef-
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
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,
who reported a biasinthe taxabeing studied andthe locations in
multiplefronts.First,itappears thatcharismatictaxa and locations
or events (e. g., wolf reintrod uction to Yellowston e National Park )
derstandingoftheecolog yoffear.Second,manystudiesarelimited
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
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-
10 of 15 
   CHITWOOD eT al .
withpredatorswith differenthunting techniques,willbeimportant
to under standing th e effect s of fear on ungula tes. We know that
et al., 2015, but see Dröge et al., 2017). However, the majorit y of
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
may limit disease spread by reducing host densities or selecting
infected individuals (Packer et al., 2003), but they could simulta-
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
numerous zoonotic pathogens transmitted via parasites, how they
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
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-
tified overlapwithoneanotherextensively; recognizingtheyoccur
inanincreasingly anthropogenicworld (Bergeretal., 2020) willbe
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
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-
explaining predator–prey dynamics in complex systems. However,
more valuable ifit embraces complexity and expands beyond the
few species and systems that have driven the development of the
compriseafoundationforfutureresearch tolinkbehavior,physiol-
ogy,trophic cascades, and management alltogether as one,rather
We thank the A ssociate Edit or and two ano nymous review ers for
thought fulcommentsthatimprovedthemanuscript.
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);
M. Colter Chitwood
Carolina Baruzzi
Marcus A. Lashley
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Research on the ecology of fear has highlighted the importance of perceived risk from predators and humans in shaping animal behavior and physiology, with potential demographic and ecosystem-wide consequences. Despite recent conceptual advances and potential management implications of the ecology of fear, theory and conservation practices have rarely been linked. Many challenges in animal conservation may be alleviated by actively harnessing or compensating for risk perception and risk avoidance behavior in wild animal populations. Integration of the ecology of fear into conservation and management practice can contribute to the recovery of threatened populations, human–wildlife conflict mitigation, invasive species management, maintenance of sustainable harvest and species reintroduction plans. Here, we present an applied framework that links conservation interventions to desired outcomes by manipulating ecology of fear dynamics. We discuss how to reduce or amplify fear in wild animals by manipulating habitat structure, sensory stimuli, animal experience (previous exposure to risk) and food safety trade-offs to achieve management objectives. Changing the optimal decision-making of individuals in managed populations can then further conservation goals by shaping the spatiotemporal distribution of animals, changing predation rates and altering risk effects that scale up to demographic consequences. We also outline future directions for applied research on fear ecology that will better inform conservation practices. Our framework can help scientists and practitioners anticipate and mitigate unintended consequences of management decisions, and highlight new levers for multi-species conservation strategies that promote human–wildlife coexistence.
Vigilance allows animals to monitor their surroundings for signs of danger associated with predators or rivals. As vigilance is costly, models predict that it should increase when the risk posed by predators or rivals increases. In addition, vigilance is expected to decrease in larger groups that provide more safety against predators. Risk and group size are thus two key determinants of vigilance. Together, they could have additive or interactive effects on vigilance. If risk and group size interacted, the magnitude of the group-size effect on vigilance would vary depending on the level of risk experienced by animals, implying that the benefits of sociality in terms of vigilance vary with risk. Depending on the model, vigilance is predicted to decrease more rapidly with group size at low risk or at high risk. Little work has directly focused on the interaction between risk and group size, making it difficult to understand under which conditions particular interactive effects arise and whether interactive effects are common in natural study systems. I review the vast literature on vigilance in birds and mammals to assess whether interactive effects between risk and group size are common, and if present which pattern occurs more frequently. In studies involving predation risk, a large proportion reported no statistically significant interactive effects. In other cases, vigilance decreased with group size more rapidly at low or high risk with no overwhelming pattern. In studies involving risk posed by rivals, vigilance often decreased with group size more rapidly at low than at high risk as predicted if the need to monitor rivals increases in larger groups. Low statistical power to detect interactive effects might have been an issue in several studies. Lack of interactive effects, on the other hand, might suggest constraints or limits on the ability of animals to adjust vigilance to current risk or group sizes. Interactive effects on vigilance have implications for the evolution of sociality and for our understanding of phenotypic plasticity of predator- and competitor-induced defenses and deserve more attention in future studies.
Studies on invertebrates and small vertebrates demonstrated the underappreciated importance of the non-consumptive effects (NCE) of predators on their prey. Recently, there has been a growing interest for such effects in large vertebrates. Here, we review the empirical literature on large carnivore-ungulate systems to map our knowledge of predation NCE (from trait modification to the consequences on prey populations), and identify the gaps in our approaches that need to be fulfilled to reach a comprehensive understanding of these NCE. This review reveals (i) biases in the studies towards North American (and to a lesser extent African) ecosystems, protected areas, and investigation of NCE by wolf Canis lupus (and to a lesser extent African lion Panthera leo); (ii) a diversification of the systems studied in the past decade, which led to contrasted conclusions about the existence of NCE; (iii) that most existing work studied the effects caused by one predator only, even in ecosystems characterized by a rich carnivore community; and (iv) that the majority of the literature on NCE focused on the anti-predator behavioural responses of prey, whereas this is only the tip of the iceberg of NCE. Indeed, little is known on the other NCE components (energetic costs, stress, reproduction, survival, and population dynamics) and the links between the different components. Linking anti-predator behavioural responses to demography is thus the key challenge ahead of us to fully understand the NCE of predators on their prey in large mammals.