Biol. Rev. (2013), 88, pp. 550–563. 550doi: 10.1111/brv.12014
Dangerous prey and daring predators:a review
Shomen Mukherjee∗,† and Michael R. HeithausDepartment of Biological Sciences, Florida International University, 3000 NE 151ST, North Miami, FL 33154, USA
ABSTRACT
How foragers balance risks during foraging is a central focus of optimal foraging studies. While diverse theoretical andempirical work has revealed how foragers should and do manage food and safety from predators, little attention hasbeen given to the risks posed by dangerous prey. This is a potentially important oversight because risk of injury cangive rise to foraging costs similar to those arising from the risk of predation, and with similar consequences. Here, wesynthesize the literature on how foragers manage risks associated with dangerous prey and adapt previous theory tomake the first steps towards a framework for future studies. Though rarely documented, it appears that in some systemspredators are frequently injured while hunting and risk of injury can be an important foraging cost. Fitness costs offoraging injuries, which can be fatal, likely vary widely but have rarely been studied and should be the subject of futureresearch. Like other types of risk-taking behaviour, it appears that there is individual variation in the willingness totake risks, which can be driven by social factors, experience and foraging abilities, or differences in body condition.Because of ongoing modifications to natural communities, including changes in prey availability and relative abundanceas well as the introduction of potentially dangerous prey to numerous ecosystems, understanding the prevalence andconsequences of hunting dangerous prey should be a priority for behavioural ecologists.
Key words: foraging behaviour, predator injury, predator-prey interaction, prey avoidance, risk of injury.
CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 550II. What makes prey dangerous? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 551
III. Frequency of injuries from dangerous prey . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 551IV. Ethology of reducing the risk of injury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 555V. Costs of hunting dangerous prey . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 556
VI. A framework for investigating foraging on dangerous prey . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 556(1) Interpreting the foraging costs of hunting dangerous prey . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 556(2) Is there intraspecific variation in willingness to take risks? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 558
VII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 561VIII. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 561
IX. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 561
I. INTRODUCTION
Studies of predator–prey interactions continue to be oneof the most fascinating and important aspects of ecologicalresearch. The intense focus on this topic can be attributedto the central role of foraging in the lives of predatorsand their prey, and the importance of predation in driving
* Address for correspondence (Tel: +27 714390560; E-mail: [email protected])† Present address: School of Life Sciences (Biological & Conservation Sciences), University of KwaZulu-Natal, Westville Campus, PO
Box 54001, Durban 4000, Republic of South Africa.
population, community, and evolutionary dynamics. Morerecently, behavioral ecologists have begun to investigatethe population and ecosystem consequences of predators inmodifying the behaviour of their prey [see Lima & Dill (1990),Lima (1998) and Brown & Kotler (2004) for reviews], whichcan have profound consequences for prey populations andthe dynamics of their communities [see reviews by Werner
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society
Daring predators 551
& Peacor (2003), Schmitz, Krivan & Ovadia (2004), Preisser,Bolnick & Benard (2005), Heithaus et al. (2008) and Creel &Christanson (2008)].
Predator–prey studies, especially of prey choice bypredators, are becoming increasingly important due toanthropogenic modification of ecosystems. For example,changes in energetic demands instigated by climate changecould modify predator foraging needs and decisions, ascould the introduction of exotic prey species or reductions innaturally important prey. Predators have more at stake whilehunting than simply the risk of missing a meal if unsuccessful.Some potential prey may harm or even kill their predator, orthe habitat in which particular prey are found may pose aninjury or mortality risk to a predator. While the potential forpoisonous prey to harm predators has been widely consideredin studies of diet choice, as has foraging under the risk ofpredation, there has been less attention focused on foragingbehaviours and decisions of predators hunting other types ofdangerous prey.
The ability of predators to recognize dangerous prey mayvary widely depending on the novelty of such prey (e.g. exoticprey). Regardless, the decisions of when to attack or avoidsuch prey and the potential costs of doing so could be animportant aspect of ecological dynamics. Here, we reviewour current understanding of interactions between dangerousprey and their predators, and suggest a framework for futurestudies of such situations.
II. WHAT MAKES PREY DANGEROUS?
Prey exhibit a wide array of secondary defences that maybe physical, chemical, or behavioural (Edmunds, 1974;Ruxton, Speed & Kelly, 2004, Table 1). Weapons anddefensive structures include hooves, spines, flukes, horns,tusks, shell, teeth, and noxious chemicals among others.While some structures are permanent body parts, others areinduced in response to increased predation risk. For example,Daphnia lumholtzi has a rounded head when planktivorousfish are rare (e.g. during the winter months) or absent, buthave a sharp helmet and long extended tail spine, whichreduces predation, when predators are present (Greene,1967; Agrawal, 2001). Although some structures used indefence by prey have likely evolved for other purposes suchas intraspecific conflicts (e.g. sexual selection etc.; Edmunds,1974), they still may serve an important anti-predator roleand pose substantial risks to predators.
Certain prey use chemicals to deter or injure predators(i.e. for more than modifying their palatability). Forexample African bombardier beetles (Stenaptinus insignis) sprayhot quinonoid liquid towards attacking predators (Eisner& Aneshansley, 1999). In deep-sea habitats, consumingbioluminescent prey can increase the chances of a predatorbeing attacked by their own predators (Haddock, Moline &Case, 2010). Prey behaviour, such as kicking and biting whenattacked or counter-attacking predators, also may influencetheir danger to predators. For example, female white-tailed
deer (Odocoileus virginianus) will face and attack coyotes todeter them (Garner & Morrison, 1980) and honey bees maysmother and kill predatory wasps that try to attack their hive(Ono et al., 1995).
The overall level of danger posed by a particular preytype may extend beyond its own attributes. Indeed, habitatcharacteristics may influence injury and mortality risk topredators as could the particular tactics used to hunt prey,but these sources of danger to predators have been largelyoverlooked with respect to injury risk. For example preysuch as Nubian ibex (Capra ibex; Kotler, Gross & Mitchell,1994) and elk (Cervus elaphus; Mao et al., 2005) take shelter onsteep cliff faces to take advantage of its inaccessibility to theirpredators. Similarly, a fast pursuit in an undulating terraincould put a predator at risk of a fall causing fracture or limbdislocation. Risk of injury could be one of the reasons whypredators such as cougars (Dickson, Jenness & Beier, 2004)prefer to hunt in less undulating terrain. Physical threats inhabitats can include the presence of dense thickets or thornyvegetation, that can inflict debilitating injuries, particularlyto eyes (e.g. in owls, see Holt & Layne, 2008) or limbs.The presence of a predator’s own predator in the habitat isanother component of the risks of hunting particular prey.The latter situation has been the subject of considerableresearch (e.g. Lima & Dill, 1990; Donadio & Buskirk, 2006;Frid, Burns & Baker, 2009) and is not considered furtherhere.
III. FREQUENCY OF INJURIES FROMDANGEROUS PREY
There is little information on how frequently predatorsare injured by their prey (Table 1). This can be partiallyattributed to the difficulty in measuring prey-inflicted injurieswithout close inspection. Therefore, studies of injuries topredators generally are limited to studies of hard parts(e.g. teeth, bones) and therefore surely underestimate actualinjury rates to predators. To our knowledge, no studies haveestimated mortality rates from foraging-related injuries.
Injuries have been relatively well studied in raptors andcarnivores, and can be fairly common (Table 1). Dislocationof joints (Ackermann & Redig, 1997), and broken toes, talons,flight feathers, and injured eyes are widely documentedin raptors. A study in Canada found that 5.9% of 1120American kestrels had hunting-related injuries (Murza,Bortolotti & Dawson, 2000). In another study 14% of 98individuals sampled from three species of raptors in northernArkansas, USA, had injuries (Bedrosian & St. Pierre, 2007).Inspection of museum specimens of accipter hawks have alsorevealed that hunting injuries may be relatively common(18.6% of 339 individuals) (Roth, Jones & French, 2002).
Carnivores also appear to be injured frequently by theirprey. High rates of fractured canines were recorded formany species of carnivores (see table 3 in Van Valkenburg,2009). These included 5.4% of lions (Panthera leo), 9.2%of tigers (Panthera tigris), 9.8% of leopards (Panthera pardus),
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society
552 Shomen Mukherjee and Michael R. Heithaus
Tab
le1.
Are
pres
enta
tive
listo
fqua
ntita
tive
stud
ies
and
anec
dota
lobs
erva
tions
cont
aini
ngev
iden
ceof
inju
ry,a
ndri
sk-r
educ
ing
beha
viou
rs,o
fpre
dato
rshu
ntin
gda
nger
ous
prey
Pred
ator
taxa
Prey
Pred
ator
inju
ry
Ris
k-re
duci
ngbe
havi
our
ofpr
edat
or
Typ
eof
evid
ence
(qua
ntita
tive
stud
yor
anec
dota
levi
denc
e)R
efer
ence
s
Inve
rteb
rate
sSe
ast
ar(L
epta
ster
ias
hexa
ctis
)Sn
ail(
Am
phis
saco
lum
bian
a)Im
mob
iliza
tion
ofse
ast
arar
mdu
eto
bite
inju
ryon
radi
alne
rve
Mos
tlyav
oida
nce.
Sea
star
drap
esits
elft
ight
ly,a
ndm
anoe
uvre
sits
arm
sso
that
the
snai
lcan
not
exte
ndits
prob
osci
s
Qua
ntita
tive
Bra
ithw
aite
etal
.(20
10)
Snai
l(Sin
istr
oful
gur
sini
stru
m)
Biv
alve
(Mer
cena
ria
mer
cena
ria)
Dam
age
thei
row
nsh
ell
Snai
lssh
ould
dela
yat
tack
ing
larg
ebi
valv
esun
tilth
eyre
ach
the
shel
l-thi
cken
ing
stag
e.
Qua
ntita
tive
Die
tl(2
003)
Cru
stac
ean
(Can
cer
mag
iste
)C
lam
(Pro
toth
aca
stam
ina)
Cla
wda
mag
ePr
efer
red
clam
sof
the
smal
lest
size
clas
sQ
uant
itativ
eJu
anes
&H
artw
ick
(199
0)A
nts
Afr
ican
bom
bard
ier
beet
le(S
tena
ptin
usin
sign
is)
Che
mic
alir
rita
nt(p
-ben
zoqu
inon
es)
Avo
id/r
elea
sepr
ey∗
Qua
ntita
tive
Eis
ner
&A
nesh
ansle
y(1
999)
Ant
lion
(Myr
mel
eon
caro
linu
s)A
nt(C
ampo
notu
sflo
rida
nus)
Che
mic
alir
rita
nt(fo
rmic
acid
)Fe
eds
onan
tsw
ithou
tru
ptur
ing
the
acid
sac
Qua
ntita
tive
Eis
ner
etal
.(19
93)
Spid
ers(
Ara
neus
trifol
ium
and
Arg
iope
trifas
ciat
a)B
eean
dw
asp
Stin
g∗A
void
phys
ical
cont
acta
ndus
ew
ebto
subd
ueda
nger
ous
prey
Qua
ntita
tive
Oliv
e(1
980)
Hor
net(
Ves
pam
anda
rina
)B
ee(A
pis
cera
na)
Let
hals
ting
Hor
nets
atta
ckm
ostly
duri
ngau
tum
n,w
hen
they
need
extr
apr
otei
nto
rear
new
quee
nsan
dm
ales
Qua
ntita
tive
Ono
etal
.(19
95)
Afr
ican
pone
rine
ant
(Pac
hyco
ndyl
apa
chyd
erm
a)
Cen
tiped
eB
ite∗
Cen
tiped
eshe
ldfr
oman
teri
orpa
rtof
the
body
,an
dst
ung
onve
ntra
lfac
ew
here
neur
alch
ain
pass
es
Qua
ntita
tive
Dej
ean
&L
acha
ud(2
011)
Zel
uslo
ngip
esC
ater
pilla
r(S
podo
pter
afr
ugip
erda
)
Bite
∗A
void
sat
tack
ing
med
ium
and
larg
eca
terp
illar
sQ
uant
itativ
eC
ongi
,Fri
tus
&Fi
lho
(200
2)
Fish
esG
reat
whi
tesh
ark
(Car
char
odon
carc
hari
s)C
alifo
rnia
sea
lion
Bite
∗B
itean
dre
leas
epr
eyA
necd
otal
Tri
cas
&M
cCos
ker
(198
5)B
lueg
illsu
nfish
(Lep
omis
mac
roch
irus
)D
aphn
ia(D
aphn
ialu
mho
ltzi
)D
aphn
iasp
ine
lodg
edon
the
top
offis
hm
outh
Avo
idan
cebe
havi
our.
Ori
enta
teda
phni
asu
chth
atth
ean
teri
orsp
ine
ente
rsth
ebu
ccal
cavi
tyfir
st
Qua
ntita
tive
Swaf
fer
&O
’Bri
en(1
996)
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society
Daring predators 553
Tab
le1.
(con
t.)
Pred
ator
taxa
Prey
Pred
ator
inju
ry
Ris
k-re
duci
ngbe
havi
our
ofpr
edat
or
Typ
eof
evid
ence
(qua
ntita
tive
stud
yor
anec
dota
levi
denc
e)R
efer
ence
s
Rep
tiles
Kom
odo
mon
itor
(Var
anus
kom
odoe
nsis
)W
ater
buffa
loes
Phys
ical
trau
ma∗
Qui
ckat
tack
onbu
ffalo
leg,
tote
arte
ndon
sA
necd
otal
Auf
fenb
erg
(198
1)
Bur
ton’
sle
gles
sliz
ard
(Lia
lis
burt
onis
)W
ater
skin
ks(E
ulam
prus
heat
wol
ei)
Bite
∗L
arge
prey
alw
ays
atta
cked
onhe
ad,o
rne
ck,t
opr
even
tthe
mfr
ombi
ting.
Pred
ator
can
retr
acti
tsey
es.
Qua
ntita
tive
Wal
l&Sh
ine
(200
7)
Nor
ther
nPa
cific
ratt
lesn
akes
(Cro
talu
sor
egan
us)a
ndM
alay
pit-
vipe
rs(C
allo
sela
sma
rhod
osto
ma)
Mic
eB
ite∗
Rel
ease
larg
em
ice
afte
ra
pred
ator
yst
rike
buto
ften
reta
insm
alle
rin
divi
dual
sin
thei
rja
ws
Qua
ntita
tive
Kar
dong
(198
6)an
dB
arr,
Wie
burg
&K
ardo
ng(1
988)
Ret
icul
ate
pyth
on(P
ytho
nre
ticu
latu
s)Po
rcup
ine
(Hys
trix
brac
hyur
a)Ph
ysic
alin
jury
from
quill
s∗A
void
ance
∗A
necd
otal
Shin
eet
al.(
1998
)
Bir
dsPr
edat
ory
bird
s(e
.g.
kitt
iwak
e–
Ris
satr
idac
tyla
,her
ring
gull
–L
arus
arge
ntat
us)
Fulm
ars
(Gen
us–
Ful
mar
us,D
aption
,T
hala
ssoi
ca,
Pag
odro
ma,
Mac
rone
ctes
Pred
ator
isdr
ench
edw
ithoi
l,w
hich
mat
tsth
eir
feat
hers
and
dest
roys
insu
latio
n
Unk
now
nA
necd
otal
War
ham
(197
7)
Rap
tors
(Fal
cope
regr
inus
,O
tus
asio
,F
alco
colu
mba
rius
)
Unk
now
nL
uxat
ion
ofth
eel
bow
Unk
now
nA
necd
otal
Ack
erm
ann
&R
edig
(199
7)
Rap
tors
(But
eoja
mai
cens
is,F
alco
spar
veri
us,A
ccip
iter
coop
erii
)
Unk
now
nM
issi
ngta
lons
,m
issi
ngto
es,
win
gfr
actu
re,i
ris
dam
age
Unk
now
nA
necd
otal
Bed
rosi
an&
St.P
ierr
e(2
007)
Bar
red
owl(
Str
ixva
ria)
Rod
ent
Bite
/dea
th∗
Unk
now
nA
necd
otal
Gib
son
etal
.(19
98)
Lon
g-ea
red
owl(
Asi
oot
us)
Unk
now
nE
yein
jury
(from
hunt
s)U
nkno
wn
Ane
cdot
alH
olt&
Lay
ne(2
008)
Am
eric
anke
stre
l(F
alco
spar
veri
us)
Rod
ent(
Mus
mus
culu
s)B
ite∗
Bir
dsin
good
cond
ition
avoi
ded
dang
erou
spr
eyQ
uant
itativ
eM
urza
etal
.(20
00)
Buz
zard
(But
eobu
teo
ovul
pinu
s)R
oden
tB
ite∗
Bir
dsin
good
cond
ition
avoi
ded
dang
erou
spr
eyQ
uant
itativ
ePe
arlm
an&
Tsu
rim
(200
8)R
apto
r(A
ccip
iter
stri
atus
,A
.co
oper
ii,A
.ge
ntilis
)U
nkno
wn
Frac
ture
inpe
ctor
algi
rdle
Unk
now
nA
necd
otal
Rot
het
al.(
2002
)
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society
554 Shomen Mukherjee and Michael R. Heithaus
Tab
le1.
(con
t.)
Pred
ator
taxa
Prey
Pred
ator
inju
ry
Ris
k-re
duci
ngbe
havi
our
ofpr
edat
or
Typ
eof
evid
ence
(qua
ntita
tive
stud
yor
anec
dota
levi
denc
e)R
efer
ence
s
Mam
mal
sK
iller
wha
le(O
rcin
usor
ca)
Stin
gray
(Das
yatis
sp.)
Dea
thA
void
ance
∗A
necd
otal
Dui
gnan
etal
.(20
00)
Chi
mpa
nzee
(Pan
trog
lody
tes)
Prim
ates
(Col
obus
and
Cer
copi
thec
ussp
ecie
s)Po
tent
ialf
orph
ysic
alin
jury
from
bite
∗
Gro
uphu
ntin
gQ
uant
itativ
eB
oesc
h(1
994)
and
Stan
ford
etal
.(19
94)
Tig
er(P
anth
era
tigr
is)
Porc
upin
eFa
cial
inju
ryfr
omqu
illA
void
ance
∗A
necd
otal
Cor
bett
(194
6,19
57)
Wild
dogs
(Lyc
aon
pict
us)
Ung
ulat
esD
eep
cuts
,bro
ken
teet
h,in
jure
dlim
bs
Gro
uphu
ntin
g,re
stra
inin
ghe
ad(e
.g.
whi
lehu
ntin
gho
gs)
Ane
cdot
alC
reel
&C
reel
(200
2)
Coy
ote
(Can
isla
tran
s)W
hite
taile
dde
er(O
doco
ileu
svi
rgin
ianu
s)Ph
ysic
alin
jury
∗A
void
ance
∗A
necd
otal
Gar
ner
&M
orri
son
(198
0)A
fric
anlio
n(P
anth
era
leo)
Ele
phan
t(L
oxod
onta
afri
cana
)Po
tent
ialf
orph
ysic
alin
jury
orev
ende
ath
∗
Gro
uphu
ntQ
uant
itativ
eL
over
idge
etal
.(20
06)
Wol
ves
(Can
islu
pus)
Elk
(Cer
vus
elap
us)
Pote
ntia
lfor
phys
ical
inju
ryor
even
deat
h∗
Lar
ger
body
size
ofw
olve
spr
ovid
edpr
edat
ory
adva
ntag
e
Qua
ntita
tive
Mac
Nul
tyet
al.(
2009
)
Mar
supi
als
(Das
yuru
svi
vern
nus,
Das
yuru
sha
lluc
atus
,D
asyu
roid
esby
rnei
and
Pha
scog
ale
tapo
ataf
a)an
ddo
mes
ticca
t(F
elis
catu
s)
Rod
ent
Bite
∗A
ttac
kfr
omba
ckor
flank
Qua
ntita
tive
Pelli
s&
Offi
cer
(198
7)
Mar
tin(M
arte
sam
eric
ana)
,ly
nx(L
ynx
cana
dens
is),
fishe
r(M
arte
spe
nnan
t)an
dre
dfo
x(V
ulpe
svu
lpes
)
Porc
upin
eQ
uills
embe
dded
inst
omac
hlin
ing
Avo
idan
ce∗
Ane
cdot
alQ
uick
(195
3)
Dir
ew
olf(
Can
isdi
rus),
coyo
te(C
anis
latr
ans),
sabr
e-to
othe
dca
t(S
milod
onfa
talis)
and
Am
eric
anlio
n(P
anth
era
atro
x)
56he
rbiv
ore
spec
ies
Frac
ture
dto
oth†
Unk
now
nQ
uant
itativ
eV
anV
alke
nbur
g&
Her
tel(
1993
)
Car
nivo
res
(36
spec
ies)
Not
men
tione
dFr
actu
red
toot
h†U
nkno
wn
Qua
ntita
tive
Van
Val
kenb
urg
(200
9)
∗ Dat
ano
tspe
cific
ally
prov
ided
inst
udy.
Est
imat
esar
eba
sed
onna
tura
lhis
tory
ofpr
edat
oran
dpr
ey.
† Too
thfr
actu
res
also
occu
rdu
eto
food
habi
ts(c
hew
ing
bone
s).
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society
Daring predators 555
9.6% of spotted hyenas (Crocuta crocuta), 9.8% of grey wolves(Canis lupus), 17.3% of stoats (Mustela erminea) and 12% ofweasels (Mustela frenata). Since carnivores drive their caninesinto moving and struggling prey, the observed breakagerates are likely to be due to injuries sustained duringhunting (Van Valkenburg & Hertel, 1993). While these dataprovide compelling evidence that injuries during hunting arecommon in carnivores, they are certainly underestimates. Nodata are available for the proportion of individuals injuredor killed by prey through injuries to soft tissues or other partsof the body. Such injuries, however, are known to occur. Forexample, Creel & Creel (2002) found that African wild dogsmay incur deep cuts, broken teeth and injured limbs.
IV. ETHOLOGY OF REDUCING THE RISK OFINJURY
At one extreme, predators can simply avoid huntingdangerous prey even though they are capable of attackingand killing them. For example, a meta-analysis of leoparddiet studies suggests that they prey upon larger sized prey,such as Cape buffalo (Syncerus caffer), plains zebra (Equusquagga) and giraffes (Giraffa camelopardalis), less frequently thanexpected because they are too dangerous to hunt (Haywardet al., 2006). Some seas stars (Leptasterias hexactis) avoid snail(Amphissa columbiana) prey because they defend themselvesby biting into the radial nerve of the sea star, which canimmobilize an arm for several days (Braithwaite, Stone &Bingham, 2010). Orb-web spiders tend to grab and bitenon-venomous prey that gets caught in their web, but fordangerous prey (such as wasps and bees) they avoid physicalcontact and instead use webbing to wrap and subdue them(Olive, 1980, Fig. 1).
Predators can minimize their risk of prey-inflicted injuriesbehaviourally by minimizing contact or handling time (seeFig. 1; Table 1). By swiftly attacking and injuring dangerousprey, and then leaving it to die or become less active,predators can reduce their contact time with dangerousprey. For example Komodo dragons (Varanus komodoensis)target the legs of large and dangerous prey (e.g. waterbuffaloes). A sudden attack on the prey’s leg reduces thechances of their own injury, but leaves the prey crippled withtorn tendons and an infected wound, making them morevulnerable to future attacks (Auffenberg, 1981). Similarly,great white sharks (Carcharodon carcharias) appear to use a bite-and-spit (release) hunting tactic for dangerous Californiasea lions (Zalophus californianus), which results in the sea lionsbleeding to death (or going into shock) after an attack. Sharksdo not use this tactic for the less dangerous elephant seal(Mirounga angustirostris, Tricas & McCosker, 1985) and do notappear to use it when hunting smaller sea lions in otherlocations (Klimley, 1994; Klimley, Pyle & Anderson, 1996;Martin et al., 2005). Ant lions (Myrmeleon carolinus) are able tokill formic-acid-spraying ants (Camponotus floridanus) withoutinducing the ants to spray, and while feeding on the deadants they suck out the ant’s body contents without puncturing
0
10
20
30
40
50
60
Orthoptera Lepidoptera Diptera Orthoptera Lepidoptera Diptera
Num
ber
of a
ttac
ks
bite attacks wrap attacks
Araneus Argiope
Fig. 1. Differences in attack strategies upon safe and dangerousprey in orb web spiders. Spiders of the genera Araneus andArgiope are willing to risk direct contact (bite and inject venom)to capture large but safe prey (Lepidoptera and Diptera). Butthey avoid direct contact and instead use their web to wrap,subdue and hunt dangerous prey (Orthopera). Data from Olive(1980).
the ant’s formic acid sac (Eisner, Baldwin & Conner, 1993).Being more careful (i.e. increasing hunting or handling time)also can reduce the risk of injury. Grasshopper mice takesignificantly longer to subdue scorpions with neurotoxins(Centruroids spp.) compared to those species that do not havethese toxins (Vaejovis spp.; Rowe & Rowe, 2006).
The direction and position of an attack also plays animportant role in reducing the chances of injury. Forexample terrestrial predators such as domestic cats (Feliscatus) likely reduce their chances of injury by avoidinga frontal attack; instead they attack their prey from theback or the flanks (Pellis & Officer, 1987). Similar attackbehaviour has been observed in Asiatic lions (Leo leo persica)hunting water buffaloes in the Gir forests of western India(S. Mukherjee, personal communication). African wild dogs(Lycaon pictus) are able to successfully tackle armed prey suchas warthogs (Phacochoerus aethiopicus, which have dangeroustusks) only if they manage to restrain their head since itreduces their chances of injury from the warthog’s tusks(Creel & Creel, 2002). Australian limbless lizards (Lialisburtonis), lacking venom and constriction capabilities, useprey-size-specific hunting tactics. They almost always attacklarge lizard prey on the head or in the neck region therebyreducing their chances of being bitten (Wall & Shine, 2007).The predator lizards always wait for their larger lizard preyto be incapacitated before eating them, but consume smallerlizard prey immediately, even while it is still struggling (Wall& Shine, 2007). Finally, African ponerine ants (Pachycondylapachyderma) grab small and less dangerous prey (termites) bytheir thorax, but catch more dangerous prey (centipedes) bythe anterior part of their body and often sting them (Dejean& Lachaud, 2011).
Group hunting can reduce the per capita risk of an individualbeing injured when hunting large and dangerous prey. Forexample, in African wild dogs both hunting success andthe size of prey killed increases with pack size (Creel &Creel, 1995, 2002). Interestingly, however, the proportion
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society
556 Shomen Mukherjee and Michael R. Heithaus
of the total attacks (i.e. frequency) that are on dangerousprey (e.g. adults of impala, Aepyceros melampus, wildebeest,Connochaetes taurinus, warthog, zebra) does not change withpack size (Creel & Creel, 2002). In African lions, althoughsociality is suggested to have evolved to reduce the probabilityof infanticide (Packer, Scheel & Pusey, 1990) and increasedterritory-holding potential (McComb, Packer & Pusey, 1994;Grinnell, Packer & Pusey, 1995), group living also facilitatescapturing large or dangerous prey (see Packer & Ruttam,1988). Scheel (1993) found that prides of five or morelionesses were more likely to attack prey such as buffaloes,topi (Damaliscus korrigum) or kongoni (Alcelaphus buselaphus)compared to smaller prides. Individual lions also prefer tojoin group hunts only when hunting large and dangerousprey such as zebra and Cape buffalo (Scheel & Packer,1991). Like mammals, social insects may also minimizerisk and maximize hunting success by working together.For example, African ponerine ants (Pachycondyla pachyderma)hunt small and less dangerous prey (termites) solitarily, butseveral workers cooperate when catching dangerous preysuch as Scolopendra centipedes (Dejean & Lachaud, 2011).Hence, in order to reduce the risk of injury, predators mayprefer to hunt in larger groups than would be optimal formaximizing energy intake rates alone. Although data to testthis hypothesis specifically are not currently available, therich literature on the advantages of group hunting amongpredators (e.g. Packer et al., 1990; Boesch, 1994; Creel &Creel, 1995) and group formation for defence among prey(e.g. Berger, 1979) suggests that such dynamics are likely.
V. COSTS OF HUNTING DANGEROUS PREY
Understanding the fitness consequences of huntingdangerous prey is critical for integrating these costs andbenefits into our understanding of ecological dynamics.Unfortunately, few studies have quantified such costs. Inpart, this is due to the wide variation in the costs of evensingle encounters with dangerous prey. Avoiding dangerousprey entirely only carries the cost of a lost resource of amissed successful hunt. When predators pursue dangerousprey, however, the costs can be extreme. Killer whales(Orcinus orca) have died from injuries inflicted from the spinesof stingrays (Duignan et al., 2000) and rays also have killeddolphins foraging on other prey in habitats with high raydensities (Walsh et al., 1988, McLellan, Thayer & Pabst,1996). Similarly, live rodent prey can inflict lethal internalinjuries to owls (Gibson, Gibson & Bardelmeier, 1998) andlarge carnivores in Africa can be killed or badly injuredby their ungulate prey (Creel & Creel, 2002). An injuredpredator can also become more vulnerable to its competitors.For instance hyenas may kill lions injured during hunts(Schaller, 1972).
Sublethal impacts also can be extreme. Predators attackinga porcupine can end up with quills embedded in their limbs,body, or face, which will negatively impact future foraging(Quick, 1953). While trying to open their bivalve prey,
some snails (Sinistrofulgur sinistrum) may damage their ownshell and become more vulnerable to their own predators(Dietl, 2003). Some of the most obvious sublethal costsof hunting dangerous prey are reduced foraging efficiencythrough increased handling time, energetic and lost foragingtime costs of recovering from injuries and decreased abilityto capture particular prey types. For example, in Dungenesscrabs (Cancer magister), claw damage (chela breakage andclaw-tooth wear) due to fatigue failure (injury due to repeatedforce cycles) is one of the most important factors determiningboth crab foraging efficiency and the size of the prey crabschoose (Juanes & Hartwick, 1990). Crabs with damaged clawsbecome less efficient in opening their bivalve prey (Protothacastamina, Juanes & Hartwick, 1990, Fig. 2). Furthermore, longperiods of starvation because of an injury can lead to changesin foraging behaviour and willingness to incur risks thatcan increase the probability of accruing additional injuriesduring foraging. Murza et al. (2000) found that handicapped(broken flight feather or missing talons) American kestrels(Falco sparverius) are less willing to risk injury or spend energyin hunting dangerous prey.
VI. A FRAMEWORK FOR INVESTIGATINGFORAGING ON DANGEROUS PREY
Under what conditions are predators more or less likelyto attack dangerous prey? Although few studies havefocused on this specific question, the diverse literatureon optimal diet theory and foraging under the risk ofpredation offer important insights. Although the diets ofpredators foraging on mobile prey may be determinedprimarily by the effectiveness of anti-predator behaviour (Sih& Christensen, 2001), profitability remains an importantconcept when investigating predator foraging choices. Inmost cases, profitability refers to the quotient of the netenergetic gain from consuming the resource divided byhandling time (the time required to pursue, capture andconsume prey). Profitability is used as a proxy of fitness basedon the assumption that maximizing net energy intake ratealso maximizes fitness (Stephens & Krebs, 1986). Obviously,when predators hunt dangerous prey, this formulation ofprofitability is inadequate since attacking a particular preyitem can incur fitness costs as outlined above (e.g. reducedforaging ability, early death). Indeed, the absence of suchforaging costs from foraging models may explain why prey-choice data from the field do not match the predictions ofsimple foraging models (Creel & Creel, 2002). Hence, thereis a need to consider the risk of injury in foraging models forpredators hunting behaviourally responsive and dangerousprey.
(1) Interpreting the foraging costs of huntingdangerous prey
Although a framework for understanding the costs of huntingdangerous prey might seem to derive easily from that of
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society
Daring predators 557
1.5 2.0 2.5 3.0 3.5 4.0 4.5
Clam length (cm)
0
200
400
600
800
1000C
lam
bre
akin
g tim
e (s
)
worn
old
new
1.5 2.0 2.5 3.0 3.5 4.0 4.5
Clam length (cm)
0
200
400
600
800
1000
Cla
m e
atin
g tim
e (s
)
Fig. 2. Simulated regression equations from table 1 of Juanes& Hartwick (1990) show variations in clam breaking and eatingtime (the two components of handling time) of Dungeness crabswith ‘new’ (freshly moulted), ‘old’, and ‘worn’ (claw teeth fileddown) claws. Comparison of regression slopes (using equality-of-slope test) for both ‘old’ and ‘worn’ crabs to ‘new’ crabs showedsignificant differences in slope for eating time between ‘old’and ‘new’ crabs (P = 0.001). However for other comparisons,where slopes were homogeneous, analysis of covariance wasused to compare adjusted means between the groups. Thisshowed significant differences in eating time between worn–new(P=0.0001; higher in worn crabs), and also in breaking timebetween old–new (P = 0.003; higher in old) and worn–newcrabs (P = 0.006; higher in worn) over the range of clamstested. High breaking and eating times in ‘worn’ crabs can beconsidered similar to foraging costs of risk of injury to a predator.Since larger clams required more energy to open, the crabs alsohad an increased chance of claw muscle fatigue, hence higherrisk of injury.
hunting unpalatable or chemically defended prey, the costsare more likely to be akin to those of foraging under the riskof predation. This stems primarily from the uncertainty inthe consequences of hunting dangerous prey. The costs(e.g. sickness) of consuming chemically defended prey,as long as they are recognizable, are likely to be fairlypredictable. Hunting dangerous prey, however, may leadto a wide range of costs – from none at all to death –that may occur with different probabilities that foragersmay be able to assess. This is similar to making trade-offs
between foraging opportunities and reducing predationrisk.
Models addressing the foraging costs of predation risk canbe adapted to investigate the costs of foraging while huntingdangerous prey. Prey encounter rates and handling timeare critical factors influencing foraging decisions (Holling,1959; Schoener, 1971). A predator’s harvest rate (f ) can becalculated using Holling’s (1959) disc equation:
f = Ta × N
1 + (Ta × Tb × N )(1)
where, T a = prey encounter rate, T h = prey handlingtime and N = total number of prey. Dangerous prey canaffect the harvest rate in two ways. If predators take moretime to subdue and handle dangerous prey, T h will behigher (e.g. Juanes & Hartwick, 1990, Fig. 2). If predatorscontinue to encounter prey at a constant rate (T a), foragingon dangerous prey will result in lower harvest rates for thepredator (Fig. 3A). Therefore, a shift from safe to dangerousprey could result in considerably reduced energy intake ratesfor predators. Such may be the case for native predators facedwith increasing populations of dangerous invasive prey. Therelationship between energetic gains possible from attackingdangerous prey and increased handing time, discounted forthe fitness consequences of injury and probability of injurywhile foraging on that prey, should be critical to determiningthe probability that predators will attack a dangerous preyspecies.
Changing encounter rates would have a similar effect,but may operate through different mechanisms. Attackingdangerous prey and sustaining injury would increase therecovery time for predators, thereby reducing T a. For apredator hunting dangerous prey, if T h is held constant,even a large magnitude of change (e.g. eightfold) in T adoes not increase the harvest rate of a predator (Fig. 3B).Hence the more dangerous the prey, the lower is the harvestrate. Regardless of the mechanism involved, the differencebetween the harvest rate curves of dangerous and safe preytypes indicates the predator’s risk from its prey (Berger-Talet al., 2009). The greater the difference in risk between preytypes, the greater the difference in these curves, and thehigher the risk to the predator.
Data on predator hunting behaviour and success,specifically the relationship between the total time spenthunting a given prey and the number of attacks/attempts(i.e. physical contact with prey) required to successfully huntit, may provide insights into the perceived risk of injuryfrom prey when direct observations of prey-inflicted injuriesare not available. The least dangerous prey should requirerelatively short hunting times to capture and, in general,fewer attempts should be required for a successful hunt (areaI of Fig. 4). For African wild dogs this category of prey wouldinclude piglets, fawns and ungulate yearlings (Creel & Creel,2002). A second category of prey is one requiring moreattempts for a successful capture, but is quickly subdued(area II, Fig. 4). Finding a prey to fit this category is likelyto be biologically challenging since number of attempts
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society
558 Shomen Mukherjee and Michael R. Heithaus
0 10 20 30 40 50 60
Prey density
0
2
4
6
8
10
12
14
16
18
20
22
24 (A)
(B)
Har
vest
rat
e, f
(#
kille
d/da
y)
Safe prey (Th=0.032)
Dangerous prey (Th=0.256)
(Th=0.064)
(Th=0.128)
Ta=1.38 (fixed)
0 10 20 30 40 50 60
Prey density
0
2
4
6
8
10
12
14
16
18
20
22
24
Har
vest
rat
e, f
(#
kille
d/da
y)
(Ta=1.38)
(Ta=0.173)
(Ta=0.69)
(Ta=0.345)
Th = 0.256 (fixed)
Fig. 3. Simulated harvest rate curves [using Holling’s (1959)disc equation] for a predator, showing the effect of varying prey(A) handling time (T h), and (B) encounter rate (T a).
and hunting time are generally positively correlated. Agood example of such a prey would be Thompson’s gazelle(Eudorcas thomsonii), which are good at escaping, but whencaught by a cheetah (Acinonyx jubatus) are killed swiftly. Preythat require many attempts before a hunt is successful aswell as relatively long times to capture should generally bethe most dangerous prey for a predator (area III in Fig. 4).Many attempts are needed because the predator has tocatch and release its prey several times in order to avoidphysical injury. It also helps tire the prey so that the predatorcan easily subdue it at a later stage. Buffaloes, which havebeen observed to injure and even kill lions (Mangani, 1962;Mitchell, Shenton & Uys, 1965; Makacha & Schaller, 1969)fit such a description. A fourth category of prey includesspecies which require long times to capture and subdue, butfew attempts are generally successful (area IV in Fig. 4). Thiscould be either because the prey has to be stalked for along time before an attack, or because habitat characteristicsfavour the prey (e.g. hunting in a difficult terrain). Forexample, a snow leopard hunting blue sheep (Pseudois nayaur)in the steep slopes of the Himalayas has to reach a fairly closedistance (i.e. long stalking time) before attempting to attack,
Num
ber
of a
ttack
s pe
r su
cces
sful
hun
t
Time spent during an individual hunt
(II) (III)
(IV)(I)
Fig. 4. The relationship between the total time spent huntinga given prey and the number of attacks/attempts required tosuccessfully hunt can provide insights into a predator’s risk ofinjury. Prey that fall in area I are the easiest (few attempts andshort hunting time) to catch (least dangerous). Prey in area IIare tricky (more attempts) to catch, but biologically it maybedifficult to find such a prey since the number of attempts bya predator is generally positively correlated with hunting time.Prey in area III are difficult to catch (more attempts and longhunting time) and likely to be the most dangerous. Prey that fallin area IV require a long time to stalk, hence long hunting time,but are captured swiftly.
but once they reach this position, are likely to be successful.While number of hunting attempts per successful hunt, andtotal time spent hunting will typically covary positively (seeScheel, 1993), factors such as aggressiveness of the prey(i.e. prey defence) and the predator’s energetic state andpersonality (both discussed later in Section IV.2) will alsoinfluence this relationship.
(2) Is there intraspecific variation in willingness totake risks?
Theory based on food versus predation-risk trade-offs canprovide a basis for developing insights into when predatorsshould risk injury. For example, an approach similar to thatof Lima & Dill (1990) can be used to quantify risk of injuryP(Injury) for a predator, as follows:
P(Injury
) = 1 –exp (–αiT ) (2)
where α is the rate of encounter between a predator anda dangerous prey, i is the probability of injury given anencounter, and T is the time spent vulnerable during anencounter. We can think of α, i and T as the basiccomponents of risk of injury, and these are assessable bya predator. The rate of encounter will depend on variousfactors such as prey density, search tactics, habitat structure,etc. The probability of injury, i, given an encounter, isdependent on a set of conditional probabilities in thesituation in which an encounter occurs, the predatorattacks, and potentially gets injured (see Fig. 5), where i
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society
Daring predators 559
Encounter situation(for a predator)
Detects prey No encounter
1-p p
Avoids prey(prey too dangerous)
Attacks prey
a 1-a
Captures prey Prey escapes
1-c c
Predator gets injured Successful capture
s1-r -s
Predator releases prey(prey too dangerous)
r
Fig. 5. Schematic representation of a predator hunting adangerous prey. The symbols adjacent to the arrows representthe conditional probability of the predator following a certainpathway. Only a portion of all encounters lead to potentialinjury to the predator.
can be defined as:
i = (1–p
)(1–a) (1–c) (1– r –s) (3)
where 1-p is the probability of detecting a prey, 1-a is theprobability that the predator decides to attack the prey, 1-cis the probability that it captures the prey, s is the probabilitythat the capture is successful, r is the probability that itreleases the prey after capture since it is dangerous, and1-r-s is the probability that the predator gets injured. Mostof these sub components (see Fig. 5) can be assessed by thepredator. For example, after sighting a prey, the predatorcan assess the level of danger posed by that potential preyitem and may choose to avoid it or to attack. If it doesdecide to attack it, the predator may choose to releaseits prey depending on its assessment of the probability ofinjury and the potential severity of any possible injury.Time, T , in the context of risk of injury, can be thoughtof as time spent actually pursuing the dangerous prey,and this again can be managed by the predator. Thus,predators would be expected to manage their risk of injuryat least to some extent at multiple points in a predator–preyencounter.
Brown’s (1988, 1992) model can be interpreted to suggestthat a predator should stop hunting a dangerous prey whenits harvest rate or reward (f ) equals sum of its metabolic cost(c), missed opportunity cost (MOC ) and cost of risk of injury(RI ; Berger-Tal et al., 2009).
f = c + MOC + RI . (4)
MOC represents the alternatives that the predator misses,e.g. hunting less dangerous prey, or simply resting. Thecost of risk of injury (RI ) has units of energy per unit timeor resources per unit time. The currency of risk of injury,γ , can be converted into the currency of f by multiplyingthe risk of injury by the marginal rate of substitution ofenergy (MRS) for safety. The MRS depends upon the fitnessformulation, and is the ratio of survivor’s fitness (F ) to themarginal fitness value of energy (MVE, ∂F/∂e; Brown, 1992;Brown & Kotler, 2004). Therefore, following Brown (1992),the energetic cost of risk of injury (RI ) to a predator is:
RI = γ F(
∂F∂e
) (5)
This equation suggests that as the value of acquiring energyincreases for a predator, its overall cost of RI is reduced,and hence the predator should be willing to take greaterrisks (Berger-Tal et al., 2009). This is consistent with state-dependent foraging theory which suggests that individualsthat are in a poor state (e.g. close to starvation) are morelikely to take greater risks while foraging (McNamara &Houston, 1987) because their MVE is greater and costs ofpredation are lower (Charnov, 1976; Brown, 1988). Diversefield studies have provided support for state-dependentforaging under predation risk (e.g. Godin & Smith, 1988;Heithaus et al., 2007; Berger-Tal et al., 2010). Berger-Talet al. (2009) extended this to injury costs and tested whetherRI is a true foraging cost to a predator (red fox, Vulpesvulpes). They found that foxes exploited safe patches moreintensively, by foraging for a longer time and also removingmore food, compared to risky patches. They also found thathungrier foxes allocated more time to foraging from riskierpatches. Other studies support state-dependent foraging ondangerous prey. For example, lions in Hawange NationalPark, Zimbabwe, are more likely to hunt elephant calves(which are strongly protected by their herd) during the drymonths and drought years when the energetic state of lions islow (Loveridge et al., 2006). These decisions, however, mayalso be influenced by the relative abundance of alternativeprey affecting the predator’s MOC.
State-dependent decisions about attacking dangerousprey, however, may not always occur in a consistent manner.For instance, foragers in poor condition may be more likelyto be injured by dangerous prey (high RI ) and hence avoidthem. Murza et al. (2000) found that injured male Americankestrels (Falco sparverius) were more reluctant to attack largeand potentially dangerous rodent prey compared to non-handicapped birds. Perhaps injured birds have a highercost of missed opportunity, hence preferring to rest andrecover and thus are reluctant to attack. Predators may alsobe willing to take more risk when their food resources areabundant, since the costs of experiencing a negative payoffcan be recuperated rapidly. For example, in chimpanzees(Pan troglodytes), both hunting rate and the probability ofhunting upon encountering red colobus monkeys (Procolobusspp.) are positively correlated with seasonal consumption of
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society
560 Shomen Mukherjee and Michael R. Heithaus
ripe drupe fruits (Gilby & Wrangham, 2007). These fruitsare a preferred food and they are associated with elevatedreproductive performance by females (Gilby & Wrangham,2007).
In some cases injury to a predator can lead to inter-specific conflict and further costs. For example, large cats inAsia and Africa may resort to killing humans (less profitablebut easier prey) after suffering an injury. Corbett (1946,1957) found that some man-eating leopards (Panthera pardus)and tigers, which killed several hundred villagers in northernIndia, suffered from a missing (or broken) tooth or claw, whileothers had injuries from porcupine quills or gunshot wounds.
It is likely that predators of different age, sex, andreproductive classes vary in their willingness to attackdangerous prey. Clark’s (1994) asset protection principlesuggests that the larger the reproductive asset of an individual,the more inclined it is to protect it. Following this, one mightexpect pregnant females to take less risk for two main reasons.They might be less adept at avoiding injury (physically lessagile, e.g. Magnhagen, 1991), but they also have more tolose (i.e. greater immediate loss of fitness) if they are injuredor killed than a non-pregnant female or a male. Hence,following Equations (4) and (5), since F is high for a pregnantfemale, it also has a high cost of RI .
Reproductive value can also depend on the age of theindividual. For example, adult redshanks (Tringa totanus)minimize their risk of predation at the cost of reducedenergetic intake rate, while juveniles maximize their intakerate at the cost of higher predation risk (Cresswell, 1994).Variations in anti-predator behaviours between sexes and ageclasses have also been reported. Male and yearling yellow-bellied marmots (Marmota flaviventris) reduce their foragingbehaviour under risk of predation more than females andadult marmots (Lea & Blumstein, 2011). Such decisionsalmost certainly will apply with regard to the probability ofan individual hunting dangerous prey.
Social rank might also affect willingness to attackdangerous prey since it is related to their fitness. For example,in spotted hyenas (Crocuta crocuta) even though low- andhigh-ranked females have similar hunting success, it is thelow-ranked females who hunt more often (Holekamp et al.,1997), and hence are more prone to risk of injury fromtheir prey. Direct fitness benefits of risk-taking behaviourhave been documented in primates. For example, differentspecies of Colobus and Cercopithecus monkeys are hunted bychimpanzees (Boesch, 1994; Stanford et al., 1994), which areone of the few primates that hunt for meat, even thoughthese prey can potentially be dangerous (can fight back andbite, Gomes & Boesch, 2009). After a successful hunt, femalechimpanzees often beg for meat from males, and the malesare more likely to share the meat with these females thanwith other males (Gomes & Boesch, 2009). Females not onlybenefit energetically, but also by reducing the potential riskof being injured while hunting (Boesch, 1994; Gomes &Boesch, 2009). Successful males gain direct fitness advantageby sharing their meat since female chimpanzees copulatemore frequently with males that share meat, thereby directly
increasing the propensity of the males to father offspring(Gomes & Boesch, 2009).
Recent studies have shown important roles of personalitytraits on the foraging decisions of animals [see Wilson et al.(1994), Sih, Bell & Johnson (2004) and Reale et al. (2007)for reviews], with some individuals being inherently moreaggressive and bold than others (Riechert & Hedrick, 1993;Maupin & Riechert, 2001). It is possible that boldnesscould be related to propensity to attack risky prey, and thiscould be referred to as the predator’s ‘daringness’ (Brown &Kotler, 2004; Berger-Tal et al., 2009). Under standardizedconditions, the smaller the difference in hunting behaviour(e.g. harvest rate) of a predator between dangerous and safeprey, the more daring (i.e. willingness to risk injury) is thepredator (Berger-Tal et al., 2009). The relationship betweena predator’s body size and that of its prey will also affect theprobability of injury; therefore, we might expect larger indi-viduals of a population to be more likely to hunt dangerousprey. In Yellowstone National Park, USA, larger wolves arebetter at strength-related tasks (grappling and subduing elk)compared with smaller individuals (MacNulty et al., 2009).
Do predators take risk of injury into account when decidingwhere to hunt? Although previous studies have consideredhow physical features of the environment affect prey-captureprobabilities (Cresswell & Quinn, 2004; Hebblewhite,Merrill & McDonald, 2005; Hopcraft, Sinclair & Packer,2005; Heithaus et al., 2009; Wirsing, Cameron & Heithaus,2010), how physical danger posed by microhabitat or habitattype affects hunting decision and success of predators is poorlyunderstood. Indeed, predator avoidance of certain habitattypes (i.e. prey refugia) is largely studied in the context of howeasily predators are detected by their prey (i.e. prey–predatorencounter rate). What is largely overlooked is the extent towhich predators avoid certain areas to minimize their risk ofinjury. For example wolves avoid steep slopes (see Kauffmanet al., 2007) most likely because it helps reduce their chancesof injury from falling, and hence these areas likely act asrefuges for their prey. Resource selection functions (Boyce &McDonald, 1999; Manly et al., 2002) not only form anefficient framework for quantifying the spatial probabilityof predator–prey encounter rates and kills in ecologicallandscapes (Hebblewhite et al., 2005), but also could provideinsights into a predator’s spatial probability of risk of injurywhile hunting. Decisions made by predators hunting indangerous landscapes are likely to mirror those made byanimals foraging under the risk of predation, but with lowerfitness costs.
The selection of a more dangerous prey (or a daring preda-tor) can be driven by escalation or coevolution (Vermeij,1994; Brodie & Brodie, 1999). While predators accumulateadaptations (including behaviours) that increase their hunt-ing success, prey adapt to reduce their risk of being killed. Ina game between daring predators and dangerous prey, thereis the intriguing possibility that there would be selection forprey adaptations (either physical or behavioural) that wouldincrease risk to predators and, therefore, require even moredaring predators. For example, could daring in predators
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society
Daring predators 561
select for more aggressive prey that are willing to confrontpredators? Aggression in prey has several advantages beyondpotentially reducing predation risk including enhancedresource (food, mate, offspring, etc.) defence. Previousstudies have found that there is higher correlation betweenaggressiveness and boldness (via correlative selection) inpopulations facing strong predation pressure (Bell & Sih,2007). In certain prey species this may translate to increasedaggression towards the predator, thereby increasing thepredators RI. The prey’s aggression may feedback andinfluence the predator’s behaviour. The predator may eitheravoid the prey, or show increased boldness by attackingthe prey while risking injury. Hence risk-taking by daringpredators may ultimately be related to ‘daring’ behaviour inthe prey themselves. This hypothesis remains to be tested.
VII. CONCLUSIONS
(1) Predators that hunt dangerous prey represent a specialclass of prey–predator interactions that have not yet beenwell integrated into our understanding of foraging behaviourand predator–prey games theory. It is likely that mostforagers pay a risk of injury foraging cost, with these costsbeing greater for predators than herbivores.
(2) Understanding the foraging costs of hunting dangerousprey and the frequency and costs of prey-inflicted injurieslikely will provide important insights into the dynamics ofsome communities.
(3) Just as anti-predator behaviours of prey help stabilizepredator–prey dynamics in fear-driven systems (Brown,Laundre & Gurung, 1999), the foraging decisions andbehavioural responses of predators to minimize risk of injurymay play an important role in at least some predator–preyforaging systems.
(4) Both theoretical and empirical studies are still neededto answer basic questions about the frequency and severityof injuries to predators hunting across a range of ecologicalconditions, the fitness costs of these injuries, and the tacticsemployed to balance energy gain and costs of injury.While these costs and risk-reducing behaviours amongpredators seem to have been investigated to some extent ininvertebrates (Table 1) we need similar quantitative studiesin other groups.
(5) Although it will be a challenge to quantify costs of riskof injury in the wild, the collection of such data especiallyin situations where there are changes in prey availability(that might affect willingness to take risks) or invasions ofpotentially dangerous prey, should be an important avenueof future research for behavioural ecologists.
VIII. ACKNOWLEDGEMENTS
Funding was provided by the Florida InternationalUniversity College of Arts and Sciences, National ScienceFoundation (grants OCE0745606, DEB-9910514). Thanks
to Alison Cooper, Burt Kotler, Keren Embar, Oded Berger-Tal and an anonymous reviewer for their valuable comments.
IX. REFERENCES
Ackermann, J. & Redig, P. (1997). Surgical repair of elbow luxation in raptors.Journal of Avian Medicine and Surgery 11, 247–254.
Agrawal, A. A. (2001). Phenotypic plasticity in the interactions and evolution ofspecies. Science 294, 321–326.
Auffenberg, W. (1981). Behavioral Ecology of the Komodo Monitor. University PressFlorida, Gainesville.
Barr, A. D., Wieburg, S. A. & Kardong, K. V. (1988). The predatory strikebehavior of the mamushi (Agkistrodon b. blomhoffii) and the Malay Pitviper (Calloselasma
rhodostoma). Japanese Journal of Herpetology 12, 135–138.Bedrosian, B. E. & St. Pierre, A. M. (2007). Frequency of injuries in three raptor
species wintering in northern Arkansas. Wilson Journal of Ornithology 119, 296–298.Bell, A. & Sih, A. (2007). Exposure to predation generates personality in three spined
sticklebacks (Gasterosteus aculeatus). Ecology Letters 10, 828–834.Berger-Tal, O., Mukherjee, S., Kotler, B. P. & Brown, J. S. (2009). Look
before you leap: is risk of injury a foraging cost? Behavioral Ecology and Sociobiology 63,1821–1827.
Berger-Tal, O., Mukherjee, S., Kotler, B. P. & Brown, J. S. (2010). Complexstate-dependent game between owls and gerbils. Ecology Letters 13, 302–310.
Berger, J. (1979). Predator harassment as a defense strategy in ungulates. American
Midland Naturalist 102, 197–199.Boesch, C. (1994). Cooperative hunting in wild chimpanzees. Animal Behaviour 48,
653–667.Boyce, M. S. & McDonald, L. L. (1999). Relating populations to habitats using
resource selection functions. Trends in Ecology & Evolution 14, 268–272.Braithwaite, L. F., Stone, B. & Bingham, B. L. (2010). Defensive behaviors of
gastropod Amphissa columbiana. Journal of Shellfish Research 29, 217–222.Brodie, E. D. III & Brodie, E. D. Jr. (1999). Predator–prey arms races: asymmetrical
selection on predators and prey may be reduced when prey are dangerous. Bioscience
49, 557–568.Brown, J. S. (1988). Patch use as an indicator of habitat preference, predation risk,
and competition. Behavioral Ecology and Sociobiology 22, 37–47.Brown, J. S. (1992). Patch use under predation risk. I. Models and predictions. Annales
Zoologici Fennici 29, 301–309.Brown, J. S. & Kotler, B. P. (2004). Hazardous duty pay and the foraging cost of
predation. Ecology Letters 7, 999–1014.Brown, J. S., Laundre, J. W. & Gurung, M. (1999). The ecology of fear: optimal
foraging, game theory, and trophic interactions. Journal of Mammalogy 80, 385–399.Charnov, E. L. (1976). Optimal foraging, the marginal value theorem. Theoretical
Population Biology 9 (129), 136.Clark, C. W. (1994). Antipredator behavior and the asset-protection principle.
Behavioral Ecology 5, 159–170.Congi, R., Fritus, A. V. L. & Filho, B. F. A. (2002). Influence of prey size on
predation success by Zelus longipes L. (Het., Reduviidae). Journal of Applied Entomology
126, 74–78.Corbett, J. (1946). Man-Eaters of Kumaon. Oxford University Press, London.Corbett, J. (1957). Man-Eaters of India. Oxford University Press, New York.Creel, S. & Christanson, D. (2008). Relationships between direct predation and
risk effects. Trends in Ecology & Evolution 23, 194–201.Creel, S. & Creel, N. M. (1995). Communal hunting and pack size in African wild
dogs, Lycaon pictus. Animal Behaviour 50, 1325–1339.Creel, S. & Creel, N. M. (2002). The African Wild dog: Behavior, Ecology and Conservation.
Princeton University Press, Princerton.Cresswell, W. (1994). Age-dependent choice of redshank (Tringa totanus) feeding
location: profitability or risk? The Journal of Animal Ecology 63, 589–600.Cresswell, W. & Quinn, J. L. (2004). Faced with a choice, sparrowhawks more
often attack the more vulnerable prey group. Oikos 104, 71–76.Dejean, A. & Lachaud, J. (2011). The hunting behavior of the African ponerine ant
Pachycondyla pachyderma. Behavioral Processes 86, 169–173.Dickson, B. G., Jenness, J. S. & Beier, P. (2004). Influence of vegetation, topography,
and roads on cougar movement in Southern California. The Journal of Wildlife
Management 69, 264–276.Dietl, G. P. (2003). Interaction strength between a predator and dangerous prey:
Sinistrofulgur predation on Mercenaria. Journal of Experimental Marine Biology and Ecology
289, 287–301.Donadio, E. & Buskirk, S. W. (2006). Diet, morphology and interspecific killing in
carnivore. The American Naturalist 167, 524–536.Duignan, P. J., Hunter, J. E. B., Visser, I. N., Jones, G. W. & Nutman, A. (2000).
Stingray spines: a potential cause of killer whale mortality in New Zealand. Aquatic
Mammals 26, 143–147.
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society
562 Shomen Mukherjee and Michael R. Heithaus
Edmunds, M. (1974). Defense in Animals: A Survey of Anti-Predator Defenses.Longman, Harlow.
Eisner, T. & Aneshansley, D. J. (1999). Spray aiming in the bombardier beetle:photographic evidence. Proceedings of the National Academy of Sciences 96, 9705–9709.
Eisner, T., Baldwin, I. T. & Conner, J. (1993). Circumvention of prey defense by apredator: ant lion vs ant. Proceedings of the National Academy of Sciences 90, 6716–6720.
Frid, A., Burns, J. & Baker, G. G. (2009). Predicting synergistic effects of resourcesand predators on foraging decisions by juvenile steller sea lions. Oecologia 158,775–786.
Garner, G. W. & Morrison, J. A. (1980). Observations of interspecific behaviorbetween predators and white-tailed deer in southwestern Oklahoma. Journal of
Mammalogy 61, 126–130.Gibson, M. J., Gibson, D. C. & Bardelmeier, D. G. (1998). Prey conquers
predator: a case study – barred owl dies from rodent-inflicted wound. Journal of
Wildlife Rehabilitation 21, 19–21.Gilby, I. C. & Wrangham, R. W. (2007). Risk-prone hunting by chimpanzees (Pan
troglodytes schweinfurthii) increases during periods of high diet quality. Behavioral Ecology
and Sociobiology 61, 1771–1779.Godin, J. J. & Smith, S. A. (1988). A fitness cost of foraging in the guppy. Nature 333,
69–71.Gomes, C. M. & Boesch, C. (2009). Wild chimpanzees exchange meat for sex on a
long- term basis. PLoS ONE 4 (4), e5116 (doi: 10.1371/journal.pone.0005116).Greene, J. (1967). The distribution and variation of Daphnia Zumholtzi (Crustacea:
Cladocera) in relation to fish predation in Lake Albert, East Africa. Journal of Zoology
151, 181–197.Grinnell, J., Packer, C. & Pusey, A. E. (1995). Cooperation in male lions: kinship,
reciprocity or mutualism? Animal Behaviour 49, 95–105.Haddock, S. H. D., Moline, M. A. & Case, J. F. (2010). Bioluminescence in the sea.
Annual Review of Marine Science 2, 443–493.Hayward, M. W., Henschel, P., O’Brien, J., Hofmeyr, M., Balme, G. &
Kerley, G. I. H. (2006). Prey preferences of the leopard (Pantherapardus). Journal of
Zoology 270, 298–313.Hebblewhite, M., Merrill, E. H. & McDonald, T. L. (2005). Spatial
decomposition of predation risk using resource selection functions: an examplein a wolf-elk predator–prey system. Oikos 111, 101–111.
Heithaus, M. R., Frid, A., Wirsing, A. J., Dill, L. M., Fourqurean, J.,Burkholder, D., Thompson, J. & Bejder, L. (2007). State-dependent risk-takingby green sea turtles mediates top-down effects of tiger shark intimidation in a marineecosystem. The Journal of Animal Ecology 76, 837–844.
Heithaus, M. R., Frid, A., Wirsing, A. J. & Worm, B. (2008). Predicting ecologicalconsequences of marine top predator declines. Trends in Ecology & Evolution 23,202–210.
Heithaus, M. R., Wirsing, A. J., Burkholder, D., Thomson, J. & Dill, L. M.(2009). Towards a predictive framework for predator risk effects: the interaction oflandscape features and prey escape tactics. The Journal of Animal Ecology 78, 556–562.
Holekamp, K. E., Smale, L., Breg, R. & Cooper, S. M. (1997). Hunting rates andhunting success in the spotted hyena (Crocuta crocuta). Journal of Zoology 242, 1–15.
Holling, C. S. (1959). Some characteristics of simple types of predation andparasitism. The Canadian Entomologist 91, 385–398.
Holt, D. W. & Layne, E. A. (2008). Eye injuries in long-eared owls (Asiootus):prevalence and survival. Journal of Raptor Research 42, 243–247.
Hopcraft, J. G. C., Sinclair, A. R. E. & Packer, C. (2005). Planning for success:Serengeti lions seek prey accessibility rather than abundance. The Journal of Animal
Ecology 74, 559–566.Juanes, F. & Hartwick, E. B. (1990). Prey selection in dungeness crabs: the effect of
claw damage. Ecology 71, 744–758.Kardong, K. V. (1986). Predatory strike behavior of the rattlesnake, Crotalus viridis
oreganus. Journal of Comparative Psychology 100, 304–313.Kauffman, M. J., Varley, N., Smith, D. W., Stahler, D. R., MacNulty, D.
R. & Boyce, M. S. (2007). Landscape heterogeneity shapes predation in a newlyrestored predator–prey system. Ecology Letters 10, 690–700.
Klimley, A. P. (1994). The predatory behavior of the white shark. American Scientist
52, 122–133.Klimley, A. P., Pyle, P. & Anderson, S. D. (1996). The behavior of white sharks and
their pinniped prey during predatory attacks. In Great White Sharks: The Biologyof Carcharodon Carcharias (eds A. P. Klimley and D. G. Ainley), pp. 175–191.Academic Press, New York.
Kotler, B. P., Gross, J. E. & Mitchell, W. A. (1994). Applying patch use to assessaspects of foraging behavior in Nubian ibex. The Journal of Wildlife Management 58,299–307.
Lea, A. J. & Blumstein, L. (2011). Age and sex influence marmot antipredatorbehavior during periods of heightened risk. Behavioral Ecology and Sociobiology 65,1525–1533.
Lima, S. L. (1998). Stress and decision making under the risk of predation: recentdevelopments from behavioral, reproductive, and ecological perspectives. Advances
in the Study of Behavior 27, 215–290.Lima, S. L. & Dill, L. M. (1990). Behavioral decisions made under the risk of
predation: a review and prospectus. Canadian Journal of Zoology 68, 619–640.
Loveridge, A. J., Hunt, J. E., Murindagomo, F. & Macdonald, D. W. (2006).Influence of drought on predation of elephant (Loxodonta africana) calves by lions(Panthera leo) in an African wooded savannah. Journal of Zoology 270, 523–530.
MacNulty, D. R., Smith, D. W., Mech, L. D. & Eberly, L. E. (2009). Body sizeand predatory performance in wolves: is bigger better? The Journal of Animal Ecology
78, 532–539.Magnhagen, C. (1991). Predation risk as a cost of reproduction. Trends in Ecology &
Evolution 6, 183–186.Makacha, S. & Schaller, G. B. (1969). Observations on lions in the Lake Manyara
National Park, Tanzania. East African Wildlife Journal 7, 99–103.Mangani, B. (1962). Buffalo kills lion. African Wildlife 16, 27.Manly, B. F. J., McDonald, L. L., Thomas, D. L., McDonald, T. L. & Erickson,
W. P. (2002). Resource Selection by Animals: Statistical Analysis and Design for Field Studies.Second Edition. Kluwer, Massachusetts.
Mao, J. S., Boyce, M. S., Smith, D. W., Singer, F. J., Vales, D. J., Vore, J. M. &Merrill, E. H. (2005). Habitat selection by elk before and after wolf reintroductionin Yellowstone National Park. The Journal of Wildlife Management 69, 1691–1707.
Martin, R. A., Hammerschlag, N., Collier, R. S. & Fallows, C. (2005).Predatory behaviour of white shakrs (Carcharodon carcharias) at Seal Island, SouthAfrica. Journal of the Marine Biological Association of the United Kingdom 85, 1121–1135.
Maupin, J. L. & Riechert, S. E. (2001). Superfluous killing in spiders: a consequenceof adaptation to food-limited environments? Behavioral Ecology 12, 569–576.
McComb, K., Packer, C. & Pusey, A. (1994). Roaring and numerical assessment incontests between groups of female lions, Panthera leo. Animal Behaviour 47, 379–387.
McLellan, W. A., Thayer, V. G. & Pabst, D. A. (1996). Stingray spine mortalityin a bottle nose dolphin, Tursiops truncates, from North Carolina waters. The Journal
of the Elisha Mitchell Scientific Society 112, 98–101.McNamara, J. M. & Houston, A. I. (1987). Starvation and predation as factors
limiting population size. Ecology 68, 1515–1519.Mitchell, B. L., Shenton, J. B. & Uys, J. C. M. (1965). Predation on large mammals
in the Kafue National Park, Zambia. Zoologica Africana 1, 297–318.Murza, G. L., Bortolotti, G. R. & Dawson, R. D. (2000). Handicapped American
kestrels: needy or prudent foragers. Journal of Raptor Research 34, 137–142.Olive, C. W. (1980). Foraging specialization in orb-weaving spiders. Ecology 61,
1133–1144.Ono, M., Igarashu, T., Ohno, E. & Sasaki, M. (1995). Unusual thermal defense
by a honeybee against mass attack by hornets. Nature 377, 334–336.Packer, C. & Ruttam, L. (1988). The evolution of cooperative hunting. The American
Naturalist 132, 159–198.Packer, C., Scheel, D. & Pusey, A. E. (1990). Why lions form groups: food is not
enough? The American Naturalist 136, 1–19.Pearlman, Y. & Tsurim, I. (2008). Daring, risk assessment and body condition
interactions in steppe buzzards Buteobuteo vulpinus. Journal of Avian Biology 39,226–228.
Pellis, S. M. & Officer, R. C. E. (1987). An analysis of some predatory behaviorpatterns in four species of carnivorous marsupials (Dasyuridae), with comparativenotes on the Eutherian cat Felis catus. Ethology 75, 177–196.
Preisser, E., Bolnick, D. I. & Benard, M. F. (2005). Scared to death? The effects ofintimidation and consumption in predator–prey interactions. Ecology 86, 501–509.
Quick, H. F. (1953). The occurrence of porcupine quills in carnivorous mammals.Journal of Mammalogy 34, 256–259.
Reale, D., Reader, S. M., Sol, D., McDougall, P. T. & Dingemanse, N. J. (2007).Integrating animal temperament within ecology and evolution. Biological Reviews 82,291–318.
Riechert, S. E. & Hedrick, A. V. (1993). A test for correlations among fitness-linked behavioural traits in the spider Agelenopsisaperta (Aranear, Agelenidae). Animal
Behaviour 46, 669–675.Roth, A. J., Jones, G. S. & French, T. W. (2002). Incidence of naturally-healed
fractures in the pectoral bones of North American accipiters. Journal of Raptor Research
36, 229–230.Rowe, A. H. & Rowe, M. P. (2006). Risk assessment by grasshopper mice (Onychomys
spp.) feeding on neurotoxic prey (Centruroides spp.). Animal Behaviour 71, 725–734.Ruxton, G. D., Speed, M. P. & Kelly, D. J. (2004). What, if anything, is the adaptive
function of countershading? Animal Behaviour 68, 445–451.Schaller, G. B. (1972). The Serengeti Lion: A Study of Predator-Prey Relations.
University of Chicago Press, Chicago.Scheel, D. (1993). Profitability, encounter rates, and prey choice of African lions.
Behavioral Ecology 4, 90–97.Scheel, D. & Packer, C. (1991). Group hunting behaviour of lions: a search for
cooperation. Animal Behaviour 4, 697–709.Schmitz, O., Krivan, V. & Ovadia, O. (2004). Trophic cascades: the primacy of
trait-mediated indirect interactions. Ecology Letters 7, 153–163.Schoener, T. W. (1971). Theory of feeding strategies. Annual Review of Ecology and
Systematics 2, 369–404.Shine, R., Harlow, P. S., Keogh, J. S. & Boeadi (1998). The influence of body
size on the food habits of a giant tropical snake, Python reticularis. Functional Ecology 12,248–258.
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society
Daring predators 563
Sih, A., Bell, A. & Johnson, J. C. (2004). Behavioral syndromes: an ecological andevolutionary overview. Trends in Ecology & Evolution 19, 372–378.
Sih, A. & Christensen, B. (2001). Optimal diet theory: when does it work, and whenand why does it fail? Animal Behaviour 61, 379–390.
Stanford, C. B., Wallis, J., Mpongo, E. & Goodall, J. (1994). Hunting decisionsin wild chimpanzees. Behaviour 131, 1–18.
Stephens, D. W. & Krebs, J. R. (1986). Foraging Theory. Princeton University Press,Princeton.
Swaffer, S. M. & O’Brien, W. J. (1996). Spines of Daphnia lumholtzi create feedingdifficulties for juvenile bluegill sunfish (Lepomis macrochirus). Journal of Plankton Research
18, 1055–1061.Tricas, T. C. & McCosker, J. E. (1985). Predatory behavior of the white shark
(Carcharodon carcharias), with notes on its biology. Proceedings of the California Academy of
Sciences 43, 221–238.Van Valkenburg, B. (2009). Costs of carnivory: tooth fracture in Pleistocene and
recent carnivorans. Biological Journal of the Linnean Society 96, 68–81.Van Valkenburg, B. & Hertel, F. (1993). Tough times at La Brea: tooth breakage
in large carnivores of the late Pleistocene. Science 261, 456–459.
Vermeij, G. J. (1994). The evolutionary interaction among species: selection, escalationand coevolution. Annual Reviews of Ecology and Systematics 25, 219–236.
Wall, M. & Shine, R. (2007). Dangerous food: lacking venom and constriction, howdo snake-like lizards (Lialisburtonis, Pygopodidae) subdue their lizard prey? Biological
Journal of the Linnean Society 91, 719–727.Walsh, M. T., Beusse, D., Bossart, G. D., Young, W. G., Odell, D. K. &
Patton, G. W. (1988). Ray encounters as a mortality factor in the Atlanticbottlenose dolphins (Tursiops truncatus). Marine Mammal Science 4, 154–162.
Warham, J. (1977). The incidence, function and ecological significance of petrelstomach oils. Proceedings of the New Zealand Ecological Society 24, 84–93.
Werner, E. E. & Peacor, S. D. (2003). A review of trait-mediated indirect interactionsin ecological communities. Ecology 84, 1083–1100.
Wilson, D. S., Clark, A. B., Coleman, K. & Dearstyne, T. (1994). Shyness andboldness in humans and other animals. Trends in Ecology & Evolution 9, 442–446.
Wirsing, A., Cameron, K. & Heithaus, M. R. (2010). Spatial responses to predatorsvary with prey escape mode. Animal Behavior 79, 531–537.
(Received 1 September 2011; revised 17 November 2012; accepted 11 December 2012; published online 21 January 2013)
Biological Reviews 88 (2013) 550–563 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society