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E n d an g ered , a p p aren tly : th e role of a p p a r e n t c o m p e titio n in
e n d a n g e re d s p e c ie s c o n se rv a tio n
N. J. D e C e s a re \ M . H e b b le w h ite \ H. S. Robinson^ & M . M usiani^
1 W ildlife Biology P ro g ra m , D e p a rtm e n t of E c o s y s te m an d C o n se rv a tio n S c ie n c e s , C ollege of F o restry an d C o n se rv a tio n , U niversity of M o n tan a ,
M isso u la, MT, USA
2 F aculty of E n v iro n m en tal D esig n , U niversity of C algary, Calgary, AB, C anada
K eyw ords
A b s tr a c t
a lte rn a te prey; c o e x is te n c e ; h y p e rp re d a tio n ;
indirect e ffe c ts; s h a r e d p re d a tio n .
Correspondence
N icholas J . D e C e s a re , W ildlife Biology
P ro g ra m , C o lleg e of F o restry an d
C o n se rv a tio n , U niversity of M o n tan a ,
M isso u la, MT 5 9 8 1 2 , USA. Tel; + 1 4 0 6 243
5236
Email; n ic k .d e c e s a re @ u m o n ta n a .e d u
R ec e iv e d 8 M ay 2 0 0 9 ; a c c e p te d 17 J u n e
2009
d o i;1 0 .1 1 1 1 /j.1 4 6 9 -1 7 9 5 .2 0 0 9 .0 0 3 2 8 .x
C o n serv atio n b iologists have re p o rte d grow ing evidence o f food-w eb in te ra c ­
tio n s as causes o f species en d an g erm en t. A p p a re n t c o m p etitio n is a n in d irect
in te ra c tio n am o n g p rey species m ed iate d by a sh ared p re d a to r, a n d h as been
increasingly linked to declines o f prey species acro ss tax a. W e review th eo retical
a n d em pirical studies o f a p p a re n t co m p etitio n , w ith specific a tte n tio n to the
m echanism s o f asy m m etry a m o n g a p p a re n tly co m p etin g prey species. A sym ­
m etry is th eo retically d riv en by niche overlap, species fitness traits, sp atial
hetero g en eity a n d g eneralist p re d a to r b eh av io r. In real-w o rld system s, h u m an ind u ced changes to ecosystem s such as h a b ita t a lte ra tio n a n d in tro d u c e d species
m ay be u ltim ate sources o f species en d an g erm en t. H ow ever, a p p a re n t co m p eti­
tio n is show n to be a p ro x im ate m echanism w hen re s u lta n t changes in tro d u ce or
subsidize a b u n d a n t p rim a ry p rey fo r p re d a to r p o p u latio n s. D e m o n stra tio n o f
a p p a re n t co m p etitio n is difficult due to th e in d irect re latio n sh ip s betw een prey
a n d p re d a to r species a n d the p o te n tia l fo r co n c u rre n t ex p loitative c o m p e titio n or
o th e r co m m u n ity effects. H ow ever, general co nclusions are d ra w n co ncerning
th e ch aracteristics o f prey a n d p re d a to r species likely to exhibit asym m etric
a p p a re n t co m p etitio n , a n d th e o p tio n s fo r recovering en d an g ered species. W hile
sh o rt-te rm m a n a g e m e n t m ay be req u ired to a v o id im m in en t ex tin ctio n in system s
d e m o n stratin g a p p a re n t co m p etitio n , w e p ro p o se ad ap tiv e c o n serv atio n efforts
d irected a t lo n g -term recovery.
In tro d u c tio n
H a b ita t d eg rad atio n a n d in tro d u ced species are ultim ate
th reats to m any species (W ilcove et al., 1998; V enter et al.,
2006), th o u g h the proxim ate m echanism s o f p o p u la tio n
decline can be indirect an d com plex. C onservation biologists
have rep o rted grow ing evidence o f food-w eb interactions as
causes o f species en d an g erm en t (Sinclair & B yrom , 2006).
E xtinction is m ore typical o f in ter-tro p h ic interactio n s such
as p red atio n th a n in tra-tro p h ic com petition (D avis, 2003),
an d p re d a to r p o p u latio n s can m ediate ecosystem change
th ro u g h altering ab u n d an ce o r b eh av io r o f prey (Schm itz
et al., 2008), as well as those o f o th er p re d a to rs (Russell
et al., 2009). A dditionally, interactions am ong in tra-tro p h ic
species can lead to extinction w hen indirectly m ed iated by
shared predation. In such cases, the extinction o f one prey
species m ay be driven by a p re d a to r p o p u latio n th a t is
enhanced by a n ab u n d a n t, a ltern ate prey species. The end
result resem bles th a t o f d irect co m petition, w here a decline
in one species coincides w ith a n increase in the other. H o lt
(1977) ap p ro p riately coined the term ‘a p p a re n t co m p etitio n ’
to describe this indirect ecological in teractio n betw een (at
least) tw o prey species a n d a shared p red ato r. Sim ilar to
exploitative co m petition, a p p a re n t co m p etitio n can be d e­
fined as a reciprocal negative in teractio n (—, —), th eo reti­
cally p ro m o tin g coexistence am o n g prey (C hase et al., 2002;
T ilm an, 2007). H ow ever, asym m etrical (—, 0) interactions
m ay be m o re com m on in n atu re (C h an eto n & B onsall,
2000), a n d could cause declines in one prey species (Fig. 1).
It is precisely this asym m etry th a t p u ts som e species a t risk
while others flourish u n d er p red atio n by a shared p red ator.
P red ato rs play im p o rta n t roles in the m ain ten an ce of
ecosystem s (R ay, 2005), a n d the resto ra tio n o f apex p re­
d ato rs is a n im p o rta n t conservation goal in m an y systems
(Berger & Sm ith, 2005). H ow ever, p re d a to r effects m ay be
intensified in h u m an -altered landscapes, w here in tro d u ced
species a n d h a b ita t alte ra tio n alter prey assem blages (K areiva et al., 2007; S hapira, S ultan & S hanas, 2008). The
d o cu m ented role o f a p p a re n t com petition in th e en d an ger­
m en t o f prey species th u s w arra n ts concern fo r all m ultipleprey systems. R esearchers have elucidated m an y details of
a p p a re n t co m petition, th o u g h a synergism o f theoretical
a n d em pirical findings is needed to unite the ‘sea o f special
cases’ w hich H o lt, G ro v er & T ilm an (1994) h a d h o p ed to
avoid. Studies o f h y p erp red atio n (M oleon, A lm araz &
S an chez-Z apata, 2008), Allee effects (A ngulo et al., 2007),
A n im a l C o n s e rv a tio n 1 3 (2 0 10 ) 3 5 3 - 3 6 2 © 2 0 0 9 T h e A u th o r s . J o u rn a l c o m p ila tio n © 2 0 0 9 T h e Z o o lo g ic a l S o c ie ty o f L o n d o n
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N. J. DeCesare etal.
Apparent com petition and endangered species
predator
1° prey
2° prey
Figure 1 Food w e b s c h e m a tic d e p ic tin g d ire c t (solid) a n d indirect
(d ash ed ) in te ra c tio n s c h a ra c te ris tic of a p p a r e n t c o m p e titio n d y n a m ic s
b e tw e e n prim ary (1 °) a n d s e c o n d a ry (2°) p re y u n d e r a s h a r e d p re d a to r;
a d a p te d fro m Flolt e t a l. (1994).
facilitation (Pope et al., 2008), indirect am ensalism (G a rro tt
et al., 2009), incidental p re d atio n (Schm idt, 2004), subsi­
dized p red atio n (G o m p p er & V an ak , 2008) a n d targ et
p red atio n (H arm o n & A ndow , 2004) all em phasize the role
o f indirect com m unity in teractio n s consistent w ith a p p a re n t
com petition. A synthesis o f results m ay b etter allow conclu­
sions to be generalized a n d conservation actio n to be
im plem ented across systems. In this review o n the role of
a p p aren t com petition in endangered species conservation,
we have three p rim ary objectives: (1) to review th e m e­
chanics o f a p p a re n t com petition dynam ics am ong p re d ato r
a n d prey, including revisiting H o lt’s (1977) original th eo re­
tical m odel; (2) to review recent studies show ing a p p a re n t
com petition a n d the sources o f hum an -in d u ced asym m etry
th a t lead to en dangerm ent; (3) to consider strategies for
detecting an d m an ag in g a p p a re n t co m p etitio n in th e d y ­
nam ics o f endangered species.
T h e o re tic a l p a r a m e t e r s of a p p a r e n t
c o m p e titio n
P re d a to r-p re y dynam ics are often quantified according to
the num eric response (num ber o f p red ato rs) an d the fu n c­
tional response (num ber o f kills p er p re d a to r per u n it time)
o f pred ato rs to prey density (Solom on, 1949; H olling, 1959).
A third, m ovem ent-based num eric response, o r aggregative
response, m ight also occur a t sh o rter tim e scales if p re d ato r
space use is driven by prey d istrib u tio n (H o lt & K o tler,
1987). T he p ro d u c t o f p re d a to r functional a n d num erical
responses is the p red atio n rate, expressed as the percentage
o f the prey p o p u la tio n lost to m ortality . A t low prey density,
a depensatory (negatively density d ependent) p red a tio n rate
w ould lead to prey extinction w hereas a reg u lato ry (posi­
tively density dependent) p red atio n rate w o u ld pro m o te
persistence (G a rro tt et al., 2009). D ep en sato ry p re d a tio n is
particularly possible in m ultiple-prey systems, w here p re ­
d ato rs can persist even if one prey species is driven to
extinction. T his p roduces a num eric response to secondary
prey w ith a positive y -intercept, a key sym ptom o f a p p a re n t
com petition (M essier, 1995). In such m ultiple-prey systems,
the shape o f the p re d a to r fu n ctio n al response becom es
354
p articu larly im p o rta n t in generating d ep en sato ry o r regula­
to ry p re d a tio n (H ebblew hite et al., 2007). Spatial h etero ­
geneity a n d p re d a to r b ehavior offer th eoretical m echanism s
fo r reg u lato ry p red atio n , discussed in detail below. A d d i­
tionally, M cL ellan e t al. (2009) used sim ulations o f a m u lti­
prey fu nctional response to show a th eoretical relax ation o f
p red a tio n o n secondary prey a t low density, driven by the
increased h andling tim e dev o ted to p rim ary prey. In general,
u n d erstan d in g the param eters driving num erical a n d func­
tio n al responses a n d ultim ately p red a tio n rate is central to
co n serv atio n o f endangered prey (Sinclair et al., 1998;
S inclair & B yrom , 2006).
Below we review the characteristics o f m ultiple-prey
systems th a t shape p re d a to r-p re y dynam ics, w ith specific
a tte n tio n to the drivers o f asym m etric effects on prey. W e
consider a single-predator, tw o-prey system (p red ato r, p ri­
m ary prey a n d secondary prey) fo r simplicity, b u t we
acknow ledge th a t each role can be occupied by m ultiple
species (O w en-Sm ith & M ills, 2008). T he first m odel o f
a p p a re n t com petition dynam ics (H olt, 1977) in co rp o rated
p aram eters fo r asym m etry a m o n g prey according to the
vital rates o f prey species, p re d a to r preference a n d caloric
benefit p er prey species. Below we discuss these and
a d d itio n al causes o f asym m etry am o n g prey species, sum ­
m arizing b o th th eoretical a n d em pirical findings in to a small
set o f im p o rta n t p aram eters fo r a p p a re n t com petition in all
systems.
N iche o v e rla p
E xploitative (shared resource) a n d a p p a re n t (shared p re d a ­
to r) com petition can occur concurrently am o n g sym patric
prey species (H o lt e t al., 1994; C hase et al., 2002). C hesson &
K u a n g (2008) recently sum m arized these interactions in
term s o f niche overlap, p, subdivided into overlap o f
resource co n su m p tio n niches p ^ , a n d source o f p red atio n
niches, p ^ . W e liken p ^ to overlap in resource preference
often m odeled in h a b ita t suitability studies (H irzel & LeLay,
2008), a n d p^ to a co m p ariso n o f H o lt’s (1977) per-capita
a tta c k rates, a, am o n g prey species (N o o n b u rg & Byers,
2005). A p p aren t com petition im plies a shared p red ato r, or
p ^ > 0 , including com pletely p ro p o rtio n ate p red atio n
a m o n g prey species (p^ = 1) a n d d isp ro p o rtio n ate selection
fo r one species ( p ^ < l) . N o o n b u rg & Byers (2005) used a
food-w eb m odel to explain coexistence o f prey species w hen
b o th exploitative a n d a p p a re n t co m p etitio n occurred sim ul­
taneously. T heir m odeling o f a single-resource system, h o w ­
ever, assum ed th a t prey species m u st com pete fo r the same
resource in o rd er to exist, w hereas H o lt’s (1977) m odel
assum ed the opposite. W h a t b o th m odels revealed is th a t
relative a tta c k rates, as one m easure o f niche overlap, can
affect persistence (Fig. 2).
C o m p e titiv e f itn e s s o f p rey s p e c ie s
H o lt’s (1977) m odel o f dynam ics am ong ap p aren tly com pet­
ing prey also param eterized the ability o f a prey species to
w ith sta n d p red atio n , as driven by life-history traits o f b o th
A n im a l C o n s e rv a tio n 1 3 (2 0 10 ) 3 5 3 - 3 6 2 © 2 0 0 9 T h e A u th o r s . J o u rn a l c o m p ila tio n © 2 0 0 9 T h e Z o o lo g ic a l S o c ie ty o f L o n d o n
N. J. DeCesare etal.
Apparent com petition and endangered species
10
Extinction of
Species 2
Coexistence
1
0
1
Figure 2 T h eo retical im p licatio n s fo r ex tin ctio n o f th e relativ e s p e c ie s
fitn e s s ratio an d n ic h e o v e rla p b e tw e e n a p rim ary (1°) an d s e c o n d a ry
(2°) p rey s p e c ie s ; a d a p te d fro m C h e s s o n & Kuang (2008).
the prey an d their fo o d source. In a d d itio n to dem ographic
traits, prey b ehavio r such as grouping m ay also affect
relative susceptibility to a p p a re n t co m petition, as p re d a to r
encounter rates decline p ro p o rtio n ately slow er fo r grouping
prey (M cL ellan et al., 2009). In exploitative co m petition
m odels, the species fitness ra tio (K1/K2 ) h as been used to
com pare average fitness a m o n g consum er species, according
to the m aintenance requirem ents o f prey species p er u n it
resource, an d their m axim um rate o f resource harvest
(M acA rth u r, 1970; C hesson, 2000; C hesson & K uang,
2008). T his ratio com pares the theo retical com petitive
ability o f prey species such as co m paring p o ten tial p o p u la ­
tio n grow th allow ed by in h eren t life history. In systems w ith
shared pred atio n , the species fitness ra tio is expanded to
include b o th resource driven gro w th rates a n d sensitivity to
p red atio n am ong ap p aren tly com peting prey (C hesson &
K uang, 2008). C oexistence can th en be theoretically rep re­
sented as a fun ctio n o f b o th the species fitness ratio an d
niche overlap am ong prey species, w here the degree o f niche
overlap constrains allow able fitness differences (Fig. 2). F o r
exam ple, w hen niche overlap am o n g tw o species is high, the
difference betw een low a n d high species fitness ratio s m ight
represent the difference betw een persistence a n d extinction
fo r a species (Fig. 2).
E ndangered species are often secondary prey to p red ato rs
subsisting on a n ab u n d a n t p rim ary prey w ith higher average
fitness (Sinclair et al., 1998), a n d prey species w o u ld be
expected to contribu te d isparately to the p re d a to r num erical
response. C o n trary to single prey systems (p^ = 0) w ith
regulatory p red atio n , asym m etric a p p a re n t co m petition
am ong m ultiple prey (p^ > 0) produces a positive y-intercept
in the num eric response to secondary prey, d epensatory
p red atio n , a n d th u s a m echanism o f extinction via a p p a re n t
com petition. The lack o f num eric response to secondary
prey is a hypothesized link to declines o f th reate n e d species
in several m ultiple-prey systems (A ngulo et al., 2007; H e b ­
blew hite et al., 2007).
S p a tia l h e te r o g e n e ity
Spatial heterogeneity can be a stabilizing fa c to r in the
dynam ics o f b o th exploitative a n d a p p a re n t co m petition
(H olt, 1984; Snyder, B orer & C hesson, 2005; T ilm an, 2007).
In a previous section, we discussed niche overlap, o r the
sym patry o f species’ resource requirem ents in en vironm en­
tal space. H ere we consider th e spatial arran g em en t of
en v ironm ental niche resources, w hich determ ines the degree
o f actualized spatial overlap o r sep aratio n am ong species in
n a tu ra l ecosystem s (H irzel & L eLay, 2008). Spatial sep ara­
tio n o f ap p aren tly com peting prey species can decouple
sh ared p re d atio n dynam ics by isolating p re d a to r-p re y rela­
tionships distinctly am o n g heterogeneous h ab itats. H o w ­
ever, this is dep en d en t u p o n the scale o f p re d a to r m ovem ent
a m o n g each p rey’s resource patches (H olt, 1984); spatial
sym patry should th u s be m easured according to th e m ove­
m ents o f the p re d a to r (H olt, 1984). T his th eoretical finding
offers tw o m echanism s o f a p p a re n t com petition even in
situations o f com plete h a b ita t p artitio n in g a n d n o direct
overlap o f fo o d resources am o n g prey. F irst, p re d a to rs can
exhibit m ovem ents a t the individual level (w ithin-generation) th a t encom pass h a b ita t o f b o th prey a n d elicit a p p a r­
e n t co m p etitio n (H olt, 1984). Second, a spill-over effect of
p re d a to r em igration from source (occupied by p rim ary
prey) to sink (occupied by secondary prey) h a b ita ts can also
indirectly link prey species in a p p a re n t com petition w ithin a
p re d a to r m e tap o p u la tio n (H a rm o n & A ndow , 2004; R an d
& L o u d a, 2006).
S patial heterogeneity can also create refuges, o r space
u n exploited by p red ato rs. W e categorize these refuges as
either n o t visited by p red ato rs (ecological refuges; e.g.
Schm idt, 2004) or n o t available to p re d a to rs (stru ctural
refuges; e.g. F o rrester & Steele, 2004). Refuges can induce
positive density dependence in the p re d a tio n rate fo r lowdensity secondary prey (F o rrester & Steele, 2004) by p ro ­
tecting a n increasing p ro p o rtio n o f the prey p o p u latio n
fro m p red a tio n as density decreases. G iven asym m etric
a p p a re n t co m p etitio n (num eric response to secondary prey
w ith a positive y-intercept), the shape o f the fu nctional
response to secondary prey distinguishes w hether dep ensa­
to ry pre d atio n to w ard s extinction o r reg u lato ry pre d a tio n at
low density (M essier, 1995; G a rro tt et al., 2009). Sinclair
e t al. (1998) fo u n d th a t endangered prey species could be
conserved only if they fo u n d spatial refuge fro m p red atio n
a t low num bers. T hus spatial refuges provide one o f few
em pirically su p p o rted m echanism s o f preventing dep ensa­
to ry p re d a tio n a n d extinction o f secondary prey (Sinclair
e t al., 1998).
G e n e ra lis t p r e d a tio n b e h a v io r
A p p aren t com petition dynam ics are typically associated
w ith generalist p red ato rs, capable o f foraging o n m ultiple
prey species. A population-level p attern o f generalist p red a­
tio n can be the result o f generalist individual p red ato rs, or
locally specialized p re d a to rs th a t a p p e a r collectively general
(H a rm o n & A ndow , 2004). H a rm o n & A ndow (2004)
suggested th a t shared p red atio n systems require each indi­
vidual p re d a to r to be a generalist, as locally specialized
p re d a to rs w ould spatially decouple the dynam ics o f each
prey species. W e suggest th a t spill-over o r m eta p o p u la tio n
A n im a l C o n s e rv a tio n 13 (2 0 10 ) 3 5 3 - 3 6 2 © 2 0 0 9 T h e A u th o r s . J o u rn a l c o m p ila tio n © 2 0 0 9 T h e Z o o lo g ic a l S o c ie ty o f L o n d o n
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N. J. DeCesare etal.
Apparent com petition and endangered species
effects, as discussed above, m ay offer a n exception. A b u n ­
d a n t p rim ary prey m ay result in an a b u n d a n t p re d ato r
source p o p u latio n , th u s m a in tain in g high p re d a to r density
dispersers in sink h ab itats via dispersal. In this w ay, p rim ary
prey in source h a b ita t m ay negatively im pact secondary prey
in sink h a b ita t despite local specialization o f p red ato rs on
each.
P re d a to r preferences a n d foraging strategies can also be
dynam ic w ith respect to prey density (H olt, 1977), clim ate
(O w en-Sm ith & M ills, 2008) o r o th er covariates, th o u g h
m any p re d a to r-p re y m odels assum e them to be fixed (G a r­
ro tt et al., 2007). C hanges in prey selection have recently
been em pirically linked to stabilizing (Siddon & W itm an ,
2004) a n d destabilizing (O w en-Sm ith & M ills, 2008) p o p u la ­
tio n effects. W h eth e r called frequency-dependent selection
(M erilaita, 2006), optim al foraging (H olt, 1984), ap o static
selection (M erilaita & R u x to n , 2009) o r prey sw itching
(G a rro tt et al., 2007), plasticity in p re d a to r preference
implies shared p red a tio n an d th u s a p p a re n t com petition.
M ore im portan tly , such plasticity m ay reduce p red atio n
rates fo r secondary prey a t low density. This offers an
ad d itio n al hypothesized m echanism o f the Type III fu n c­
tional response, a n d as such m ig h t p ro m o te coexistence of
ap p aren tly com peting prey species if p red atio n pressure
relaxes w ith declined density. Effects o f prey switching
w o u ld vary according to the behav io ral plasticity o f the
p re d a to r a n d the relative vulnerability o r p rofitability o f
prey species (G a rro tt e t al., 2007).
E m pirical s t u d i e s o f a s y m m e tric
a p p a r e n t c o m p e titio n a n d s p e c ie s
d e c lin e
O u r overview highlights the critical relationships existing
betw een a p p a re n t co m petition, p re d atio n rates an d d y ­
nam ics o f prey species. A sym m etry in a p p a re n t co m petition
h as th eoretical im plications fo r endangered species decline,
th o u g h we have show n p o ten tial m echanism s fo r relaxed
p red a tio n a t low prey density. H ere we use exam ples in the
literatu re to identify the em pirical conditions associated
w ith asym m etry in a p p a re n t com petition. T ypical o f all
exam ples is h u m an -in d u ced change to resource, prey or
p re d a to r com m unities (T able 1). C hanges a t the resource
level include a lteratio n o f h a b itats w hich affect the density
a n d range o f prey species (H arrin g to n et al., 1999; W ittm er
et al., 2007; C ooley et al., 2008). H u m an s also affect
p re d a to r a n d prey com m unities w ith in tro d u ced species
Table 1 H y p o th e siz e d c a s e s of s p e c ie s d e clin e in d u c e d by a sy m m e tric a p p a re n t c o m p e titio n a m o n g prey, including p a ra m e te r s s u c h a s th e ir
role of d eclining s p e c ie s a s prim ary (1 °) o r s e c o n d a ry (2°) p re y to th e p re d a to r, re s o u rc e n ic h e o v e rla p (p*^), relative s p e c ie s fitn e s s ratio
(K i= fitn e ss of a lte rn a te prey, K2 = fitn e s s o f declining prey; all v a lu e s a s s u m e d > 1 ) , and th e s u s p e c te d u ltim a te c a u s e of a s y m m e tr y a m o n g
s y m p atric p rey
R ole of
S h a re d
declining
D eclining s p e c ie s
A lte rn a te p rey
p re d a to r
prey
Island fox
Feral pig
G olden e a g le
2°
N one
K i /K2
U ltim ate c a u s e
High
S p e c ie s in troduction
R e fe re n c e s
R o e m e r e t a l . (2001),
A ngulo e t a l. (2007)
C a s c a d e fro g s
T rout
G arter s n a k e
2°
N one
High
S p e c ie s in troduction
P o p e e t a l . (2008)
M ac q u a rie Island
R abbit
Feral c at, w e k a
2°
N one
High
S p e c ie s in troduction
Taylor (1979)
Conilurine ro d e n ts
R abbit
Feral c at, fox
2°
High
High
S p e c ie s in troduction
S m ith & Q uin (1996)
Skinks
R abbit
Feral c at, fe rre t
2°
N one
High
S p e c ie s in troduction
N orbury (2001)
G u a n ac o
S h e e p , h are, red
C o u g ar
2°
High
High
S p e c ie s in troduction
Baldi e t a l. (2004), N ovaro
P rzew alsk i h o rs e
L iv esto ck , red d e e r W olf
2°
M o d e ra te High
S p e c ie s in troduction
V an D uyne e t a l . (2009)
W o o d la n d caribou
D eer, elk, m o o s e
C o u g ar
2°
Low
High
H um an d is tu rb a n c e
Kinley & A p p s (2001)
W o o d la n d caribou
M o o se
W olf
2°
Low
High
H um an d is tu rb a n c e
W ittm e r e t a l . (2007)
M ule d e e r
W h ite -ta ile d d e e r
C o u g ar
2°
M o d e ra te Low
H um an d is tu rb a n c e
p a ra k e e t
deer
& W alk er (2005)
R o binson e t a l . (2002),
C ooley e t a l . (2008)
V a n co u v e r island
B lack-tailed d e e r
C ougar, w olf
2°
Low
M o d e ra te H um an d is tu rb a n c e
B ryant & P a g e (2005)
M ule d e e r
C o u g ar
2°
Low
Low
H um an d is tu rb a n c e
G ibson (2006)
H arrington e t a l . (1999)
m a rm o t
Sierra N ev ad a bighorn
sh eep
R oan a n te lo p e
W ild e b e e s t, zebra
Lion
2°
High
High
H um an su b sid y
D e se rt to rto ise
H u m an (garbage)
C o m m o n rav en
2°
N one
High
H um an su b sid y
K ristan & B o atm an
(2003), K ristan e t al.
(2004)
S e a b ird s
H u m an (fish
Gull
2°
N one
High
d isca rd s)
H um an su b sid y
O ro & M artinez-A brain
(2007), Sanz-A guilar
e t a l. (2009)
Elk
356
B ison
W olf
r
M o d e ra te Low
P re d a to r re in tro d u ctio n G a rro tt e t a l . (2009)
A n im a l C o n s e rv a tio n 1 3 (2 0 10 ) 3 5 3 - 3 6 2 © 2 0 0 9 T h e A u th o r s . J o u rn a l c o m p ila tio n © 2 0 0 9 T h e Z o o lo g ic a l S o c ie ty o f L o n d o n
N. J. DeCesare etal.
(C lavero & G arcia-B erth o u , 2005). In co m b in atio n , h a b ita t
alteratio n an d intro d u ced species are m a jo r sources o f
species endangerm en t (W ilcove et al., 1998), a n d we show
th a t the m echanism o f such declines is often asym m etric
a p p a re n t com petition.
C om m on to m o st systems linking a p p a re n t co m petition
an d species endang erm en t is a p re d a to r p o p u la tio n su p ­
p o rted by a n ab u n d a n t p rim ary prey species. A now classic
exam ple is th a t o f a p p a re n t com petition am o n g endangered
island foxes Urocyon littoralis a n d feral pigs Sus scrofa
(R oem er et al., 2001; A ngulo et al., 2007) in the C alifornia
C hannel Islands. In tro d u c e d to the islands by hum ans, feral
pigs have high species fitness, a n d becam e a b u n d a n t o n the
islands w here island foxes, a n endem ic p re d ato r, also
occurred. Pigs a n d foxes d id n o t com pete directly (p ^ = 0),
b u t ab u n d a n t pig p o p u latio n s allow ed the colon izatio n of
a n apex p red ato r, golden eagles Aquila chrsaetos, native to
m ain lan d C alifornia (p^ > 0). Eagle p o p u latio n s subsidized
by pigs were im plicated in im m ediate crashes o f fox p o p u la ­
tions on three islands, including tw o local ex tirpations
(C ourcham p, W oodroffe & R oem er, 2003). R oem er et al.
(2001) referred to this p h en o m en o n as ‘h y p erp red atio n ,’ a
term w ith specific reference to the effects o f in tro d u ced prey
o n native prey via shared p red a tio n (Sm ith & Q uin, 1996).
H ow ever, o u r review reveals th a t the role o f p rim ary prey
can be filled by b o th in tro d u ced a n d native species. F o r
exam ple, sim ilar dynam ics are suspected w ith declines of
th reaten ed w o o d lan d carib o u R angifer tarandus caribou
across C an ad a, b u t w ith o u t in tro d u ced prey. W o lf Canis
lupus p o p u latio n s m ay be subsidized by m oose Alces alces,
w hose increasing density a n d range are associated w ith
forestry conversion o f m a tu re forests to p referred early serai
stages (W ittm er et al., 2007; M cL ellan et al., 2009).
C ougar Pum a concolor p re d a tio n on b o th w o o d lan d
carib o u an d m ule deer Odocoileus heminous m ay be sim ilarly
elevated by ab u n d a n t, native w hite-tailed deer Odocoileus
virginianus po p u latio n s enhanced by forestry a n d agricul­
tu re (K inley & A pps, 2001; R o b in so n , W ielgus & G william ,
2002). D ynam ics betw een m ule deer a n d w hite-tailed deer
are fu rth er com plicated w ith exploitative co m petition
( p ^ > 1) fo r shared resources (R o b in so n et al., 2002; C ooley
et al., 2008). In the P ata g o n ia n steppe, native g u an aco Lam a
guanicoe declines are associated w ith b o th exploitative
com petition w ith in tro d u ced sheep Ovis aries, E u ro p ean
h are Lepus europaeus an d red deer Cervus elaphus (Baldi
et al., 2004) a n d a p p a re n t co m p etitio n m ed iated by elevated
p u m a po p u latio n s (N o v aro & W alker, 2005). Sheep re ­
m ovals increased som e g u an aco p o p u latio n s, b u t oth er
com petitors rem ain as sources o f b o th exploitative an d
a p p a re n t com petition. T h o u g h p re d a to r lim itatio n is a
leading hypothesis fo r some th reaten ed gu an aco p o p u la ­
tions, con cu rren t exploitative com petition can com plicate
conclusions (N o v aro & W alker, 2005).
C om m on ravens Corvus corax are a n exem plary general­
ist p re d a to r (W hite, 2006) w hose gro w th in the M ojave
D esert w as linked to hum an -in d u ced fo o d subsidy from
garbage (K ristan, B o arm an & C rayon, 2004). P re d a tio n by
ravens w as a significant source o f m o rtality fo r juvenile
Apparent com petition and endangered species
desert tortoises Gopherus agassizii, a th reaten ed species.
P re d a tio n risk fo r tortoises increased w ith p roxim ity to
raven aggreg atio n sites, m an y o f w hich were linked to
a n th ro p o g en ic subsidies (K ristan & B oarm an, 2003). T hus,
ravens m ed iated a n indirect negative effect o f h u m an s on
desert tortoises. In term s o f niche overlap,
= 0 but
> 0,
a n d a th eoretical species fitness ra tio w ould be infinitely
skew ed to w ard h u m a n garbage; this co m b in atio n suggests
p ro b ab le to rto ise extinction (Fig. 2). K rista n & B o arm an
(2003) also fo u n d spill-over raven p red a tio n into areas
u n asso ciated w ith garbage, su p p o rtin g o u r th eoretical co n ­
clusion th a t ap p a re n t com petition m ay be driven by general­
ist p re d a tio n by b o th individuals a n d popu latio n s. The
h u m a n subsidy o f a n o th e r generalist p re d a to r, the yellow ­
legged gull Larus michahellis, is associated w ith sim ilar
negative effects o n th reaten ed seabird species in m arine
environm ents (O ro & M artin ez-A b rain , 2007; Sanz-A guilar
e t al., 2009).
A p p aren t com petition has also been recently im plicated
in declines o f the follow ing species: Sierra N ev ad a bighorn
sheep Ovis canadensis californiana (G ibson, 2006); V an cou­
ver Islan d m arm o ts M arm ota vancouverensis (B ryant &
Page, 2005); R o a n antelope H ippotragus equinus (H arrin g ­
to n et al., 1999); m ultiple conilurine ro d e n t species (Sm ith &
Q uin, 1996); C ascades frogs R ana cascadae (Pope et al.,
2008); the now extinct M acq u arie Islan d p a ra k e e t Cyanoram phus novaezelandiae erythrotis (T aylor, 1979). A rich
literatu re o f experim ental studies has also developed d o cu ­
m enting p red a to r- a n d p arasito id -m ed iated a p p a re n t com ­
p etitio n in invertebrate a n d p la n t com m unities (van Veen,
M o rris & G o d fray , 2006). C oexistence am o n g prey species
h as been regulated by shared resources (Jones, G o d fray &
v an V een, 2009), p re d a to rs (Tschanz, Bersier & Bacher,
2007), a n d parasites (M orris, Lewis & G o d fray , 2004) an d
the degree o f spatial sep aratio n am o n g prey species (Bonsall
e t al., 2005; C ronin, 2007), an d p re d a tio n o n a single prey
species h as b o th increased (M orris et al., 2004) an d d e­
creased (T schanz et al., 2007) w ith the a d d itio n o f a second
prey species.
Review o f the m an y species a n d systems studied revealed
p ractical p attern s linking theo retical m echanism s to b o th
the occurrence a n d stren g th o f a p p a re n t com petition in
n a tu ra l systems (Table 1). F irst, sh ared p re d a tio n am ong
prey species inherently im plies some level o f realized a p p a r­
e n t co m p etitio n ju s t as sh ared resources im ply exploitative
co m p etition fo r food. M a n y exam ples o f asym m etric a p p a r­
e n t com petition occur in the absence o f exploitative com pe­
tition. T hus, increased co n sid eratio n o f p re d a tio n as a
crucial c o m p o n en t o f the niche o f species a n d niche overlap
a m o n g species is w arran ted . G iven p re d atio n niche overlap
a m o n g prey, theo ry predicts th a t p rim ary prey species
should experience reg u lato ry p red atio n , b u t secondary prey
should be m o re susceptible to d ep en sato ry p red a tio n (Sin­
clair et al., 1998). In o u r review o f asym m etry in a p p a ren t
co m p etition this pred ictio n is well supp o rted , w ith rare or
endangered species often succum bing to a p re d a to r p o p u la ­
tio n th a t is otherw ise sustained by a n a b u n d a n t p rim ary
prey (T able 1). T his p a tte rn is less the result o f being
A n im a l C o n s e rv a tio n 13 (2 0 10 ) 3 5 3 - 3 6 2 © 2 0 0 9 T h e A u th o r s . J o u rn a l c o m p ila tio n © 2 0 0 9 T h e Z o o lo g ic a l S o c ie ty o f L o n d o n
357
Apparent com petition and endangered species
secondary prey, th a n th a t o f coexisting w ith a p rim ary
prey species th a t has d isp ro p o rtio n ately h igher grow th
rates o r species fitness. T ypically the result o f in tro d u ced
species o r h u m an subsidy to native species, the presence
o f a p rim ary prey w ith higher species fitness appears
consistently linked to declines in endangered prey species
(Table 1). A lso com m on to cases o f asym m etry are general­
ist p red ato rs, such as canids, felids o r corvids, w hich forage
beyond the spatial scale o f h a b ita t p artitio n in g betw een
prim ary an d endangered prey (T able 1). T his likely reduces
the p o ten tial fo r ecological refuges from p red a tio n an d
prom otes o p p o rtu n istic p re d a tio n o n endangered prey
(Schm idt, 2004).
W ith b o th o b servational a n d experim ental studies, re­
searchers have developed these links betw een th eoretical
m echanism s an d th e dynam ics o f a p p a re n t com petition.
H ow ever, there rem ains m u ch need fo r fu rth e r research.
The spatio-tem p o ral relationship betw een prey density an d
p re d a to r preference o r prey sw itching, in shared p red atio n
systems is a key questio n facing conservation practitio n ers
today. F o r exam ple, w hen red u ctio n o f p rim ary prey density
is one m anagem en t strategy, hyp o th etical outcom es m ight
include b o th a sh o rt-term rise (changes in p re d a to r p refer­
ence) a n d a long-term decline (changes in p re d a to r density)
in p red atio n rates o n endangered prey. A dditionally, the
sustaining effect o f spatial refuges has been docum ented
(Sinclair et al., 1998), b u t m o re research is w arra n te d o n the
spatial relationship betw een p re d a to r foraging, prey density
a n d fine-scale h a b ita t p artitio n in g a m o n g prey species (Orrock. W itter & R eichm an, 2008).
C o n s e rv a tio n c h a lle n g e s a n d
s o lu tio n s
C onservation biologists face tw o difficult challenges co n ­
cerning a p p a re n t co m p etitio n a n d the decline o f prey spe­
cies. F irst, researchers m u st reliably d em o n strate w here an d
how a p p a re n t com petition occurs, including the identifica­
tio n o f m echanism s responsible fo r asym m etry am ong prey
species. Second, m anagers m u st quickly prescribe m an ag e­
m ent to reverse declines, considering b o th ultim ate (e.g.
h a b ita t alteratio n a n d in tro d u ced species) a n d proxim ate
(predation) causes.
E fforts to detect a p p a re n t com petition will benefit from
the increased acknow ledgm ent o f its role in com m unity
dynam ics in all systems o f shared pred atio n . In this review,
we identify several m echanism s com m only associated w ith
asym m etry in these dynam ics, a n d th u s w ith probable
species decline (T able 1). Tw o recent studies o f w o lf p re d a ­
tio n in m ulti-prey systems provide exam ples fo r highlighting
these m echanism s. V an D uyne et al. (2009) studied w olf
p red atio n in a system contain in g b o th dom estic a n d native
ungulates, including the endangered Przew alski horse Equus
feru s przewalskii. T hey did n o t discuss a p p a re n t co m petition
as a facto r in Przew alski horse recovery b u t describe a
system w ith several characteristics fo u n d to be indicative of
a p p aren t com petition in o u r review, including: (1) shared
p red atio n u n d e r a w ide-roam ing generalist p red ato r; (2)
358
N. J. DeCesare etal.
subsidized dom estic an d a b u n d a n t native com peting prey
w ith h igher relative species fitness; (3) a p re d a to r diet
suggesting the use o f dom estic prey as p rim ary prey and
a b u n d a n t native ungulates as p referred prey; (4) a n u lti­
m ately hu m an -d riv en subsidy to the p re d a to r’s prey base.
T hus, asym m etric a p p a re n t com petition should be consid­
ered as a m echanism o f decline, w ith au g m en tatio n o f
dom estic a n d o th er native ungulates as a n ultim ate source
o f d ep en sato ry p re d atio n u p o n the endangered Przew alski
horse. In a n o th e r system, G a rro tt et al. (2009) recently
pred icted th a t d ep en sato ry w o lf p red a tio n observed on elk
C. elaphus w as due to a p p a re n t co m p etitio n w ith bison
Bison bison. In this case the declining species, elk, are the
p re d a to r’s p rim ary prey, a n d the ultim ate cause o f depensa­
to ry p red a tio n m ay be a n inflated initial density before
w o lf re in tro d u c tio n (W hite, O lm sted & K ay, 1998). These
relationships are inconsistent w ith those typically associated
w ith en d an g erm en t in o u r review (T able 1). C ontinued
m o n ito rin g is encouraged a n d m ay reveal new p a ttern s as
elk density low ers to a level m ore ch aracteristic o f the
h istoric system.
M an y possibilities are available to researchers a n d m a n ­
agers aim ed to assess asym m etry in a p p a re n t co m petition
systems. W hile experim ental m eth o d s are rarely possible
w hen dealing w ith endangered o r w ide-ranging species,
quasi-experim ental ap p ro ach es using n atu rally occurring
tre atm e n t a n d co n tro l landscapes offer one m eans o f sep ar­
atin g the effects o f resource a n d p red a tio n niche overlap
a m o n g prey (R an d & L o u d a, 2004; A ngulo et al., 2007).
P re d a to r exclosure or rem oval experim ents m ay also offer a
m eans o f detecting the role o f shared p re d a tio n in stru ctu r­
ing prey com m unities (Spiller & Schoener, 1998), th o u g h we
discuss the use o f p re d a to r rem oval as a conservation
strategy below. Sinclair et al. (1998) suggested th a t m a n ­
agers m o n ito r p er-cap ita rates o f change fo r prey species, to
directly assess if m o rtality is depensatory. T his could
stren g th en ju stificatio n fo r conservation actio n b u t should
be com bined w ith research aim ed to u n d e rstan d m echanistic
causes. O rro c k et al. (2008) fo u n d th a t p re d ato rs can dictate
th e spatial scale over w hich com petition occurs, fu rth er
ju stifying the im p o rtan ce o f p red ato r-d riv en spatial scale
fo r research a n d conservation. C o m p etitio n kernels involve
m ap p in g the spatial intensity o f com petition am ong species
(M orris, Lewis & G o d fray , 2005), a n d extending this co n ­
cept to include a p p a re n t com petition m ay aid in identifying
th e a p p ro p ria te scale fo r conservation actions. E ach o f the
m echanism s discussed above should be considered w hen
designing research o r m o n ito rin g p ro g ram s in systems o f
a p p a re n t com petition. P revious observ atio n al app roaches
have included m easu rem en t o f resource a n d p red a tio n niche
overlap (C an t e t al., 2006; C ooley et al., 2008; P ope et al.,
2008), prey fitness o r p re d a tio n rates (R oem er et al., 2001;
R o b in so n et al., 2002; W ittm er et al., 2007), a n d p re d a to r
fu n ctio n al a n d num eric responses (N o rb u ry , 2001), as well
as correlative analyses o f resource, prey a n d p red ato r
density d a ta over space o r tim e (T aylor, 1979; H a rrin g to n
et al., 1999; R oem er et al., 2001; R o b in so n et al., 2002;
P ope et al., 2008). In all studies, we encourage explicit
A n im a l C o n s e rv a tio n 13 (2 0 10 ) 3 5 3 - 3 6 2 © 2 0 0 9 T h e A u th o r s . J o u rn a l c o m p ila tio n © 2 0 0 9 T h e Z o o lo g ic a l S o c ie ty o f L o n d o n
N. J. DeCesare etal.
acknow ledgm ent o f un tested assum ptions in discussion of
a p p a re n t com petitio n an d its co n trib u tio n to species decline.
C onservation solutions to asym m etric a p p a re n t com peti­
tio n will vary according to the m echanism s driving asym ­
m etry am ong prey, including co n sid eratio n o f b o th ultim ate
an d proxim ate causes o f decline. In a p p a re n t co m petition
systems, the search fo r proxim ate cause will likely p o in t to
p re d a to r a n d /o r p rim ary prey density. A s such, co n tro l of
p re d a to r or p rim ary prey density is a p o p u la r strategy for
conservation problem s involving p red atio n o r co m petition
stressors (L essard et al., 2005; S anz-A guilar et al., 2009).
These ‘sym ptom atic’ ap p ro ach es to m an ag e m en t directed a t
p red atio n risk a n d com petition can be a q uick fix fo r species
recovery, th o u g h ‘system ic’ m an ag em en t o f the ultim ate
cause fo r decline (hu m an d isturbance) m ay be necessary for
long-term recovery (L essard et al., 2005; Sinclair & B yrom ,
2006). F o r exam ple, while p re d a to r rem oval m ay be an
effective short-term m eans o f releasing pressure from en ­
dangered prey (L essard e t al., 2005; Sanz-A guilar et al.,
2009), con cu rren t p rim ary prey co n tro l o r h a b ita t m an ag e­
m en t is required to address asym m etry am ong com peting
prey species (C ourch am p et al., 2003; L essard et al., 2005;
G ibson, 2006; O ro & M artin ez -A b rain , 2007). C onversely,
eradication o f com peting prey w ith o u t p re d a to r con tro l
m ay, in fact, enhance p re d a tio n u p o n endangered prey by
generalist pred ato rs (C o u rch am p et al., 2003), a m a n ag e­
m en t p a rad o x in need o f fu rth e r research. B oth cost an d
effectiveness vary w ith co n tro l strategy (B axter et al., 2008),
an d com plete erad icatio n o f p re d a to r o r p rim ary prey
po p u latio n s m ay be unreachable w ith o u t isolation from
sources o f im m igration (M o rriso n et al., 2007). T hus m e th ­
ods to address p re d a tio n levels m ay provide sh o rt-term
relief, b u t ultim ately the source o f asym m etry am o n g co m ­
peting prey should be resolved. H u m a n alte ra tio n o f global
ecosystem s has shifted the em phases o f conservation from
‘equilbria’ a n d ‘clim ax com m unities’ to adap tiv e m a n ag e­
m en t in the face o f regim e shifts (C h ap m an , 2006; deY oung
et al., 2008; C o n tam in & Ellison, 2009). In this light, we
encourage adaptive m an ag e m en t practices th a t ack n o w l­
edge short-term uncertain ty w ith o u t being p aralyzed by it,
while setting in place lo ng-term p latfo rm s fo r m o n ito rin g
an d scientific inference to best address the ultim ate sources
o f change.
C o n c lu s io n s
O u r review clearly identified the role o f a p p a re n t com peti­
tio n in species declines across taxa. W hile scenarios m ay
have distinct causes a n d unique qualities, we encourage the
recognition o f a p p a re n t com petition dynam ics as a m ech a n ­
ism o f decline in m ultiple-prey systems. W e have show n th a t
asym m etry am ong prey species can exist in a p p a re n t co m ­
petitio n u n d er shared p red atio n ju s t as previously show n for
exploitative com petition fo r sh ared resources. C ontin u ed
research linking hypothesized m echanism s o f asym m etry to
em pirical results will strengthen the th eoretical fo u n d a tio n
from w hich to base recovery pro g ram s fo r m an y endangered
species. U ltim ate causes m ay include in tro d u ced species.
Apparent com petition and endangered species
ecosystem d istu rb an ce o r clim ate change, each resulting in
increased p rim ary prey a n d p re d a to r p o p u latio n s to the
detrim en t o f endangered prey species. W e have identified a
nu m b er o f recognizable sym ptom s o f asym m etry in a p p a r­
en t com petition dynam ics, a n d we encourage future re­
search a n d adap tiv e m an ag em en t directed to w a rd the
refinem ent o f indicato rs fo r prey en d an g erm en t in such
systems. F inally, as the m easures em ployed in real-w orld
con serv atio n biology dep en d u p o n consensus o f a m ajority
o f stakeholders (V an D yke, 2008), the ethics, practicality
a n d long-term sustainability o f m anaging fo r a given species
using co n tro l o f its p re d a to rs o r prey com p etito rs should be
carefully evaluated. W hile sh o rt-term m an ag em en t m ay be
req u ired to avoid im m inent extinction, we p ropose adaptive
con serv atio n efforts directed a t lo ng-term results.
A c k n o w le d g m e n ts
W e th a n k J. Berger, S. M ills a n d D . Pletscher fo r th o u g htful
discussion. J.-M . G aillard, N . P ettorelli a n d X . L am bin
pro v id ed valuable com m ents a n d suggestions. F u n d in g was
pro v id ed by the U niversity o f M o n ta n a , U niversity of
C algary, C a n ad ian A ssociation o f P etroleum P roducers,
P ark s C an ad a, R oyal D u tc h Shell, W o rld W ildlife F u n d
a n d the A lb erta C o n serv atio n A ssociation.
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