Indirect Effects and Traditional Trophic Cascades: A Test Involving Wolves, Coyotes, and
Pronghorn
Author(s): Kim Murray Berger, Eric M. Gese, Joel Berger
Source: Ecology, Vol. 89, No. 3 (Mar., 2008), pp. 818-828
Published by: Ecological Society of America
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Ecology, 89(3), 2008, pp. 818-828
? 2008 by the Ecological Society of America
INDIRECT EFFECTS AND TRADITIONAL TROPHIC CASCADES:
A TEST INVOLVING WOLVES, COYOTES, AND PRONGHORN
Kim
Murray
Eric
Berger,1,2,4
M.
and
Gese,3
Joel
Berger2
1
Department of Wildland Resources,
Conservation Society, Northern Rockies
2
Wildlife
Utah State University, Logan, Utah 84322-5230 USA
Field Office, 205 Natural Science Building, University ofMontana,
59812 USA
Missoula, Montana
of Agriculture, Wildlife Services, National Wildlife Research Center, Department of Wildland Resources,
Utah State University, Logan, Utah 84322-5230 USA
United States Department
Abstract.
The
at
interactions
mesocarnivore
cascades
model
trophic
food
chain.
However,
from intraguild pr?dation,
resulting
2001
September
distribution
and
2004, we used
in the southern Greater
spatial and
Yellowstone
consumer-resource
as
such
interactions,
important mediators
trophic-level
may also be
to August
abundance
on
is based
in a
link
release
From
cascades.
wolf
traditional
each
of
seasonal
in
heterogeneity
to evaluate
Ecosystem
from the extirpation
of
release
of coyotes
mesopredator
(Canis
latrans),
resulting
on pronghorn
for high rates of coyote pr?dation
(Canis
lupus), accounts
(Antilocapra
fawns observed
in some areas. Results
of this ecological
in wolf
americana)
perturbation
and pronghorn
at wolf-free
neonatal
survival
and wolf-abundant
densities,
coyote densities,
sites support
the existence of a species-level
a trophic
That wolves
trophic cascade.
precipitated
was
evidenced
rates that were
cascade
four-fold
at sites used
by fawn survival
higher
by
whether
wolves
A negative
correlation
between
the hypothesis
that
coyote and wolf densities
supports
interactions
between
the two species
facilitated
in fawn survival.
the difference
interspecific
Whereas
densities
of resident coyotes were similar between wolf-free
and wolf-abundant
sites,
of transient coyotes was
the abundance
lower in areas used by wolves.
Thus,
significantly
wolves.
differential
on
effects of wolves
limit coyote
contributes
wolves
densities.
Our
be an important mechanism
may
by which
the hypothesis
that mesopredator
release of
on pronghorn
fawns, and demonstrate
pr?dation
coyotes
solitary
results
support
to high rates of coyote
of alternative
food web pathways
coyotes
the importance
in structuring
the dynamics
of
terrestrial
systems.
americana; Canis latrans; Canis
Key words:
Antilocapra
release hypothesis; predator-prey; Program MARK.
Introduction
carnivores
Large
of
ecological
still harbor
ecosystems
Most
fragmentation,
disease,
and Rabinowitz
Woodroffe
Berger
Ecosystem
the structure
shape
et al.
(Ray
apex
are declining
species
over
can
communities
predators
human
and
2005),
yet
persecution
as a result of conflicts
the latter often
livestock
(Johnson
2006).
In addition
et al.
2001,
et al.
Ogada
to threatening
2003,
the survival
of
these
the loss of large carnivores
carries broader
species,
as a
for
the
maintenance
of
implications
biodiversity
result of indirect effects at lower trophic levels (Crooks
and
Soul?
1999, Henke
in the absence
(Canis
lupus)
in herbivore
1996,Woodroffe and Ginsberg 1998,
2001),
of grizzly
in
the
and Bryant
bears
(Ursus
southern
1999).
For
arctos)
Greater
instance,
and wolves
Yellowstone
in
both
willow
densities
and
a concomitant
in the
decrease
trees on
of canopy
saplings
et
islands
in Venezuela
al.
2001).
(Terborgh
as predation
have
cascades
been
defined
Trophic
related
that
in inverse
result
of
effects
patterns
number
of
and
seedlings
or biomass
abundance
across
multiple
trophic
in
levels
a food web (Micheli et al. 2001). Although the classic
cascade
on
is based
a
three-tiered
of
system consisting
and
et
al.
herbivores,
plants
(Hairston
1960),
can involve more
than three trophic
levels and
predators,
cascades
apply to anymultilink linear food web interaction(Polis
et
al.
pattern
received 5 February 2007; revised 19 June 2007;
Manuscript
Editor: J.M. Fryxell.
accepted 9 July 2007. Corresponding
4Address
for correspondence:
Wildlife
Conservation
Field Office, 205 Natural
Science
Society, Northern Rockies
of Montana,
Montana
59812
Missoula,
Building, University
USA.
E-mail: [email protected]
ex
numbers
alces)
reduction
and the attendant
diversity of neotropical
the extirpation
songbirds
(Berger et al. 2001).
Similarly,
of vertebrate
led to a 10- to 100-fold
increase
predators
loss,
(Weber
resulting
(Alces
a
in
communities
few
1996).
to habitat
moose
(GYE),
panded,
function
(Schaller
due
globally
and
lupus; carnivore competition; mesopredator
2000).
In
of biomass
systems
with
control,
top-down
that emerges
depends
on
of trophic
levels (Fig.
1). In even-numbered
with four or more
trophic levels, herbivores
and
communities
because
overgraze
plant
vores
Oksanen
818
are
held
et al.
in check
by
1981, Fretwell
apex
carnivores
1987). The
the
the number
food
can
chains
expand
mesocarni
(Fig.
loss of primary
1;
March
SPECIES-LEVEL TROPHIC CASCADE
2008
819
carnivores
Apex
Mesocarnivores
O
i
Herbivores
o
o
i
Vegetation
o
O
O
_I
release
hMesopredator
'
Fig.
1. Hypothesized
Park,
relationships among trophic levels and changing trophic structure in Grand Teton National
of organisms at each
Wyoming, USA. The weights of the arrows indicate the relative strengths of the effects. Relative abundance
release in coyotes is thought to have occurred between the 1930s
trophic level is indicated by the size of the circles. Mesocarnivore
in northwestern Wyoming.
and 1999 as a consequence
of the extirpation of wolves
carnivores
a
from
food
four-tiered
structure
trophic
a
to
three-tiered
chain
shifts
the
in which
system
can increase
(Fig.
et
release
(Soul?
of secondary
carnivores
populations
termed mesopredator
1). This process,
of both
al.
1988), affects the persistence
and
groundnest pr?dation
increased
birds through
by
scrub-nesting
raccoons
skunks
(Procyon
mephtis),
striped
(Mephitis
einereoargenteus;
Rogers
lotor), and grey foxes (Urocyon
1998,Crooks and Soul? 1999).
and Caro
test predictions
of the
experimentally
release hypothesis
using
large carnivores
of appropriate
by an absence
hampered
to
Efforts
mesopredator
have
been
baselines
to measure
which
against
spatial and temporal
difficulties
associated
controls,
and
a
changes,
logistical
and
lack
of
ethical
of
large-scale
manipulations
terrestrial communities
2005).
(Polis et al. 2000, Steneck
a consequence,
the
As
natural
involving
experiments
or
reintroduction
where
systems
opportunities
with
to
of large carnivores
absent
offer important
the effects of apex predators
recolonization
they have
to evaluate
been
(Gittleman and Gompper 2001).
The
of
recolonization
wolves
to Grand
National Park (GTNP), Wyoming, USA,
point.
were
Wolves
the
1930s
extirpated
and were
by
Wyoming
years until their reintroduction
from
Teton
is a case in
northwestern
for nearly
70
to Yellowstone
National
absent
Park (YNP) in 1995 (Smith et al. 2003). During late
1997, dispersingwolves fromYNP recolonized GTNP
(U.S. Fish andWildlife Service, unpublisheddata). In the
were
the
(Canis
latrans)
the GYE.
How
throughout
and coyotes
ever, wolves
play different trophic roles in
in their prey.
the system, as evidenced
by size differences
adult
elk (Cervus
take
Whereas
wolves
moose,
regularly
absence
dominant
of wolves,
canid
and
elaphus),
bison
prey dispro
coyotes
(Bison bison),
and neonatal
small mammals
ungulates
on
portionately
(Paquet 1992,Arjo et al. 2002).
To
on
research
date,
carnivores
has
focused
trophic cascades
involving
large
on cascades
precipitated
by direct
interactions
and
Peterson
(McLaren
predator-prey
et al.
et al. 1998, Berger
et al. 2001, Ripple
1994, Estes
et al. 2001, Fortin
et al. 2005). Here we
2001, Terborgh
investigated
indirect
recolonizing
direct
and
potential
on pronghorn
wolves
as mediated
neonatal
survival,
(Antilocapra
cana)
distribution
a major
exert
of neonate
predator
ference
on
effects
competition
pronghorn
coyotes
(Fig.
through
extreme
the
form
intraguild
personal
of
interference
is
prey
and Gese
competition
in which
consumed
In
communications).
inter
Berger
1995a,
(Peterson
1).Wolves
both
2007), and intraguildpr?dation (Polis and Holt
an
of
ameri
in the
by changes
of a mesocarnivore,
coyotes,
and abundance
top-down
effects
the
1992),
(M. Hebblewhite,
absence
of wolves,
therefore expand
and threaten
may
populations
the persistence
of pronghorn
by limiting
populations
fawn recruitment.
the mesopredator
release
Following
we
tested
three primary
(1)
hypothesis,
predictions:
coyote
survival
of pronghorn
fawns
is positively
associated
with
wolf density, (2) survival of pronghorn fawns is
associated
negatively
inverse
relationship
densities.
with
coyote
characterizes
coyotes
density,
coyote
and
and
(3) an
wolf
Methods
predator
Study
The
study
area
took place
and field
in Grand
(GTNP), Wyoming, USA,
sites
Teton
National
Park
and on the adjacent Bridger
KIM MURRAY BERGER ET AL.
820
89, No.
3
States, the locations
of
Vol.
Ecology,
Montana
Fig. 2. Map
showing the location of the Greater Yellowstone
study sites, and place names.
Teton National Forest (BTNF), fromSeptember 2001 to
August 2004 (Fig. 2). The Park is bordered to the
southeast by theNational Elk Refuge (NER), a 100-km2
area
secure winter
to provide
in 1912
established
Ecosystem
for livestock
grazing;
consequently,
tion at both
sites has
been
m. Within
to >4000
selected
in wolf
variation
Ranch
denning
pup
and
(Bromus
habitat
Antelope
either
habitat
tata),
brush
grasses
Antelope
only
during
Flats
season.
of
not used
(A.
Elk
when
2).
In
(November
was used by
contrast,
by wolves
the
during
by shrub-steppe
We
Ranch
and
to wolf
pr?dation
was
most
sensors
mortality
bitter
locations
obtained
Stipa,
and Elk Ranch
sites are periodically
likely
to occur
1987). Coyotes were equipped with VHF
eight-hour
Antelope
Poa.
coyotes
(Peterson
foothold
coyotes with padded
1995a). We
captured
or with a net-gun
fired from a helicopter
(Gese
arb?sculo),
understory
at
captured
sites. No
at the Gros
restric
Ventre
site because
captured
on access
winter
of
recovery
during
precluded
carcasses
due
the
when
coyote
mortality
during
period
Isanti, Minnesota,
and
brome
tions
Systems,
associated
vegeta
were
t?den
Bromus,
of coyotes
Flats
Antelope
(Artemesia
and
native
smooth
of coyotes
the movements
monitored
the Elk
replaced
and monitoring
Handling
sagebrush
tridentata),
the genera
Flats
site (GV)
site was
by big
The
(May-September)
(Fig.
sagebrush
(Purshia
Ventre
lands,
temporal
by wolves
the winter
sites are characterized
dominated
low
occurred
winter
(AF)
All
and
abundance.
extensively
rearing
the Gros
of protected
spatial
and
used
throughout
periodically
whereas
April),
wolves
array
to exploit
distribution
was
site (ER)
and
this broad
sites
three
some
with
inermis Leyss).
forelk (Smith et al. 2004). Elevation ranges from 1900m
we
in the western United
(GYE)
used
to monitor
The
ranges
used
compass
(Gese
by ground
survival
et al.
bearings
1990).
with
collars with
Telemetry
(Advanced
USA).
and
and
For
Point
and
aerial
telemetry
sequential
were
develop
coyote
ground
locations,
intersecting
angles
traps
et al.
between
home
>3
20?
160? were
and
were
SPECIES-LEVEL TROPHIC CASCADE 821
2008
March
Novia
Truro,
1990). Locations
(White and Garrott
the program
Locate
II (Pacer,
home
and
ranges by the
Scotia,
Canada),
used
estimated
using
fixed-kernel density method (Worton 1989) with the
"adehabitat" package (Calenge 2006) in program R (R
Core
Team
Development
we
an
ad
hoc
used
ranges,
To
2006).
estimate
home
parameter
(/zad hoc)
smoothing
or under-smoothing.
overto prevent
This
involves choosing
the smallest
increment of the
designed
method
in a contiguous
(/zref) that results
no lacuna
that
contains
home
range polygon
= 0.9 X
/zad hoc
hve{, 0.8 X /zref, etc.; J. G. Kie,
reference
95%
bandwidth
kernel
(i.e.,
Estimation
We
Resident
defined
ated
resident
(pre-whelping)
and
individuals
collared)
on scat deposition
based
located
?7.5
along
were
Transects
walked
indices
of coyote
abundance
transects were
Scat
surveys.
km of unimproved
of
initially cleared
all
for three weeks
each
once/week
For
2001).
(Gese
sizes based
pack
tions of animals
known
on
road
scats
and
site.
and
observa
ground-based
affiliative behaviors
such as
displaying
or territorial
and
traveling,
hunting,
resting
together,
maintenance
1978). For 2003 and 2004, we
(Camenzind
at the Elk Ranch
calculated
densities
resident
coyote
and Antelope Flats sitesby dividing thenumber of adult
in each pack by the size of the pack's
(>1 year) coyotes
contour.
Esti
home
the 95% probability
range using
at a site were
mates
to
for all packs
then averaged
a
site-specific
transient
coyote
determine
estimated
and Antelope
Flats
collared
transients
2003.
We
conducted
year
and
to
extensive
the
had
total
as
variance.
and
at
densities
on
sites based
2003
used
mean
the ratio
radio-collared
the
Flats
Antelope
sites
by
density
Coyote
For
2003
site were
density
scat
r2 =
the origin,
through
and
=
2004,
estimated
was
Summer
number
of adults
available
deposition
0.912,
P =
directly
at the Elk Ranch
the
following
at both
sites in
surveys
densities
in the
would
increase
wolves
calculate
latter estimates
for the
(November
seasonal
their presence
because
at kills
thus, might
at carcasses.
To
of coyotes
we
divided
the
number
densities,
competition
less tolerant
wolf
of wolves
season
pack's
wolves
Seasonal
in the pack
each
seasonal
home
range.
were estimated
using
and,
the
by
size
of
the
home
ranges for
as for
procedures
the same
coyotes.
of neonate
and monitoring
Capture
pronghorn
We
monitored
the survival
fawns
of pronghorn
at the Antelope
June 2002
Flats
site during
captured
and Elk Ranch
sites during
2004, and at the Gros Ventre
June 2003-2004.
All fawns were equipped
with expand
able,
breakaway
sensors
mortality
VHF
with
radio-collars
(mass
?60
four-hour
g; Advanced
Telemetry
a
Isanti, Minnesota,
Systems,
weighed
USA),
using
canvas
a
from
and
based
scale,
sling hung
spring
aged
on observation
of
of birth or the degree of desiccation
were
the umbilicus
and Moodie
(Byers
1990). Fawns
until
the fall migration.
Statistical
We
evaluated
and
correlation
or multivariate
linear regression
simple
regression
for each
of the
bivariate
values
comparison,
variable were subject to measurement
error;
independent
than
thus, we
not meet
did
relationship
was
indirect
density;
between
wolf
confounded
Ventre
1. No
estimate
of coyote
using Eq.
Ventre
for the Gros
site in 2002
the assumptions
of
regression
analysis (Gotelli and Ellison 2004). Furthermore, the
coyote
at the Gros
wolf
because
(regression
(1)
between
coyote density
and fawn
density
and wolf
coyote
using
density
density
rather
used correlation
analysis. We
analysis
hypothesized
fawn survival
index.
analysis
the relationships
fawn survival,
pronghorn
and
survival,
abundance
0.011):
1.644 X scat deposition
coyote
coyote
on
collars
numbers
on
on
based
included
in
we
total
radio
densities
coyote
assessments
of relative
between
relationship
2003 and 2004 and
determined
based
sizes
pack
winter
on the
were
estimates
based
density
in the pack, whereas
winter
estimates
the number of adults and pups. Pups were
BTNF.
weekly
of coyotes
that
captures
helicopter
=
of collars
largest number
26)
(n
of resident
and
transient
coyotes
to estimate
in too few packs
coyotes
for 2002, we estimated
coyote densities
and
of radio
because
of
on known
based
(May-September)
monitored daily for the first 60 days of life,and then
We
Ranch
coyotes
baseline
Densities
deployed.
were
to produce
estimates
combined
we had
density for both sites. Because
and
the Elk
of wolf densities
then
spring and fall
we
determined
individuals,
aerial
at each
there
April) periods (U.S. Fish and Wildlife Service, unpub
make
spring
were
densities
summer
or territory. Densities
of
pack
a
of
assessed
combination
using
sizes of known
(i.e., radio
pack
were
coyotes
followed
were
territories,
with a particular
surveys
was handled
and collaring
of wolves
by the
and Wildlife
Service. Radio-tracking
of wolves
as for coyotes.
the same procedures
Seasonal
Capture
U.S.
Fish
wolf
scat deposition
of 2003.
Estimation
as
or
either
residents
coyotes
defended
well
coyotes
actively
whereas
transients were not associ
all
classified
transients.
densities
of coyote
the spring
to seasonal
lished data).
These
periods
corresponded
shifts in centers of activity between
the wolf pack's
den
in the
site in GTNP
and the state-run elk feed grounds
data).
unpublished
we did not conduct
because
until
analysis
by
(Cohen
a
uses
analysis
that minimizes
and
y) distance
thus, we
al.
wolf
density
and
in
by changes
that the relationship
expected
be
and
fawn
survival
would
density
the coyote
et
between
and mediated
variable
in a multivariate
correlation
2003).
Although
slightly different
line-fitting algorithm
both
the vertical
and horizontal
(i.e., x
of each point from the regression
line,
KIM MURRAY BERGER ET AL.
822
0.7
E
??
m Elk Ranch
D Gros Ventre
Ecology,
Vol.
3
89, No.
Antelope Flats
0.6-1
o
o
0.5
o
o
0.4
o
c
0.3
0.2 H
0.1
c
CD
o
Fig. 3.
are means
0.0
Coyote densities
? 2 SE.
the correlation
2002
2003
(resident and transient combined)
to that produced
is identical
coefficient
We
on
based
for each
or
survived
evaluated
37 models
covariates
(gender
ates
encounter
individual
encounter
fawn
of pronghorn
fawns for the first
a known
fate model
in Program
life using
(White and Burnham 1999). The analysis was
MARK
cohort
wolf
that
density)
at capture,
newborns
indicated
and
birthweight)
summer wolf
survival.
we
single
the
whether
For
mass
at birth based
on the following relationship (modified from Byers
1997) as follows:
=
birthweight
-
at capture
weight
in days).
0.2446(age
global
S was
where
model
was
considered
estimated
survival
examine
sites
site (wf), and year (y) to
in fawn survival
among
for site (s), wolf-free
differences
variables
possible
and
that were
years
covariates.
used
We
not
captured
Akaike's
the group
by
Information
Criterion
adjusted for small sample sizes (AICC) and Akaike
to rank models
and Anderson
2002).
(Burnham
the top-ranked
from
AICC) model
Using
(i.e., minimum
to assess
the initial analyses, we fit one additional
model
weights
whether
an
townsendii)
observed
in white-tailed
jackrabbits
irruption
at the Gros Ventre
site might account
in fawn
increase
survival
at
highest
the Antelope
of resident
?
0.025)
at the
coyotes
were
similar to
=
whereas
0.687),
densities
transient
were
=
significantlylowerat Elk Ranch (1 0.188 ? 0.019 vs. X
?
0.039
With
0.005,
t test, P
Student's
to wolves,
respect
were
densities
<
0.001;
highest
Fig. 4).
at the Elk
Ranch siteduring thewinter of 2003 (0.061 wolves/km2),
and
site during
the summer of
Wolves
made
only rare
(0.015 wolves/km2;
Fig. 5).
to the Antelope
Flats
site; thus, wolf density at this
at the Elk
lowest
visits
site was
effectively
(5g+m+c+sw+ww),
g was
probability,
c was
sw
coyote
birthweight,
gender, m was
density,
was
summer wolf
and ww was
winter
wolf
density,
tested models
that included
also
density. We
dummy
=
t test, P
2003
(2)
The
they
those at theElk Ranch site (1 = 0.232 ? 0.029, Student's
and winter
density,
fawns that were not
calculated
were
densities
coyote
because
Flats site in 2003 (0.479 ? 0.065 coyotes/km2) and
lowest at the Elk Ranch site in 2004 (0.215 ? 0.002
covari
group
all analyses
our field sites.
Values
and wolf densities
Coyote
Total
2002-2004.
from
outside
Fig. 3). Densities
coyotes/km2;
Flats
site (X = 0.251
Antelope
the 60-day
period. We
the effects of individual
during
to assess
and
a
with
histories,
died
density,
on fawn
(coyote
censored
to areas
dispersed
survival
estimated
of
were
coyotes
by linear regression (Gotelli and Ellison 2004).
60 days
2004
at the three field sites in northwestern Wyoming,
Ranch
zero
Pronghorn
We
2003,
for all years.
neonatal
survival
included 108marked individuals (19 in 2002, 44 in
and
45
in 2004)
in the analysis
of fawn
survival,
distributedby siteas follows:ER = 27,GV = 30, and AF
=
51. On
the basis
fawn
survival
weight,
and
of minimum
contained
coyote
AICC,
parameters
density
(Table
the best model
for gender,
1). However,
of
birth
the top
ranked model had just 13.7% of the Akaike weights
there was considerable
(Table
1), indicating
as to which
of the highly ranked candidate
B Elk Ranch
(Lepus
for an
uncertainty
was
models
Antelope Flats
in 2004.
Results
Coyote
We
radio-collared
Flats
at
sites. The
percentage
transients was 51%
Antelope
as residents and
=
17), respectively.
soon after capture
addition
captures
38 coyotes
In
three cases,
for
its status
to the three coyotes
the Elk
Ranch
of coyotes
and
classified
18) and 49% (n
(n=
too
the animal
died
to be
of unknown
determined.
status,
In
seven
Residents
Transients
4. Comparison
of resident and
transient coyote
densities at sites with radio-collared
coyotes in northwestern
2003-2004. Values are means ? 2 SE.
Wyoming,
Fig.
March
823
SPECIES-LEVEL TROPHIC CASCADE
2008
0.08
^
Elk Ranch, winter
DGros
IElk Ranch, summer
Ventre, winter
co
CD
_>
O
0.04 4
?
c
CD
?
Fig.
wolves
0.00
2002
2004
2003
5. Seasonal wolf densities at two sites in northwestern Wyoming,
did not use the site.
of fawn
the best predictor
actually
and Anderson
2002). Coyote
of the top-ranked
models,
of 62.4%
weight
(Table
of this single variable
density
a
with
survival
the overall
1). Thus,
(Burnham
in all nine
appeared
cumulative
Akaike
importance
to model
likely contributed
as a model
that included
only
uncertainty,
=
1.311) at
coyote
(AAICC
density was nearly as good
included
both
fawn survival as one that also
predicting
selection
gender and birthweight(Table 1).Models
variables
and
for coyote
wolf
densities
that suggested
models
comparable
the sites independent
differed among
densities (Table 1).
survival
Model-averaged
that included
estimates
outperformed
fawn
survival
that
of coyote
and wolf
and
(Burnham
Anderson 2002) during the first 60 days of life ranged
The Antelope
2002-2004.
a
from
of S =
low
Flats
at
0.049
site is not shown because
the Antelope
2).
(Table
K\
AICC
AAICC
coyote
0.002)
weight (?
?
-0.496
results
=
0.413 ?
0.266, Wald
of
negatively
P = 0.009;
0.263, Wald
fawns was
of male
Survival
from the
the parameter
estimates
corre
survival was negatively
= ?12.313
?
Wald
3.875,
density
(?.
with birth
and positively
correlated
fawn
correlation
correlated
Fig.
6a)
test,
lower
P =
analysis,
with coyote
and
positively
test, P =
relationship
was negative
0.062).
fawn
Based
density
correlated
Akaike
weight
Model
likelihood
Ss+g+m
Ss+g ~
0.000
0.353
1.311
1.563
1.800
2.011
2.119
2.278
2.428
2.725
2.769
2.826
2.870
3.360
3.587
3.725
3.734
3.894
4.148
4.298
4.906
4.917
0.137
0.115
0.071
0.063
0.056
0.050
0.048
0.044
0.041
0.035
0.034
0.033
0.033
0.026
0.023
0.021
0.021
0.020
0.017
0.016
0.012
0.012
1.000
98.611
0.838101.124
0.519104.198
0.458102.333
0.407
98.209
98.420
0.366
0.347
98.528
0.320100.889
0.297101.039
0.256101.336
0.250103.539
0.243105.714
0.238103.640
0.186104.131
97.750
0.166
0.155
97.888
0.155100.143
0.143102.505
0.126
98.311
0.117100.708
0.086101.315
0.086103.528
Sg+m+ww
Ss+m
4
4
112.300
112.311
5.297
5.308
0.010
0.010
0.071 103.908
103.919
Sg+m+c+ww+sw
Swf+y+g+m
Sg+c+ww+sw
Sc+ww+sw
?wf+g+m+c+ww
Sm+c+ww+sw
Ss
3
111.921
4.918
on
=
(?
the
was
survival
=
-0.882,
(r
with winter
between
and winter wolf
coyote
=
P = 0.036; Fig.
-0.740,
(r
6c).
107.003
107.357
108.314
108.566
108.804
109.014
109.122
109.282
109.431
109.729
109.772
109.829
109.873
110.364
110.590
110.728
110.737
110.897
111.151
111.302
111.910
111.921
Sg+m+c+j
Sg+m+c+sw
5g+m+c+ww
Sg+c+sw
Sg+c+ww
Swf+g+m
5wf+g
Swf
Sc+sw
Sc+ww
0.116).
than for females
wolf density (r = 0.791, P = 0.034; Fig. 6b), and the
4
3
2
3
5
5
5
4
4
4
3
2
3
3
6
6
5
4
6
5
5
4
Sg+m+c
Sg+C
Sc
Sm+C
in
on
Based
model,
top-ranked
lated with
=
test, P
Table
1. Model
selection results for survival (S) of pronghorn fawns during the first 60 days of
life at three study sites in northwestern Wyoming, USA, 2002-2004.
Model
site
Flats
=
2003, to a high of S 0.440 at theElk Ranch site in 2004
0.012
Deviance
0.086
105.688
0.070
Notes: Although we tested 37 models, we present results only formodels with Akaike weights >
are: g, gender; m, birthweight; c, coyote density; j, an irruption in the
0.01. Abbreviations
population of white-tailed jackrabbits; sw, summer wolf density; ww, winter wolf density; wf, wolf
free site; s, site; and y, year.
t Number of estimable parameters,
including the intercept.
densities
Summer
KIM
824
MURRAY
Table
2. Model-averaged
estimates
{S, with SE and confi
dence limits) of pronghorn fawn survival during the first 60
days of life at three study sites in northwestern Wyoming,
2002-2004.
S
Site
with
0.447,
coyote
wolves
The
were
resulted
Despite
the
0.055
0.037
0.043
0.070
0.011
0.040
0.291
0.193
0.218
densities,
winter
with
fawn
correlated
et al. 2001,
to
model
on
is based
each
in a food
link
that
alternative
large
through
been
have
systems
ignored.
largely
also exert
carnivores
such as wolves
on
top-down
influence
carnivores
which
pathways
However,
large
top-down
forcing
and intra
interference
competition
through
interactions
also
be
and
these
may
pr?dation,
systems
guild
of cascades.
important mediators
a
That
wolves
precipitated
species-level
cascade
(sensu Polis
1999) is evidenced
by more
four-fold
in neonatal
difference
(Table
between
during
2). The
coyote
that
facilitated
survival.
were
corresponding
and wolf densities
interactions
interspecific
increase
the observed
Whereas
similar
mean
between
and
by
summer
negative
correlation
supports
between
the hypoth
these species
densities
wolf-free
trophic
than a
at sites used
survival
or both winter
either winter,
wolves
esis
et
et al. 2005, Hebblewhite
Fortin
extent
the
in pronghorn
fawn
of resident
coyotes
and wolf-abundant
sites
= 0.232 ? 0.29
=
(X 0.251 ? 0.025 coyotes/km2and X
respectively;
coyotes/km2,
the mean
abundance
of
cantly
in areas
lower
vs. X
coyotes/km2
t test, P <
Student's
of wolves
mechanism
transient
was
coyotes
=
used by wolves
(X
=
?
0.005
0.039
of
transient
coyote
with wolves
accounting
(Berger and Gese
mortality
between
correlations
strong
wolf densities,
and
for winter
fawn
coyote
the
survival,
wolf
the hypotheses
is largely indirect
among
and mediated
the sites, as
in coyote
by differences
of the winter wolf
inclusion
no additional
variable
in the model
density
explained
variation
in fawn survival beyond
that already
captured
by the coyote density variable.
not
have
in coyote
in GTNP
densities
as
For
those
documented
elsewhere.
large
were
reduced
densities
instance,
coyote
by
reportedly
and coyotes
50% in YNP
following wolf reintroduction,
Thus,
0.188
?
as
were
et al.
Smith
GTNP
in mortality
and
contrast,
eight
years
of
the small
at sites with
of refugia
are
of coyotes
extirpation
1995/?). In contrast, GTNP
wolves.
and without
to
the
For
lesser
instance,
and
(2314 km2)
to have
thought
rapid
in
abundance
coyote
based on differential
in coyote
size of the area
corresponding
to the
contributed
from
is not
Isle Royale
(Peterson
and a
closed
spatially
a small portion
of the
only
single wolf pack
occupied
it is likely the
Park during the course of this study. Thus,
additional
in GTNP
will experience
coyote population
as
reductions
and wolves
a relative
continues
to increase
the Park
from which
the wolf
population
into areas of
expand
they are currently
between wolves
and
absent.
coyotes
abundance
Furthermore,
may
competition
been mediated
by
have
densities
of prey. Elk
are
in GTNP
in theneighborhood of 6 elk/km2,rising to?76 elk/km2
when
elk
are
during
winter
elk are
the primary
prey of wolves
(Smith
increase wolf
abundance
may
on
concentrated
feed
grounds (based on data from Smith et al. 2004). As
signifi
0.019
coyotes
cause
within
contributed
likely
densities we detected.
factors
reduction
lack
In
2003).
densities
population
Several
at carcasses
where
agonistic
et al.
2003),
tolerance
encounters
of
are most
likely to occur (Switalski 2003).
coyotes/km2;
differential
effects
rates
Isle Royale
has declined by ?33%
0.687),
2007). This hypothesis is further
from
extirpated
the arrival of wolves in the late 1940s (Krefting 1969,
their relative
be an
may
coyotes
solitary
important
limit coyote
wolves
by which
populations
by differences
67%
by wolves,
from pr?dation,
the highest
ranked
Burnham
Table
1;
in neonatal
survival
Effects
of changes
and pronghorn
density
population
on
(Berger and Gese
supported
t test, P =
Student's
0.001).
killed
respectively
no
resident
whereas
in any of
density did not appear
< 2;
with AICC
models
(i.e., models
This
and Anderson
supports
2002).
on fawn survival
that the effect of wolves
variable
been
(Paine
Terborgh
al.
2005),
areas,
2007).
and
46%
averaged
Reductions
interaction?
trophic-level
research on top-down
1980). Consequently,
of large carnivores
effects resulting from reintroductions
has focused on cascades
by direct predator
precipitated
et al. 2001,
prey interactions
(Berger et al. 2001, Ripple
chain
coyotes
And,
2007).
of predation-related
for 83%
and Gese
site (Berger
2007).
densities
but neither
26%
transient
Annual
and wolf-abundant
Gese
coyote
cascades
trophic
at
interactions
traditional
consumer-resource
and
2004.
of transient
in wolf-free
deaths
significant.
a
those
0.417
0.581
0.454
0.657
correlated
positively
and negatively
0.314),
?
P = 0.185),
-0.521,
(r
precipitate
66%
(Berger
Discussion
Did
In contrast,
0.141
0.228
0.127
0.244
also
P =
density
was
statistically
relationship
coyotes were
at the wolf-abundant
of resident
0.071
0.094
0.085
0.112
0.149
0.049
0.097
2002
2003
2004
was
density
survival (r =
upper
and no wolves
Site with coyotes
Antelope Flats
Antelope Flats
Antelope Flats
wolf
lower
CL
CL
SE
Sites with coyotes and wolves
0.255
Gros Ventre 2003
0.390
Gros Ventre 2004
Elk Ranch 2003
0.259
0.440
Elk Ranch 2004
95%
and
3
in
coyotes
rates
mortality
at the wolf-free
site, and
and
resident
89, No.
Vol.
Ecology,
of
specific mortality
GTNP
between
2001
27%
95%
ET AL.
BERGER
modeling
Demographic
differences
in fawn survival
abundant
areas
were
indicates
between
sufficient
that
the
wolf-free
to alter
observed
and wolf
the trajectory
of
March
2008
SPECIES-LEVEL TROPHIC CASCADE 825
the pronghorn
in GTNP
from a declining
to
population
trend
in
Still, for increases
increasing
(Berger 2007).
summer
survival
of pronghorn
to result
fawns
in an
an
actual
increase
several
conditions
in the pronghorn
must
be met.
from
mortality
and not compensa
First,
must
be additive
pr?dation
et
al.
found
tory (Boyce
1999). We
coyote
compensatory
collared
fawns.
predation-related
(Berger
in GTNP,
population
no
evidence
and
2007),
of any
in
mortality
radio
for com
prospects
pensatory
appear
density-dependent
mortality
unlikely
in the Park
given that the current pronghorn
population
is <10%
of its historical size (Berger 2003). Second,
the summer must also survive their first
surviving
to be recruited
winter
as yearlings.
into the population
for
Whereas
prospects
density-dependent
population
fawns
appear
unlikely
on
the winter
regulation
conditions
managed
the Bureau
by
on
summer
the
"crucial
winter
for
range"
overwinter
to
stemming
survival
in
reductions
any
from habitat
loss. Thus,
0.6
O
pronghorn
typically lower than those of adults (Gaillard et al.
1998), this age class is likely to be differentially
susceptible
0.5
some
Game
and
Fish
Department,
Cheyenne,
is currently undergoing
USA)
rapid conver
to development
of natural
As
gas wells.
rates
survival
are
of juvenile
ungulates
(Wyoming
Wyoming,
sion due
0.4
0.6
lands
Management
190 km beyond Park borders, stronglydiffer.Habitat
designated
0.3
Density (no. coyotes/km2^
range,
on
located
range,
of Land
-r
0.2
0.4
O^
0.2 4
carrying
capacity
in summer
increases
of
fawns may
be
offset
increases
in
by
or
in no net change,
mortality,
resulting
even a decrease,
in the pronghorn
Third,
population.
fawns
their
first winter must
the
surviving
complete
overwinter
0.0 ^
0.00
0.01
0.02
0.03
0.04
0.05
0.06
0.07
0.06
0.07
Density (no. wolves/km2)
return migration
the following
to be recruited
spring
into the Park population.
data
indicate
that
Telemetry
80-85%
of fawns return to the Park each
approximately
the remainder
summer
to other
year, with
dispersing
M.
ranges
(K.
Berger,
unpublished
data).
Although
for forage
alter
could
the proportion
of
competition
fawns
showing
to
philopatry
appears
possibility
their
natal
the
given
unlikely
this
range,
low
population
density.
Contributing
The
has
detection
often
species
been
can
Although
complex
be
weak
and
the food web
to a
due
factors
of trophic cascades
elusive
because
diffuse
in terrestrial
interactions
(Polis
systems
between
et al.
2000).
in Greater Yellowstone
large number
of sympatric
is
carnivores
and herbivores (Berger and Smith 2005), the focal chain
we
studied
pronghorn
was
are
relatively
effectively
simple
in
predator-free
structure.
Adult
owing
to their
speed (Byers 1997), and while bobcats (Lynx rufus)and
golden
eagles
tors of fawns
are
chrysaetos)
(Aquila
in some areas
(Beale
important
preda
and Smith
1973,
at our
low densities
Byers
1997), both
species occur at
field sites (K. M.
Wolves
Berger, personal
observations).
do kill pronghorn
fawns
but
their
opportunistically,
large body mass (18-80 kg) relative to coyotes (11-18
0.00
0.01
0.02
0.03
0.04
0.05
Density (no. wolves/km2)
Fig. 6. Correlations
between (a) observed pronghorn fawn
survival and coyote density, (b) observed pronghorn
fawn
survival and wolf density, and (c) coyote and wolf densities at
three sites in northwestern Wyoming,
2002-2004. Note that the
lines are fitted using correlation analysis (Gotelli and Ellison
2004), which uses a slightly different line-fitting algorithm
linear regression.
than
KIM
826
MURRAY
BERGER
kg) makes it energetically inefficientforwolves to hunt
neonates
for pronghorn
systematically
(3-4 kg) with the
same intensity as coyotes
1985, Byers
1997).
(Gittleman
accounted
for 71%
of total
coyotes
Consequently,
and
mortality,
97%
of predation-related
in our system
(Berger
fawns
pronghorn
effects of changes
in coyote
to
been
easier
have
may
compensatory
pr?dation.
Anthropogenic
densities
may
have
Thus,
2007).
fawn survival
on
pr?dation
discern
due
to
that have
been
lack
severe
reduced
by
populations
or over-harvesting
weather
may
by humans
from
recruitment
sustained
poor
resulting
et
(Gasaway
pr?dation
thousand
a
of
in pronghorn
changes
population
to the strength of the
contributed
coyotes and pronghorn.
Specifically,
between
interaction
of
mortality,
al.
1983).
experience
levels
of
Although
summered
have
winter
a
historically
pronghorn
was reduced
in the
1948), the population
(Deloney
late 1800s as a consequence
of market
Since the
hunting.
never
turn of the 20th century,
the population
has
Park
more
numbered
than the low 400s,
and
is currently
?200
variation
that was
in survival
adequately
explained
the
model
that included
for 5.6%
(Table
additional
variation
we
Thus,
1),
(Burnham
there was
concluded
in the jackrabbit
irruption
in fawn survival
increase
the
Finally,
coyotes
in coyote
of
settlement,
of migratory
Populations
by
2007).
(Berger
forces
bottom-up
when
may be regulated
ungulates
are
carnivore
densities
determined by the supply of residentherbivores (Sinclair
alternative
However,
1995).
predator
or
populations
(Polis
predators
on reproductive
prey may
1999).
enable
Because
maintain
high
densities
of
pronghorn
females
rely
to
and
synchrony
predator
swamping
et al. 2001),
low pronghorn
(Gregg
to the number
relative
of coyotes
sustained
by
to
herbivores
such as elk may
allow
coyotes
maximize
fitness
densities
resident
effectively
suming a
the pronghorn
by con
population
of
the
fawns
each
produced
large proportion
a predator-pit;
Holling
1965). The possibility
regulate
year (i.e.,
of a predator-pit
between
fawn
is suggested
by a positive
survival
and
pronghorn
=
=
0.004) inGTNP
density (r2 0.257, P
and 2004 (Berger 2007).
The
stable
strength
of the interaction
an
also
neonates
alternative
prey may
at
fawns
pronghorn
coyotes
with
are
experiencing
provisioning
site in 2004
coyotes
=
40 950
an opportunity
are
kg). Coyotes
and scavengers
predators
biomass
a
during
generalist
are limited
opportunistic,
their densities
and
by the availability of prey during winter (Gese 2004).
the availability
Thus,
elk carcasses
of abundant
on
the
is likelyto subsidize thewinter diets of coyotes and
NER
maintain
at artificially
inGTNP
the population
densities.
elk
because
Furthermore,
variation
temporal
and harsh winters,
in elk mortality
on
carcasses
stable
that may
tion
food
supply
elevated
feeding
associated
suppresses
the NER
provide
with mild
a
the coyote
popula
That
elk
fluctuations.
buffer
from
weather-dependent
resource
is an important
carrion
for coyotes
associated
to explore
that
"aggregations"
seasonal
food
of transient
migration
the ER and AF
sites
and
pups.
provided
carcass
of gross
kg
form
on
is suggested
the NER
this
An irruptionin the jackrabbit population at theGros
Ventre
41 000
each winter (Camenzind 1978). Indeed, the availability
pronghorn
of
(3-4 kg), and the absence
on
increase
coyotes'
dependence
a critical
when
adult
juncture
energetic
of elk
mortality
of
and
demands
Overwinter
population
do not occur
jackrabbits
(Lepus californicus)
in northwestern
Wyoming
(Best 1996), and white-tailed
are functionally,
if not actually,
in
extinct
jackrabbits
Jackrabbits
average
on theNational Elk
typicalwinter (i.e., 7500 elk X 2% mortality X 273 kg/elk
results
in the seasonal
subsidy
from both
and resident
coyotes
data).
(K. M.
unpublished
Berger,
Conclusions
be enhanced
(Berger et al. 2006).
are similarly sized
prior
of 7500 elk
relationship
black-tailed
GTNP
elk
area
the coyote
by a lack of alternative
are an important
prey. Notably,
although
jackrabbits
of coyote diets in some areas
1972),
component
(Clark
may
pronghorn
most
averages 2-3% (Smith 1991), resulting in an
on theNER
estimated
by changes
of
alteration
by
between 1981
between
et al. 2004).
(Smith
between
interaction
enhanced
from human
Refuge
to an
contributed
the
currently
2002).
that an
site in 2004.
whereas
Specifically,
and the surrounding
availability.
out of GTNP
migrated
to human
evidence
be
may
pronghorn
densities
resulting
resource
Anderson
population
at the GV
strength
and
and
weak
densities
with
low densities
of
relatively
coupled
to consume
allow
may
coyotes
pronghorn
nearly all of
fawns produced
in the
the estimated
?150
pronghorn
summer
the Akaike
of
some
for our
support
suggesting
and
Anderson
However,
(Burnham
2002).
hypothesis
a similar deviance
to the top-ranked
this model
had
^
a result of adding
and
the AAICC
2 was
model,
to
little
another
the
that explained
model
parameter
weights
now winter just south of GTNP
each
3
not
model.
The
by the top-ranked
variable
accounted
jackrabbit
animals (Berger 2003). Thus, relatively high coyote
Park
89, No.
Vol.
Ecology,
a dummy
we
this idea. Specifically,
variable
included
of
in the model
the jackrabbit
representing
irruption
fawn survival to test for evidence
estimated
of additional
few
in the
ET AL.
In
contrast
herbivore
of
but rather as a
by a top carnivore,
in
effects mediated
by changes
corre
abundance.
The
strong, negative
lations
between
densities
and
and
coyote
fawn survival,
release
mesopredator
extirpation
in
not
pr?dation
indirect
mesocarnivore
of
management
restoration
holds
of
wolves
contributes
America,
on pronghorn
fawns
both
the changes
studies,
previous
that we
observed
resulted
populations
from direct
result
with
wolf
coyotes,
and coyote
that
the hypothesis
the
from
resulting
densities,
support
throughout
to high rates
observed
and
promise
much
of North
of coyote pr?dation
from
in some areas. Thus,
conservation
for reducing
perspectives
coyote
wolf
pr?dation
March
rates
deer
SPECIES-LEVEL TROPHIC CASCADE 827
2008
on
neonatal
as
such
ungulates
(Odocoileus
mule
pronghorn,
white-tailed
and
deer
hemionus),
we expect
In particular,
that
as
in places
such
emerge
where
the pronghorn
National
Park,
in recent years,
has declined
precipitously
(Odocoileus
virginianus).
should
similar
cascades
Yellowstone
population
on pronghorn
pr?dation
reduced
have
reportedly
coyote
wolves
fawns
is high,
the coyote
and
population
by as much as 50% (Caslick 1998, Smith et al. 2003). Our
results
strong
provide
cascade
southern
precipitated
and
GYE,
the
demonstrating
evidence
wolf
by
of a species-level
recolonization
trophic
in the
a growing
body of research
in
forces
of top-down
importance
support
interac
the dynamics
of consumer-resource
structuring
and Peterson
tions in terrestrial systems (McLaren
1994,
et al.
et al. 2001, Ripple
et al. 2001, Terborgh
Berger
2001,
et al. 2005).
Fortin
Acknowledgments
This work was funded by Grand
the Biological
Division
Resources
Teton
of
National
Park
and
the U.S.
Geological
the
01CRAG0031,
Survey under Cooperative
Agreement
Wildlife
National
Wildlife Conservation
Society, the USDA
the NatureFlight
Research Center at Utah State University,
We
thank
and the Earth Friends Foundation.
Foundation,
Renee
and the many
Nordell,
Wulff, Noah Weber, Mike
volunteers who assisted with fawn captures and data collection.
J. Estes, D. Rosenberg, M. Conner, P. Budy, and J. Bissonette
provided helpful comments. Research protocols were approved
at Utah
by Institutional Animal Care and Use Committees
State University
Research Center
(Approval
#1111)
and
the National
Wildlife
(QA-1193).
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