Neonatal mortality of elk driven by 
climate, predator phenology and predator 
community composition
Authors: K. Griffin, M. Hebblewhite, H. Robinson, P. 
Zager, S. Barber-Meyer, D. Christianson, S. Creel, N. 
Harris, M. Hurley, & D. Jackson
This is the final version of record of an article which has been published in final form at 
http://dx.doi.org/10.1111/j.1365-2656.2011.01856.x. This article is covered under 
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Made available through Montana State University’s ScholarWorks 
scholarworks.montana.edu 
Griffin K, Hebblewhite M, Robinson H, Zager P, Barber-Meyer S, Christianson D, Creel S, 
Harris N, Hurley M, Jackson D ( 2011) Neonatal mortality of elk driven by climate, predator 
phenology and predator diversity. Journal of Animal Ecology 80: 1246-1257
http://dx.doi.org/10.1111/j.1365-2656.2011.01856.x 

Introduction
One of the biggest challenges facing animal ecologists is
determining whether mortality by predators is additive or
compensatory (Boyce, Sinclair & White 1999). Compensa-
tory mortality is defined when an increase in one mortality
source causes a decline in another, that is, non-independence
between different mortality hazards (Heisey & Patterson
2006). Climate is an important mediating factor because it
can interact with both resource availability and the strength
of predation (Melis et al. 2009). In temperate ungulates,
whether predation is additive or compensatory is expected to
be mediated by winter severity (Post et al. 1999; Hebblewhite
2005). However, the effects of summer climate on forage and
female elk body conditionmaymask climate-predation inter-
actions during winter (Cook et al. 2004). Compensatory
mortality can also arise because of competition amongst pre-
dators (Williams, Nichols & Conroy 2002; Heisey & Patter-
son 2006) and need not be restricted to the classic definition
of compensation that focuses on hunting and overwinter
mortality. For example, analyses of wolf (Canis lupus) and
elk (Cervus elaphus) dynamics suggest that wolf predation
might be compensatory to mortality from other predators
(Vucetich, Smith & Stahler 2005; Garrott, White & Rotella
2009). Testing for compensatory mortality is further compli-
cated by effects of age structure (Coulson, Gaillard & Festa-
Bianchet 2005;Wilmers, Post &Hastings 2007).
In general, ungulate population dynamics are determined
by the interplay of high and constant adult female survival
and high variation in juvenile survival (Gaillard et al. 2000;
Raithel, Kauffman & Pletscher 2007). Therefore, juvenile
survival often determines population trajectories (Gaillard
et al. 2000; Raithel, Kauffman & Pletscher 2007), although
this depends on the manner of environmental variation act-
ing on a population (Coulson, Gaillard & Festa-Bianchet
2005). Because of the vulnerability of juvenile ungulates to
density-dependence, climate-induced mortality should be
more compensatory with predator caused mortality in juve-
niles than in adults (Gaillard et al. 2000). However, many of
the studies included in recent reviews were from populations
without ecologically effective densities of large predators.
Recent studies have shown that variation in population
growth rate, adult and juvenile vital rates, may be lower in
ungulate populations with predation, likely because preda-
tion interacts with climate to reduce population size and fluc-
tuation (Hebblewhite 2005; Wilmers, Post & Hastings 2007).
Thus, the extent to which predation is influenced by climatic
variation on juvenile mortality remains unclear.
The expanding recovery of large carnivores in temperate
systems emphasizes the importance of understanding mecha-
nisms of compensatory mortality. With increasing cougars
(Puma concolor), gray wolves (Boitani 2003) and brown bears
(U. arctos) in Europe and North America (Swenson et al.
1995; Pyare et al. 2004), ungulate ecologists need to under-
stand additive and compensatory mortality under different
predator and climatic conditions. At one extreme, Linnell,
Aanes & Andersen (1995) suggested diverse predator com-
munities might render predation additive in mortality of
juvenile ungulates. Alternatively, high intraspecific competi-
tion and functional redundancy among carnivores in tropical
systems suggests mortality could be compensatory (Caro &
Stoner 2003). Efforts to unravel these relationships are fur-
ther complicated by the diversity of predators and ungulates
(Linnell, Aanes & Andersen 1995) and that most studies of
ungulate mortality are conducted at limited spatial and tem-
poral scales.
Separating compensatory vs. additive mortality is difficult
because mortality is often mediated (i.e. confounded) by cli-
matic variability. Experimental or comparative approaches
that manipulate body condition or food availability, or pred-
ator ⁄harvest levels are therefore needed to critically test the
compensatory mortality hypothesis (Bartmann, White &
Carpenter 1992; Tveraa et al. 2003; White, Zager & Gratson
2010; Sandercock et al. 2011). Unfortunately, the difficulty
of predator removal andmanipulating body conditionmakes
experimental approaches to test predator-caused compensa-
tion difficult with free-ranging ungulates. Instead, observa-
tional approaches have used temporal variation, for
example, in wild boar (Sus scrofa) mortality rates from hunt-
ing and natural causes to test for additive vs. compensatory
mortality using regression (Toigo et al. 2008) or state-space
modelling (Servanty et al. 2010). Ultimately, these
approaches are inferentially weaker than experiments (Sand-
ercock et al. 2011) and suffer some statistical shortcomings
(Schaub & Lebreton 2004), but offer precious insights into
the potential for compensatory mortality in important
applied settings.
We adopted a comparative approach that exploited tem-
poral and spatial variation in neonatal mortality, climate and
predation across 12 elk populations to test two mechanisms
for compensatory mortality. First, we tested whether preda-
tor mortality was compensatory with climatic variation
(compensatory climate–predator mortality hypothesis), and
second, whether predator-caused mortality of neonate elk
was compensatory amongst predator species (compensatory
predator-mortality hypothesis). We analysed survival data of
neonatal elk using parametric survival models and estimated
cause-specific mortality in a competing risks framework
(Heisey & Patterson 2006; Murray & Patterson 2006). Cli-
mate itself could mediate predator mortality in two different
ways. First, maternal condition could exert the greatest effect
on neonate survival through either the amount of female fat
reserves in the fall or the severity of winter climate prior to
calving. Alternately, neonate mortality could be primarily
driven by negative effects of stochastic spring snowfalls or
positive effects of precipitation or temperature during the
spring and summer of calf birth (Clutton-Brock et al. 1987;
Unsworth et al. 1999; Pettorelli et al. 2007). For the preda-
tor-mortality hypothesis, if mortality is additive, then preda-
tion would be expected to overwhelm climate effects (Linnell,
Aanes & Andersen 1995). Thus, predation effects should
increase with increasing number of predator species. Alter-
nately, the compensatory predation-mortality hypothesis
predicts that as the number of predator species increases,
Neonate elk calf survival across the north-western USA 1247
 2011 TheAuthors. Journal ofAnimal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 1246–1257
survival stabilizes; indicating one predator species is replac-
ing another in its effect on neonate survival. We tested
whether mortality by each predator was compensatory or
additive by regressing the cause-specific mortality rate
(accounting for competing risks; Heisey & Patterson 2006) of
neonatal elk for each study area against that same area’s
neonatal survival. A negative linear relationship between
cause-specific mortality and survival would suggest additive
mortality (Williams, Nichols & Conroy 2002).
Materials andmethods
DATA COMPILAT ION
We synthesized 12 data sets on neonatal elk survival collected across
five states in the north-western United States from 1973 to 2007
(Fig. 1, Table 1). We define neonatal survival as the first 93 days of
life, approximately 20 May – 31 August (see survival modelling
below). We refer readers to the original studies for detailed descrip-
tions of their study areas, which covered wide climatic (Table S1),
topographic, vegetative (e.g. coniferous forest, montane, shrub
steppe) and predator community gradients in the north-western Uni-
ted States. Oregon contained two study areas, one in the south-west
Cascade Mountains (D. Jackson, unpublished data) and the other in
the Blue Mountains of north-east Oregon (Rearden 2005; B. John-
son, pers. comm.). One study occurred in the Blue Mountains of
Washington (Myers et al. 1998). Four study areas were located in
Idaho: two along the Lochsa ⁄North ForkClearwater River (Schlegel
1986; White, Zager & Gratson 2010), one along the South Fork
Clearwater River (White, Zager & Gratson 2010) and one along the
Salmon River (Compton 2009). Two study areas were located in
Montana: one in the Garnet Mountains (Raithel 2005; Harris 2007)
and another in the Gallatin Valley (Christianson 2008). InWyoming,
two studies were located in Jackson Hole (Smith & Anderson 1998;
Smith et al. 2006) and one was in Yellowstone National Park
(Barber-Meyer,Mech &White 2008).
The original data were collected using comparable field methods to
capture and radio-mark neonatal elk. All calves were tagged with
either radio ear tags or radiocollars. We estimated age at capture
according to Johnson’s (1951) criteria and then calculated birth date
by subtraction. To standardize predicted birth weight across study
areas, we used step-wisemodel selection to select the best linear regres-
sion of capture weight, capture age, sex and study area (e.g. Smith,
Robbins & Anderson 1997). Radio-marked calves were monitored
from the ground and air (using both fixed-wing aircraft and helicop-
ters). Monitoring intensity was high inMay and June with an average
of 7Æ9 observations per week (range 3–14 per week) and then declined
through July (average 4Æ6 observations per week; range 1–14 per
week) and August (3Æ8 observations per week; range 1–7 per week).
Mortality signals were investigated usually within 1–2 days; however,
some carcasses took longer to reach because of weather and logistics.
We censored animals if the radio transmitter detached prematurely or
if mortality occurred the same day as capture and mortality was
capture related (n = 16). Studies used a combination of field-based
and laboratory-based (DNA identification of predators, disease
profiling) necropsy procedures to investigate cause of mortality. For
consistency, we collapsed 19 total mortality causes to five broad
categories (cougar, wolf, coyote, ursid and other) that reduced mis-
classification and resolution inconsistencies across studies (Table S2).
STATIST ICAL ANALYSES
Survival modelling
We used Weibull parametric survival models to estimate neonatal
survival and test for covariate effects on mortality hazard across all
12 populations (Hosmer, Lemeshow&May 2008).We choseWeibull
parametric models because they were more parsimonious than non-
parametric models because of the strong exponential decay in neona-
tal survival (Murray & Patterson 2006). We used shared frailty
(Vaida & Xu 2000; Cleves, Gould & Gutierrez 2002; Hosmer, Leme-
show &May 2008), akin to including a random effect, to account for
among-group heterogeneity in survival within each of the 12 study
Fig. 1. Location of 12 study areas in the north-western USA, from 1973 to 2007. Black circles indicate study areas with three major predators
(cougar, black bears and coyotes); grey squares indicate areas with three major predators prior to 2001 and four major predators (same preda-
tors as three-predator system plus wolves) after 2001; and black triangles indicate areas with five predators (same predators as the four-predator
system plus grizzly bear). Note that two different studies occurred in Jackson Hole, WY between which additional predator species moved into
the area.
1248 K. A. Griffin et al.
 2011 TheAuthors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 1246–1257
areas. Inferentially, inclusion of shared frailty allows valid popula-
tion-level inferences across the north-western United States, and we
report population-averaged covariate effects here (Cleves, Gould &
Gutierrez 2002). For inferences for individual study sites (subject-
specific effects), we refer readers to original studies.
We tested our hypotheses about predator community composition
(three, four or five predators) and climate using the hazard ratio
(expbx) and its significance estimated from parametric Weibull mod-
els (Hosmer, Lemeshow & May 2008). As the hazard ratio increases
>1, mortality increases and survival decreases. We also estimated
survival as a function of the number of predator species using the
Kaplan–Meier product limit estimator (Hosmer, Lemeshow & May
2008). We used a left-staggered entry and right censored design with
time at risk based on age (Fieberg &DelGiudice 2009) where individ-
ual neonate elk entered into the analysis on age at capture and exited
at death or censor event (end of study or 94 days); therefore survival
is a function of age (days). We graphed the scaled-score residuals and
Martingale residuals to test model fit (Hosmer, Lemeshow & May
2008) and removed four extreme outliers (with no effect on results,
unpublished data).
We used a comprehensive model selection strategy to select the
best Weibull survival model by considering plausible combinations
of covariates based on candidate models from each of the original
studies for each study area, for a total of 116 potential models. We
did not include covariates that were too correlated (| r | >0Æ5) or con-
founded (Hosmer, Lemeshow & May 2008) in the same model. We
selected the top model(s) using Akaike’s Information Criteria
(Burnham& Anderson 1998). Based on their importance in previous
studies (Smith, Robbins & Anderson 1997; Smith et al. 2006; Harris
2007; Raithel, Kauffman & Pletscher 2007; Barber-Meyer, Mech &
White 2008), we considered the following ‘base’ covariates as fixed
and included them in all subsequent models: sex (male, female),
estimated birth weight [sex-specific regression (Smith, Robbins &
Anderson 1997)] and estimated birth date (Johnson 1951).
Climate
We considered two main climatic mechanisms for compensatory cli-
mate mortality; (i) effects of maternal condition on neonate survival
attributed to the previous summer forage availability or previous
winter severity; (ii) effects on neonate survival because of precipita-
tion over the spring of birth year. Of course, separating effects of
spring climate between maternal effects and direct neonatal effects
through forage availability is challenging because of overlapping
effects on neonatal condition, but comparing these two climatic
effects provides a broad test of potential mechanisms. We used cli-
mate data from the Western US Cooperative Observer Program
weather station that was in or closest to each study area (Western
Regional Climate Center 1986). Summer maternal condition was
indexed by the total precipitation (cm), the average daily maximum
temperature (C) of the previous summer (May–August) and their
interaction. Winter maternal condition was indexed by the average
minimum daily temperature (C) and winter total snow (cm) in the
previous winter (December–May) before calving as well as their
interaction. Spring climate effects on neonate elk survival were
indexed by the total precipitation (cm) and the average maximum
daily temperature (C) in the current spring (March, April orMay, as
well as the average of March-April), and their interaction. We also
explored whether mean daily temperatures had more explanatory
power, but they did not (unpublished data). Finally, we tested for the
effect of total snow (cm) in June as a measure of rare, stochastic,
weather events on neonates.
Number of predator species
Quantitative data on absolute predator densities were not available
for most study areas; therefore, we defined three different predator
communities by the number of predator species present (e.g. Linnell,
Aanes & Andersen 1995). Study areas with three predator species
Table 1. Summary of studies conducted on neonate elk in the north-westernUSA, including study area, citations, years, number of collared and
dead calves, number of predator species and three-month survival rates (Kaplan–Meier [KM]) across studies
State Location Researcher ⁄Publications Years
N collared ⁄
mortality
Number of
Predatorsa
KMSurvival
(SE)
OR SWCascades Jackson, unpubl. data. 2002–2005 155 ⁄ 29 3 0Æ75 (0Æ04)
NE – Blue
Mountains
Johnson, unpubl. data.,
Rearden 2005
2002–2007 444 ⁄ 145 3 0Æ61 (0Æ03)
WA BlueMountains Myers et al. 1998 1993–1997 50 ⁄ 10 3 0Æ75 (0Æ07)
ID Lochsa Schlegel 1986 1973–1979 137 ⁄ 57 3 0Æ44 (0Æ05)
Lochsa ⁄
North Fork
White, Zager &
Gratson 2010
1997–2001, 2004 161 ⁄ 86 3 prior to 2001;
4 after 2001
0Æ41 (0Æ04)
South Fork
Clearwater
White, Zager &
Gratson 2010
1997–2004 221 ⁄ 96 3 prior to 2001;
4 after 2001
0Æ49 (0Æ04)
Salmon Compton 2009 2005–2006 112 ⁄ 35 4 0Æ67 (0Æ05)
MT Garnets Raithel 2005; Raithel,
Kauffman& Pletscher 2007;
Harris 2007
2002–2006 220 ⁄ 38 3 0Æ81 (0Æ03)
Gallatin Christianson 2008 2005 29 ⁄ 15 5 0Æ48 (0Æ09)
WY JacksonHole Smith et al. 2006 1990–1992 165 ⁄ 22 3 0Æ84 (0Æ03)
JacksonHole Smith et al. 2006 1997–1999 154 ⁄ 42 5 0Æ70 (0Æ04)
Yellowstone
National Park
Barber-Meyer,Mech&
White 2008
2003–2006 151 ⁄ 96 5 0Æ31 (0Æ04)
Total 1999 ⁄ 671
aPredator composition: 3 = cougar, coyote, and black bear; 4 = cougar, coyote, black bear, andwolf; 5 = cougar, coyote, black bear, wolf,
and grizzly bear.
Neonate elk calf survival across the north-western USA 1249
 2011 TheAuthors. Journal ofAnimal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 1246–1257
included cougar, coyote and black bear (Ursus americanus); four-
predator systems also had gray wolves, and five-predator systems
included grizzly bears (Fig. 1). In the three- and four-predator sys-
tems, ‘‘ursid’’-caused mortality represented only black bears but in
the five-predator system it represented mostly grizzly bear but also
some black bear because of the challenge in discriminating mortality
caused by the two species (Zager & Beecham 2006; Barber-Meyer,
Mech & White 2008). The effect of these predator communities was
modelled using categorical covariates for four and five predators in
comparison with three. The strongest experimental comparison in
our study area for predation was between 1990–1992 (three preda-
tors) and 1997–1999 (five predators) when both wolves and grizzly
bears became established in Jackson Hole, Wyoming (Smith et al.
2006). Therefore, we conducted a restricted analysis on just this study
area following similar methods as described above (but without a
frailty term), as well as an analysis with all sites excluding Jackson
Hole to provide an interpretive check on our global model.
CAUSE-SPECIF IC MORTALITY
To test whether predator mortality was additive or compensatory,
we estimated cause-specific mortality using cumulative incidence
functions (CIF; Heisey & Patterson 2006). CIFs allow the estimation
of cause-specific mortality in the presence of competing mortality
risks (Heisey & Patterson 2006). Competing risks occur when an indi-
vidual is subjected to more than one potential cause of mortality, and
the occurrence of one event prevents the occurrence of others. If mor-
tality hazards from different mortality sources are independent, mor-
tality hazard is said to be additive; if there is non-independence
between mortality sources, mortality is compensatory (Williams,
Nichols & Conroy 2002; Heisey & Patterson 2006). We classified
mortality as ursid, cougar, coyote, or wolf, as well as nonpredator
caused mortality (disease, starvation, etc); other sources of mortality
were rare (Table S2). Given the difficulty of distinguishing scaveng-
ing from predator mortality in the case of disease-related mortalities
(Smith et al. 2006), we may have misclassified some disease-related
mortalities as predation, likely underestimating the degree of com-
pensatorymortality.
We tested the compensatory predator-mortality hypothesis among
study areas in threeways. First, we examined how cause-specificmor-
tality changed as the number of predator species across areas
increased. If mortality was completely additive, we would expect an
increase in the risk of mortality as the number of predator species
increased. Conversely, if mortality was compensatory, we would
expect the risk of mortality to plateau because of the substitution of
mortality between different predator species. To test this, first, we
compared the hazard ratios (eb) between our three (baseline), four
and five predator systems. If there was no difference between our four
and five predator systems, for example, then predation by grizzly
bears could be considered compensatory to that by the other four
predators. We explicitly tested for changes in cause-specific mortality
(CIF) of a single predator and other competing risks with increasing
number of predators in a system Pepe & Mori (1993). This tests the
hypothesis of equality in the CIF of a mortality cause (e.g. cougar
predation) with another mortality cause while testing for equality in
the remaining competing risks (Pintilie 2006). A significant increase
in CIF of ursid predation in the presence of grizzly bears (five preda-
tor system) with no change in CIF of the remaining mortality factors
would be considered additive. Next, for each predator species, we
compared the relationship between cause-specific mortality rate and
neonatal elk survival using linear regression (Williams, Nichols &
Conroy 2002; Murray et al. 2010). If predation by a predator species
was additive, then survival should decrease with increasing predator-
specific mortality hazard, and the slope (b) for perfectly additive
mortality should be b = 1. If predation was perfectly compensatory,
survival should remain constant (b = 0) with increasing cause-spe-
cific mortality. This is a conservative and potentially biased test for
additive mortality because of the potential negative sampling covari-
ance between cause-specific mortality hazard from a specific cause
and total mortality (Schaub & Lebreton 2004). For example, total
mortality will increase if a cause-specific mortality rate increases, to
some unknown degree, even if 100% (Schaub & Lebreton 2004).
Therefore, this bias would render it more difficult to detect compen-
satory mortality. Other regression or state-space approaches suffer
similar limitations; yet recent studies have used such approaches to
gain valuable insight into whether mortality causes are compensatory
in the absence of experimental manipulations (Murray et al. 2010).
Finally, because the effects of predation and climate can interact
on mortality (e.g. Hebblewhite 2005), we considered the interaction
between number of predators and both summer and winter climatic
variables in Weibull survival models. If predator-mortality increased
with climatic severity (drought, winter severity), this is consistent
with neonatal mortality also being partially compensatory through
the interaction between an ostensibly density-dependent mortality
cause, predation, and a density-independent mortality cause, climate.
In this sense, in the absence of a predation*climate interaction, neo-
natal mortality hazard would be lower and calf survival would
increase.
Results
We determined the fate of 1999 radio-marked elk calves
across the 12 study areas from 1973 to 2007, with the major-
ity of individuals marked from 1990 to 2007. Sample sizes in
each study area ranged from 29 (Gallatin, MT) to 444 (Blue
Mountains, OR), with an average of 196 (Tables 1, S2).
Mean capture date of elk calves was 3 June, study area means
ranged from 26May to 7 June, an overall range from 10May
to 18 July (Table S3). Mean birth date was 31 May, ranging
over 1 week from 23 May to 4 June (Table S2); overall birth
dates ranged from 8 May to 16 July. Average age at capture
was 3 days (range 0–10) (Table S2), andmean capture weight
was 21Æ5 kg and varied from 17Æ6 to 28Æ0 kg across study
areas. Sex ratio of captured elk calves was 0Æ9:1 males to
females, which varied across study areas from 0Æ6 to 1Æ3 and
was not significantly different from a 50:50 sex ratio
(v2 = 2Æ28, df = 1,P = 0Æ131, see Table S3 for details).
SURVIVAL MODELL ING
The Kaplan–Meier 3-month (93 day) survival rate of neona-
tal elk calves across all 12 studies was 0Æ61 (SE = 0Æ01) and
ranged from 0Æ31 (SE = 0Æ04) to 0Æ84 (SE = 0Æ03) (Table 1).
Overall Kaplan–Meier summer survival rates varied among
study areas with different predator community composition.
Average survival was 0Æ65 (SE = 0Æ01) with three predators,
0Æ55 (SE = 0Æ03) with four, and 0Æ50 (SE = 0Æ03) with five
(Fig. 2).
The top neonatal elk survival model was a function of the
base covariates (sex, birth date and birth weight), predator
community composition (three, four or five predators),
1250 K. A. Griffin et al.
 2011 TheAuthors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 1246–1257
previous summer average maximum temperature, May pre-
cipitation, and the interaction between May precipitation
and four predators (Table 2). The second ranked model was
a function of base covariates, number of predator species,
May precipitation and previous summer maximum tempera-
ture, and the interaction betweenMay precipitation and both
four and five predators (DAIC = 1Æ7). Despite some model
selection uncertainty, because there was sufficient weight and
similarities between the top two models, we focus our results
on these (Table 2) and report hazard ratios for both in
Table 3. Including frailty improved model fit over the fixed-
effect survival model (LRT of h = 0 in equation 1,
v2 = 139Æ5, P < 0Æ00005; also, DAIC of the top-ranked
model without frailty = 85; note both tests are potentially
optimistic, Cleves, Gould &Gutierrez 2002). Variance in sur-
vival among study areas was significant (h = 0Æ351,
SE = 0Æ148), confirming substantial within-study-area cor-
relation in survival. Expressed as a proportion of the total
variance in our Kaplan–Meier survival rate, our survival
model explained 40Æ1% of the variation in survival across all
study areas (Vaida & Xu 2000; Cleves, Gould & Gutierrez
2002). We emphasize our inferences from the top shared-
Table 2. Top tenWeibull neonatal elk survival models showing number of parameters (k), deviance (Dev), change in AIC compared to the best-
ranked model (D AIC), and Akaike model weights (w) across the north-western United States. The base model included sex (male, female,
unknown), birth date, and birth weight, as well as twoWeibull survival parameters, and a random effect term (seven base parameters). Climatic
coefficients are previous summer mean maximum temperature (PSt), May precipitation (Mp), mean May minimum temperature (MMt), June
snow (Js), total snow (TSnow) andmean winter minimum temperature (WMt). Number of predator species was Pred 4 and Pred 5, respectively;
covariate interactions are indicated by*
Model
rank Model k Dev DAIC w
1 PSt + Mp + Pred 4 + Pred5 + Mp*Pred4 11 )1837Æ6 0Æ0 0Æ659
2 PSt + Mp + Pred 4 + Pred5 + Mp*Pred4 + Mp*Pred5 12 )1837Æ4 1Æ7 0Æ287
3 PSt + Mp + Pred4 + Pred5 + Mp*Pred4 + Mp*Pred5
+ PSt*Pred4 + PSt*Pred5
14 )1837Æ1 5Æ1 0Æ050
4 WMt + PSt + MMt + Mp + Js 11 )1844Æ0 12Æ8 0Æ001
5 WMt + PSt + MMt + Mp 10 )1845Æ4 13Æ7 0Æ001
6 PSt + MMt + Mp + Pred5 10 )1845Æ6 14Æ1 0Æ001
7 WMt + PSt + MMt + Mp + Js + Pred5 12 )1843Æ4 14Æ1 0Æ001
8 WMt + PSt + MMt + Mp + Js + TSnow 12 )1843Æ8 14Æ4 <0Æ001
9 WMt + PSt + MMt + Mp + Js + Pred4 12 )1843Æ8 14Æ5 <0Æ001
10 WMt + PSt + MMt + Mp + Pred5 11 )1844Æ8 14Æ5 <0Æ001
Table 3. Mortality hazard ratios for the top twoWeibull survival models for neonate elk survival in the north-westernUnited States, 1973–2007.
See Table 2 for descriptions of the two top models. As the risk of mortality hazard increases, survival decreases such that a hazard ratio >1Æ0
means lower survival. The reference category for sex is male and for number of predator species is three predators
Covariate
No. 1Model No. 2Model
Hazard Ratio P 95%CI HazardRatio P 95%CI
Female 1. 09 (0Æ087) 0Æ30 (0Æ93 – 1Æ27) 1Æ09 (0Æ087) 0Æ30 (0Æ93 – 1Æ27)
Birth weight 0Æ98 (0Æ011) 0Æ06 (0Æ96 – 1Æ00) 0Æ98 (0Æ011) 0Æ05 (0Æ96 – 1Æ00)
Birth date 1Æ00 (0Æ007) 0Æ730 (0Æ98 – 1Æ01) 1Æ00 (0Æ007) 0Æ74 (0Æ98 – 1Æ01)
Prev. summer max temp 1Æ11 (0Æ033) <0Æ0001 (1Æ05 – 1Æ18) 1Æ11 (0Æ033) <0Æ0001 (1Æ05 – 1Æ18)
May precip. 1Æ01 (0Æ015) 0Æ43 (0Æ98 – 1Æ04) 1Æ01 (0Æ015) 0Æ38 (0Æ98 – 1Æ04)
4 Predators 2Æ98 (0Æ858) <0Æ0001 (1Æ69 – 5Æ24) 3Æ01 (0Æ869) <0Æ0001 (1Æ71 – 5Æ30)
5 Predators 2Æ39 (1Æ009) 0Æ04 (1Æ04 – 5Æ47) 3Æ12 (1Æ929) 0Æ07 (0Æ93 – 10Æ48)
May precip*4 predators 0Æ90 (0Æ022) <0Æ0001 (0Æ86 – 0Æ95) 0Æ90 (0Æ022) <0Æ0001 (0Æ86 – 0Æ95)
May precip*5 predators – 0Æ95 (0Æ078) 0Æ56 (0Æ81 – 1Æ12)
Fig. 2. Kaplan–Meier estimates of neonate elk survival for the first
3 months of life as a function of number of predator species across
the north-western USA. Data from 12 studies that occurred between
1973 and 2007.
Neonate elk calf survival across the north-western USA 1251
 2011 TheAuthors. Journal ofAnimal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 1246–1257
frailty model should be interpreted as the population-aver-
aged effects across all 12 study areas representing the average
elk calf survival experience, adjusting for covariates, and not
the expectation within any specific study area.
Covariate effects in terms of hazard ratios (HR) from the
top two models are reported in Table 3. No significant effect
of sex on survival was found in either model (P = 0Æ30), nor
was birth date related to hazard (P = 0Æ73). Survival
increased with increasing birth weight, as expected (i.e.,
increasing weight decreased mortality hazard, Table 3). Sur-
vival decreased in the top model as the number of predator
species increased from three (reference case) to include
wolves (HR = 2Æ98, P < 0Æ0001) and wolves and grizzly
bears (HR = 2Æ39, P = 0Æ04). There was no difference in
hazard ratios between wolves and wolves and grizzlies
(P = 0Æ35), supporting our interpretation of increasing com-
pensatory mortality as the number of predators increased.
When adult females experienced hot summers, survival of
calves the following summer decreased (HR = 1Æ11,
P < 0Æ0001) over and above the effect of birth weight, which
was also in the model. Increasing May precipitation had no
main effect on survival by itself (HR = 1Æ01,P = 0Æ43), only
through its interaction with predation (Table 3). In both top
models, increasing May precipitation increased survival of
calves (Fig. 3); however, the interaction was only significant
in areas with four predators (HR = 0Æ90, P < 0Æ0001).
Analysis of the restricted Jackson Hole data before (1990 –
1992) and after (1997 – 1999) grizzly bear and wolf recovery
showed the same two top models and hazard ratios
(Table S4), as did the analysis excluding Jackson Hole data
from the overall data (M. Hebblewhite., unpubl. data), con-
firming our interpretation of the overall models.
CAUSE-SPECIF IC MORTALITY
We detected 671 mortalities across the 1999 marked calves,
70% of which occurred within the first 30 days (median age
of death = 14 days). Average cause-specific mortality rates
were 0Æ15 (SE = 0Æ01) for ursids, 0Æ11 (SE = 0Æ01) for cou-
gars, 0Æ02 (SE < 0Æ01) for coyotes, 0Æ01(SE < 0Æ01) for
wolves, 0Æ04 (SE = 0Æ01) for nonpredators and 0Æ06
(SE = 0Æ01) for all other mortalities (Table S5). In predator
communities with wolves (four predators), cougar-caused
mortality declined from 0Æ14 (SE = 0Æ01) to 0Æ07
(SE = 0Æ02) (Pepe-Mori test of the hypothesis that cougar
mortality did not change with additional predators,
P < 0Æ001), and ursid predation marginally increased (Pepe-
Mori test P £ 0Æ08) from 0Æ11 (SE = 0Æ01) to 0Æ16
(SE = 0Æ02). See Table S6 for full details of tests. Including
wolves in the system added only a small amount of wolf-
caused mortality, 0Æ04 (SE = 0Æ01), with essentially no
change in coyote predation (P = 0Æ17) (Figs 4 and 5). With
both wolves and grizzly bears, cougar predation declined to
negligible levels (P < 0Æ001) to <0Æ01 (SE < 0Æ01), ursid
predation significantly increased (P < 0Æ001) almost dou-
bling to 0Æ30 (SE = 0Æ03) while coyote predation remained
similar (P = 0Æ18) from 0Æ03 (SE = 0Æ01) to 0Æ04
(SE = 0Æ01).Wolf predation changed in systems with grizzly
bears, despite similar hazards (P = 0Æ08; four predators,
wolf mortality rate = 0Æ04, SE = 0Æ01 vs. five preda-
tors = 0Æ04, SE = 0Æ01) (Figs 4 and 5), because the timing
of wolf-caused mortality shifted. Without grizzly bears, wolf
predation occurred later, but peaked earlier with grizzly
bears (Figs 4 and 5). Timing of bear mortality, however,
always peaked early from day 0 to 30 and was the most
important overall source of neonatal mortality (Fig. 5).
Across systems, the timing of coyote and cougar mortality
during the early 0–30 days did not change either (Fig. 5).We
found no relationship between nonpredator caused mortality
rates and overall survival (Table S2, S5).
Fig. 3. Neonatal elk survival at day 100 as a function ofMay precipi-
tation (cm) under different number of predator species across the
north-westernUnited States, 1973–2007.
Fig. 4. Cause-specific mortality (3 months) for neonate elk by num-
ber of predator species for major predators using cumulative inci-
dence function analysis. ‘‘Ursid’’ in the three and four-predator
system represents only black bear but in the five-predator system ‘‘ur-
sid’’ represents both black and grizzly bear. Bars represent 95% con-
fidence intervals. Significant differences for a predator species
between mortality hazard in different predator communities are
marked with an *(P = 0Æ05) or **(P = 0Æ01) using Pepe & Mori
(1993) tests.
1252 K. A. Griffin et al.
 2011 TheAuthors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 1246–1257
Comparing the relationship between CIF mortality rate
and neonatal survival among study areas revealed that only
ursid predation appeared additive (Fig. 6, linear b = )1Æ01,
P < 0Æ001, R2 = 0Æ76, n = 12 studies), showing that sur-
vival decreased linearly with increasing ursid predation. For
all other predators, cause-specific mortality was not signifi-
cantly related to survival, and coefficients were all between 0
and 1, supporting the partially compensatory hypothesis,
although among-study area sample sizes were low for some
tests. For example, there was no additive relationship
between neonatal survival and coyote (b = 0Æ74, P = 0Æ79,
R2 = 0Æ01, n = 12), cougar (b = )0Æ16, P = 0Æ81, R2 =
0Æ01, n = 12) or wolf predation (b = )0Æ74, P = 0Æ71,
R2= 0Æ04, n = 6).
Discussion
Survival patterns of approximately 2000 neonatal elk in the
north-western United States were consistent with the com-
pensatory-mortality hypothesis via two important mecha-
nisms. The compensatory-mortality hypothesis predicts that
as the number of predator species increase, neonatal survival
will stabilize, indicating that one predator is replacing
another in its effect on neonate survival. As the number of
predator species increased, neonates survival declined, and
bears and cougars were the dominant predators of neonates.
Based on hazard ratios, survival declined most between three
and four predator communities, but not as much with the
addition of a major calf predator, grizzly bears. Analysis of
competing risks suggested that this was because of inter-
specific compensation between cougars with increasing
ursids, especially grizzly bears, but that unlike other preda-
tors, bear predation was additive with other causes of preda-
tion. Predation by ursids on neonates was consistent with
additive mortality compared to other predators whose mor-
tality was at least partially compensatory, emphasizing the
key role of ursids in setting the stage for neonate survival.We
also found evidence for climatic-predation interaction that
may lead to compensatory predation mortality. Increased
precipitation during May likely increased forage quality for
ungulates, reducing mortality in systems with four or five
predators. Therefore, given the evidence for compensatory
mortality from the interaction of climate and predation,
interspecific competition amongst predators, and evidence
Fig. 5. Instantaneous smoothed hazard functions (relative probability of mortality) showing timing of mortality on neonatal-elk calves since
capture across the north-western United States by each of the 4 main predator species as a function of changing predator community composi-
tion (three predators; black bears, coyotes, cougars; four predators including wolves, and five predators including grizzly bears). We calculated
smoothed hazards using the unconditional (population averaged) Epanechnikov kernel smoothing at the mean covariate value for all continu-
ous covariates for females. Hazards are graphed with 95% confidence intervals. Note the different magnitude of the Y-axis especially between
Ursid and all other mortality.
Fig. 6. Neonate elk survival by cause-specific mortality by the major
predators across the north-western United States. Linear regressions
are displayed for all species; however, only one category, ursids, was
significant (P £ 0Æ001), confirming that only ursid mortality was
additive (see text for details).
Neonate elk calf survival across the north-western USA 1253
 2011 TheAuthors. Journal ofAnimal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 1246–1257
for compensatorymortality by all predators except bears, the
effect of neonatal predation on population dynamics may be
weaker than expected if all predation was additive.
Our results supported the effects of spring ⁄ summer tem-
perature and precipitation on neonate survival more so than
effects of winter severity, consistent with the important role
of summer forage on ungulates (McArt et al. 2009; Parker,
Barboza & Gillingham 2009). We found a negative effect of
hotter previous summers on neonate survival 1 year later
over and above the effects of cooler and wetter summers on
calf birth weight. These effects may have been driven by long-
term drought conditions experienced in many study areas in
the 1990s (e.g. in Yellowstone National Park; Vucetich,
Smith & Stahler 2005). However, effects of spring climate
were less certain (Table 2), perhaps because of variation in
the mechanisms of spring climate downscaling across our 12
study areas (Pettorelli et al. 2005). For example, many stud-
ies report a positive effect of spring climate on neonate sur-
vival (Albon, Clutton-Brock & Guiness 1987; Raithel 2005;
Harris 2007), but Smith et al. (2006) reported mean April
temperatures, and others found March or May climate pat-
terns drove neonate survival. Across all 12 areas, we found
that calf survival increased with increasing May precipita-
tion, but interestingly, only in the presence of four or five pre-
dators. May precipitation could influence calf survival
through effects on summer forage quality and quantity on
both lactation and forage intake by the calf (Cook et al.
2004). May precipitation patterns could also drive spring for-
age phenology, and hence, neonatal survival (Pettorelli et al.
2005, 2007). Alternately, because the effects of precipitation
were only apparent in systems with increased predation,May
precipitation could influence spatial distribution of forage
that indirectly affects vulnerability to predation (Hegel et al.
2010). The obvious next step to tease apart these competing
mechanisms is analyses that combine spatial measures of for-
age quality ⁄quantity (such as NDVI, Pettorelli et al. 2005),
climate and predation. Regardless, our results emphasize the
potential for climate-mediated compensatory mortality
occurring during spring and summer in addition to classic
winter starvation-mediatedmortality (Singer et al. 1997).
The survival rates we observed in our study are consistent
with positive population growth of elk only under certain
ecological conditions. Given that annual elk calf survival
explains  73% of the variation in population growth rate
(Raithel, Kauffman & Pletscher 2007) and a mean adult
female survival rate reported by Raithel, Kauffman & Plet-
scher (2007) of 0Æ873 (which included our study areas), our
observed calf survival rates could be consistent with growing
(three predator systems), stable (four predators) and declin-
ing elk populations (five predators). This simple approach
emphasizes the importance of understanding both adult and
annual calf survival, not just neonatal survival, to assess
impact of predators. Consistent with this coarse interpreta-
tion, however, recent experimental predator reductions in
Idaho (White, Zager & Gratson 2010) also show that reduc-
ing bear densities increased neonate calf survival, consistent
with our finding of bear predation being a dominant cause of
additive mortality for neonates. Moreover, our restricted
analysis of the Jackson Hole area following recovery by
wolves and grizzly bears represents pseudo-experimental evi-
dence for strong effects of grizzly bears, but not wolves, on
calf survival (supporting information table S4). However,
recent experimental manipulations of winter food (Bishop
et al. 2009) and densities of two of four main predators (Hur-
ley et al. 2011) of another ungulate, mule deer (Odocoileus
hemionus), suggest that the effects of food availability on
juvenile survival were stronger than effects of predator
removal. Thus, mortality caused by climate–predator inter-
actions and competition among predators may make efforts
to increase population growth rate of elk through predator
control challenging.
Our results emphasize the strongly additive and ‘preemp-
tive’ role of early predation by ursids on neonates and
emphasizes that the phenology of predationmay dictate juve-
nile survival patterns. This echoes recent studies that empha-
size the critical importance of bear predation to neonatal calf
survival (Linnell, Aanes & Andersen 1995; Gustine et al.
2006; Zager & Beecham 2006; Barber-Meyer, Mech & White
2008). Across our 12 study areas, we found 0Æ01 to 0Æ44 prob-
ability of mortality as a result of predation by black and ⁄or
grizzly bears, which additively explained approximately 50%
of the variance in neonatal survival. Furthermore, when griz-
zly bears were in a system, mortality from ursids doubled.
Additive bear mortality may be a result of ‘predation phenol-
ogy’ in the timing of the pulse of ursid mortality on neonates.
Bear predation peaked within the first 2 weeks of a neonate’s
life during the critical ‘hiding’ period when female elk hide
their calves (Fig. 5). Following the hiding period, elk cow–
calf pairs form large groups and bear predation declines to
almost zero. In contrast, mortality by other predators
occurred throughout the summer, after the pulse of bear pre-
dation (Fig. 5). Thus, in a competing risks framework, ear-
lier bear predation out-competed later predators. Bear
predation may be additive because bears become specialist
predators during early calving before body condition can
start to mediate vulnerability to predation (White, Zager &
Gratson 2010). Alternately, increased bear predation could
simply be attributed to spatial overlap. For example, ungu-
late avoidance of low-elevation valley bottoms during calving
effectively reduces predation by canids (Hebblewhite & Mer-
rill 2007), but perhaps not by bears which often select the
same forage as ungulates during calving (Nielsen et al. 2003).
Functional redundancy among the predator community
may have been an important compensatory mechanism sug-
gested by the decelerating mortality hazard with the addition
of wolves and wolves and grizzlies. Declining cougar preda-
tion in the presence of wolves and grizzly bears is suggestive
of interspecific competition.Wolves are known to be effective
competitors with cougars and coyotes through interference
and exploitative competition (Kortello, Hurd & Murray
2007; Berger, Gese & Berger 2008; Hebblewhite & Smith
2009). Similarly, grizzly bears can be an important natural
cause of mortality for black bears (Hebblewhite, Percy &
Serrouya 2003), and wolves and grizzly bears also compete
1254 K. A. Griffin et al.
 2011 TheAuthors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 1246–1257
both directly and indirectly (Hebblewhite & Smith 2009).
Puzzlingly, however, calf survival was lower in systems that
contained wolves (four or five predator systems), despite the
fact that these systems had low wolf mortality rates. These
results might be consistent with the hypothesis that wolves
affect calf recruitment through indirect risk effects (Creel
et al. 2007). Thus, the addition of new carnivore species to
already diverse predator communities may not affect neona-
tal survival additively, but mortality could also manifest
through indirect effects.
Our study suffers some of the inferential weaknesses of
observational studies, regardless of the large number of
calves, as we only had 12 populations to compare across, and
would be strengthened if more of our studies were experimen-
tal manipulations. Thus, some caution is warranted. For
example, we were unable to measure predator densities to
explicitly test the effects of predator density on neonatal sur-
vival. Our results could therefore be because of other uncon-
trolled differences among study areas that were correlated
with the number of predator species such as predator density,
habitat fragmentation or human harvest. For example, there
was an east–west gradient in bear to cougar predation that
may reflect regional trends in carnivore abundance, not the
predator community per se. Moreover, as previously men-
tioned, our tests for additive or compensatory mortality were
biased towards detecting additive mortality (Schaub & Lebr-
eton 2004) and limited by low sample sizes of systems for
some predators, such as wolves (n = 6), for example. How-
ever, we believe our results warrant consideration for several
reasons. First, our survival estimates and estimates of risk
factors matched the results of previous analyses within indi-
vidual study areas well. The restricted analysis with the
before-after comparison in Jackson Hole corroborated our
pooled model results almost exactly (Table S4), and our data
included the predator manipulation study in Idaho con-
ducted by White, Zager & Gratson (2010). Our survival
model also predicted ‘out-of-sample’ survival well in Yellow-
stoneNational Park under drought conditions before wolves’
recolonized (Singer et al. (1997) calf survival estimate of
0Æ646 [SE = 0Æ132], compared to that predicted by model 1
of 0Æ585 [SE = 0Æ06]). Second, our shared-frailty Weibull
survival modelling framework addressed unobserved, shared
heterogeneity among populations that was unrelated to the
measured covariates, including predator density. Shared-
frailty models could explain 41% of observed variation in
survival across studies, and while this is quite high for an eco-
logical study, it certainly leaves a substantial degree of varia-
tion that could be attributed to unmeasured variables. These
results should aid management of elk populations across a
gradient of predator communities across the north-western
United States and allow basic predictions of neonate survival
for the first 3 months under different ecological conditions.
We encourage future studies to examine elk calf survival in
areas with known or experimentally manipulated predator
densities. Finally, because overwinter calf survival was not
addressed in this study, there may be important compensa-
tion between additive summer bear mortality and winter
causes of mortality, especially because wolf mortality
increases during mid to late winter with increasing snow
depth (Smith et al. 2004).
Future studies should also examine whether primary pro-
ductivity will buffer survival against predation and climate.
We did not incorporate spatial measures of primary produc-
tivity (e.g. NDVI) here, although such analyses are the obvi-
ous next step. Regardless, based on recent studies, we can
make future predictions. In one of themost compelling recent
meta-analyses, Melis et al. (2009) showed predation and pri-
mary productivity interacted in roe deer (Capreolus capreo-
lus) across 79 populations in continental Europe spanning a
wide latitudinal gradient. At a low primary productivity
(northern latitudes), predation had a dramatic effect on roe
deer, reducing densities almost 50%. Yet at high primary
productivity, no difference between roe deer densities with
and without predation was found. Therefore, we predict that
predation will be largely compensatory where primary pro-
ductivity is high and mostly additive where primary produc-
tivity is low.
Acknowledgements
Funding and support were provided by the RockyMountain
Elk Foundation (Project no. NA090047), The University of
Montana, the Idaho Department of Fish and Game, Mon-
tana Fish Wildlife and Parks, Washington Department of
Fish andWildlife, the Oregon Department of Fish andWild-
life, and USFWS Wildlife Restoration Pittman-Robertson
contracts W-98-R 40855 131000 and 20855 131000. We
thank Enzo Coviello for advice on competing risks analysis.
We thank Tom Toman and Dan Pletscher for support in ini-
tiating the analysis. We especially thank all agencies that
shared their data and knowledge and all the field technicians
who participated in data collection. L.D. Mech should have
been a co-author, but elected to remove himself because of
conflicts with the USGS peer review system. We thank L.D.
Mech, M. Festa-Bianchet, J. Fieberg, the Editors and anony-
mous reviewer for extremely helpful comments.
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Handling Editor: TimCoulson
Supporting Information
Additional Supporting Information may be found in the online ver-
sion of this article.
Table S1. Summary climate statistics for all 12 elk calf survival study
areas.
Table S2. Cause of mortality as originally categorized by researchers
compared tomortality codes used in our analyses.
Table S3. Summary statistics for all study areas.
Table S4.Hazard ratios for the top neonatal elk survival model using
only data from JacksonHole.
Table S5. Neonatal elk survival and cause-specific mortality to
100 days of life by study area andmajor predators.
Table S6. Result of Pepe-Mori tests of equality in cause-specific mor-
tality between areas with differing numbers of predators.
As a service to our authors and readers, this journal provides sup-
porting information supplied by the authors. Such materials may be
re-organized for online delivery, but are not copy-edited or typeset.
Technical support issues arising from supporting information (other
thanmissing files) should be addressed to the authors.
Neonate elk calf survival across the north-western USA 1257
 2011 TheAuthors. Journal ofAnimal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 1246–1257