Journal of Mammalogy, 99(5):1021–1031, 2018

DOI:10.1093/jmammal/gyy115
Published online September 26, 2018

Merriam Award Paper

Wolves for Yellowstone: dynamics in time and space
Mark S. Boyce*,
Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada
* Correspondent: [email protected]

The reintroduction of gray wolves (Canis lupus) to Yellowstone National Park is the most celebrated ecological

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experiment in history. As predicted by population models, the rapid recovery of a wolf population caused both
temporal and spatial variability in wolf–ungulate interactions that likewise generated temporal and spatial
variation in the expression of trophic cascades. This has amplified spatial variation in vegetation in Yellowstone,
particularly with willow (Salix spp.) and cottonwood (Populus spp.) in riparian areas, with associated changes
in food webs. Increasing influences of grizzly bears (Ursus arctos), cougars (Puma concolor), and bison (Bison
bison) are making what initially was predominantly an elk–wolf interaction into an increasingly complex system.
Outside Yellowstone, however, humans have a dominant influence in western North America that overwhelms
trophic cascades resulting in what appear to be bottom-up influences on community structure and function.
Complex and unexpected ecosystem responses to wolf recovery in Yellowstone reinforce the value of national
parks and other protected areas as ecological baseline reserves.

Key words: bison, Canis lupus, Cervus elaphus, ecological modeling, elk, hunting, predator–prey dynamics, trophic cascades, wolf,
Yellowstone National Park

The reintroduction of gray wolves (Canis lupus) into park managers recognized that herbivory was altering vege-
Yellowstone National Park is a well-known ecological exper- tation, leading park managers to implement culls to contain
iment, albeit with a lack of replication, randomization, and the elk population (Houston 1982; Barmore 2003). Public
controls (Kauffman et al. 2013; Ford and Goheen 2015). The pressure prompted Senator Gale McGee from Wyoming to
trophic cascade that resulted in vegetation being released insist in 1967 that the National Park Service terminate the
from herbivory caused by wolf predation on elk (Cervus ela- elk culls. Terminating the elk cull inside the park initiated a
phus) is purported to be among the most significant advances period when elk numbers were allowed to reach levels where
in conservation biology of this century (Estes et al. 2011; their abundance would undergo “natural regulation” imposed
Ripple and Beschta 2012). I began research on large mam- by the interaction between herbivory and vegetation, i.e.,
mals in the Greater Yellowstone Ecosystem in 1977, thus extensive starvation of elk during severe winters (Houston
my involvement in the ecology of the area spans more 1982; Merrill and Boyce 1991). Consistent with a review
than 40 years. I will draw from this long-term perspective of management of wildlife in national parks (Leopold et al.
to reflect on the ecology of wolf recovery in Yellowstone, 1963), the park management committed to restoring wolves
framed largely on my research and that of my students and to limit elk abundance (Weaver 1978; Despain et al. 1986).
colleagues. Eventually, in 1995, 14 wolves from Alberta were released in
Yellowstone, supplemented by another 17 Canadian wolves in
1996 (Smith and Ferguson 2012).
Brief History of Wolves in Yellowstone
Although Yellowstone was designated as a national park in
1871, early park management did not provide the protec-
Materials and Methods
tion for wildlife that it does today (Schullery 2003). In fact, Modeling wolf recovery.—During the 1980s, the National
the park deliberately eliminated wolves and cougars (Puma Park Service began accumulating research and public consul-
concolor) by 1926. Within a few years, numbers of elk in tations required to reintroduce wolves. Because of previous
Yellowstone had increased substantially, and by the 1930s, research that we had done on population dynamics of elk in

© 2018 American Society of Mammalogists, www.mammalogy.org

1021
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the Greater Yellowstone Ecosystem (Sauer and Boyce 1983; Northern Range were monitored by the Northern Yellowstone
Boyce 1989; Merrill and Boyce 1991), in 1988, John Varley Cooperative Wildlife Working Group in most years using aerial
(Director, Yellowstone Center for Resources) persuaded me surveys for minimum estimates of abundance not corrected for
to develop a model to anticipate probable consequences of variation in sightability. Wolves were monitored by park biolo-
wolf recovery to populations of wild ungulates in the park. gists led by Douglas W. Smith following the releases in 1995
I proceeded to build a computer simulation model of a pred- and 1996, and beginning in 2004 wolves also were monitored
ator–prey system focusing primarily on elk–wolf interac- using GPS telemetry.
tions but including alternative prey of bison (Bison bison), We used resource selection functions (Mao et al. 2005),
moose (Alces alces), and mule deer (Odocoileus hemionus) step-selection functions (Fortin et al. 2005a), and state-based
that were sufficiently abundant to potentially influence wolf models (Forester et al. 2007) to document patterns of habitat
recovery. Predation on multiple prey was modeled using a selection in the context of the distribution of wolves. In addi-

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multispecies Holling Type III functional response (Abrams tion, we used resource selection functions to study the distri-
and Allison 1982) to accommodate learning by wolves and bution of sites where wolves killed elk across the Northern
density dependence (Maynard Smith 1974). Range and performed that analysis each year 1996–2005 to
Parameterization of the elk components of the model relied study vulnerability of elk to the spatial distribution of wolves
extensively on data compiled by Houston (1982) for elk popula- and vegetation (Kauffman et al. 2007). More recently, Kohl
tions in the park, and studies of the interaction between wolves et al. (2018) used our telemetry data for elk and data for
and elk in Riding Mountain National Park (Carbyn 1980). Data wolves collected and maintained by park biologists in an
on predation by wolves on deer (Odocoileus spp.) and moose analysis of the daily variation in activity by elk and wolves
were based on studies in Michigan, Minnesota, Canada, and to reveal that they interact in diel patterns of movement and
Alaska (Pimlott 1967; Mech 1970; Garton et al. 1990), whereas habitat selection.
the only data for wolf predation on bison were from Wood We revisited the simulation model 10 years after wolf reintro-
Buffalo National Park (Carbyn and Trottier 1987). John Varley duction in the context of adaptive management (Walters 1986),
later asked me to expand my original model focused on the i.e., to evaluate how well we predicted system dynamics and to
Northern Range (Boyce 1990) to include the Jackson elk herd adjust the model based on new data (Varley and Boyce 2006).
and the population along the North Fork of the Shoshone River Vegetation responses.—In the context of trophic cascades,
east of the park (Boyce and Gaillard 1992). I focus attention on woody plants, in particular aspen (Populus
Stabilizing features of the model included density depend- tremuloides), willow (Salix spp.), and cottonwood (P. tricho-
ence for ungulates presumed to be limited by their interac- carpa and P. angustifolia and hybrids) that are heavily browsed
tion with vegetation (Houston 1982; Sauer and Boyce 1983; by both elk and bison.
Merrill and Boyce 1991), the logistic functional response To study responses of willows to herbivory, 18 stands of
affording density-dependent predation at low densities, and willows across Yellowstone’s Northern Range were identified,
density dependence for wolves because of territorial behavior and stems were sampled in 2001. Thin cross-sections of stems
(Cubaynes et al. 2014). In addition, Montana Department of were used to measure growth by Salix boothii and S. geyeriana
Fish, Wildlife, and Parks had published guidelines for hunter each year from 1989 to 2001. Variation in growth of willows
quotas that were density dependent with more licenses being was modeled relative to browsing, snow depth, elevation, and
issued when elk numbers on the Northern Range were high watershed area, and information-theoretic methods were used
(table 2 in Varley and Boyce 2006). to select the best statistical models (Beyer et al. 2007). During
Based on studies of elk ecology on Yellowstone’s Northern the winter of 2003–2004, 7 stands of S. geyeriana were moni-
Range, key to the simulation models was stochastic variation in tored 7 times from December through March to document the
winter severity (Houston 1982) and summer forage production seasonal pattern of browsing by elk (Varley 2007).
(Merrill and Boyce 1991). These climate-based perturbations Hydrology is an important factor for riparian vegetation.
to carrying capacity ensured realistic levels of variation among Marshall et al. (2013) performed 4 replicates of an experimen-
model predictions; indeed, it was nearly impossible to obtain tal manipulation of browsing with fenced exclosures and dams
the same simulation result twice. I programmed a user-friendly to simulate the effect of beavers during 2001–2010. Height and
interface and we distributed the model on 5 ¼-inch floppy dis- biomass of individually marked willow stems were recorded
kettes to high schools, universities, and government agency annually for replicated controls, fenced exclosures, dammed
personnel, encouraging users to explore alternative decisions sites, and dammed sites with exclosures. All research was
on how wolf recovery might be managed. approved by university animal care and conformed to ASM
Monitoring dynamics.—For the decade following the rein- guidelines (Sikes et al. 2011).
troduction of wolves, we participated in monitoring elk move-
ments and abundance (Fortin et al. 2005a, 2005b; Mao et al.
2005). Elk were captured in winters of 2000–2002 using net- Results
gunning and collared initially with VHF transmitters, and Modeling.—The wolf–ungulate model was presented to the
later with GPS telemetry then monitored by Julie Mao (Mao United States Congress in support of proposed wolf recovery
et al. 2005) and Shaney Evans (Evans et al. 2006). Elk on the (Boyce 1990; Boyce and Gaillard 1992). Model predictions
 MERRIAM AWARD PAPER—WOLVES FOR YELLOWSTONE 1023

depended on the management alternatives selected by the user, on winter ranges secured in part by the Rocky Mountain Elk
but always resulted in a reduction in the number of elk (Boyce Foundation, expanding the winter range for elk by about 40%
1995). Yet, density-dependent mechanisms for ungulates and (Taper and Gogan 2002). These deficiencies in the original
wolves ensured that the model predicted long-term persistence model structure were accommodated in a revised model that
of wolves and all ungulates in the park. Indeed, in over 100,000 included elk population structure (Varley and Boyce 2006).
iterations of the model, all 4 ungulates and wolves persisted Even after making these adjustments, however, during the sec-
for 100 years (Boyce 1995). Including additional subpopula- ond decade after wolf reintroduction, the number of elk aver-
tions in the model also contributed to the stability of the system aged lower than predicted by the simulation model (MacNulty
because fluctuations were not entirely synchronous; therefore, et al. 2016). I believe that this is because bear (Ursus arctos and
fluctuations in one subpopulation helped to offset those in oth- U. americanus) and cougar (P. concolor) predation was higher
ers (Boyce and Gaillard 1992; Boyce 1995). Consistently, wolf than we had anticipated. In particular, grizzly bears have been

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numbers throughout the entire park have been remarkably con- shown to be highly effective predators on elk calves (Singer et al.
stant for the past decade at about 100 animals (Fig. 1). 1997; Barber-Meyer et al. 2008), reducing recruitment by about 7
Simulations correctly predicted elk and wolf numbers calves/100 cows (Lukacs et al. 2018). Numbers of bears have not
observed during the first decade after wolf reintroduction increased appreciably within the park subsequent to wolf reintro-
(Fig. 2). Early years after wolf reintroduction were dominated duction (Boyce et al. 2001a, 2001b; van Manen et al. 2016), but
by a simple wolf–elk interaction, so the model was most likely predation by bears on elk calves has increased (Barber-Meyer
to work during the initial period. However, despite these good et al. 2008; Griffin et al. 2011). Displacement of wolves by bears
predictions, we learned that several assumptions and compo- at kill sites also does not appear to be compensated by increased
nents of the original model (Boyce 1990; Boyce and Gaillard kill rate by wolves (Tallian et al. 2017). Cougars are highly capa-
1992) were incorrect. First, we underestimated the extent to ble predators on elk and compete with wolves for prey, although
which wolves specialized on elk as prey (White and Garrott they appear to be a subordinate predator (Elbroch et al. 2015).
2005), which required revision to the multispecies functional Another major change in the large mammal community in
response. Another shortcoming was failure to recognize the the past decade has been that the number of bison using the
strong age selectivity by wolves and hunters (Fig. 3). Hunters Northern Range has increased to over 4,000 animals, possi-
preferentially kill bulls but when they kill cow elk they prima- bly due to reduced competition with elk. Wolves certainly kill
rily kill prime-age females of high reproductive value (Wright bison (Carbyn and Trottier 1987), but bison are more formida-
et al. 2006); cows learn to avoid hunters to the extent that indi- ble and dangerous prey; thus, when elk are available they are
viduals older than about 9–10 are essentially “bullet proof” preferred over bison. Consequently, change in the distribution
(Thurfjell et al. 2017). In contrast, wolves killed primarily of large herbivores in the park has been one of the most signifi-
young and old and as a consequence the per capita influence cant responses to wolf predation and this was not anticipated in
of hunters on elk populations was much greater than for those our predator–prey models.
killed by wolves (Vucetich et al. 2005; Wright et al. 2006). Monitoring dynamics.—We found that that the interaction
Progressively more elk also began wintering outside the park between elk and wolves was highly seasonal. During spring

Fig. 1.—Census of wolves (Canis lupus) in Yellowstone National Park, 1995–2017, including a breakdown for the Northern Range and the interior
portions of the park. Courtesy of Yellowstone National Park.
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Fig. 2.—Time series projections from the WOLF5 model (Boyce and Gaillard 1992; Boyce 1995) compared with survey data for the Northern
Range elk (Cervus elaphus) population, 1995–2004 (from Varley and Boyce 2006).

Fig. 3.—Age distributions of female elk (Cervus elaphus) killed by hunters versus wolves (Canis lupus), 1995–2001. Elk calves killed by wolves
is 49% of the total. The line is the reproductive value for females of each age class (adapted from Wright et al. 2006).

and summer, wolf activity was greatest near dens and rendez- also a substantial year effect, meaning that habitat selection by
vous sites, and resource selection functions for elk showed that wolves varied over time (Uboni et al. 2015). Kill sites varied as
they avoided wolves by selecting higher elevations, less-open the wolf population became established and began to saturate
habitats, more-burned forest, and steeper slopes after wolf rein- the Northern Range. During the first 5 years after wolf reintro-
troduction. During winter, however, wolves appeared to track duction, the distribution of elk kills could be attributed in part to
the distribution of elk so that elk were unable to select habitats the distribution of wolf packs, with remaining variation attrib-
where they might avoid wolves; consequently winter habitat utable to landscape and vegetation variables. However, as the
selection by elk did not change much before and after wolf Northern Range became saturated with wolf pack territories by
reintroduction (Mao et al. 2005), although in the presence of year 2000, only landscape and vegetation variables contributed
wolves elk tended to move out of aspen stands toward open to the distribution of kill sites (Kauffman et al. 2007), again
grasslands or conifer forests (Fortin et al. 2005a). amplifying how the predator–prey system changed over time.
Consistent with these elk-based patterns of habitat selection, Using our data on elk, Kohl et al. (2018) emphasized that
wolves showed highly seasonal patterns of habitat selection, but not only was the interaction between wolves and elk highly
 MERRIAM AWARD PAPER—WOLVES FOR YELLOWSTONE 1025

seasonal, but it also varied within the day, as had been shown
by Forester et al. (2007). Wolf and elk activity are highly cre-
puscular (Boyce et al. 2010), and the “landscape of fear” is very
different during the day and night than during these dawn and
dusk activity periods (Kohl et al. 2018). This does not dimin-
ish the landscape of fear patterns as reflected by the influence
of topography and vegetation on the distribution of wolf kills
(Kauffman et al. 2007), but informs a dynamic landscape of
fear helping to interpret behavioral observations where elk
appeared to ignore wolves during the day.
Vegetation responses.—Foraging by herbivores, especially

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elk and bison, has substantial consequences to vegetation in
Yellowstone National Park (Houston 1982; National Research
Council [NRC] 2002; Barmore 2003). Indeed, concern over
excessive herbivory precipitated elk culling programs during
1930–1967 and ultimately contributed to wolf reintroduction.
Willows, aspen, and cottonwoods were most severely browsed
by elk and bison, and reduced browsing resulting from wolf
recovery is the expression of a trophic cascade (Ripple and
Beschta 2012). Herbaceous grassland plants are important for-
age for elk and bison as well (Merrill and Boyce 1991; Merrill
et al. 1993), but these plants appear to be resilient to grazing
(Frank et al. 2016). Yet, grazing amplifies sensitivity of plants
to site variation in moisture and nutrients (Frank et al. 2017).
Browsing by elk prior to wolf reintroduction had suppressed
growth of willows across Yellowstone’s Northern Range
(Beyer et al. 2007; Varley 2007). Cross-sectioned willow stem
annuli that reflect plant growth for S. boothii and S. geyeri-
ana show an overall increase in growth at 17 sites across the
Northern Range during years following wolf reintroduction,
presumably due to reduced browsing by elk (Fig. 4). The best
statistical models of willow growth included covariates for ele- Fig. 4.—Growth by 2 species of willow, Salix boothii and S. geyeri-
vation, climatic conditions, and the presence of wolves (Beyer ana, before and after wolf (Canis lupus) reintroduction in 1995 meas-
et al. 2007). Most important, however, is the enormous varia- ured by dendrochronology (Beyer et al. 2007). Each line is a separate
tion among sites. This reflects substantial site variation relative sampling site illustrating substantial variation in the response of wil-
to soil type, soil moisture, topography, and vegetation (Tercek lows to wolf recovery. Courtesy of H. Beyer.
et al. 2010). Some sites were released from herbivory, whereas
other sites continued to experience substantial herbivory, continued to suppress willows, revealed by dramatic growth
largely by elk (Varley 2007). Note that these results in Fig. 4 of willows inside an exclosure built in 1958, but no willows
from the analysis by Beyer et al. (2007) are through 2001, persisting outside the exclosure (Fig. 7). I visited this site in
before the elk population had begun to decline as a numerical 1985 with Don Despain (plant ecologist, Yellowstone Center
response to wolves, contrary to the interpretation by Creel and for Resources), who pointed out that although willow were
Christianson (2009). browsed to the ground every year, the density of stems outside
Experimental manipulations of the water table and herbiv- the exclosure was the same as inside. By 2012, however, no
ory revealed clear results (Fig. 5). Exclosures to eliminate her- willow sprouts could be found outside the exclosure although
bivory enhanced willow growth above that in the control sites, willows remained robust within the exclosure. Persistent heavy
and even stronger response was observed when dams were con- browsing appeared to have killed the plants.
structed to simulate beaver dams. The most exaggerated growth Browsing had largely eliminated cottonwoods from
by willows was observed at plots behind dams inside exclo- Yellowstone with only a few old trees remaining (NRC 2002;
sures (Marshall et al. 2013). Beschta 2005). However, several flooding events from 1995–
I visited the Northern Range of Yellowstone in October 2012 2008 resulted in widespread establishment and recruitment of
at the nadir of elk abundance following wolf reintroduction. over 1.3 million cottonwoods and an expectation that some
Site variation in willow recovery was highly evident. Figure 6 of these will survive to form mature stands (Rose and Cooper
illustrates that willow growth on the Blacktail Plateau is vig- 2017). Occasional flooding is crucial to the establishment of
orous at a site where willows were suppressed prior to wolf riparian cottonwoods and release from herbivory is needed for
reintroduction. However, south of Mammoth, elk and bison recruitment. Thus, for cottonwoods as well as for willows, we
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Fig. 7.—An exclosure 1 km south of Mammoth showing tall wil-
low inside the fenced exclosure, constructed in 1958. I could find no
evidence of willow stems outside the exclosure when this photo was
Fig. 5.—Height response of willows (Salix spp.) to 4 replicated treat- taken in October 2012. Photo by M. S. Boyce.
ments of herbivory using exclusion fences to eliminate grazing and
dams to simulate beaver (Castor canadensis) dams. White lines are 1988, however, that few saplings were able to escape herbivory
mean response with shading of 95% prediction intervals for controls (Forester et al. 2007; Romme et al. 2011), and high-predation-
in gray, unbrowsed in red, dammed in blue, and both grazing exclo- risk sites were browsed as well (Kauffman et al. 2010).
sure and dammed in purple. Dashed line at 200 cm is height required
Consequences of herbivory can be very different among
to escape herbivory (from Marshall et al. 2013).
seasons, e.g., elk are typically grazers but browsing is most
likely to occur in winter (Fig. 8). Thus, sampling aspen in late
summer is not likely to show much site variation in browsing.
The ability for a trophic cascade to be expressed also is easily
overwhelmed by site and seasonal influences (Marshall et al.
2013). Topography, soils, hydrology, and vegetation all interact
to create variation among sites that influences both prey and
predator (Bilyeu et al. 2008). Recently, with reduced elk brows-
ing, aspen appear to be recovering in a few stands, especially in
eastern portions of the Northern Range (Painter et al. 2015), but
not on a broad scale across the Northern Range (Kimble et al.
2011; Kauffman et al. 2013). Again, the outcome is high spatial
variability caused by site characteristics and elk herbivory.

Discussion
Several topics regarding wolves in Yellowstone have attracted
Fig. 6.—Willow growth evident in the Blacktail Plateau of Yellowstone debate and differences of interpretation, mostly surrounding
National Park, October 2012. A bedded bison (Bison bison) is in the trophic cascades (Terborgh and Estes 2010). During the first
middle of the photograph for scale. Photo by M. S. Boyce. few years after wolf reintroduction, wolves were few and elk
still were abundant, leading Beyer et al. (2007) to conclude
have observed a trophic cascade, albeit associated with flood- that behavioral responses released selected willow stands
ing conditions required for cottonwood establishment. from herbivory. Creel and Christianson (2009) failed to rec-
Most controversial, however, is the nature of a trophic cas- ognize that no decline in elk abundance had occurred during
cade for aspen. Like cottonwoods, aspen require exceptional the period studied by Beyer et al. (2007) and incorrectly sug-
conditions to permit recruitment of young trees, especially gested that the willow response could have been a numerical
from seed. Based on sampling of aspen conducted in August response. Likewise, during the first 5 years after wolf reintro-
and September 1999, Ripple et al. (2001) suggested that due duction, the distribution of wolf home ranges contributed to
to elk avoiding wolves, aspen might escape herbivory. This the distribution of elk kills on the Northern Range (Kauffman
could be facilitated by post-fire suckering of aspen (Romme et al. 2007). But after that initial period, the landscape became
et al. 1995). Aspen were browsed so heavily after the fires of saturated with wolf home ranges and we found that the
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Fig. 8.—Accumulated browsing by elk (Cervus elaphus) on willows at 7 stands on the Northern Range, 2003–2004 (from Varley 2007). Patterns
of browse removal are indicated by symbols as: early pattern (▲), abrupt pattern (◊), and gradual pattern (● ).

distribution of wolf-killed elk was related to topography and Responses of vegetation to herbivory show remarkable spa-
vegetation (Kauffman et al. 2007), e.g., elk are easier prey in tial variation. The willow story appears reasonably clear: some
riparian areas (Bergman et al. 2006). The upshot is that both drainages began to support good willow growth and popula-
behavioral and numerical responses have been documented in tions of willows and songbirds recovered (Beschta and Ripple
Yellowstone and these have varied in space and time. I believe 2016). However, other sites continue to receive heavy browsing
that the consensus will be that numerical declines in elk have even at reduced elk densities, and might require many decades
contributed more to trophic cascades than has behavioral to recover from 70 years of heavy browsing by elk and loss
avoidance of wolves, yet behavioral responses clearly exist of beavers (Hobbs and Cooper 2013). Likewise, cottonwoods
(Kohl et al. 2018). As vegetation has recovered at some sites, are recovering not only due to release from elk but largely in
we are now witnessing complex interactions between pre- response to perturbations created by occasional flooding events
dation risk and attraction to forage (Gallagher et al. 2017). (Rose and Cooper 2017); again, this is creating a highly heter-
Clearly, habitat selection by wolves in Yellowstone has varied ogeneous riparian landscape in the park.
over time (Kauffman et al. 2007; Uboni et al. 2015; Kohl et al. The dynamics of aspen and elk continue to perplex us. Beetle
2018). Likewise, habitat selection by elk varies seasonally (1979) and Gruell (1979) noted that declining aspen could be
(Mao et al. 2005) and differs among scales (Boyce et al. 2003). attributed to heavy browsing by elk as well as an absence of
Indeed, this heterogeneity in space and time is a hallmark of fire. Small fires were ineffective because resprouting aspen
the expression of a trophic cascade. attracted heavy herbivory, preventing recovery (Bartos and
My simulation models worked well during the first decade Mueggler 1979). So, we presumed that what was needed were
after wolf reintroduction, when the system was dominated by large fires so that aspen had opportunity to escape elk herbivory.
the simple predator–prey interaction between wolves and elk. The extensive fires of 1988 gave us the presumed remedy, but
Density dependence for wolves was debated, and my earlier elk numbers were so high that aspen could not escape herbiv-
models were questioned for assuming density dependence in ory even though there was extensive resprouting and aspen seed
wolves based on their well-known territorial behavior. Yet, this establishment (Romme et al. 2011). Subsequent to wolf recov-
assumption clearly was supported after wolf populations had ery, we observed that in the presence of wolves, elk tended to
stabilized and intraspecific interactions were shown to be the move away from aspen stands toward either open grasslands
most common cause of mortality among wolves (Cubaynes or coniferous forests (Fortin et al. 2005a). Yet, Kauffman et al.
et al. 2014). My assumption of a Type III (logistic) functional (2010) found that aspen stands were still suffering heavy elk
response will always be challenging to verify statistically browsing even in high-predation-risk sites. I believe that there
because at low densities we seldom have the sample sizes to are 3 probable explanations: 1) our radiocollars were set to a
show the convex portions of the logistic curve (Marshal and 5-h fix schedule and with such a long period between fixes, we
Boutin 1999). The logistic functional response is an important could not obtain good resolution in a step-selection function
assumption because it contributes to the stability of the system (Fortin et al. 2005a); 2) interactions between wolves and elk
and is highly likely to occur in mammalian carnivores where are highly dynamic in space and time; and 3) we treated all
learning is a mechanism behind the form of the functional aspen stands as equal in the analysis, whereas in reality there
response (Maynard Smith 1974; Boyce 2005). is substantial variation in the perceived threat of wolf approach
1028 JOURNAL OF MAMMALOGY

among stands because of variation in cover and topography. Superior), whereas at finer scales, trophic cascades amplify
Nevertheless, Painter et al. (2015) present evidence that some spatial variation in predation risk and consequent herbivory.
stands of aspen in Yellowstone are now recovering, but there Indeed, spatial heterogeneity arising from trophic cascades at
is not convincing evidence that this is driven by a behaviorally small scales could be what stabilizes the system at the larger
mediated response by elk to wolves (Kauffman et al. 2013). population scale.
Clearly, resolution the dynamics of herbivory and trophic cas- National parks and protected areas serve a crucial function
cades in aspen warrants continuing study. as ecological baseline reserves from which we can evaluate
Although the demonstration that wolves in Yellowstone how humans are affecting nature (Sinclair 1983; Boyce 1991,
National Park have shaped a trophic cascade is fascinating 1992, 1998). The National Park Service has adopted ecological
ecology, it is not clear that trophic cascades will occur in other process management, minimizing interference when possible,
areas. We also cannot be confident that these observations have allowing predation, herbivory, fire, and flooding to shape the

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conservation implications for wolf management and ecosystem ecosystem (White et al. 2013), and this policy allowed wolf
restoration elsewhere (Estes et al. 2011; Ripple and Beschta recovery with the fascinating dynamics that have emerged. The
2012; Wolf and Ripple 2018). We need to be cautious about most immediate threat to this park policy is the increasing bison
overextending the ecological results from wolf reintroduction population that has precipitated political pressure to limit their
in Yellowstone to applications outside parks, where livestock abundance for fear that heavy grazing and browsing by bison
management (Morehouse and Boyce 2011) and hunting have might “damage” vegetation. We do not know how bison will
a major influence on ecosystem structure and function (Mech affect Yellowstone, but surely we will learn a great deal more
2012; Muhly et al. 2013). if we allow the bison population to take its course rather than
A principle emerging from wolf recovery in Yellowstone is intervening in a fashion that will be arbitrary to the underlying
that trophic cascades have caused increased spatial and temporal ecological system. Whatever influence we can have as scien-
heterogeneity. This is evident in the large spatial and temporal tists, we must insist that the National Park Service maintain
variation in growth of willows (Beyer et al. 2007; Varley 2007; its policy of ecological process management for their Crown
Marshall et al. 2013), aspen (Kimble et al. 2011; Brodie et al. Jewell that is Yellowstone National Park.
2012; Painter et al. 2015), and cottonwoods (Rose and Cooper
2017). Spatial and temporal variation in predation risk means
that the landscape of fear creates an additional source of var- Acknowledgments
iation (Abrams 2000). Movement ecology demonstrates how I am honored to have been selected by the American Society
both predators and prey interact in a landscape driven by spatial of Mammalogists for the C. Hart Merriam Award. I thank my
variation in both energy resources and risk (Fortin et al. 2005a, students for field study and data analysis including H. Beyer,
2005b; Harvey and Fortin 2013; Gallagher et al. 2017). For D. Fortin, J. M. Gaillard, C. J. Johnson, J. S. Mao, A. T.
example, vegetation resources attract elk to riparian habitats and Morehouse, J. Sauer, and N. Varley. I am indebted to col-
aspen stands, but these can be risky places because wolves are leagues for insights and collaboration: J. Fryxell, D. Houston,
able to approach and kill prey in these areas (Fortin et al. 2005a; M. Haroldson, N. T. Hobbs, M. J. Kauffman, D. R. McNulty, L. D.
Bergman et al. 2006; Beyer 2006; Ripple and Beschta 2012). Mech, E. H. Merrill, B. Patterson, J. Peek, G. Plumb, P. Turchin,
In addition, site variation in topography and hydrology create M. G. Turner, R. O. Peterson, A. R. E. Sinclair, D. W. Smith,
variation in soil moisture that has a large influence on growth J. Varley, and P. J. White. Thanks to J. Mao, D. Fortin, N. Varley,
of vegetation and thereby the attractiveness of sites to herbi- and E. Heske for helpful review comments on the manuscript.
vores (Fortin et al. 2005b; Tercek et al. 2010; Brodie et al. 2012; Funding has been provided by the Campfire Conservation Fund,
Marshall et al. 2013; Frank et al. 2017; Raynor et al. 2017). National Park Service, National Science Foundation (grant
The interplay between predator–prey interactions and spatial #0078130), Alberta Conservation Association, Natural Sciences
heterogeneity includes important connections to scale (Boyce and Engineering Research Council of Canada (grant #364323-
et al. 2003, 2017). Classic studies of predator–prey interac- 07), Safari Club International, University of Wyoming, and
tions showed how spatial heterogeneity can stabilize popula- University of Alberta.
tion dynamics and enhance persistence (Huffaker 1958), as
we observed when modeling multiple wolf–ungulate popula-
Literature Cited
tions in the Greater Yellowstone (Boyce and Gaillard 1992).
Abrams, P. A. 2000. The impact of habitat selection on the spatial
Yet, at finer scales in Yellowstone, we have seen trophic-level
heterogeneity of resources in varying environments. Ecology
interactions amplifying spatial heterogeneity through a trophic
81:2902–2913.
cascade. Movement among foraging patches might constitute Abrams, P. A., and T. B. Allison. 1982. Complexity, stability, and
a “shell game” by bison (Harvey and Fortin 2013) and elk functional response. American Naturalist 119:240–249.
(Boyce et al. 2003; Seidel and Boyce 2016) to avoid wolves, Barber-Meyer, S. M., L. D. Mech, and P. J. White. 2008. Elk calf
another mechanism amplifying spatial and temporal variation survival and mortality following wolf restoration to Yellowstone
in herbivory. The Huffaker effect applies to wolf–ungulate sys- National Park. Wildlife Monographs 169:1–30.
tems at large scales, where some subpopulations might wink Barmore, W. J. 2003. Ecology of ungulates and their win-
in and out (e.g., Isle Royale and Michipicoten Island in Lake ter range in northern Yellowstone National Park: research and
 MERRIAM AWARD PAPER—WOLVES FOR YELLOWSTONE 1029

synthesis, 1962–1970. Yellowstone Center for Resources, Boyce, M. S., and J.-M. Gaillard. 1992. Wolves in Yellowstone,
Mammoth, Wyoming. Jackson Hole, and the North Fork of the Shoshone River: simu-
Bartos, D. L., and W. F. Mueggler. 1979. Influence of fire on veg- lating ungulate consequences of wolf recovery. Pp. 4/71–4/111 in
etation production in the aspen ecosystem in western Wyoming. Wolves for Yellowstone? A report to the United States Congress,
Pp. 75–79 in North American elk: ecology, behavior and manage- vol. 4. Research and analysis (J. D. Varley and W. G. Brewster,
ment (M. S. Boyce and L. D. Hayden-Wing, eds.). University of eds.). National Park Service, Yellowstone National Park, Mammoth,
Wyoming, Laramie. Wyoming.
Beetle, A. A. 1979. Jackson Hole elk herd: a summary after 25 years Boyce, M. S., D. I. MacKenzie, B. F. J. Manly, M. Haroldson,
of study. Pp. 259–262 in North American elk: ecology, behavior and D. Moody. 2001b. Negative binomial models for abundance
and management (M. S. Boyce and L. D. Hayden-Wing, eds.). estimation of multiple closed populations. Journal of Wildlife
University of Wyoming, Laramie. Management 65:498–509.
Bergman, E. J., R. A. Garrott, S. Creel, J. J. Borkowski, R. Jaffe, Boyce, M. S., C. Mallory, A. Morehouse, C. Prokopenko,

Downloaded from https://academic.oup.com/jmammal/article/99/5/1021/5107035 by guest on 21 August 2023

and F. G. R. Watson. 2006. Assessment of prey vulnerability M. Scrafford, and C. Warbington. 2017. Defining landscapes
through analysis of wolf movements and kill sites. Ecological and scales to model landscape–organism interactions. Current
Applications 16:273–284. Landscape Ecology Reports 2:89–95.
Beschta, R. L. 2005. Reduced cottonwood recruitment following Boyce, M. S., et al. 2003. Scale and heterogeneity in habitat selec-
extirpation of wolves in Yellowstone’s Northern Range. Ecology tion by elk in Yellowstone National Park. Écoscience 10:421–431.
86:391–403. Boyce, M. S., et al. 2010. Temporal autocorrelation functions for
Beschta, R. L., and W. J. Ripple. 2016. Riparian vegetation recov- movement rates from global positioning system radiotelem-
ery in Yellowstone: the first two decades after wolf reintroduction. etry data. Philosophical Transactions of the Royal Society B
Biological Conservation 198:93–103. 365:2213–2219.
Beyer, H. L. 2006. Wolves, elk and willow on Yellowstone’s National Carbyn, L. N. 1980. Ecology and management of wolves in Riding
Park’s Northern Range. M.Sc. thesis, University of Alberta, Mountain National Park, Manitoba. Canadian Wildlife Service,
Edmonton, Alberta, Canada. Edmonton, Alberta, Canada.
Beyer, H. L., E. H. Merrill, N. Varley, and M. S. Boyce. 2007. Carbyn, L. N., and T. Trottier. 1987. Responses of bison on their
Willow on Yellowstone’s Northern Range: evidence for a trophic calving grounds to predation by wolves in Wood Buffalo National
cascade? Ecological Applications 17:1563–1571. Park. Canadian Journal of Zoology 65:2072–2078.
Bilyeu, D. M., D. J. Cooper, and N. T. Hobbs. 2008. Water tables con- Creel, S., and D. Christianson. 2009. Wolf presence and increased
strain height recovery of willow on Yellowstone’s Northern Range. willow consumption by Yellowstone elk: implications for trophic
Ecological Applications 18:80–92. cascades. Ecology 90:2454–2466.
Brodie, J., E. Post, F. Watson, and J. Berger. 2012. Climate Cubaynes, S., D. R. MacNulty, D. R. Stahler, K. A. Quimby, D.
change intensification of herbivore impacts on tree recruitment. W. Smith, and T. Coulson. 2014. Density-dependent intraspe-
Proceedings of the Royal Society B 279:1366–1370. cific aggression regulates survival in northern Yellowstone wolves
Boyce, M. S. 1989. The Jackson elk herd: intensive wildlife manage- (Canis lupus). Journal of Animal Ecology 83:1344–1356.
ment in North America. Cambridge University Press, Cambridge, Despain, D., D. Houston, M. Meagher, and P. Schullery. 1986.
United Kingdom. Wildlife in transition: man and nature on Yellowstone’s Northern
Boyce, M. S. 1990. Wolf recovery for Yellowstone National Park: Range. Roberts Rinehart, Boulder, Colorado.
a simulation model. Pp. 3–5 to 3–58 in Wolves for Yellowstone? Elbroch, L. M., P. E. Lendrum, J. Newby, H. Quigley, and D.
A report to the United States Congress, vol. 2. Research and anal- J. Thompson. 2015. Recolonizing wolves influence the realized
ysis (J. D. Varley and S. H. Fritts, eds.). National Park Service, niche of resident cougars. Zoology Studies 54:41.
Yellowstone National Park, Mammoth, Wyoming. Estes, J. A., et al. 2011. Trophic downgrading of planet earth.
Boyce, M. S. 1991. Natural regulation or the control of nature. Science 333:301–306.
Pp. 183–208 in The greater Yellowstone ecosystem: redefining Evans, S., L. D. Mech, P. J. White, and G. A. Sergeant. 2006.
America’s wilderness heritage (R. B. Keiter and M. S. Boyce, Survival of adult female elk in Yellowstone following wolf restora-
eds.). Yale University Press, New Haven, Connecticut. tion. Journal of Wildlife Management 70:1372–1378.
Boyce, M. S. 1992. Intervention versus natural regulation philosophies Ford, A. T., and J. R. Goheen. 2015. Trophic cascades by large car-
for managing wildlife in national parks. Oecologia Montana 1:49–50. nivores: a case for strong inference and mechanism. Trends in
Boyce, M. S. 1995. Anticipating consequences of wolves in Ecology and Evolution 30:725–735.
Yellowstone: model validation. Pp. 199–209 in Ecology and con- Forester, J. D., et al. 2007. State-space models link elk movement to
servation of wolves in a changing world (L. Carbyn, S. Fritts, and landscape characteristics in Yellowstone National Park. Ecological
D. Seip, eds.). Canadian Circumpolar Institute, Edmonton, Alberta, Monographs 77:285–299.
Canada. Fortin, D., H. Beyer, M. S. Boyce, D. W. Smith, and J. S. Mao.
Boyce, M. S. 1998. Ecological-process management and ungulates: 2005a. Wolves influence elk movements: behavior shapes a trophic
Yellowstone’s conservation paradigm. Wildlife Society Bulletin cascade in Yellowstone National Park. Ecology 86:1320–1330.
26:391–398. Fortin, D., J. M. Morales, and M. S. Boyce. 2005b. Elk winter
Boyce, M. S. 2005. Wolves are consummate predators. Quarterly foraging at fine scales in Yellowstone National Park. Oecologia
Review of Biology 80:87–92. 145:335–343.
Boyce, M. S., B. M. Blanchard, R. R. Knight, and C. Servheen. Frank, D. A., R. L. Wallen, E. W. Hamilton III, P. J. White, and J.
2001a. Population viability for grizzly bears: a critical review. D. Fridley. 2017. Manipulating the system: how large herbivores
International Association for Bear Research and Management, control bottom-up regulation of grasslands. Journal of Ecology
Monograph Series No. 4. 106:434–443.
1030 JOURNAL OF MAMMALOGY

Frank, D. A., R. L. Wallen, and P. J. White. 2016. Ungulate con- Marshal, J. P., and S. Boutin. 1999. Power analysis of wolf-moose
trol of grassland production: grazing intensity and ungulate species functional responses. Journal of Wildlife Management 63:396–402.
composition in Yellowstone Park. Ecosphere 7:e01603. Marshall, K. N., N. T. Hobbs, and D. J. Cooper. 2013. Stream
Gallagher, A. J., S. Creel, R. P. Wilson, and S. J. Cooke. 2017. hydrology limits recovery of riparian ecosystems after wolf rein-
Energy landscapes and the landscape of fear. Trends in Ecology & troduction. Proceedings Royal Society B 280:20122977.
Evolution 32:88–96. Maynard Smith, J. 1974. Models in ecology. Cambridge University
Garton, E. O., R. L. Crabtree, B. B. Ackerman, and G. Wright. Press, Cambridge, United Kingdom.
1990. The potential impact of a reintroduced wolf population on Mech, L. D. 1970. The wolf: the ecology and behavior of an endan-
the northern Yellowstone elk herd. Pp. 3–59 to 3–91 in Wolves gered species. Natural History Press, Garden City, New York.
for Yellowstone? A report to the United States Congress, vol. Mech, L. D. 2012. Is science in danger of sanctifying the wolf?
2. Research and analysis (J. D. Varley and S. H. Fritts, eds.). Biological Conservation 150:143–149.
National Park Service, Yellowstone National Park, Mammoth, Merrill, E. H., and M. S. Boyce. 1991. Summer range and elk pop-

Downloaded from https://academic.oup.com/jmammal/article/99/5/1021/5107035 by guest on 21 August 2023

Wyoming. ulation dynamics in Yellowstone National Park. Pp. 263–273 in
Griffin, K. A., et al. 2011. Neonatal mortality of elk driven by cli- The greater Yellowstone ecosystem: redefining America’s wilder-
mate, predator phenology and predator community composition. ness heritage (R. B. Keiter and M. S. Boyce, eds.). Yale University
Journal of Animal Ecology 80:1246–1257. Press, New Haven, Connecticut.
Gruell, G. E. 1979. Wildlife habitat investigations and management Merrill, E. H., M. K. Bramble-Brodahl, R. W. Marrs, and M.
implications on the Bridger-Teton National Forest. Pp. 63–74 in North S. Boyce. 1993. Estimation of green herbaceous phytomass from
American elk: ecology, behavior and management (M. S. Boyce and Landsat MSS data in Yellowstone National Park. Journal of Range
L. D. Hayden-Wing, eds.). University of Wyoming, Laramie. Management 46:151–156.
Harvey, L., and D. Fortin. 2013. Spatial heterogeneity in the strength Morehouse, A. T., and M. S. Boyce. 2011. From venison to beef:
of plant-herbivore interactions under predation risk: the tale of seasonal changes in wolf diet composition in a livestock grazing
bison foraging in wolf country. PLoS ONE 8:e73324. landscape. Frontiers in Ecology and the Environment 9:440–445.
Hobbs, N. T., and D. J. Cooper. 2013. Have wolves restored ripar- Muhly, T., M. Hebblewhite, M. S. Boyce, D. Paton, J. A. Pitt, and
ian willows in northern Yellowstone? Pp. 179–194 in Yellowstone’s M. Musiani. 2013. Humans strengthen bottom-up effects and weaken
wildlife in transition (P. J. White, R. A. Garrott, and G. E. Plumb, trophic cascades in a terrestrial food web. PLoS ONE 8:e64311.
eds.). Harvard University Press, Cambridge, Massachusetts. National Research Council (NRC). 2002. Ecological dynam-
Houston, D. B. 1982. The northern Yellowstone elk: ecology and ics on Yellowstone’s Northern Range. National Academy Press,
management. Macmillan, New York. Washington, D.C.
Huffaker, C. B. 1958. Experimental studies on predation: dispersion Painter, L. E., R. L. Beschta, E. J. Larsen, and W. J. Ripple. 2015.
factors and predator-prey oscillations. Hilgardia 27:795–835. Recovering aspen follow changing elk dynamics in Yellowstone:
Kauffman, M. J., J. F. Brodie, and E. S. Jules. 2010. Are wolves sav- evidence of a trophic cascade? Ecology 96:252–263.
ing Yellowstone’s aspen? A landscape-level test of a behaviorally Pimlott, D. H. 1967. Wolf predation and ungulate populations.
mediated trophic cascade. Ecology 91:2742–2755. American Zoologist 7:267–278.
Kauffman, M. J., J. F. Brodie, and E. S. Jules. 2013. Are wolves sav- Raynor, E. J., H. L. Beyer, J. M. Briggs, and A. Joern. 2017.
ing Yellowstone’s aspen? A landscape-level test of a behaviorally Complex variation in habitat selection strategies among individuals
mediated trophic cascade: reply. Ecology 94:1425–1431. driven by extrinsic factors. Ecology and Evolution 7:1802–1822.
Kauffman, M. J., N. Varley, D. W. Smith, D. R. Stahler, D. Ripple, W. J., and R. L. Beschta. 2012. Trophic cascades in
R. MacNulty, and M. S. Boyce. 2007. Landscape heterogene- Yellowstone: the first 15 years after wolf reintroduction. Biological
ity shapes predation in a newly restored predator–prey system. Conservation 145:205–213.
Ecology Letters 10:690–700. Ripple, W. J., E. J. Larsen, R. A. Renkin, and D. W. Smith. 2001. Trophic
Kimble, D. S., D. B. Tyers, J. Robison-Cox, and B. F.Sowell. cascades among wolves, elk, and aspen on Yellowstone National
2011. Aspen recovery since wolf reintroduction on the northern Park’s Northern Range. Biological Conservation 102:227–234.
Yellowstone winter range. Rangeland Ecology and Management Romme, W. H., M. G. Turner, L. L. Wallace, and J. S. Walker.
64:119–130. 1995. Aspen, elk and fire on the Northern Range of Yellowstone
Kohl, M. T., et al. 2018. Diel predator activity drives a dynamic National Park. Ecology 76:2097–2106.
landscape of fear. Ecological Monographs. doi:10.1002/ecm.1313 Romme, W. H., et al. 2011. Twenty years after the 1988 Yellowstone
Leopold, A. S., S. A. Cain, C. M. Cottam, I. N. Gabrielson, and fires: lessons about disturbance and ecosystems. Ecosystems
T. L. Kimball. 1963. Wildlife management in the national parks. 14:1196–1215.
Transactions of the North American Wildlife and Natural Resources Rose, J. R., and D. J. Cooper. 2017. The influence of floods and her-
Conference 28:28–45. bivory on cottonwood establishment and growth in Yellowstone
Lukacs, P. M., et al. 2018. Factors influencing elk recruitment National Park. Ecohydrology 10:e1768.
across ecotypes in the western United States. Journal of Wildlife Sauer, J. R., and M. S. Boyce. 1983. Density-dependence and survival
Management 82:698–710. of elk in Northwestern Wyoming. Journal of Wildlife Management
MacNulty, D. R., D. R. Stahler, C. T. Wyman, J. Ruprecht, and 47:31–37.
D. W. Smith. 2016. The challenge of understanding northern Schullery, P. 2003. The Yellowstone wolf: a guide and sourcebook.
Yellowstone elk dynamics after wolf reintroduction. Yellowstone University of Oklahoma Press, Norman.
Science 24:25–33. Seidel, D., and M. S. Boyce. 2016. Varied tastes: home range impli-
Mao, J. S., et al. 2005. Habitat selection by elk before and after wolf cations of foraging patch selection. Oikos 125:39–49.
reintroduction in Yellowstone National Park. Journal of Wildlife Sikes, R. S., and the Animal Care and Use Committee of the
Management 69:1691–1707. American Society of Mammalogists. 2016. 2016 Guidelines
 MERRIAM AWARD PAPER—WOLVES FOR YELLOWSTONE 1031

of the American Society of Mammalogists for the use of wild Van Manen, F. T., et al. 2016. Density dependence, whitebark pine,
mammals in research and education. Journal of Mammalogy and vital rates of grizzly bears. Journal of Wildlife Management
97:663–688. 80:300–313.
Sinclair, A. R. E. 1983. Management of conservation areas as eco- Varley, N. 2007. Gray wolf (Canis lupus) effects on ecological com-
logical baseline controls. Pp. 13–22 in Management of large munities. Ph.D. dissertation, University of Alberta, Edmonton,
mammals in African conservation areas (R. N. Owen-Smith, ed.). Alberta, Canada.
Haum, Pretoria, South Africa. Varley, N., and M. S. Boyce. 2006. Adaptive management for reintro-
Singer, F. J., A. Harting, K. K. Symonds, and M. B. Coughenour. ductions: updating a wolf recovery model for Yellowstone National
1997. Density dependence, compensation and environmental Park. Ecological Modelling 193:315–339.
effects on elk calf mortality in Yellowstone National Park. Journal Vucetich, J. A., D. W. Smith, and D. R. Stahler. 2005. Influence
of Wildlife Management 61:12–25. of harvest, climate, and wolf predation on Yellowstone elk, 1961–
Smith, D. W., and G. Ferguson. 2012. Decade of the wolf, revised 2004. Oikos 111:259–270.

Downloaded from https://academic.oup.com/jmammal/article/99/5/1021/5107035 by guest on 21 August 2023

and updated: returning the wild to Yellowstone. Globe Pequot Walters, C. J. 1986. Adaptive management of renewable resources.
Press/Lyon Press, Guilford, Connecticut. Macmillan, New York.
Tallian, A., et al. 2017. Competition between apex predators? Weaver, J. 1978. The wolves of Yellowstone. Natural resources report
Brown bears decrease wolf kill rate on two continents. Proceedings no. 14. National Park Service, United States Government Printing
Royal Society B 284:20162368. Office, Washington, D.C.
Taper, M. L., and P. J. P. Gogan. 2002. The northern Yellowstone elk: White, P. J., and R. A. Garrott. 2005. Yellowstone’s ungulates after
density dependence and climatic conditions. Journal of Wildlife wolves—expectations, realizations, and predictions. Biological
Management 66:106–122. Conservation 125:141–152.
Terborgh, J., and J. A. Estes. 2010. Trophic cascades: predators, prey, White, P. J., R. A. Garrott, and G. E. Plumb. 2013. Ecological proc-
and the changing dynamics of Nature. Island Press, Washington, ess management. Pp. 3–9 in Yellowstone’s wildlife in transition (P.
D.C. J. White, R. A. Garrott, and G. E. Plumb, eds.). Harvard University
Tercek, M. T., R. Stottlemyer, and R. Renkin. 2010. Bottom-up fac- Press, Cambridge, Massachusetts.
tors influencing riparian willow recovery in Yellowstone National Wolf, C., and W. J. Ripple. 2018. Rewilding the world’s large carni-
Park. Western North American Naturalist 70:387–399. vores. Royal Society Open Science 5:172235.
T hurfjell , H., S. C iuti , and M. S. B oyce . 2017. Learning Wright, G. J., R. O. Peterson, D. W. Smith, and T. O. Lemke. 2006.
from the mistakes of others: how female elk (Cervus ela- Selection of northern Yellowstone elk by gray wolves and hunters.
phus) adjust behaviour with age to avoid hunters. PL o S ONE Journal of Wildlife Management 70:1070–1078.
12:e0178082.
Uboni, A., D. W. Smith, J. S. Mao, D. R. Stahler, and J. A. Vucetich. Submitted 13 July 2018. Accepted 5 September 2018.
2015. Long- and short-term temporal variability in habitat selec-
tion of a top predator. Ecosphere 6:51. Associate Editor was Edward Heske.