vol. 185, no. 6

the american naturalist

june 2015

Natural History Note

The Comparative Effects of Large Carnivores
on the Acquisition of Carrion by Scavengers
Maximilian L. Allen,1,* L. Mark Elbroch,2 Christopher C. Wilmers,3 and Heiko U. Wittmer1
1. School of Biological Sciences, Victoria University of Wellington, P.O. Box 600, Wellington 6140, New Zealand; 2. Panthera, New York,New York 10018; 3. Center for Integrated Spatial Research, Environmental Studies Department, University of California, Santa Cruz,
California 95064
Submitted April 21, 2014; Accepted December 18, 2014; Electronically published March 19, 2015
Online enhancements: videos. Dryad data: http://dx.doi.org/10.5061/dryad.dh2vr.

abstract: Pumas (Puma concolor) and black bears (Ursus americanus) are large carnivores that may inﬂuence scavenger population
dynamics. We used motion-triggered video cameras deployed at deercarcasses to determine how pumas and black bears affected three
aspects of carrion acquisition by scavengers: presence, total feeding
time, and mean feeding-bout duration. We found that pumas wereunable to limit acquisition of carrion by large carnivores but did limit
aspects of carrion acquisition by both birds and mesocarnivores.
Through their suppression of mesocarnivores and birds, pumas apparently initiated a cascading pattern and increased carrion acquisition by small carnivores. In contrast, black bears monopolized carrion resources and generally had larger limiting effects on carrion
acquisition by all scavengers. Black bears also limited puma feeding
behaviors at puma kills, which may require pumas to compensate
for energetic losses through increasing their kill rates of ungulates.
Our results suggest that pumas provide carrion and selectively inﬂuence species acquiring carrion, while black bears limit carrion availability to all other scavengers. These results suggest that the effectsof large carnivores on scavengers depend on attributes of both carnivores and scavengers (including size) and that competition for carcasses may result in intraguild predation as well as mesocarnivore
release.
Keywords: carrion acquisition, competition, energy distribution, mesocarnivore, Puma concolor, scavenging, Ursus americanus.

Introduction
The effects of large carnivores in structuring ecological communities, including initiating trophic cascades, are well established (Estes and Palmisano 1974; Ripple et al. 2014).
For example, by suppressing smaller carnivores, large carnivores have been shown to indirectly inﬂuence abundances* Corresponding author. Present address: Center for Integrated Spatial Research, Environmental Studies Department, 1156 High Street, University ofCalifornia, Santa Cruz, California 95064; e-mail: maxallen@ucsc.edu.
Am. Nat. 2015. Vol. 185, pp. 822–833. q 2015 by The University of Chicago.
0003-0147/2015/18506-55435$15.00. All rights reserved.
DOI: 10.1086/681004

of other species, including birds and herbivores (Estes andPalmisano 1974; Rogers and Caro 1998; Courchamp et al.
1999; Prugh et al. 2009). Large carnivores also have cascading effects solely on other carnivores; increases in graywolves (Canis lupus) in Minnesota resulted in suppressionof coyotes (Canis latrans), which in turn allowed an increase in smaller red foxes (Vulpes vulpes; Levi and Wilmers 2012). Within their respective communities, large carnivores are thought to exert population-level inﬂuenceson other species, either directly via predation or indirectly
as a result of behavioral changes to avoid predation that result in lower ﬁtness (Sargeant et al. 1987; Ripple et al. 2001,
2014; Ripple and Beschta 2004; Atwood et al. 2007). An underappreciated mechanism by which large carnivores might
affect ecological communities is through their interactions
with scavengers at carcasses, where they may increase accessto carrion resources for some species and restrict access forothers.
Scavenging is a widespread behavior whereby species
compete for limited resources in order to gain nutritional
beneﬁts and increase individual ﬁtness (Houston 1995;
DeVault et al. 2003; Selva et al. 2003; Wilson and Wilkovich 2011). For example, numerous facultative scavengers
use scavenging to increase their breeding success (e.g., Angerbjörn et al. 1991; Watson et al. 1992). In addition, recent
studies have highlighted the importance of scavenging toecosystem function and the transfer of energy between
trophic levels (DeVault et al. 2003; Selva and Fortuna 2007;
Wilson and Wolkovich 2011). Carcasses also appear to provide frequent opportunities for interactions among carnivores, and these interactions result in complex ecologicalrelationships and resource partitioning (Root 1967; Houston 1995; Selva and Fortuna 2007).
Large carnivores not only provide carrion but also play
an important role in how carrion is distributed amongscavengers (e.g., Wilmers et al. 2003a; Elbroch and Wittmer 2012; Moleón et al. 2014). For example, large carni-

Large-Carnivore Effects on Scavengers
vores provide carrion throughout the year, rather than in
the seasonal pulses characteristic of anthropogenic sources(Wilmers et al. 2003b). In addition to providing carrion,
large carnivores are also capable of opening carcasses, allowing other species access to edible portions of the carcass (Selva et al. 2003). Large carnivores, however, also directly limit scavenger species at their kills and, throughcompetition, limit the availability of carrion for other obligate and facultative scavengers when they themselves arescavenging (Hunter et al. 2006; Allen et al. 2014b).
Within western North American ecological communities, both pumas (Puma concolor) and black bears (Ursus
americanus) are large carnivores that have the potential
to affect other scavengers. Pumas are solitary predators thatfrequently kill ungulates while only occasionally scavenging themselves (Bauer et al. 2005; Knopff et al. 2010), andby regularly killing ungulates and other prey they act as
an important source of carrion to scavenger communities(Elbroch and Wittmer 2012; Allen et al. 2014b). In contrast, black bears frequently kill newborn ungulates (Pelton1982) but rarely kill adults (Svoboda et al. 2011). Therefore,
black bears rarely provide carrion for scavengers and areinstead a dominant scavenger of ungulates, including puma
kills (Murphy et al. 1998; Ruth and Murphy 2010; Allenet al. 2014b). The inﬂuence of black bears on the acquisitionof carrion by other scavengers, however, has been understudied.
The effects pumas and black bears have on the acquisition of carrion by scavengers is likely species speciﬁc. Previous research has shown that some scavengers access andexploit carrion better than others, as a result of differences
in morphology and behaviors (Root 1967; Hertel 1994;
Houston 1995; Cortés-Avizanda et al. 2012). Here, we evaluated the potential inﬂuences of competition on scavenging behaviors instead, and we attempted to determine how
pumas and black bears affect the acquisition of carrion by
scavenger classes and species. To address this question, we
conducted a series of in situ experiments at black-tailed deer
(Odocoileus hemionus columbianus) carcasses, comparing
carrion acquisition at puma kills (video 1; videos 1–3 available online) to that at matching control carcasses and at a
separate set of experimental carcasses where black bears
were either present or absent. Speciﬁcally, we analyzed three
aspects of carrion acquisition exhibited by each scavenger
species: presence or absence at carcasses, total feeding time,and mean feeding-bout duration. We used presence as aproxy of the ability of scavengers to acquire energy from agiven carcass, and we used total feeding time as a proxy forthe amount of energy a scavenger was able to gain from agiven carcass. Last, we used mean feeding-bout duration
as a proxy for the effects of predation risk perceived by scavengers, because we hypothesized that a scavenger should exhibit shorter feeding bouts at carcasses with higher per-823

Video 1: Still photograph from a video, available online, showing amale puma feeding on a black-tailed deer it killed.

ceived risk (Charnov 1976; video 2). We hypothesizedthat pumas and black bears would limit each aspect of carrion acquisition for all scavengers but that there would bevariation in the magnitude of their limitation based on the
body size of scavenger species.
Previous research demonstrated that pumas are subordinate to other large carnivores, including gray wolves, grizzly bears (Ursus arctos), jaguars (Panthera onca), and sometimes coyotes (Canis latrans; Ruth and Murphy 2010). We
thus expected pumas to have a small effect on the acquisition of carrion by large carnivores. However, pumas are
known to regularly kill smaller carnivores, and both mesocarnivores and small carnivores are present in the diet ofpumas across much of their distribution (Murphy and Ruth
2010). Because of their dominance over mesocarnivores andsmall carnivores, we expected pumas to limit all three aspects of carrion acquisition by these classes. Pumas are also
known to exhibit behaviors to minimize carcass detection
by avian species, including caching of kills and moving kills
to areas of dense overhead cover (Bischoff-Mattson and Mattson 2009; Ruth and Murphy 2010; Allen et al. 2015). Because of these behaviors, we expected pumas to limit theacquisition of carrion by avian scavengers, mainly by limiting their presence.
Black bears are capable of rapidly eating large amounts
of food (video 3), including carrion, and their large bodysize allows them to exclude other species from carrion (Murphy et al. 1998; Allen et al. 2014b). On the basis of theseobservations, we hypothesized that black bears would be capable of monopolizing carrion resources, thereby limiting
the presence and total feeding time of other scavengers. Despite their large size and occasional predation, black bears
rarely kill other carnivores (Pelton 1982; Larivière 2001).

824

The American Naturalist

Video 2: Still photograph from a video, available online, showing
an interaction between scavengers, where a gray fox ﬂees from anapproaching bobcat.

This suggests that other scavengers are not frequently indanger of injury or death from scavenging black bears,
and we therefore hypothesize that black bears would havesmall limitations on mean feeding-bout duration of otherscavengers.
Methods
Study Area
We conducted our study in the Mendocino National Forest,
California. The study area encompassed approximately
1,000 km2 (ﬁg. 1). The area was primarily forested, with elevations ranging from 396 to 2,466 m and the majority of
precipitation occurring from December through March.
The habitat and meteorological aspects of the study area
have been described in detail elsewhere (Allen et al. 2014a).
Black bears occurred at high population densities despitehunting pressure (Forrester 2014). Pumas were legally protected from hunting, occurred at low population densities,
and were the only predator in the system known to frequently
kill adult ungulates (Allen et al. 2014a). Black-tailed deer
were the most common large-ungulate prey of pumas, whilewild pigs (Sus scrofa) and tule elk (Cervus elaphus nannodes)
were present at very low densities but were not preyed on bypumas (Allen et al. 2014a). Intraguild predation by pumas
was noted in the study area, with pumas killing black bears,
coyotes, gray foxes, and raccoons (Allen et al. 2015).

compare scavenger activity at different types of black-tailed
deer carcasses. Because of the different spatial scales thatcan determine the scavenger assemblage present at a carcass, we designed our study to account for spatial characteristics and autocorrelation by determining the carcass location on the basis of habitat. For pumas, we compared theacquisition of carrion by scavengers at kills made by pumas(n p 58) to that at control carcasses (n p 58) with matching
habitat characteristics that we placed simultaneously on thelandscape. For black bears, we distributed black-tailed deercarcasses in varied habitats across the study area and compared scavenger carrion acquisition at carcasses where blackbears were present (n p 33) to that at carcasses where they
were absent (n p 46). For puma control carcasses and theblack bear experiments, we used black-tailed deer killed
through vehicle collisions that were fresh and in good condition, allowing us to replicate the freshness and decomposition state of actual puma kills.
Between June 2010 and December 2012, we captured
seven pumas and ﬁtted them with a combined ARGOS satellite GPS/radio telemetry collar (Lotek 7000SAW, New
Market, ON; Allen et al. 2014a). In order to ﬁnd fresh puma
kills, we downloaded the location data via satellite connection every 3 days and investigated any GPS clusters wherea monitored puma had spent at least 2 h within 150 m andappeared to still be present on the same day as the Argosrelayed GPS downloads (Allen et al. 2014b). We approachedthese potential feeding sites during midday, when pumas
were least active, conﬁrmed their continued presence withvery-high-frequency telemetry, and limited the duration of
our visits at the site in order to limit disturbance of thepuma and avoid possible carcass abandonment. We secured the carcass with a wire cable to hold it within 1 m ofExperimental Design and Field Methods
From January 2010 to November 2012, we used motiontriggered video cameras with infrared ﬂash to record andVideo 3: Still photograph from a video, available online, showing a
black bear scavenging on the carcass of a black-tailed deer.

Large-Carnivore Effects on Scavengers

825

Figure 1: Map of the study area in Mendocino National Forest. Each carcass type is noted on the map to show the distribution, within thegreater context of the Northern Coast Ranges.

its location for monitoring and then deployed a motiontriggered camera (Bushnell ScoutCam, Overland Park, KS)
to document the feeding behaviors of scavengers at the kill.
We set the motion-triggered cameras to record the maximum amount of activity, with 60 s of video recorded at eachtrigger and a pause of 1 s before becoming active at the next
trigger. We recorded the habitat characteristics of the site
and then found the site for the puma control carcass bymatching the habitat characteristics as closely as possible
to, in order of importance, (1) primary habitat type, (2) overhead tree species, (3) canopy cover, (4) secondary habitat
type, (5) distance to secondary habitat, and (6) elevation. Before arriving at the site of the control carcass, we prepared a
black-tailed deer carcass to provide an equivalent amountof meat in the same stage of decomposition as at the puma
kill and then secured the carcass and deployed anothercamera.
For the black bear experiments, we placed 100 blacktailed deer carcasses in a variety of habitats, in order to increase detection probabilities for all vertebrate scavengers
present in our study area. We secured each carcass in placewith a wire cable and monitored the carcass for scavenger feeding behaviors with a motion-triggered video cam-era with infrared ﬂash (Cuddeback IR, De Pere, WI). We
set the motion-triggered cameras to record the maximum
amount of activity, with 30 s of video and a pause of 60 s
before the next trigger. In order to understand the possible
effects of black bears on other scavengers, we divided carcasses into those where black bears were “present” (deﬁned
as carcasses at which they were the ﬁrst or second scavenger to arrive) and those where black bears were “absent”(deﬁned as carcasses at which they were either completely
absent or one of the last scavengers to arrive and at which
they spent ≤10 min). We removed carcasses from our analyses (1) when black bears had an unknown inﬂuence (i.e.,
when they were the third or later scavenger to arrive andspent 110 min at the carcass; n p 10) or (2) when carcasses
had incomplete data because of camera malfunctions orcamera displacements by black bears (n p 11).
Statistical Analyses
To determine the inﬂuences of pumas and black bears on
scavengers, we considered three aspects of carrion acquisition: “presence,” “total feeding time,” and “mean feedingbout duration.” Presence was calculated as the percentage

826

The American Naturalistof carcasses at which each scavenger species or class wasrecorded. We calculated the duration of a given feeding
bout by subtracting the time at the start of a visit fromthe time at the end of a visit. For visits of less than 30 s,
we considered the species or class present for 1 min rather
than 0 min, and we rounded all other visits to the closest
minute. Total feeding time was calculated as the sum of all
feeding bouts at a given carcass, and mean feeding-boutduration was calculated as the mean duration of all feeding bouts at a given carcass.
We used generalized linear models (GLMs) to analyzeeach aspect of carrion acquisition, using the program R(ver. 3.1.0; R Development Core Team 2014). The data
for these analyses are available in the Dryad Digital Repository (http://dx.doi.org/10.5061/dryad.dh2vr; Allen et al.
2015). In each analysis, we considered P ≤ .05 to be significant and P ≤ .1 to be marginally signiﬁcant. We ﬁrst tested
for the effects of pumas and black bears on scavenger species and then analyzed scavengers by classes, with each scavenger species placed into one of four classes according totheir body mass (table 1). We used each aspect of carrion
acquisition as our dependent variables and chose the appropriate distribution on the basis of the error residuals.
We used a binomial distribution with a logit link for presence, a Gamma distribution with a log link for total feeding time, and a Gaussian distribution with a log link formean feeding-bout duration. We used carcass type as our
ﬁrst independent variable (ﬁrst puma kill vs. control, thenblack bear present vs. absent). For our species analyses,
we also included the corresponding value of carrion acquisition by the other nine most frequent scavengers as independent variables. For our class analyses, we included thecorresponding value of carrion acquisition by the threeother classes. Finally, we analyzed the effects of black bears
on pumas, including puma carrion acquisition and feedingat their own kills. At puma kills, we compared puma total
feeding time and mean feeding-bout duration before andafter the arrival of black bears. We used puma total feeding time and mean feeding-bout duration as the dependent variables and whether the feeding occurred before orafter bear arrival as the independent variable. As describedabove, we used a Gamma distribution with a log link for total feeding time and a Gaussian distribution with a log link
for mean feeding-bout duration.
Following these GLM analyses, we performed post hoc
Akaike information criterion (AIC; Akaike 1974) analyses
to determine the likely cause of the observed increased scavenging of small carnivores at puma kills. We used the GLM
analyses as described above, using each aspect of carrion acquisition as our dependent variable. For our predictor variables we used models for just pumas and for the mesocarnivore and avian classes combined and then compared
the AIC weights of the models to determine the top model.
Results
Between May 2011 and November 2012, we recorded
10,775 videos of animal activity at puma kills and 9,663
videos of animal activity at puma control carcasses. From
GPS data, pumas stayed within 150 m of 58 black-tailed deerkills we monitored for a mean of 75.1 (55.9 SE) h. We set up
cameras at puma kills a mean of 39.8 (52.9 SE) h after thepuma made the kill, and we set up the paired carcasses andcameras within a mean of 1.5 (50.2 SE) h after the camera
was set up at the puma kill.
Between January 2010 and November 2012, we recorded
3,039 videos of animal activity at carcasses where blackbears were present and 9,038 videos of animal activity at
carcasses where black bears were absent. Black bears detected carcasses a mean of 48.5 (512.1 SE) h after they
were placed in the landscape. Black bears had a mean total
feeding time of 105.9 (525.6 SE) min and a mean feedingbout duration of 4.8 (50.9 SE) min.
Effects of Pumas on Scavengers
Pumas had mixed effects on the three aspects of acquisitionof carrion by speciﬁc scavenger classes and species at theirkills (table 2). Pumas did not limit large carnivores overall,
but among large carnivores, pumas signiﬁcantly limited thepresence of domestic dogs (z114 p 22.40, P p .0166) andmarginally limited the presence of coyotes and the mean

Table 1: Species for each scavenger class
Scavenger class

Scavenger species

Large carnivore
Mesocarnivore
Small carnivore
Avian

Black bear (Ursus americanus), coyote (Canis latrans), domestic dog (Canis familiaris), puma (Puma concolor)
Bobcat (Lynx rufus), ﬁsher (Martes pennanti), gray fox (Ucrocyon cinereoargenteus), raccoon (Procyon lotor)
Ringtail (Bassariscus astutus), striped skunk (Mephitis mephitis), western spotted skunk (Spirogale gracilis)
Bald eagle (Haliaeetus leucocephalus), common raven (Corvus corax), golden eagle (Aquila chrysaetos), greathorned owl (Bubo virginianus), northern goshawk (Accipiter gentilis), red-tailed hawk (Buteo jamaicensis),turkey vulture (Cathartes aura)

Note: Species composition for each of the four scavenger classes we tested for inﬂuences from pumas and black bears. Scavenger species were grouped intoclasses on the basis of their mass.

82.8
60.3
22.4
36.2

62.1
15.5
27.6
36.2
13.8
22.4
48.3
6.9
13.8
22.4

72.4
8.6
22.4
25.9
1.7
17.2
37.9
15.5
17.2
19.0

Control

79.3
44.8
25.9
37.9

Kill

.3852
.4126
.7715
.0796
.0166
.4637
.1454
.0680
.2564
.4568

.4052
.0845
.3213
.7972

P

145.9 (98.5–193.2)
7.8 (21.7 to 17.3)
29.1 (4.6–53.5)
8.0 (1.9–14.1)
7.0 (7.0–7.0)
8.3 (.2–16.5)
81.4 (11.0–151.9)
51.0 (220.2 to 122.2)
45.0 (226.1 to 116.1)
66.5 (27.8–105.1)

136.1 (90.3–181.8)
58.8 (29.7–87.8)
47.0 (7.7–86.3)
50.4 (43.6–57.2)

Kill

151.8 (81.2–222.3)
37.7 (234.0 to 109.3)
47.9 (21.9–73.8)
16.5 (6.6–26.3)
28.0 (2.3 to 56.3)
82.3 (2.2 to 164.9)
96.3 (48.8–143.9)
36.5 (21.6 to 74.6)
20.2 (23.8 to 44.2)
178.8 (57.3–300.2)

127.3 (72.4–182.3)
135.1 (93.3–177.0)
26.8 (5.6–48.0)
152.9 (65.9–239.8)

Control

Mean total feeding time in minutes (95% CI)

.5134
.0386
.7557
.2533
.6344
.0004
.0075
.1299
.0313
.2818

.6564
.0021
.4589
.0132

P

8.91 (6.64–11.18)
1.68 (.76–2.59)
3.07 (1.40–4.73)
1.46 (1.01–1.92)
1.40 (1.40–1.40)
1.95 (.47–3.43)
2.29 (1.68–2.89)
2.96 (1.73–4.19)
3.95 (2.68 to 8.58)
4.40 (2.12–6.68)

7.90 (5.84–9.96)
2.33 (1.73–2.93)
3.89 (.84–6.95)
3.28 (2.05–4.52)

Kill

13.78 (9.24–18.33)
1.22 (.93–1.51)
4.00 (2.49–5.51)
2.71 (1.59–3.82)
3.67 (1.04–6.30)
3.33 (2.12–4.55)
3.90 (2.98–4.82)
2.17 (1.16–3.18)
1.28 (.90–1.65)
8.32 (4.20–12.43)

8.99 (6.98–10.99)
3.77 (3.01–4.54)
1.53 (1.10–1.95)
5.56 (3.81–7.31)

Control

.0868
.8432
.6084
.4544
.9571
.2379
.0123
.6861
.0082
.3228

.6481
.0046
.2293
.0366

P

Mean feeding-bout duration in minutes (95% CI)

Note: We report the effects on scavenger classes and species for each variable at puma kills and control carcasses. We report the percentage of carcasses where a scavenger was present and the mean and 95%
conﬁdence intervals (CI) for total feeding time and mean feeding-bout duration. We also report the P value from our generalized linear models, with statistically signiﬁcant P values indicated by boldface.

Class:
Large carnivore
Mesocarnivore
Small carnivore
Avian
Species:
Black bear
BobcatCommon raven
CoyoteDomestic dog
FisherGray fox
RingtailSpotted skunk
Turkey vulture

Scavenger

Presence (%)

Table 2: Effects of pumas on three aspects of carrion acquisition by scavengers (presence, total feeding time, and mean feeding-bout duration)

828

The American Naturalist

feeding-bout duration of black bears (table 2). Pumas also
marginally limited the presence of mesocarnivores (table 2)
while signiﬁcantly decreasing both their total feeding time
(t60 p 23.22, P p .0021) and their mean feeding-bout duration (t60 p 22.95, P p .0046). Among mesocarnivores,
pumas signiﬁcantly limited the total feeding times of three
species, bobcat (t13 p 23.53, P p .0386), ﬁsher (t22 p
24.85, P p .0004), and gray fox (t49 p 22.82, P p .0075),
while also signiﬁcantly decreasing the mean feeding-boutduration of gray foxes (t49 p 22.63, P p .0123). Finally, pumas signiﬁcantly decreased the total feeding time of avian
scavengers (t42 p 22.60, P p .0132) as well as their mean
feeding-bout duration (t42 p 22.17, P p .0366).
Pumas apparently had positive effects on the acquisitionof carrion by small carnivores. For example, small-carnivore
total feeding time was 75% longer at puma kills than atcontrol carcasses, and their mean feeding-bout duration
was 2.6 times longer at puma kills than at control carcasses.
Among small carnivores, ringtails marginally increased theirpresence at puma kills (table 2), while spotted skunks signiﬁcantly increased their total feeding time (z17 p 2.61, P p.0313) and mean feeding-bout duration (z17 p 3.49, P p.0082). Using a post hoc AIC analyses, we found that the

combined effect of the presence of mesocarnivore and avian
classes was more important than the presence of pumas on
small-carnivore presence (wAIC [AIC weight] p 1.00 vs.
wAIC p 0.00). Total feeding times of mesocarnivores andavian scavengers were slightly better than puma presence
at explaining small-carnivore total feeding time (wAIC p
0.58 vs. wAIC p 0.42), while presence of pumas was muchbetter than the combined mean feeding-bout durations of
mesocarnivores and birds at explaining the mean feedingbout duration of small carnivores (wAIC p 0.81 vs. wAIC p0.19). This suggests that pumas may initiate a cascading effect among scavenger classes by limiting the presence andtotal feeding times of mesocarnivore and avian scavengers
and thus allowing small carnivores to increase access to carrion at their kills (ﬁg. 2).
Effects of Black Bears on Scavengers
Overall, black bears had a strong limiting inﬂuence on theacquisition of carrion by scavengers. In most cases, thelimitations exhibited by black bears were of a larger magnitude than those of pumas (table 3), but they did not signiﬁcantly limit the feeding-bout duration of any class or

Figure 2: Potential cascading effects initiated by pumas at their kills. Pumas limited the total feeding times and mean feeding-bout durationsof mesocarnivores and birds. By reducing carrion acquisition by these classes, pumas apparently allowed small carnivores to increase theiracquisition of carrion. Drawings provided courtesy of Yiwei Wang.

63.0
84.8
17.4
65.2
28.3
43.5
41.3
19.6
32.6
13.0
60.9
6.5
10.9
21.7

6.1
33.3
18.2
3.0
9.1
12.1
15.2
.0
.0
51.5

Absent

18.2
27.3
6.1
60.6

Present

.0397
.2477
.5106
.2077
.1312
.2409
.0021
.9971
.9980
.0440

.0021
!.0001
.8805
.1714

P

11.0 (28.6 to 30.6)
8.3 (3.3–13.2)
9.7 (21.3 to 20.6)
1.0 (1.0–1.0)
8.0 (3.1–12.9)
11.0 (24.2 to 26.2)
12.4 (3.4–21.4)...
...
65.2 (30.6–99.9)

10.0 (2.8 to 20.8)
6.1 (3.1–9.1)
1.0 (1.0–1.0)
50.4 (26.5–74.3)

Present

217.8 (108.2–327.4)
94.3 (19.1–169.5)
36.6 (20.4–52.7)
27.1 (24.0 to 58.2)
144.7 (20.4–269.0)
177.3 (57.1–297.6)
171.2 (66.9–275.4)
7.3 (22.3 to 17.0)
19.4 (24.1 to 42.9)
222.7 (110.0–335.4)

49.7 (23.8–75.5)
269.1 (167.1–371.2)
15.0 (.0–30.0)
180.8 (109.6–252.0)

Absent

P

.0128
.0043
.3144
.0799
.0603
.3102
.0016
...
...
.0063

.0173
!.0001.0134.0003

Mean total feeding time in minutes (95% CI)

1.55 (.47–2.63)
1.89 (.48–3.30)
1.55 (.80–2.30)
1.00 (1.00–1.00)
2.22 (.70–3.75)
3.20 (.40–5.99)
1.03 (.97–1.10)...
...
3.95 (2.42–5.48)

1.55 (.80–2.30)
1.13 (.91–1.35)
1.00 (1.00–1.00)
3.13 (2.04–4.22)

Present

3.98 (2.70–5.27)
3.18 (1.24–5.12)
2.90 (1.54–4.27)
3.52 (1.34–5.69)
4.34 (2.65–6.04)
10.18 (3.09–17.27)
4.81 (3.25–6.37)
1.63 (1.01–2.25)
1.92 (.84–3.00)
9.39 (3.42–15.36)

3.82 (2.14–5.51)
4.81 (3.73–5.90)
1.74 (1.05-2.43)
6.45 (3.57–9.34)

Absent

.3965
.2482
.7662
.0988
.7114
.4531
.2020
...
...
.0086

.2584
.1441
.8893
.5284

P

Mean feeding-bout duration in minutes (95% CI)

Note: We report the effects on scavenger classes and species for each variable at carcasses where black bears were present and absent. We report the percent of carcasses where a scavenger was present and themean and 95% conﬁdence intervals (CI) for total feeding time and mean feeding-bout duration. We also report the P value from our generalized linear models, with statistically signiﬁcant P values indicated byboldface.

Class:
Large carnivore
Mesocarnivore
Small carnivore
Avian
Species:
BobcatCommon raven
CoyoteDomestic dog
FisherGolden eagle
Gray fox
RingtailSpotted skunk
Turkey vulture

Scavenger

Presence (%)

Table 3: Effects of black bears on three aspects of carrion acquisition by scavengers (presence, total feeding time, and mean feeding-bout duration)

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species. Black bears exhibited the largest limitation on carrion acquisition for mesocarnivores. For example, mesocarnivores fed 44 times longer at carcasses where black bears
were absent than at those where bears were present. Blackbears signiﬁcantly limited mesocarnivore total feeding time
(t47 p 29.06, P ! .0001) and presence (z114 p 24.11, P !
.0001). Among mesocarnivores, black bears signiﬁcantly
limited bobcat total feeding time (t14 p 24.29, P p.0128) and presence (z77 p 22.06, P p .0397) as well asgray fox total feeding time (t32 p 23.46, P p .0016) andpresence (z77 p 23.08, P p .0021).
Black bears signiﬁcantly limited the acquisition of carrion
by large carnivores by limiting both their presence (z77 p
23.08, P p .0021) and their total feeding time (t34 p
22.52, P p .0173). Black bears also signiﬁcantly limited
the total feeding time of small carnivores (t9 p 23.74,
P p .0134) and completely excluded ringtails and spottedskunks from carcasses where they were present. Black bears
signiﬁcantly limited the total feeding time of the avian class(t48 p 23.97, P p .0003) and two avian species: common
ravens (t30 p 23.22, P p .0043) and turkey vultures(t22 p 23.21, P p .0063). Among scavengers, the only exception to limitation was the presence of turkey vultures,
which were present at signiﬁcantly more carcasses where
black bears were also present (z77 p 2.01, P p .0440).
Effects of Black Bears on Pumas
Black bears affected puma carrion acquisition by limiting
their presence, total feeding time, and feeding-bout duration. In particular, pumas scavenged at 15.2% of carcasses
where black bears were absent but did not scavenge at anyof the carcasses where black bears were present. At carcasses where black bears were absent, total feeding time
for scavenging pumas was 53.9 (95% conﬁdence interval[CI] p 225.3 to 133.0) min, and their mean feeding-boutduration was 11.1 (95% CI p 22.1 to 24.3) min.
Black bears also affected puma feeding behaviors at theirown kills, affecting how quickly pumas abandoned theirkills as well as their total feeding time and mean feedingbout duration. After the arrival of a black bear, pumas did
not return to 72.4% of their kills and returned only once
to another 13.8%. Before black bear arrival, pumas fed fora total feeding time of 106.5 (95% CI p 66.2–146.9) min,and after bear arrival, they fed for 16.8 (95% CI p 3.3–
30.2) min, resulting in a signiﬁcant limitation (t33 p
24.46, P ! .0001). Black bears did not signiﬁcantly limit
puma mean feeding-bout duration (t33 p 21.07, P p.2943). Black bears fed for a total mean feeding time of
145.9 (95% CI p 98.5–193.2) min at puma kills, suggesting that pumas could still have fed on the carcasses theyabandoned after the arrival of black bears. The usurpationof puma kills was not without risk, as in one instance a

puma killed a subadult black bear that had been feedingon its kill.
Discussion
Many species are facultative scavengers to some degree,and, in some food webs, there is a greater amount of energy transferred through the scavenging of carrion than
through direct predation (Wilson and Wolkovich 2011).
Thus, the importance of carrion resources in driving andstructuring ecological communities is increasingly being
recognized (DeVault et al. 2003; Wilmers et al. 2003a; Wilson and Wolkovich 2011; Cortés-Avizanda et al. 2012;
Moleón et al. 2014). Given the importance of carrion, anyvariables inﬂuencing access to these resources are likely toaffect scavenger population dynamics, the composition offacultative scavengers in ecological communities, and potentially ecosystem function (Angerbjörn et al. 1991; Watson et al. 1992; Selva and Fortuna 2007; Wilson and Wolkovich 2011; Moleón et al. 2014). Despite low sample sizes
for some scavenger species (e.g., we recorded only 14 bobcats and 13 ringtails at our 58 active puma kills and 58 matching control carcasses), we found that pumas and black bears
both affected aspects of carrion acquisition by other scavengers. General trends suggested that pumas varied in theireffects on scavenger classes, while black bears limited all scavengers and were generally more effective at monopolizing
carcasses than pumas.
Pumas provided carrion through their kills to diverse
vertebrate scavengers and had species-speciﬁc effects on
scavengers. While pumas did not limit other large carnivores within their communities, they limited the total
feeding times and mean feeding-bout durations of both
mesocarnivores and birds. This suggests that pumas are effective at excluding smaller, subordinate competitors but
not dominant competitors. In the case of these subordinate
scavengers, most of their feeding is likely occurring whilepumas are absent from their kill or after they abandon it,
rather than through direct usurpation. Since energy intake
of scavengers from carrion can inﬂuence ﬁtness and reproductive ability (e.g., Angerbjörn et al. 1991; Watson et al.
1992), these interactions with pumas may very well affectthe population dynamics of scavengers.
We also observed a surprising trend, where the limitation by pumas of carrion acquisition by mesocarnivores
and avian scavengers apparently led to an increase in all
three aspects of carrion acquisition by small carnivores attheir kills. This suggests a cascading pattern in the acquisition of carrion among scavengers and may provide an alternate explanation for observed intraguild cascades among
carnivores (e.g., Levi and Wilmers 2012). The cascading
patterns initiated by large carnivores, intraguild or otherwise, may include how large carnivores increase small-Large-Carnivore Effects on Scavengers
carnivore acquisition of carrion, in conjunction with otherresources (e.g., Hardin 1960).
The effects on carrion acquisition attributable to blackbears were less intricate than those of pumas but, surprisingly, were of a greater magnitude. Black bears monopolized carrion resources they found and had the largest limitations on the total feeding times of all scavengers. Given
that black bears are unlikely to provide signiﬁcant amountsof carrion to other scavengers through their own kills (sensu
Svoboda et al. 2011), this result suggests that black bears
were an important limitation on other scavengers. Blackbears limited all three aspects of carrion acquisition for every
scavenger class and for nearly every scavenger species (thepresence of turkey vultures was higher at carcasses where
black bears were present, while black bears completely excluded ringtails and spotted skunks), although none of theeffects on mean feeding-bout duration were signiﬁcant.
The high magnitude of their effects suggests that blackbears, like other dominant scavengers (Cortés-Avizanda
et al. 2010, 2012), act as a major limitation on energy transfer with regard to carrion resources in ecological communities. We thus hypothesize that black bears are dominant
over other scavengers because of their ability to eat large
quantities of food quickly rather than because they use
their large size to actively exclude other scavengers.
Black bears also affected pumas at their kills, supporting
the growing body of evidence that solitary felids are negatively affected by dominant scavengers that can usurp
their kills (Murphy et al. 1998; Hunter et al. 2006; Krofel
et al. 2012; Allen et al. 2013; Elbroch and Wittmer 2013).
Pumas abandoned 72.4% of their kills once black bears arrived, a behavior similar to that of cheetahs (Acinonyx jubatus), which limit risk by abandoning their kills after thearrival of dominant scavengers (Hunter et al. 2006). The
abandonment of kills likely limits the energetic intake ofpumas and could force pumas to kill more often to meettheir energetic requirements (Murphy et al. 1998; Elbroch
and Wittmer 2013; Allen et al. 2014a; Elbroch et al. 2014).
Facultative scavengers are not generally believed to affectpopulation dynamics of species they consume during scavenging (Wilson and Wolkovich 2011). However, if blackbears are causing pumas to increase their kill rates, they
may be indirectly affecting prey populations in ways that
could have wider repercussions for the ecological community (sensu Elbroch and Wittmer 2013).
Pumas and black bears clearly have important but different effects on the acquisition of carrion by scavengers.
Pumas were a source of carrion for scavengers across different trophic levels and also may have initiated a cascading pattern of energy availability through their limitationof mesocarnivores, which increased access for smaller carnivores. The inﬂuences of pumas on how energy in carrion resources is distributed may constitute keystone ef-

831

fects, in that they enhance biodiversity (Elbroch and Wittmer 2012). Changes in puma abundances may therefore
have unexpected and important effects on ecological communities. In contrast, black bears were a dominant scavenger that greatly limited the ability of all other scavengers to take advantage of carrion resources. Further, blackbears limited access of pumas at their own kills. Our results thus provide evidence that black bears directly affectthe scavenger community and suggest that black bears
may also have important indirect effects on other aspectsof the ecological community, including ungulate populations, through their effects on top predators. More generally, our results highlight the complexity of possible interactions, including competition among scavengers andlarge carnivores at ungulate carcasses, and the potential effects of this competition on the structure and dynamics of
ecological communities.
Acknowledgments
All capture methods were approved by the independent Institutional Animal Care and Use Committee at the University of California, Davis, and the Wildlife Investigations
Lab of the California Department of Fish and Wildlife. The
California Department of Fish and Wildlife and the University of California at Davis generously provided funding
for the project. We thank D. Casady, K. Cripe, B. Evans,
J. Golla, B. Millsap, C. Wiley, and many ﬁeld technicians
for their help on the project. Two anonymous reviewers
provided helpful comments on a previous draft of the manuscript.
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Natural History Editor: Mark A. McPeek“The American antelope . . . was ﬁrst made known to the scientiﬁc world through Lewis and Clark, who found it in 1804 on the Upper
Missouri. . . . They are exceptionally gregarious in their habits, although the immense bands of thousands in which they formerly assembled
are now broken up by the advancement of civilization, which has absolutely expelled them from those regions where they were met with ingreat numbers a quarter of a century since. Then they were most abundant in California, where they sometimes almost literally covered theplains and the foot-hills west of the Sierras, and where now a solitary wanderer is rarely heard of.” From “The American Antelope, or Prong
Buck” by J. D. Caton (The American Naturalist, 1876, 10:193–205).