The University of Notre Dame
Predation on Yellow-Bellied Marmots (Marmota Flaviventris)
Author(s): Dirk H. van Vuren
Source: American Midland Naturalist, Vol. 145, No. 1 (Jan., 2001), pp. 94-100
Published by: The University of Notre Dame
Stable URL: http://www.jstor.org/stable/3083083
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Am. Midl. Nat. 145:94-100
Predation on Yellow-belliedMarmots (Marmotaflaviventis)
DIRKH. VANWREN
Department of Wildlife,Fish, and Conservation Biology, Universityof California, Davis 95616
ABSTRACT.
I determined cause-specific mortality of yellow-bellied marmots (Marmotaflaviventrzs) to assess the importance of predation as a mortality factor. Contrary to earlier
findings based on visual observation, almost all (98tFo)mortality during the summer active
season was caused by predation. Coyotes ( Canis latrans) were the most important predators,
black bears ( Urfollowed by badgers ( Taxidea taxus), American martens (Martes amer7>cana),
sus amer7canus)and raptors, probably golden eagles (Aguila chrysaetos).Predation on marmots is cryptic; none of the predation events were observed and, in most cases, the marmot
was consumed or removed so quickly and completely that searching for carcass remains
would have been fruitless.
INTRODUCTION
Predationhas importantbehavioral,ecological and evolutionaryeffects on prey species.
The riskof predationmayinfluence foragingbehavior(Kotleret al., 1991), socialbehavior
(Fitzgibbon,1990) and habitatselection (Berger,1991). Further,removalof individualsby
predatorsmay have consequencesfor population dynamics(Reid et al., 1995) and biogeography (Sievertand Keith, 1985), as well as the evolution of antipredatordefenses (Lima
and Dill, 1990).
Predationon some large vertebratescan be evaluatedthrough observation(e.g.,Fitzgibbon, 1990), but for medium and small species the act of predationis seldomwitnessedand
the animal may be entirely consumed, leaving no evidence. Disappearanceof a marked
individualis an unreliableindicatorof predationbecause animalsmay disappearfor other
reasons (Murie, 1992; Waseret al., 1994). Moreover,even when predation is established,
identificationof the predator,an importantfactorin understandingthe effectsof predation
on the prey,may be difficult (Major,1991).
The yellow-belliedmarmot (Marmotaflaviventris)is a large (2-4 kg), ground-dwelling
squirrelthat is widelydistributedin westernNorth America.Anecdotalaccountsshow that
severalmammalianand avianpredatorspreyupon yellow-belliedmarmots(Fraseand Hoffmann, 1980), with potential effects on marmotforaging behavior (Armitage,1982;Carey
and Moore, 1986), habitatselection (AndersenandJohns, 1977), socialbehavior(Armitage
and Johns, 1982) and mating system (Armitage,1986). However,because predation on
marmotsis rarelyobserved (Fraseand Hoffmann, 1980), the magnitudeof predationand
the identity of the predatorsresponsibleis rarely,if ever, known. Such is the case for a
population of yellow-belliedmarmotsin the East RiverValleyin Colorado that has been
studiedintensivelysince 1962 (Armitage,1991). Althoughcoyotes ( Canislatrans)and goldwere known to prey on these marmots (Armitageand Downen eagles (Aguila chrysaetos)
hower, 1974;Armitage,1982), observationsof predationwere rare (Armitage,1982), suggesting that it was not a majorcause of mortality(Armitageand Downhower,1974). Radiotelemetry,however,can circumventbiases that affect visual observationas a means of detecting predation. My objective was to use radiotelemetryto assess the importance of
predation on yellow-belliedmarmots by determining cause-specificmortalityduring the
summeractiveseason.
94
2001
VAN VUREN: YELLOW-BELLIED
MARMOTS
95
METHODS
The studywas conducted from 1984 through 1995 in the East RiverValleynear Rocky
Mountain Biological Laboratory(RMBL),Gunnison County,Colorado. Topographywas
typicalof a glaciated,high-altitudevalley;slopes were gentle on the valleyfloor, elevation
285s2930 m, but rose abruptlyto ca. 3900 m elevationon surroundingpeaks.Vegetation
was an interspersionof subalpinemeadowsrich in forbs,aspen (Popoulastremuloides)woodlands and spruce (Picea spp.) forests, with dense patches of willows (Salix spp.) along
streams.Areas above timberline supported alpine meadows and shrubs, or were largely
devoid of vegetation.
Yellow-belliedmarmotswere common in the valleyand lived in discretehabitatpatches,
typicallyopen meadowsrelativelyfree of trees and shrubsthat contained rocks (boulders,
outcrops or talus) under which burrowswere excavated (Svendsen,1974). Largerpatches
were inhabited by colonies that supported as many as 12 adult (22-y old) females and
usuallyone adultmale, and smallernoncolonialpatcheswere inhabitedby one adultfemale
and sometimesan adult male (VanVuren and Armitage,1994). About 60 to 100 adult and
yearlingmarmotslived in the studyarea. Marmotshibernatedfrom Septemberuntil early
May.
Each summerfrom 1984 through 1993 I instrumented13 to 51 marmotswith radiotransmittersfor a total of 295 marmots.All marmotswere ear-taggedfor identificationand dyemarkedfor visual recognition. Transmitterswere surgicallyimplanted into the peritoneal
cavity;surgeryand the implantedtransmitterhad no effect on subsequentgrowth,survival
or reproduction (VanVuren, 1989). Transmitterswere constructedas sealed cylinders21
mm in diameterand 90 mm long, with a massof 35 g (c4% of bodymass).Eachtransmitter
was coated with a layer of surgicalgradebeeswax2 mm thick; the beeswaxrendered the
transmitterphysiologicallyinert and also retainedtooth impressionswhen bitten by a predator.Mostmarmotswere yearlings(ca. 1-2 kg) when firstinstrumented(VanVuren, 1990).
Transmittershad an expected life of 2 y, but some expired prematurely;transmitterswere
replaced in some marmots.Thus, the time a given marmot carried a transmittervaried
from a few weeks to 5 y, but was usually1-2 y.
Resident mammalianpredatorsthat might prey upon marmotsincluded coyotes, black
bears (Ursus americanus), badgers (Taxidea taxas), Americanmartens (Martes atrcana)
and long-tailedweasels (Mustela frenata). Red foxes (Valpes valpes) and mountain lions
(Puma concolor)were potentialpredators,but were rarelyrecordedin the vicinity.Resident
avian predatorsincluded golden eagles, red-tailedhawks (Buteo jamaicensis), Swainson's
hawks (B. swainsoni) and goshawks(Accipiter gentilis). Great horned owls (Babo virginianus) were common, but owls are nocturnalwhereasmarmotsare diurnal.
I radiolocatedmarmotsevery1-3 d throughoutthe activeseason (May-September).Mortalitywas suggestedby a constantsignal that did not varyin location or intensity,then was
confirmedby recoveryof the transmitter.Causeof deathwasdeterminedbasedon evidence
found at the site. I assignedpredationas the cause if the carcasshad been bitten or eaten.
In most cases I identified the predatorbased on tooth impressionsin the beeswaxcoating
of the transmitter,which I compared with the dentition of museum specimens of mammalian predatorscollected from the area.
For transmittersfound on the ground surface,I identified mammalianpredators,except
badgers,on the basisof tooth impressions.I assignedbadgersas the predatorwhen I found
the transmitterwithin a marmotburrowthat had been recentlyexcavatedby a badger;such
excavationsare unmistakablein appearance.Raptorstypicallypluck the fur from larger
mammalianpreybefore eating;thus, I assignedraptorsas the predatorwhen the transmitter
THEAMERICAN
MIDLAND
NATURALIST
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145(1)
TABLE 1. Cause-specific mortality of yellow-bellied marmots (n = 97) near Rocky Mountain Biological Laboratory, Colorado, 1984-1995
Cause of mortality
n
%
Human activities
Died underground, cause unknown
Predator
Coyote
Badger
American marten
Black bear
Raptor
Unidentified predator
2
2
93
46
10
7
7
6
17
2
2
96
47
10
7
7
6
18
wasrecoveredon the surfaceof the ground,had no tooth impressionsand wasaccompanied
by large quantitiesof marmotfur.
My analysiswas based on three assumptions.First, a recovered transmittermeant the
marmotwas dead. Although channel catfish (Ictalarus panctatus) can expel an implanted
transmitterfrom the peritonealcavity(Summerfeltand Mosier,1984), marmotsapparently
cannot. No instrumentedmarmotwas recapturedwithout its transmitter,nor was any marmot recapturedor observedafter its transmitterhad been recovered.
Second, I assumed that a transmitterrecoveredfrom a carcassthat had been bitten or
eaten meant the marmot had died from predation. The alternative,that some marmots
died abovegroundof other causesand subsequentlywere scavenged,is possiblebut unlikely.
Becausemarmotsseek refuge in their burrows,mortalityunrelatedto predationwouldhave
to be sudden. Since 1962 sick or dead marmots21-y old have been observedaboveground
only twice (Armitageand Downhower,1974;K. B. Armitage,pers. comm.).
Third, I assumed that tooth impressionsin the transmitteridentified the predatorresponsibleratherthan a subsequentscavenger.Becausebeeswaxis soft at body temperature
but hardens as it cools, I could distinguishtooth impressionsmade at the time of death
from those made after the transmitterhad cooled.
RESULTS
Ninety-seveninstrumentedmarmotsdied during the active season (Table 1). Two died
because of human activities,one from being struck by a vehicle and the other from a
gunshot wound. Two more died undergroundin burrowsthat showed no sign of disturbance by badgers;cause of death was unknownbut was attributedto naturalfactors.
The remaining93 marmotswere killed by predators.Of these, 46 were killed by coyotes.
Coyote tooth impressionsin transmittersincluded canines,incisors,premolarsand molars.
In two cases tooth impressionsmatched those of both red foxes and coyotes, but I ruled
out foxes because of their rarityin the studyarea. Coyotefur was sometimesfound entangled on shrubsbeside the transmitter.In all cases, remainsof the marmotwere limited to
a few tufts of fur, often including the tip of the tail and sometimesportionsof the digestive
tract.Transmitterswere found in every habitatin the studyarea and at elevationsranging
from the valleyfloor to 3840 m, well above timberline.I never found a transmitterin or
near a coyote den or in a coyote scat.
Ten marmotswere killed by badgers.None of the transmittershad tooth impressions,
but all were found buried with part or all of the marmot carcassunder 210 cm of loose
2001
MARMOTS
VUREN: YELLOW-BELLIED
VAN
97
of the marmot, still buried
inside the burrow.In two cases I found the entire carcass
soil
occurredwhen the marmot
uneaten 7-10 d after death. Fivebadger-causedmortalities
and
when marmotsare
temporarily
killed in a "flight"burrow,a shallowburrowoccupied
was
(Armitage,1988).
threatened
impressionsin transmitterswere
Seven marmotswere killed by martens. Marten tooth
of the marmot and in the
to canines. In five of these cases I found no remains
limited
werefound in conifer
transmitters
two I found portionsof the digestivetract.All seven
other
The largestmar1984).
McCullough,
and
the preferredhabitatof martens (Hargis
forests,
4 kg at the time of death in late
killed by a martenwas a 4-y-oldmale that weighed ca.
mot
August.
impressionswere made by canines
Seven marmotswere killed by blackbears.Most tooth
remainsexcept a few hairsand,
marmot
no
buta few were by incisorsand molars.I found
in a varietyof habitatsbut were
inone case, the tip of the tail. Transmitterswere found
found in or near a bear den or in a bear scat.
never
were found on open steep slopes
Six marmotswere killed by raptors.All six transmitters
quantitiesof fur, I found some
large
to
addition
above3100 m with little vegetation;in
I found golden eagle feathersbeside
piecesof everted skin and a few bones, but no flesh.
twoof the transmitters.
not be identified. All 17 transSeventeen marmotswere killed by predatorsthat could
tooth impressions,none were
any
had
none
mitterswere found on the ground surface,
and occasionallya portion of the
accompaniedby marmotremainsother than a few hairs
of badgeractivity.These circumstancdigestivetractand none were associatedwith evidence
were killed by coyotes;indeed, I
most
essuggest coyotes, bears or martens.I suspect that
coyote scat.
a
from
marmots
laterrecoveredthe eartagsof 1 of the 17
showed a clumped distribution
marmots
predator-killed
of
The locations of transmitters
marmotcolonies at the north
(Fig.1) . One clusterof locationsencompassedthree adjacent
of the EastRiverand Rock
confluence
endof the studyarea, 50>1000 m northwestof the
1 km belowthe confluence
about
beginning
River,
Creek.Anotherclusterwasalong the East
canyon;some marmots,
steep-walled
narrow,
a
enters
here
withCopper Creek. The river
on the rim above.A
foraged
and
mostlynoncolonial, lived in burrowsin the canyon wall
willowsthat supdense
of
area
an
thirdclusterwas on the east slope of Gothic Mountain,
portedfew marmots.
DISCUSSION
I suspectthat these predators
Coyotesand bears left little, if any,of the marmotcarcass.
biting into the transeventually
it,
killing
after
began feeding on the marmotimmediately
with gut contents or the tail tip.
mitterwhich was then discardedas inedible, often along
perhapsthe remainderof the carcass
The marmotwas consumed entirelyon the spot, or
small (ca. 1 kg) to haveconsumed
wascarriedoff. Martensleft similarevidencebut were too
remainderof the carcassaway.
the
dragged
evidently
the entire carcass,so afterfeeding they
from a large portion of the skin to
In contrast,badgersleft much of the carcass,ranging
apparentlyhad cached the unthe entire carcass,and buried it under loose soil. Badgers
carnivores(Macdonald,1976).
other
and
eaten portion, a behaviorreported for badgers
burrowswhose entrances
flight
of
out
dug
were
badgers
Half of the marmots killed by
by badgers (Andersenand
lacked the encirclementof rocks thought to resistenlargementburrowsthat were at least
from
Johns, 1977). The other half, however,were excavated
associationbetween marmotburrows
partiallyprotected by rocks,indicatingthat the close
from badger predation.
protection
provide
always
not
does
and rocks (Svendsen,1974)
evertedskin, presumably
and
fur
Raptorsalso left substantialremains,especiallyplucked
THEAMERICAN
MIDLAND
NATURALIST
98
*.
145(1)
-
.
o
.
.
.
Avery
Pk
.
.
O ^
.
.
.
Gothic
Mtn 8
*
-
.
.
.
.
Red Rock
8
Pk
*
0
-
1
km
Snodgrass
Mtn
8)
FIG. 1
Locationsof 73 yellow-belliedmarmotskilled by predators (solid triangles) near Rocky
MountainBiologicalLaboratory(RMBL),Colorado,198s1995. Localitiesknown to be inhabitedby
marmotsare indicatedas colonies (solid circles) or noncolonialsites (open circles).An additional20
marmotswere killed at locationsoutside the area coveredby the map. Mortalitiesappearclusteredin
three areas:one encompassesthree marmotcolonies located 50s1000 m northwestof the confluence
of the East Riverand Rock Creek;another is along the East River,beginning about 1 km below the
confluence with CopperCreek;and the third is on the east slope of Gothic Mountain
to facilitatedigestion.Surprisingly,however,I found no flesh and few bones, indicatingthe
raptorconsumedpart of the carcassand carriedoff the rest. Onlygolden eagles seem large
enough to consume and carryso much, so I conclude that theywere most likelythe raptor
responsible,a conclusion that is supported by discoveryof golden eagle feathers at two
locations.Yellow-belliedmarmotswere the most importantprey of golden eagles in eastern
Washington(Marrand Knight,1983).
The risk of predation was not uniformly distributedthroughout the study area. One
cluster,which occurred on a slope that supportedthree of the six marmotcolonies in the
2001
MARMOTS
VAN VUREN: YELLOW-BELLIED
99
studyarea, may have resultedfrom a greateravailabilityof marmotsratherthan predation
risk per se. However,the other two clusters appear to be "populationsinks," areas that
attractmarmots (similarto "dispersalsinks";Lidicker,1975), but which have an unusually
high risk of mortality(Knightet al., 1988). One such sink was located in a narrowcanyon
where many marmots,both residents and dispersers,were killed. Dispersersoften moved
down the canyon.Further,severalsites there had suitableburrowsand foragingareasthat
attractedresident marmots,mostlynoncolonial. However,patches of willowsand grovesof
spruce or aspen providedconcealmentfor predators;marmotsusuallyavoidhigh vegetation
that can hide predators (Armitage,1982). Also, predatorsapproachingalong the canyon
rim mayhave been visuallyscreened from marmotsmovingbetweenburrowsin the canyon
wall and foraging areas behind the rim. The other sink was on the east slope of Gothic
Mountain,which also had extensive patches of willowsand groves of spruce and aspen.
Although few marmotsresided there, most that did were killed. Further,some dispersers
were killed there when followinga discontinuousscarpthat extended acrossthe east slope
of Gothic Mountain,parallelto the EastRiver.Apparentlythese two areascontainedhabitat
features that were attractiveto marmots,but which also made them especiallyvulnerable
to predation;marmotsmay face such trade-offsin habitatselection (Armitage,1982).
Predationon yellow-belliedmarmotsis cryptic.None of the predationeventsdocumented
in my studywere observed,despite the fact that severalmarmotswere killed in areaswhere
behavioralobservaiionswere conducted frequently.Indeed, only two predaiion events on
marmotswere observedin the same studyarea in >5000 h of behavioralobservaiionsover
20 y (Armitage,1982);in contrast,I documented93 deathsdue to predatorsin 12 y.Further,
in most casespredator-killedmarmotswere consumedor removedso quicklyand completely that intensivesystemaiicsearchesto locate remainsof carcasseswould havebeen fruitless;
I often had difficultydoing so even with the assistanceof a radiotransmitter.
My studydemonstratesthat, contraryto earlierfindingsbased on visualobservaiion(Armitage and Downhower,1974), predaiion is the dominant cause of mortalityamong these
marmots during the aciive season, accouniing for 98% of naturalmortaliiies.Thus, predaiion is an importantfactor in the behavior,ecology and evoluiion of yellow-belliedmarmots.
Acknowledgments. This study was initiated at the Department of Systematics and Ecology, University
of Kansas, as part of my dissertation research, and was conducted at RMBL. Financial support was
provided by the University of California Agricultural Experiment Station, RMBL, University of Kansas,
American Society of Mammalogists, Sigma Xi, Theodore Roosevelt Memorial Fund of the American
Museum of Natural History, Lee R. G. Snyder Memorial Fund and by a University of Kansas General
Research Grant and National Science Foundation grants to K. B. Armitage. I thank C. M. Salsbury, C.
M. Lenihan and M. P. Bray for help in data collection, and K. B. Armitage for assistance throughout
the project.
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SUBMITTED12 NOVEMBER1999
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7JUNE
2000