are pumas subordinate carnivores, and does it matter? · 2018. 1. 24. · wallach et al. (2015)...

Submitted 15 November 2017Accepted 4 January 2018Published 24 January 2018

Corresponding authorL Mark Elbrochmelbrochpantheraorg

Academic editorJan Schipper

Additional Information andDeclarations can be found onpage 13

DOI 107717peerj4293

Copyright2018 Elbroch and Kusler

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

Are pumas subordinate carnivores anddoes it matterL Mark Elbroch1 and Anna Kusler12

1Panthera New York NY United States of America2Department of Biology Pace University PleasantvilleBriarcliff Pleasantville NY United States of America

ABSTRACTBackground Interspecific competition affects species fitness community assemblagesand structure and the geographic distributions of species Established dominancehierarchies among species mitigate the need for fighting and contribute to the realizedniche for subordinate species This is especially important for apex predators many ofwhich simultaneous contend with the costs of competition withmore dominant speciesand the costs associated with human hunting and lethal managementMethods Pumas are a widespread solitary felid heavily regulated through huntingto reduce conflicts with livestock and people Across their range pumas overlapwith six apex predators (gray wolf grizzly bear American black bear jaguar coyotemaned wolf) two of which (gray wolf grizzly bear) are currently expanding in NorthAmerica following recovery efforts We conducted a literature search to assess whetherpumas were subordinate or dominant with sympatric apex predators as well as withthree felid mesocarnivores with similar ecology (ocelot bobcat Canada lynx) Wealso conducted an analysis of the spatial distributions of pumas and their dominantsympatric competitors to estimate in what part of their range pumas are dominantversus subordinateResults We used 64 sources to assess dominance among pumas and other apexpredators and 13 sources to assess their relationships with felid mesocarnivoresEvidence suggested that wolves grizzly bears black bears and jaguars are dominantover pumas but that pumas are dominant over coyotes and maned wolves Evidencesuggested that pumas are also dominant over all three felid mesocarnivores with whichthey share range More broadly pumas are subordinate to at least one other apexcarnivore in 10799252 (475) of their 22735268 km2 range across North and SouthAmericaDiscussion Subordinate pumas change their habitat use suffer displacement at foodsources likely experience increased energetic demands from harassment exhibitincreased starvation and are sometimes directly killed in competitive interactionswith dominant competitors Nevertheless we lack research clearly linking the costsof competition to puma fitness Further we lack research that assesses the influenceof human effects simultaneous with the negative effects of competition with othersympatric carnivores Until the time that we understand whether competitive effectsare additive with human management or even potentially synergistic we encouragecaution among managers responsible for determining harvest limits for pumas andother subordinate apex carnivores in areas where they are sympatric with dominantspecies This may be especially important information for managers working inregions where wolves and brown bears are recolonizing and recovering and historiccompetition scenarios among multiple apex predators are being realized

How to cite this article Elbroch and Kusler (2018) Are pumas subordinate carnivores and does it matter PeerJ 6e4293 DOI107717peerj4293

Subjects Biodiversity Conservation Biology Ecology Natural Resource ManagementKeywords Puma concolor Subordinate Dominance Competition Gray wolf Grizzly bearAmerican black bear Jaguar Apex predators

INTRODUCTIONThe outcome of interspecific competition affects species fitness community assemblagesand structure and the geographic distributions of species (Schoener 1983 Polis amp Holt1992 Le Bourlot Tully amp Claessen 2014 Droumlge et al 2017) Much of competition isindirect and competitors generally assess the competitive abilities (eg resource holdingpotential Parker amp Stuart 1976) of their opponents before deciding to engage themresulting in established species hierarchies that mitigate the need for fighting (Arnott ampElwood 2008) In fact the established lsquolsquosuperiorityrsquorsquo (Crombie 1947) of one species overanother contributes to Hutchinsonrsquos (1957) differentiation between the fundamental andrealized niche A speciesrsquo enemies include both predators and competitors both of whichlimit an animalrsquos distribution to its realized niche (eg wild dogs Lycaon pictus in Droumlgeet al 2017) This is especially important for carnivores in multi-carnivore guilds in whichcompetition contributes to intraguild killing (Polis amp Holt 1992 Donadio amp Buskirk 2006)and whether a species self-regulates its population through various social mechanisms oris instead regulated by another predator (Wallach et al 2015)

Carnivores disproportionately influence ecological functions in natural systems andare culturally important (Ripple et al 2014) Most carnivores however are also fearedand persecuted because of perceived and real threats to human safety and because theykill livestock household pets and game species we value (Ordiz Bischof amp Swenson 2013Ripple et al 2014 Elbroch Feltner amp Quigley 2017) Not all carnivores are ecologicallyequivalent however and size betrays stark differences in small versus large carnivoresCarbone Teacher amp Rowcliffe (2007) found that carnivores lt20 kg exhibited differenthunting strategies and energetic budgets than carnivores gt20 kg and Wallach et al (2015)found that carnivores lt15 kg exhibited additional differences in life history strategiesthan those species gt15 kg Specifically Wallach et al (2015) reported that carnivoresgt15 kg self-regulate through social mechanisms and density-dependence whereas smallercarnivores are generally limited by predation by larger carnivores Wallach et al (2015)subsequently used 15 kg to differentiate between lsquolsquoapex predatorsrsquorsquo and smaller carnivoresFor our review we also utilized the 15-kg cutoff

Apex predators too are not ecologically equivalent and vary in size morphologyweapons and life history strategies (Kleiman amp Eisenberg 1973 Bekoff Daniels ampGittleman 1984 Sandell 1989) These differences have resulted in established thoughsometimes variable dominance hierarchies aswell as the uniquemorphology andbehaviorsutilized by subordinate species coping with the pressures of interspecific competition Forexample pumas (Puma concolor) and cheetahs (Acinonyx jubatus) appear to withstandhigh levels of kleptoparatism without obvious influences on their fitness (Scantlebury et al2014 Elbroch et al 2017a) and coyotes (Canis latrans) wild dogs (Lycaon pictus) leopards(Panthera pardus) and cheetahs utilize temporal and spatial competition refuges and other

Elbroch and Kusler (2018) PeerJ DOI 107717peerj4293 222

movement strategies to mitigate interactions with dominant competitors (Durant 1998Arjo amp Pletscher 1999 Vanak et al 2013 Droumlge et al 2017)

The position a species occupies in a dominance hierarchy of a multi-carnivore guildinfluences its ecology (eg foraging strategies and temporal space use Droumlge et al 2017)but external ecological factors such as resource distributions also influence the strategiessubordinate species utilize to coexist with dominant competitors or whether they exhibitsubordinate behaviors at all (Karanth et al 2017) Evidence strongly supports the theorythat size determines the outcomes of competitive interactions and the structure ofdominance hierarchies in general larger carnivores dominate smaller carnivores (Schoener1983Donadio amp Buskirk 2006De Oliveira amp Pereira 2014)Nevertheless this is not alwaysthe case Striped skunks (Mephitis mephitis) bobcats (Lynx rufus) and wolverines (Gulogulo) compensate for their smaller size by being more aggressive and wielding uniqueweapons (Krebs et al 2004 Allen et al 2016)

Determining whether or not a species is dominant or subordinate may also be importantin applied conservation andmanagementMost of the worldrsquos apex predators are hunted byhumans often for trophies (Ordiz Bischof amp Swenson 2013) and whereas carnivores haveevolved strategies to cope with interspecific competition they are less prepared to withstandthe intensity ofmodernhumanhunting (Cooley et al 2009Darimont et al 2015)Humansdiffer from other predators in that they disproportionately target other carnivores and adultanimals which constitute the reproductive capital of populations (Darimont et al 2015)In the case of subordinate species already under pressures of interspecific competitionhuman impacts may lead to unexpected population fluctuations or declines For examplefollowing the recovery of a tiger population in India subordinate leopards shifted theirdiet increased their conflicts with people through livestock depredation and subsequentlysuffered rapid declines in their numbers (Harihar Pandav amp Goyal 2011)

Pumas are awidespread solitary felid heavily regulated through sport hunting tomitigateconflicts with livestock and people (Treves 2009 Murphy amp MacDonald 2010 Mattson2014) Across their range in North and South America pumas overlap with six other apexpredators (as defined by Wallach et al 2015) Grizzly (or lsquolsquobrownrsquorsquo) bear (Ursus arctos)and gray wolf (Canis lupus) populations are currently expanding in North America andincreasingly overlapping managed puma populations already under pressure from humanharvest If pumas are dominant over bears and wolves the expansion of these potentialcompetitors should not influence puma fitness or population dynamics significantly Butif pumas are subordinate to one or both of these recovering species conservation mangersmay need to adjust human harvest to accommodate for the additional ecological stressof new competition The first step then is to determine whether pumas are indeed asubordinate carnivore and if so ascertain to which apex carnivores they are subordinate

In this paper we had three objectives First we reviewed the published literature togather empirical evidence for whether pumas are dominant subordinate or equal intheir competitive interactions with the following apex predators grizzly bear Americanblack bear (Ursus americanus) gray wolf coyote maned wolf (Chrysocyon brachyurus)and jaguar (Panthera unca) Following established theory we predicted that size woulddetermine competitive outcomes and that social carnivores and larger carnivores would


dominate pumas (Donadio amp Buskirk 2006 De Oliveira amp Pereira 2014) Second wegathered information on interactions with three ecologically-similar felid mesocarnivores(bobcat Canada lynx Lynx canadensis and ocelot Leopardus pardalis) with which thepotential for competition with pumas over resources is also likely Third we assessed theextant spatial distribution of pumas and quantified in what portion of their range theyare the dominant predator versus a subordinate under other sympatric apex predatorsManagers and scientists can then refer to this map as they consider hunting limitsconservation priorities and research questions for the species

SURVEY METHODOLOGYLiterature searchWe searched for evidence of dominance and subordination among species interactionsin the published literature We conducted independent searches using Google Scholarand Web of Science utilizing puma-species pairings and the following keywords pumapuma concolor cougar mountain lion jaguar Panthera onca bear black bear grizzly bearUrsus wolf wolves gray wolf Canis lupus coyote C latrans ocelot Leopardus pardalisbobcat Lynx rufus maned wolf Chrysocyon brachyurus Canada lynx L canadensis Weare confident this approach captured most publications in English but we are less surewhat percent of Spanish publications were identified successfully

Types of competition and awarding dominanceWe sought evidence for outcomes from the following four types of interspecific interactions(1) Exploitation competition (EC) describes indirect interactions in which a dominant

species superior at gathering using or acquiring a shared resource reduces theavailability of the shared resource for the subordinate species (Tilman 1982) Forexample if a subordinate species shifts its diet in the presence of a dominant thechange may be interpreted as exploitation competition (Hayward amp Kerley 2008)

(2) Interference competition (IC) defined as aggression or direct contests in which adominant species blocks a subordinate species from a resource (Case amp Gilpin 1974)In natural systems it can be difficult to interpret between exploitive and interferencecompetition (Schoener 1983) For example pumas reduce their intake of elk (Cervuscanadensis) in the presence of wolves (eg Kortello Hurd amp Murray 2007) but it isunclear whether wolves are better at killing this prey or whether wolves are directly(chasing pumas) or indirectly blocking pumas from elk by forcing elk to shift tohabitats in which pumas hunt less often IC may also elevate to physical contests inwhich the subordinate species is killed described next

(3) Interspecific competitive killing (CK) defined as a dominant species killing asubordinate species but not eating them (Lourenco et al 2013)

(4) Intraguild predation (IGP) defined as a dominant predator killing and consuming asubordinate predator (Holt amp Polis 1997 Lourenco et al 2013)Differentiating between these four categories however proved challenging Schoener

(1983) emphasized the difficulty in interpreting mechanisms of competition (EC vs IC)from field data and acknowledged that both mechanisms may contribute to specific animal


interactions and behaviors Likewise differentiating CK from IGP required knowledge onwhether the prey (subordinate carnivore) was consumed in its entirety (Lourenco et al2013) and this information was lacking in most published papers we read Therefore wesimplified the four categories to two (1) non-lethal competition (NLC) inclusive of allforms of EC and IC and (2) lethal competition (LC) inclusive of CK and IGP

We tallied the number of publications that provided evidence for whether pumaswere dominant or subordinate in interactions with each sympatric carnivore species andawarded dominance to the species in the pairing with the most evidence (highest numberof publications) supporting dominance

Geographic analysis to determine where pumas are dominant versussubordinateBased upon our results determining which species were dominant over pumas and whichwere subordinate we assessed coarse spatial patterns across the extant range of pumas Weacquired distribution maps for pumas and the species to which they were subordinate fromthe International Union for Conservation of Nature (IUCN) (Wildlife Conservation Society2008 IUCN 2010 IUCN 2015 IUCN 2016 IUCN SSC Bear Specialist Group IUCN andIBA 2017) IUCN rangemaps are polygons for Geographic Information Systems (GIS) thatrepresent extant ranges where a species is likely to occur based upon known occurrences ofthe species habitat preferences and subsequent modeling and other expert knowledge ofthe species and its range (IUCN 2017) We utilized the Union tool in ArcGIS 100 to createa single distribution for the dominant species removing any redundancy where speciesoverlapped Then we used the Overlay tool to quantify in what proportion of a their rangepumas are dominant versus subordinate to one or more competitors

RESULTSOur initial searches in Web of Science and Google Scholar yielded 72 potential papers thatin turn yielded another 15 scientific accounts (eg old graduate theses and state reports)for our review of competition between pumas and sympatric apex predators In the endwe utilized a refined list of 64 distinct sources in our review those that were discarded didnot address competition between apex predators or were redundant publications of earlierfindings We found evidence that wolves dominated pumas in 78 (n= 18) of 23 sourcesgrizzly bears dominated pumas in 100 of 4 sources black bears dominated pumas in67 (n= 6) of 9 sources jaguars dominated pumas in 60 (n= 15) of 25 sources coyotesdominated pumas in 19 (n= 3) of 16 sources and zero examples in which maned wolvesdominated pumas (Table 1 Fig 1) In contrast we found evidence that pumas dominatedwolves in 22 (n= 5) of 23 sources black bears in 44 (n= 4) of 9 sources coyotes in81 (n= 13) of 16 sources and maned wolves in 67 (n= 2) of 3 sources (Table 2 Fig 1)We also found 10 sources that did not detect dominance in either species where jaguarsand pumas were sympatric (Table 2)

We utilized 13 distinct sources to assess puma interactions with three large sympatricfelid mesocarnivores and the literature suggested that pumas were dominant over allthree species We found three sources reporting pumas killing ocelots (Crawshaw 1995


Table 1 Puma subordination Evidence of puma subordination to sympatric apex carnivores the number of sources (n) supporting the conjec-ture and the citations of the sources

Species pairing n NLC LC

Wolf dominant over puma 18 Puma spatial displacement RileyNesslage amp Maurer (2004) KortelloHurd amp Murray (2007) Bartnicket al (2013) Lendrum et al (2014)Puma displacement at carcassesand kleptoparasitism of puma killsUSFW (1995) Ruth amp Hornocker(1996) Kunkel et al (1999)Hornocker Wildlife Institute (2001)Akenson Akenson amp Quigley (2005)Kortello Hurd amp Murray (2007)Ruth amp Buotte (2007) Elbroch et al(2017c) Puma prey switching dueto wolves Kortello Hurd amp Murray(2007) Bartnick et al (2013) Elbrochet al (2015)

Direct killing of pumas Schmidt ampGunson (1985)White amp Boyd (1989)Boyd amp Neal (1992) Kunkel et al(1999) Jimenez et al (2006) KortelloHurd amp Murray (2007) Ruth (2004a)Ruth amp Buotte (2007) Elbroch et al(2015) Puma starvation attributed tocompetition Ruth (2004a) KortelloHurd amp Murray (2007) and Elbroch etal (2015)

Grizzly bear dominant over puma 4 Puma displacement at carcassesand kleptoparasitism of puma killsMurphy et al (1998) Ruth amp Buotte(2007) LM Elbroch amp HB Quigley2018 unpublished data

Direct killing of pumas Ruth (2004b)

Black bear dominant over puma 6 Puma displacement at carcassesand kleptoparasitism of puma killsMurphy et al (1998) Ruth (2004b)Allen et al (2014a) Elbroch et al(2014) and Allen et al (2015)

Direct killing of pumas LM Elbrochamp HB Quigley 2018 unpublisheddata (black bear killed and consumedthree kittens in same litter)

Jaguar dominant over puma 15 Spatial and temporal displacementof pumas Schaller amp Crawshaw Jr(1980) Emmons (1987) Scognamilloet al (2003)Moreno Kays ampSamudio Jr (2006) De Azevedo(2008) Harmsen et al (2009) Pavioloet al (2009) Romero-Munoz etal (2010) Sollmann et al (2012)Palomares et al (2016) Palomares etal (2017) Change in puma diet whensympatric with jaguarsMoreno Kaysamp Samudio Jr (2006)

Direct killing of pumas Crawsha Jr ampQuigley (1984) Crawshaw amp Quigley(1991) Harmsen et al (2009) Ruth ampMurphy (2010) De Oliveira amp Pereira(2014)

Coyote dominant over puma 3 Puma displacement at carcassesand kleptoparasitism of puma killsHarrison (1990) Stanford (2013)

Direct killing of pumas Logan ampSweanor (2001)

NotesNLC non-lethal competition LC lethal competition

Loacutepez-Gonzaacutelez amp Gonzaacutelez-Romero 1998 Martins Quadros amp Mazzolli 2008) but twoadditional references that indicated pumas and ocelots may not influence each other (Davis2009Massara et al 2016)Weonly foundone reference to pumas killingCanada lynx (Ruthamp Murphy 2010) and nothing further about puma-lynx competition We found six papers


Figure 1 The apex predators of North and South America and their relative competitive relationshipwith pumas (E) Bold arrows denote dominance and point from the dominant species to the subordinateThin arrows denote some evidence to the contrary (A) gray wolf (Canis lupus) (B) grizzly bear (Ursusarctos) (C) American black bear (Ursus americanus) (D) jaguar (Panthera unca) (E) puma (Puma con-color) (F) maned wolf (Chrysocyon brachyurus) (G) coyote (Canis latrans) Drawings by Mark Elbroch

Full-size DOI 107717peerj4293fig-1

documenting puma predation of bobcats (Ackerman Lindzey amp Hemker 1984 BurtonPerez amp Tovar 2003Hass 2009 Koehler amp Hornocker 1991 Lopez-Gonzaacutelez 1994 LowreyElbroch amp Broberg 2016) and three references reporting spatial displacement of bobcatsby pumas (Koehler amp Hornocker 1991 Burton Perez amp Tovar 2003 Lewis et al 2015)


Table 2 Puma dominance and equality Evidence of (1) puma dominance over and (2) equality to sympatric apex carnivores the number ofsources (n) supporting the conjecture and the citations of the sources


DominancePuma dominant over wolf 5 ndash Direct killing of wolves Schmidt

amp Gunson (1985) Ruth (2004a)Mexican Wolf Blue Range AdaptiveManagement Oversight Committeeand Interagency Field Team (2005)Jimenez et al (2008) LM Elbroch ampHB Quigley 2018 unpublished data(1 subadult wolf killed and consumedby an adult female puma)

Puma dominant over grizzly bear 0 ndash ndashPuma dominant over black bear 4 ndash Direct killing of black bears

Cunningham Gustavson amp Ballard(1999) Elbroch et al (2014) Nichols(2017) LM Elbroch amp HB Quigley2018 unpublished data (adult femalepuma kills and consumes black bearcub of the year)

Puma dominant over jaguar 0 - ndashPuma dominant over coyote 13 Spatial and temporal displacement of

coyotes Koehler amp Hornocker (1991)Wang Allen amp Wilmers (2015)Mahoney (2017)

Direct killing of coyotes AckermanLindzey amp Hemker (1984) Boyd ampOrsquoGara (1985) Arjo (1998)Murphyet al (1998) Koehler amp Hornocker(1991) Atwood (2006) Ruth ampBuotte (2007) De la Torre amp De laRiva (2009) Knopff et al (2010)Lowrey Elbroch amp Broberg (2016)LM Elbroch amp HB Quigley 2018unpublished data (multiple pumaskilling and consuming multiplecoyotes)

Puma dominant over maned wolf 2 ndash Direct killing of maned wolvesMazzolli (2009) De Oliveira amp Pereira(2014)

EqualityJaguar and puma equal 10 Inferred because spatialtemporal

activity patterns were similar Taberet al (1997) Scognamillo et al (2003)Foster Harmsen amp Doncaster (2010)Davis Kelly amp Stauffer (2011) Fosteret al (2013) Hernaacutendez-SaintMartiacuten(2013) Gutieacuterrez-Gonzaacutelez ampLoacutepez-Gonzaacutelez (2017) Inferredbecause diet patterns were dissimilarScognamillo et al (2003) Novacket al (2005) De Azevedo (2008)Hernaacutendez-SaintMartiacuten (2015)

ndash

Maned wolf and puma equal 1 Inferred because spatialtemporalactivity patterns were similar Trolleet al (2007)

ndash



We were unable to analyze whether weight ratios correlated with dominance becauseof complications due to extreme sexual dimorphism among pumas and other carnivores(and sources not always reporting the sex of the animals involved in interactions) and thefact that social carnivores should likely be analyzed as the combined weight of all membersin an interaction (eg wolf pack) group size in interactions with social species was oftenlacking as well Overall the general pattern was suggestive that the size difference betweenpumas and other apex predators does correlate with dominance For example evidence thatjaguars are dominant is strongest in areas where jaguars are large and weigh considerablymore than pumas but more ambiguous where the two species are more similar in size(Loacutepez-Gonzaacutelez amp Gonzaacutelez-Romero 1998 Gutieacuterrez-Gonzaacutelez amp Loacutepez-Gonzaacutelez 2017)Wolf packs also appear to have a clear advantage over individual pumas but one-on-onethe outcome of competitive interactions between a wolf and a puma is less certain (Ruthamp Murphy 2010) or dependent upon differences in age (eg wolves killing puma kittensElbroch et al 2015)

Geographic analysis to determine where pumas are dominant versussubordinatePumas are subordinate to another apex carnivore in 10799252 (475) of their 22735268km2 range (International Union for Conservation of Nature 2015) across North and SouthAmerica (Fig 2)

DISCUSSIONCompetition among carnivores in multi-species guilds is complex and difficult todisentangle (Schoener 1983 Donadio amp Buskirk 2006 Lourenco et al 2013) Our reviewprovided strong evidence that pumas are both subordinate to some apex carnivores withwhich they are sympatric but dominant over others Lethal outcomes (LC) certainlyprovided compelling evidence of competition and subordination but we did not rankthem above NLC as non-lethal indirect effects can equally impact fitness (Ritchie ampJohnson 2009) Subordinate pumas switched their habitat use suffered displacement atfood sources likely experienced increased energetic demands from harassment exhibitedincreased starvation and were sometimes directly killed in competitive interactions withdominant competitors In short pumas suffered costs when sympatric with carnivoresto which they are subordinate Thus we suggest managers and researchers consider thepotentially-additive or synergistic effects of competition and lethal management on pumapopulation dynamics

We found strong evidence that gray wolves are dominant over pumas likely due to theirsocial structure and the fact that they often have the numerical advantage over pumas (Ruthamp Murphy 2010) The effects of wolves on pumas appear numerous Pumas exhibit habitat(Riley Nesslage amp Maurer 2004) and dietary shifts (Elbroch et al 2015) in the presenceof wolves and experience increased starvation as wolves re-establish in systems in whichthey were absent for some time (eg Kortello Hurd amp Murray 2007 Elbroch et al 2015)Wolves also harass pumas the energy expense of which is approximately five times greaterthan the energy expenditure of normal hunting (Bryce Wilmers amp Williams 2017) and


Figure 2 Extant puma range The extant range of pumas in North and South America The light greendenotes the portion of puma range where they are the only or dominant apex predator and the orangedenotes the portion of puma range where they are subordinate to at minimum one other apex preda-tor Source ESRI DigitalGlobe GeoEye Earthstar Geographics CNESAirbus DS USDA USGS AEGetmapping Aerogrid IGN IGP swisstopo CIS User Community



kleptoparatize and displace pumas from their kills (Bartnick et al 2013 Elbroch et al2017c) Wolves also directly kill all age classes of pumas (eg Boyd amp Neal 1992 Ruth2004a Elbroch et al 2015) even while pumas too occasionally kill wolves (eg Jimenezet al 2008) Yet even with so much suggestive evidence amassing from multiple studieswe still lack for research that clearly links competition with wolves to puma fitness (egsurvivorship fecundity)

The influence of grizzly and black bears on pumas is less studied but appears to be lesssevere than that of wolves due to the seasonal dormancy of bears that provide pumas atemporal reprieve from competition with these species The most significant competitionbetween bears and pumas documented in the literature is that bears displace pumas fromtheir kills costing pumas energetic calories in food lost and the additional efforts of huntingto procure more prey If bears displace pumas from their kills often enough pumas mayincrease their kill rates and influence other trophic levels (Elbroch et al 2014) Researchdirectly linking bear kleptoparatism to puma fitness however is lacking For examplekleptoparatism of leopard (Panthera pardus) kills negatively impacts leopard reproductivesuccess (eg Balme et al 2017) At this time we cannot currently predict whether thereexists an energetic threshold at which point bear kleptoparatism impacts puma fitnessor say definitively that it does Bears also occasionally kill puma kittens (Ruth 2004b LMElbroch amp HB Quigley 2018 unpublished data) and rarely adult pumas (M Jorgensenpers comm 2007) Pumas also occasionally kill black bears (eg Elbroch et al 2014Nichols 2017 LM Elbroch amp HB Quigley 2018 unpublished data)

Jaguar-puma interactions were the most frequently studied competitive interactionamong apex predators in the Americas In contrast to wolf-puma research which has beenconducted with marked individuals telemetry and GPS technology most jaguar-pumaresearch has been conducted with non-invasive camera trapping assessing spatial andtemporal time-sharing of habitats and to a lesser extent dietary overlap through scatanalysis Such studies offer insights into competitive interactions and mechanisms ofcoexistence however this difference in methods likely accounts for the large number ofpublications in which researchers report that they did not detect any competition betweenjaguars and pumas (Table 2) Whereas some authors were certain they found evidence thatjaguars were dominant over pumas (eg Harmsen et al 2009) other researchers fromareas where jaguars are smaller and sometimes numerically fewer than pumas suggestedthe two species may be at least equal in competitive interactions or even that pumas may bedominant over jaguars (eg Gutieacuterrez-Gonzaacutelez amp Loacutepez-Gonzaacutelez 2017) We did discoverfive references that report incidents of jaguars killing pumas (eg Crawsha Jr amp Quigley1984Harmsen et al 2009) whereas we did not find a single documentation of the reverse

Most research we uncovered suggested that pumas were dominant over coyotes manedwolves and felid mesocarnivores This is not unexpected given that pumas outweigh thesespecies by a large margin (Donadio amp Buskirk 2006 De Oliveira amp Pereira 2014) Packs ofcoyotes however do occasionally push pumas from their kills (Harrison 1990) as wellas harass and kill puma kittens (Logan amp Sweanor 2001 Stanford 2013) Neverthelessthere is very little research on the outcomes of competition between pumas and smallercarnivores


Humans of course are also dominant over pumas Human hunting negatively impactspuma population dynamics as well as puma dispersal and metapopulation dynamics(Cooley et al 2009 Stoner et al 2013) Humans are generally the leading cause of death forpumas in non-hunted populations as well (Thompson Jenks amp 2014 Vickers et al 2015)At finer scales pumas shift their activity patterns and habitat use to avoid humans andhuman infrastructure (Sweanor et al 2008 Wilmers et al 2013) as well as abandon foodsources when humans are detected (Smith Wang amp Wilmers 2015)

In the absence of human hunting pumas self-regulate (Seidensticker et al 1973Wallachet al 2015) and exhibit the complex social structures (Wallach et al 2015 Elbroch et al2017b) and hunting strategies (Carbone Teacher amp Rowcliffe 2007) that identify them asapex predators We are however clearly lacking research to help us understand howpumas cope with the stressors of competition with dominant apex carnivores Further welack research that assesses the influence of human non-lethal and lethal effects on pumassimultaneous with the negative effects of competition with other sympatric carnivoresApex predators did not evolve like prey species to contend with top-down selectionpressures (Darimont et al 2015) and therefore human-caused mortalities may be additiveto other natural causes Hunting may also influence the outcomes of competition scenariosamong sympatric carnivores through the removal of key individuals (sensu Bischof et al2017) Perhaps pumas are better adapted to handle human hunting because they arealready subordinate to other species It is also possible however that the combination ofcompetition with dominant carnivores combined with human harvest will lead to rapidpuma declines in some populations

CONCLUSIONSManaging species in complex systems is difficult especially with cryptic species like pumasthat are laborious and expensive to monitor in order to track population dynamicsElucidating the direct and indirect effects of competition in species interactions in naturalmulti-species systems is equally challenging and a topic very much pursued in currentecology (egDroumlge et al 2017 Karanth et al 2017) Our review if nothing else highlightshow little we know about the competitive interactions between pumas and other apexcarnivores or more generally the costs accrued by apex predators during competitiveinteractions with dominant species Therefore we encourage further research intocompetition among apex predators as well as research assessing the effects of competitionin managed systems where pumas and perhaps other predators are hunted as wellUntil the time that we understand whether competitive effects are additive with humanmanagement or even potentially synergistic resulting in unexpected disproportionatedeclines in subordinate predators we encourage caution among managers responsible fordetermining harvest limits for pumas and other subordinate apex carnivores in areas wherethey are sympatric with dominant species Our review for example suggested that pumasare negatively impacted by wolves more than grizzly bears This is important informationfor managers working in regions where wolves and brown bears are recolonizing andrecovering and historic competition scenarios among multiple apex predators are beingrealized


ACKNOWLEDGEMENTSThank you to our team members studying pumas in the southern Yellowstone Ecosystemfor lively discussions relevant to this paper In particular we thank Jennifer Feltner for herassistance gathering references in the early stages of this research

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by The Summerlee Foundation National Science Foundation(graduate fellowship) the Community Foundation of Jackson Hole Pace UniversityEcoTour Adventures PC Fund for Animals Charitable Trust The Tapeats Fund The Leeand Juliet Folger Fund L Westbrook the Scully Family R and L Haberfeld Hogan LLCL and R Holder S and L Robertson R and L Heskett F and B Burgess J Morgan ASmith D Bainbridge T Thomas and many additional donors that contributed throughthe Community Foundation of Jackson Holersquos Old Billrsquos Fun Run many of which wereanonymous The funders had no role in study design data collection and analysis decisionto publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsThe Summerlee Foundation National Science Foundation (graduate fellowship)The Community Foundation of Jackson Hole Pace UniversityEcoTour AdventuresPC Fund for Animals Charitable TrustThe Tapeats FundThe Lee and Juliet Folger FundCommunity Foundation of Jackson Holersquos Old Billrsquos Fun Run

Competing InterestsMark Elbroch is an employee of Panthera Anna Kusler is a graduate student researcherwith Panthera

Author Contributionsbull L Mark Elbroch conceived and designed the experiments performed the experimentsanalyzed the data wrote the paper prepared figures andor tables reviewed drafts of thepaperbull Anna Kusler performed the experiments analyzed the data wrote the paper revieweddrafts of the paper

Data AvailabilityThe following information was supplied regarding data availability

This is a review article and the resources exist in the public domain


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Journal of Wildlife Management 48147ndash155 DOI 1023073808462Akenson J Akenson H Quigley H 2005 Effects of wolf reintroduction on a couar

population in the central Idaho wilderness In Beausoleil RA Martorello DA edsProceedings of the 8th mountain lion workshop Olympia Washington Department ofFish and Wildlife 177ndash187

AllenML Elbroch LM Casady DSWittmer HU 2014a Seasonal variation in thefeeding ecology of pumas (Puma concolor) in northern California Canadian Journalof Zoology 92397ndash403 DOI 101139cjz-2013-0284

AllenML Elbroch LMWilmers CCWittmer HU 2015 The comparative effects oflarge carnivores on the acquisition of carrion by scavengers American Naturalist185822ndash833 DOI 101086681004

AllenMLWilmers CC Elbroch LM Golla JMWittmer HU 2016 The importance ofmotivation weapons and foul odors in driving encounter competition in carnivoresEcology 971905ndash1912 DOI 101002ecy1462

ArjoWM 1998 The effects of recolonizing wolves on coyote populations movementsbehaviors and food habits D Phil Thesis University of Montana Missoula

ArjoWM Pletscher DH 1999 Behavioral responses of coyotes to wolf recoloniza-tion in northwestern Montana Canadian Journal of Zoology 771919ndash1927DOI 101139z99-177

Arnott G Elwood RW 2008 Information gathering and decision making about resourcevalue in animal contests Animal Behaviour 76529ndash542DOI 101016janbehav200804019

Atwood TC 2006Wolves coyotes elk and mule deer predatorndashprey behavioral ecologyin southwest Montana D Phil Thesis Utah State University

Balme GA Robinson HS Pitman RT Hunter LT 2017 Caching reduces klep-toparasitism in a solitary large felid Journal of Animal Ecology 86634ndash644DOI 1011111365-265612654

Bartnick TD Van Deelen TR Quigley HB Craighead D 2013 Variation in cougar(Puma concolor) predation habits during wolf (Canis lupus) recovery in thesouthern Greater Yellowstone Ecosystem Canadian Journal of Zoology 9182ndash93DOI 101139cjz-2012-0147

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Bischof R Bonenfant C Rivrud IM Zedrosser A Friebe A Coulson T Mysterud ASwenson JE 2017 Regulated hunting re-shapes the life history of brown bearsNature Ecology amp Evolution 2116ndash123 DOI 101038s41559-017-0400-7

Boyd DK Neal GK 1992 An adult Cougar Felis concolor killed by Gray Wolves Canislupus in Glacier National Park Montana Canadian Field-Naturalist 106524ndash525

Boyd D OrsquoGara B 1985 Cougar predation on coyotesMurrelet 6617


Bryce CMWilmers CCWilliams TM 2017 Energetics and evasion dynamics of largepredators and prey pumas vs hounds PeerJ 5e3701 DOI 107717peerj3701

Burton AM Navarro Perez S Tovar CC 2003 Bobcat ranging behavior in relationto small mammal abundance on Colima Volcano Mexico Anales Del Instituto deBiologiacutea Serie Zoologiacutea 7467ndash82

Carbone C Teacher A Rowcliffe JM 2007 The costs of carnivory PLOS Biology 5e22DOI 101371journalpbio0050022

Case TJ GilpinME 1974 Interference competition and niche theory Proceedings ofthe National Academy of Sciences of the United States of America 713073ndash3077DOI 101073pnas7183073

Cooley HSWielgus RB Koehler GM Robinson HS Maletzke BT 2009 Does huntingregulate cougar populations A test of the compensatory mortality hypothesisEcology 902913ndash2921 DOI 10189008-18051

Crawsha Jr PG Quigley HB 1984 A ecologia do jaguar ou onca pintada no PantanalIn Relatoacuterio Final Brasiacutelia Instituto Brasileiro de Desenvolvimento Florestal 112

Crawshaw PG 1995 Comparative ecology of ocelot Felis pardalis and jaguar Pantheraonca in a protected subtropical forest in Brazil and Argentina D Phil ThesisUniversity of Florida Gainesville

Crawshaw PG Quigley HB 1991 Jaguar spacing activity and habitat use in aseasonally flooded environment in Brazil Journal of Zoology 223357ndash370DOI 101111j1469-79981991tb04770x

Crombie AC 1947 Interspecific competition Journal of Animal Ecology 1644ndash73DOI 1023071506

Cunningham SC Gustavson CR BallardWB 1999 Diet selection of mountainlions in southeastern Arizona Journal of Range Management 52202ndash207DOI 1023074003681

Darimont CT Fox CH Bryan HM Reimchen TE 2015 The unique ecology of humanpredators Science 349858ndash860 DOI 101126scienceaac4249

Davis ML 2009 Densities habitat-use and mesopredator release of the ocelot in BelizeMS Thesis Virginia Tech University

Davis ML Kelly MJ Stauffer DF 2011 Carnivore co-existence and habitat use inthe Mountain Pine Ridge Forest Reserve Belize Animal Conservation 1456ndash65DOI 101111j1469-1795201000389x

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De la Torre JA De la Riva G 2009 Food habits of pumas (Puma concolor) in a semiaridregion of central MexicoMastozoologiacutea Neotropical 16211ndash216

DeOliveira TG Pereira JA 2014 Intraguild predation and interspecific killing as struc-turing forces of carnivoran communities in South America Journal of MammalianEvolution 21427ndash436

Donadio E Buskirk SW 2006 Diet morphology and interspecific killing in CarnivoraAmerican Naturalist 167524ndash536 DOI 101086501033


Droumlge E Creel S Becker MS Mrsquosoka J 2017 Spatial and temporal avoidance of riskwithin a large carnivore guild Ecology and Evolution 7189ndash199DOI 101002ece32616

Durant SM 1998 Competition refuges and coexistence an example from Serengeticarnivores Journal of Animal Ecology 67370ndash386DOI 101046j1365-2656199800202x

Elbroch LM Feltner J Quigley H 2017Human-carnivore competition for antleredungulates do pumas select for bulls and bucksWildlife Research 44523ndash533DOI 101071WR17006

Elbroch LM Lendrum PE AllenMLWittmer HU 2014 Nowhere to hide pumasblack bears and competition refuges Behavioral Ecology 26(1)247ndash254DOI 101093behecoaru189

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Elbroch LM LevyM Lubell M Quigley H Caragiulo A 2017b Adaptive social behav-iors in a solitary carnivore Science Advances 3e1701218 DOI 101126sciadv1701218

Elbroch LM Loacutepez-Gonzaacutelez C Fitzgerald F Kusler A Quigley H 2017c Attractionndashrepulsion among top predators following reintroduction effortsMammalian Biology8666ndash69 DOI 101016jmambio201704003

Elbroch LM OrsquoMalley C Peziol M Quigley HB 2017a Vertebrate diversity benefitingfrom carrion provided by pumas and other subordinate apex felids BiologicalConservation 215123ndash131 DOI 101016jbiocon201708026

Emmons LH 1987 Comparative feeding ecology of felids in a Neotropical rainforestBehavioral Ecology and Sociobiology 20271ndash283 DOI 101007BF00292180

Foster RJ Harmsen BJ Doncaster CP 2010Habitat use by sympatric jaguars andpumas across a gradient of human disturbance in Belize Biotropica 42724ndash731DOI 101111j1744-7429201000641x

Foster VC Sarmento P Sollmann R Tocircrres N Jaacutecomo AT Negrotildees N Fonseca CSilveira L 2013 Jaguar and puma activity patterns and predatorndashprey interactionsin four Brazilian biomes Biotropica 45373ndash379 DOI 101111btp12021

Gutieacuterrez-Gonzaacutelez CE Loacutepez-Gonzaacutelez CA 2017 Jaguar interactions with pumas andprey at the northern edge of jaguarsrsquo range PeerJ 5e2886 DOI 107717peerj2886

Harihar A Pandav B Goyal SP 2011 Responses of leopard Panthera pardus to therecovery of a tiger Panthera tigris population Journal of Applied Ecology 48806ndash814DOI 101111j1365-2664201101981x

Harmsen BJ Foster RJ Silver SC Ostro LE Doncaster CP 2009 Spatial and temporalinteractions of sympatric jaguars (Panthera onca) and pumas (Puma concolor) in aneotropical forest Journal of Mammalogy 90612ndash620DOI 10164408-MAMM-A-140R1

Harrison S 1990 Cougar predation on bighorn sheep in the Junction Wildlife Manage-ment Area British Columbia MS Thesis University of British Columbia


Hass CC 2009 Competition and coexistence in sympatric bobcats and pumas Journal ofZoology 278174ndash180 DOI 101111j1469-7998200900565x

HaywardMW Kerley GI 2008 Prey preferences and dietary overlap amongstAfricarsquos large predators South African Journal of Wildlife Research 3893ndash108DOI 1039570379-4369-38293

Hernaacutendez-SaintMartiacuten AD Rosas-Rosas OC Palacio-Nuacutentildeez J Tarango-ArambulaLA Clemente-Saacutenchez F Hoogesteijn AL 2013 Activity patterns of jaguar pumaand their potential prey in San Luis Potosi Mexico Acta Zooloacutegica Mexicana29520ndash533

Hernaacutendez-SaintMartiacuten AD Rosas-Rosas OC Palacio-Nuacutentildeez J Tarango-ArambulaLA Clemente-Saacutenchez F Hoogesteijn AL 2015 Food habits of jaguar and puma ina protected area and adjacent fragmented landscape of Northeastern Mexico NaturalAreas Journal 35308ndash317 DOI 1033750430350213

Holt RD Polis GA 1997 A theoretical framework for intraguild predation AmericanNaturalist 149745ndash764 DOI 101086286018

HornockerWildlife Institute 2001 Cougar-wolf interactions in Yellowstone NationalPark competition demographics and spatial relationships Cumulative annualtechnical report Bozeman Montana

Hutchinson GE 1957 Concluding remarks Cold Spring Harbor Symposia on Quantita-tive Biology 22415ndash427 DOI 101101SQB195702201039

International Union for Conservation of Nature (IUCN) 2010 Canis lupus The IUCNRed List of Threatened Species Version 2017-2 Available at httpwwwiucnredlistorg (accessed on 06 Jue 2017)

International Union for Conservation of Nature (IUCN) 2015 Puma concolor TheIUCN Red List of Threatened Species Version 2016-3 Available at httpwwwiucnredlistorg (accessed on 11 December 2016)

International Union for Conservation of Nature (IUCN) 2016 Ursus americanus TheIUCN Red List of Threatened Species Version 2017-2 Available at httpwwwiucnredlistorg (accessed on 06 Jue 2017)

International Union for Conservation of Nature (IUCN) 2017 IUCN Spatial DataResources Available at httpwwwiucnredlistorg technical-documents red-list-training iucnspatialresources (accessed on 18 December 2017)

International Union for Conservation of Nature SSC Bear Specialist Group IUCN andIBA 2017 Ursus arctos The IUCN Red List of Threatened Species Version 2017-2Available at httpwwwiucnredlistorg (accessed on 6 June 2017)

JimenezMD Asher VJ Bergman C Bangs EEWoodruff SP 2008 Gray WolvesCanis lupus Killed by Cougars Puma concolor and a Grizzly Bear Ursus arctos inMontana Alberta and Wyoming The Canadian Field-Naturalist 122(1)76ndash78DOI 1022621cfnv122i1550

JimenezMDWoodruff SP Cain S Dewey S 2006 Wolf-elk interactions on winterrange and state-managed feed grounds in Wyoming Progress report US Fish andWildlife Service Jackson


Karanth KU Srivathsa A Vasudev D Puri M Parameshwaran R Kumar NS2017 Spatio-temporal interactions facilitate large carnivore sympatry acrossa resource gradient Proceedings of the Royal Society B 284Article 2016186DOI 101098rspb20161860

Kleiman DG Eisenberg JF 1973 Comparisons of canid and felid social systems from anevolutionary perspective Animal Behaviour 21637ndash659DOI 101016S0003-3472(73)80088-0

Knopff KH Knopff AA Kortello A Boyce MS 2010 Cougar kill rate and prey com-position in a multiprey system Journal of Wildlife Management 741435ndash1447DOI 101111j1937-28172010tb01270x

Koehler GM Hornocker MG 1991 Seasonal resource use among mountain lionsbobcats and coyotes Journal of Mammalogy 72391ndash396 DOI 1023071382112

Kortello AD Hurd TE Murray DL 2007 Interactions between cougars (Puma con-color) and gray wolves (Canis lupus) in Banff National Park Alberta Ecoscience14214ndash222 DOI 1029801195-6860(2007)14[214IBCPCA]20CO2

Krebs J Lofroth EC Copeland J Banci V Cooley D Golden H Magoun A Mulders RShults B 2004 Synthesis of survival rates and causes of mortality in North Americanwolverines Journal of Wildlife Management 683493ndash3502

Kunkel KE Ruth TK Pletscher DH Hornocker MG 1999Winter prey selection bywolves and cougars in and near Glacier National Park Montana Journal of WildlifeManagement 63901ndash910 DOI 1023073802804

Le Bourlot V Tully T Claessen D 2014 Interference versus exploitative competitionin the regulation of size-structured populations American Naturalist 184609ndash623DOI 101086678083

Lendrum PE Elbroch LM Quigley H Thompson DJ JimenezM Craighead D 2014Home range characteristics of a subordinate predator selection for refugia or huntopportunity Journal of Zoology 29458ndash66 DOI 101111jzo12153

Lewis JS Bailey LL VandeWoude S Crooks KR 2015 Interspecific interactions betweenwild felids vary across scales and levels of urbanization Ecology and Evolution55946ndash5961 DOI 101002ece31812

Logan KA Sweanor LL 2001Desert puma evolutionary ecology and conservation of anenduring carnivore Washington DC Island Press

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Loacutepez-Gonzaacutelez C Gonzaacutelez-Romero G 1998 A synthesis of current literature andknowledge about the ecology of the puma (Puma concolor) Acta Zoologica Mexicana75171ndash190

Lourenco R Penteriani V Rabaca JE Korpimaumlki E 2013 Lethal interactions amongvertebrate top predators a review of concepts assumptions and terminologyBiological Reviews 89270ndash283 DOI 101111brv12054

Lowrey B Elbroch LM Broberg L 2016 Is individual prey selection driven by chanceor choice A case study in cougars (Puma concolor)Mammal Research 61353ndash359DOI 101007s13364-016-0292-y


Mahoney PJ 2017 Spatial ecology of coyotes and cougars understanding the influenceof multiple prey on the spatial interactions of two predators D Phil Thesis UtahState University Logan

Martins R Quadros J Mazzolli M 2008Habito alimentar e interferecircncia antroacutepica naatividade de marcacatildeo territorial do Puma concolor e Leopardus pardalis (CarniacutevoraFelidae) e outros carniacutevoros na Estacatildeo Ecoloacutegica de Jureacuteia-Itatins Satildeo Paulo BrasilRevista Brasileira de Zoologia 25427ndash435 DOI 101590S0101-81752008000300007

Massara RL Paschoal AM Bailey LL Doherty PF Chiarello AG 2016 Ecologicalinteractions between ocelots and sympatric mesocarnivores in protected areas ofthe Atlantic Forest southeastern Brazil Journal of Mammalogy 971634ndash1644DOI 101093jmammalgyw129

Mattson DJ 2014 State-level management of a common charismatic predator moun-tain lions of the west In Clark SG Rutherford MB eds Large carnivore conservationintegrating science and policy in North America Chicago University of Chicago Press29ndash64

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Moreno RS Kays RW Samudio Jr R 2006 Competitive release in diets of ocelot(Leopardus pardalis) and puma (Puma concolor) after jaguar (Panthera onca) declineJournal of Mammalogy 87808ndash816 DOI 10164405-MAMM-A-360R21

Murphy KM Felzien GS Hornocker MG Ruth TK 1998 Encounter competitionbetween bears and cougars some ecological implications Ursus 155ndash60

Murphy T MacDonald DW 2010 Pumas and people lessons in the landscape oftolerance from a widely distributed felid In MacDonald DW Loveridge AJ edsBiology and conservation of wild felids Oxford Oxford University Press 431ndash452

Nichols B 2017 Foraging ecology of mountain lions in the Sierra National ForestCalifornia MS Thesis Utah State University

Novack AJ MainMB Sunquist ME Labisky RF 2005 Foraging ecology of jaguar(Panthera onca) and puma (Puma concolor) in hunted and non-hunted siteswithin the Maya Biosphere Reserve Guatemala Journal of Zoology 267167ndash178DOI 101017S0952836905007338

Ordiz A Bischof R Swenson JE 2013 Saving large carnivores but losing the apexpredator Biological Conservation 168128ndash133 DOI 101016jbiocon201309024

Palomares F Adrados B ZaninM Silveira L Keller C 2017 A non-invasivefaecal survey for the study of spatial ecology and kinship of solitary felidsin the Viruaacute National Park Amazon BasinMammal Research 62241ndash249DOI 101007s13364-017-0311-7


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Parker GA Stuart RA 1976 Animal behavior as a strategy optimizer evolution ofresource assessment strategies and optimal emigration thresholds AmericanNaturalist 1101055ndash1076 DOI 101086283126

Paviolo A Blanco YE De Angelo CD Di Bitetti MS 2009 Protection affects the abun-dance and activity patterns of pumas in the Atlantic Forest Journal of Mammalogy90926ndash934 DOI 10164408-MAMM-A-1281

Polis GA Holt RD 1992 Intraguild predation the dynamics of complex trophic interac-tions Trends in Ecology and Evolution 7151ndash155 DOI 1010160169-5347(92)90208-S

Riley SJ Nesslage GMMaurer BA 2004 Dynamics of early wolf and cougar eradi-cation efforts in Montana implications for conservation Biological Conservation119575ndash579 DOI 101016jbiocon200401019

RippleWJ Estes JA Beschta RLWilmers CC Ritchie EG Hebblewhite M Berger JElmhagen B Letnic M NelsonMP Schmitz OJ Smith DWWallach ADWirsingAJ 2014 Status and ecological effects of the worldrsquos largest carnivores Science343Article 1241484 DOI 101126science1241484

Ritchie EG Johnson CN 2009 Predator interactions mesopredator release andbiodiversity conservation Ecology Letters 12982ndash998DOI 101111j1461-0248200901347x

Romero-Munoz A Maffei L Cueacutellar E Noss AJ 2010 Temporal separation betweenjaguar and puma in the dry forests of southern Bolivia Journal of Tropical Ecology26303ndash311 DOI 101017S0266467410000052

Ruth TK 2004a Ghost of the Rockies the Yellowstone cougar project YellowstoneScience 1213ndash24

Ruth TS 2004b Patterns of resource use among cougars and wolves in northwesternMontana and southeastern British Columbia D Phil Thesis University of Idaho

Ruth TK Buotte PC 2007 Cougar ecology and cougar-carnivore interactions inYellowstone National Park Final technical report Hornocker Wildlife InstituteBozeman

Ruth TK Hornocker MG 1996 Interactions between cougars and wolves (and a bear ortwo) in the North Fork of the Flathead River Montana InMountain Lion WorkshopSacramento California Department of Fish and Game

Ruth TK Murphy K 2010 Competition with other carnivores for prey In HornockerM Negri S eds Cougar ecology and conservation Chicago University of ChicagoPress 138ndash162

Sandell M 1989 The mating tactics and spacing patterns of solitary carnivores In Git-tleman JL ed Carnivore behavior ecology and evolution Ithaca Cornell UniversityPress 164ndash182

Scantlebury DMMills MGWilson RPWilson JWMills ME Durant SM BennettNC Bradford P Marks NJ Speakman JR 2014 Flexible energetics of cheetah


hunting strategies provide resistance against kleptoparasitism Science 34679ndash81DOI 101126science1256424

Schaller GB Crawshaw Jr PG 1980Movement patterns of jaguar Biotropica12161ndash168 DOI 1023072387967

Schmidt KP Gunson JR 1985 Evaluation of wolf-ungulate predation near NordeggAlberta Second Year Progress Report 1984ndash85 Alberta Energy and NaturalResources Fish and Wildlife Division Edmonton

Schoener TW 1983 Field experiments on interspecific competition American Naturalist122240ndash285 DOI 101086284133

Scognamillo D Maxit IE Sunquist M Polisar J 2003 Coexistence of jaguar (Pantheraonca) and puma (Puma concolor) in a mosaic landscape in the Venezuelan llanosJournal of Zoology 259269ndash279 DOI 101017S0952836902003230

Seidensticker JCJ Hornocker MGWilesWVMessick JP 1973Mountain lion socialorganization in the Idaho primitive areaWildlife Monographs 351ndash60

Smith JAWang YWilmers CC 2015 Top carnivores increase their kill rates on preyas a response to human-induced fear Proceedings of the Royal Society of London BBiological Sciences 282Article 20142711 DOI 101098rspb20142711

Sollmann R FurtadoMM Hofer H Jacomo AT Tocircrres NM Silveira L 2012 Usingoccupancy models to investigate space partitioning between two sympatric largepredators the jaguar and puma in central BrazilMammalian Biology 7741ndash46DOI 101016jmambio201106011

Stanford J 2013 Coyotes tame lions on refuge JHunderground [Blog Post] Available athttpwwwjhundergroundcom20130331 coyotes-tame-lions-on-refuge

Stoner DCWolfe ML RiethWR Bunnell KD Durham SL Stoner LL 2013 De factorefugia ecological traps and the biogeography of anthropogenic cougar mortality inUtah Diversity and Distributions 191114ndash1124 DOI 101111ddi12035

Sweanor LL Logan KA Bauer JWMillsap B BoyceWM 2008 Pumandashhuman relation-ships in Cuyamaca Rancho State Park California Journal of Wildlife Management721076ndash1084 DOI 1021932007-024

Taber AB Novaro AJ Neris N Colman FH 1997 The food habits of sympatric jaguarand puma in the Paraguayan Chaco Biotropica 29204ndash213DOI 101111j1744-74291997tb00025x

Thompson DJ Jenks JA Fecske DM 2014 Prevalence of human-caused mortality in anunhunted cougar population and potential impacts to managementWildlife SocietyBulletin 38341ndash347 DOI 101002wsb390

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Treves A 2009Hunting for large carnivore conservation Journal of Applied Ecology461350ndash1356 DOI 101111j1365-2664200901729x

Trolle M Noss AJ Lima ED Dalponte JC 2007 Camera-trap studies of maned wolfdensity in the Cerrado and the Pantanal of Brazil Biodiversity and Conservation161197ndash1204 DOI 101007s10531-006-9105-y


US Fish andWildlife Service 1995 Annual report of the Rocky Mountain InteragencyWolf Recovery Program Helena Montana Washington DC US Fish and WildlifeService

Vanak AT Fortin D Thaker M OgdenM Owen C Greatwood S Slotow R 2013Moving to stay in place behavioral mechanisms for coexistence of African Largecarnivores Ecology 942619ndash2631 DOI 10189013-02171

Vickers TW Sanchez JN Johnson CK Morrison SA Botta R Smith T CohenBS Huber PR Ernest HB BoyceWM 2015 Survival and mortality of pumas(Puma concolor) in a fragmented urbanizing landscape PLOS ONE 100131490DOI 101371journalpone0131490

Wallach AD Izhaki I Toms JD RippleWJ Shanas U 2015What is an apex predatorOikos 1241453ndash1461 DOI 101111oik01977

Wang Y AllenMLWilmers CC 2015Mesopredator spatial and temporal responses tolarge predators and human development in the Santa Cruz Mountains of CaliforniaBiological Conservation 19023ndash33 DOI 101016jbiocon201505007

White PA Boyd DK 1989 A cougar Felis concolor kitten killed and eaten by graywolves Canis lupus in Glacier National Park Montana Canadian Field-Naturalist103408ndash409

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Wilmers CCWang Y Nickel B Houghtaling P Shakeri Y AllenML Kermish-Wells J Yovovich VWilliams T 2013 Scale dependent behavioral responsesto human development by a large predator the puma PLOS ONE 860590DOI 101371journalpone0060590


Subjects Biodiversity Conservation Biology Ecology Natural Resource ManagementKeywords Puma concolor Subordinate Dominance Competition Gray wolf Grizzly bearAmerican black bear Jaguar Apex predators

INTRODUCTIONThe outcome of interspecific competition affects species fitness community assemblagesand structure and the geographic distributions of species (Schoener 1983 Polis amp Holt1992 Le Bourlot Tully amp Claessen 2014 Droumlge et al 2017) Much of competition isindirect and competitors generally assess the competitive abilities (eg resource holdingpotential Parker amp Stuart 1976) of their opponents before deciding to engage themresulting in established species hierarchies that mitigate the need for fighting (Arnott ampElwood 2008) In fact the established lsquolsquosuperiorityrsquorsquo (Crombie 1947) of one species overanother contributes to Hutchinsonrsquos (1957) differentiation between the fundamental andrealized niche A speciesrsquo enemies include both predators and competitors both of whichlimit an animalrsquos distribution to its realized niche (eg wild dogs Lycaon pictus in Droumlgeet al 2017) This is especially important for carnivores in multi-carnivore guilds in whichcompetition contributes to intraguild killing (Polis amp Holt 1992 Donadio amp Buskirk 2006)and whether a species self-regulates its population through various social mechanisms oris instead regulated by another predator (Wallach et al 2015)

Carnivores disproportionately influence ecological functions in natural systems andare culturally important (Ripple et al 2014) Most carnivores however are also fearedand persecuted because of perceived and real threats to human safety and because theykill livestock household pets and game species we value (Ordiz Bischof amp Swenson 2013Ripple et al 2014 Elbroch Feltner amp Quigley 2017) Not all carnivores are ecologicallyequivalent however and size betrays stark differences in small versus large carnivoresCarbone Teacher amp Rowcliffe (2007) found that carnivores lt20 kg exhibited differenthunting strategies and energetic budgets than carnivores gt20 kg and Wallach et al (2015)found that carnivores lt15 kg exhibited additional differences in life history strategiesthan those species gt15 kg Specifically Wallach et al (2015) reported that carnivoresgt15 kg self-regulate through social mechanisms and density-dependence whereas smallercarnivores are generally limited by predation by larger carnivores Wallach et al (2015)subsequently used 15 kg to differentiate between lsquolsquoapex predatorsrsquorsquo and smaller carnivoresFor our review we also utilized the 15-kg cutoff

Apex predators too are not ecologically equivalent and vary in size morphologyweapons and life history strategies (Kleiman amp Eisenberg 1973 Bekoff Daniels ampGittleman 1984 Sandell 1989) These differences have resulted in established thoughsometimes variable dominance hierarchies aswell as the uniquemorphology andbehaviorsutilized by subordinate species coping with the pressures of interspecific competition Forexample pumas (Puma concolor) and cheetahs (Acinonyx jubatus) appear to withstandhigh levels of kleptoparatism without obvious influences on their fitness (Scantlebury et al2014 Elbroch et al 2017a) and coyotes (Canis latrans) wild dogs (Lycaon pictus) leopards(Panthera pardus) and cheetahs utilize temporal and spatial competition refuges and other






















































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are pumas subordinate carnivores, and does it matter? · 2018. 1. 24. · wallach et al. (2015)...

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