Behaviour 151 (2014) 819–840

brill.com/beh

Puma communication behaviours: understanding
functional use and variation among sex and age classes
Maximilian L. Allen a,∗ , Heiko U. Wittmer a and Christopher C. Wilmers baSchool of Biological Sciences, Victoria University of Wellington,
P.O. Box 600, Wellington 6140, New ZealandbCenter for Integrated Spatial Research, Environmental Studies Department,
University of California, 1156 High Street, Santa Cruz, CA, 95064, USA* Corresponding author’s e-mail address: Maximilian.Allen@vuw.ac.nz
Accepted 30 December 2013; published online 4 February 2014

Abstract
Intraspecific communication for mate selection sometimes varies between sexes based on different evolutionary life history patterns. Solitary felids use communication for territorial defence andlocation of mates, for which they use scent-marking behaviours including scraping, urine spraying, body rubbing, caterwauling, cheek rubbing, and the flehmen response, but these behaviours
are not well understood in pumas (Puma concolor). We used motion-triggered video cameras to
document the use of communication behaviours by male and female pumas, and used a seriesof experimental treatments to determine the mechanisms and importance of visual and olfactory
cues in puma scrapes. We found that pumas use the physical scrape to locate communications, andthen use urine to convey and interpret the communication itself. We also found significant differences among puma age and sex classes in the proportion of use and duration of time behaviours
were displayed. Mature males spent significantly longer durations (x = 22.1 s) on producing behaviours (scraping, body rubbing, and caterwauling behaviours) than mature females (x = 3.3 s),
and males used scraping (78.5%) and body rubbing (12.4%) behaviours at a higher proportion ofvisits than females (13.6 and 2.7%, respectively). Mature females spent significantly longer durations (x = 30.4 s) on consuming behaviours (investigating and flehmen response behaviours) thanmature males (x = 13.7 s), and females used flehmen response (30.6%) and caterwauling (9.3%)
behaviours at a higher proportion of visits than mature males (6.5% flehmen and 0.4% caterwauling). Male reproductive strategy appears based on advertisement for possible mates, while female
reproductive strategy appears based on assessment of possible mates. The use of communication
behaviours also appears to develop with age, as immature pumas rarely visited and acted as nonparticipants in communication behaviours.

Keywords
behaviour, communication, puma, Puma concolor, reproduction strategy, scent-marking,scraping, sexual dimorphism.
© 2014 Koninklijke Brill NV, Leiden

DOI:10.1163/1568539X-00003173

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1. Introduction
Communication, defined as the transfer of information by an individual orgroup to another individual or group (Gunderson, 1976), is an importantcomponent to understanding functions and evolution of animal behaviour.
Intraspecific communication is important because it is one of the key aspectsof social organization, and has been shown to directly affect individual fitness (Breed & Moore, 2011; Davies et al., 2012). The use of intraspecificcommunication for mate selection is often dramatically different between
sexes, and based on different evolutionary reproductive strategies (Logan &Sweanor, 2001; Breed & Moore, 2011; Davies et al., 2012). How drastic
the sexually dimorphic differences in communication are varies among taxonomic groups and depends upon life history patterns (Verberne & Leyhausen,
1976; Mellen, 1993).
Many solitary felids exhibit sexually dimorphic traits in both communication and life history patterns, including their use of scent-marking andcourtship behaviours (Logan & Sweanor, 2001; Sunquist & Sunquist, 2002;
Harmsen et al., 2010). Solitary felids have spatially dispersed populations
and intraspecific communication is most frequently via indirect signals
through scent-marking (Seidensticker et al., 1973; Smith et al., 1989; Bailey, 1993; Logan & Sweanor, 2001, 2010; Harmsen et al., 2010). Due tothis, their most frequent forms of communication are visual and olfactorysignals, along with less common auditory and tactile signals (Bailey, 1993;
Logan & Sweanor, 2001, 2010; Sunquist & Sunquist, 2002). In many species
males create scent-marks more often than females (Seidensticker et al.,
1973; Logan & Sweanor, 2001, 2010; Sunquist & Sunquist, 2002; Harmsen et al., 2010). Mellen (1993) documented a variety of communication
behaviours in captive felids, including scraping, urine spraying, and bodyrubbing (see Table 2 for definitions), with sexually dimorphic tendencies inmany species. However, the differences in the use of communication behaviours between sexes and the mechanisms behind mate selection among
different felid species are understudied.
Though many aspects of puma (Puma concolor) behaviour are similar
to other felids (Sunquist & Sunquist, 2002), they differ in their distribution pattern and reproductive behaviours. Most large felids inhabit equatorial
regions, and breed throughout the year (e.g., cheetahs, Acinonyx jubatus,
and jaguars, Panthera onca), while most felids that inhabit northern latitudes (i.e., Eurasian Lynx, Lynx lynx, Bobcat, L. rufus, Canada Lynx, L.

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canadensis, European Wildcat, Felis silvestris) are smaller and have very
short breeding periods during the late winter or early spring (Sunquist & Sunquist, 2002). Pumas range extends high into northern and southern latitudes
in the Americas (Sunquist & Sunquist, 2002), and unlike most other felids
in northern latitudes, they mate throughout the year (though there are otherexceptions, e.g., tiger, Pantera tigris, and leopard, Panthera pardus). Logan& Sweanor (2001, 2010) hypothesized that the result of pumas being spatially dispersed and reproductive behaviours occurring throughout the year,
has led to sexually dimorphic evolutionary reproductive strategies, including
the avoidance of males by females when they are raising young. If so, thesestrategies would extend to their use of communication behaviours, which areimportant to the success of the strategy.
Pumas use indirect methods of scent-marking and other behaviours tocommunicate with conspecifics. The most common form of puma communication is scraping (Currier, 1983; Logan & Sweanor, 2001), which is acombination of visual and olfactory signals. Scrapes are depressions in the
ground excavated by the puma’s hind feet, most commonly comprised ofleaf litter or duff, and usually accompanied by urine and occasionally faeces(Seidensticker et al., 1973; Currier, 1983; Logan & Sweanor, 2001; Elbroch,
2003). Currently, the relative importance of visual and olfactory components
in scrape communications is unknown (Logan & Sweanor, 2010). Scrapes
are regularly created along territorial boundaries or prominent travel-ways(Seidensticker et al., 1983; Logan & Sweanor, 2010), and are thought to bemade primarily by adult males and less often or not at all by females or
sub-adult males (Seidensticker et al., 1983; Logan & Sweanor, 2001, 2010;
Harmsen et al., 2010). Other communication behaviours used by pumas inconjunction with scraping behaviour include caterwauling, cheek rubbing,and the flehmen response (Verberne & Leyhausen, 1976; Mellen, 1993;
Harmsen et al., 2010; McBride & McBride, 2010; McBride & Sensor, 2012).
We initiated a study to determine intraspecific functions of scraping behaviour based on videos recorded by motion-triggered cameras placed at
known scent-marking areas of pumas in California. Our first objective wasusing an experimental treatment design to determine the mechanisms andimportance of different components of scrapes. We hypothesized that visual cues (the physical scrape) would be used to locate the scrape, while
olfactory cues (the urine) would be used to transmit signals (hypotheses foreach treatment noted in Table 1). Our second objective was to determine

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Puma communication use and variation

Table 1.
Design and hypotheses for the experimental treatment sets.
Set

0-a
0-b
0-ab
a-b
a-ab
b-ab

DesignHypotheses

0

a

b

ab

First detection

Investigation rate

Investigation duration

+
+
+
−
−
−

+
−
−
+
+
−

−
+
−
+
−
+

−
−
+
−
+
+

0<a
0<b
0 < aba<ba < abb = ab0<a0<b0 < aba<ba < abb = ab0<a0<b0 < aba>ba = abb < abThe design shows the composition of the variables present at each experimental treatment
set. The hypotheses show how we expected variables to perform against each other, including
first detection rates, investigation rates, and investigation duration. 0, control (nothing); a,puma urine; b, physical scrape; ab, puma urine and physical scrape.

whether scraping and associated behaviours were used in different proportions or durations by sex and age classes, based on the hypothesis of Logan& Sweanor (2001, 2010) that male and female pumas have evolutionarily
different breeding strategies. We first set out to determine if differences occurred in the proportion of use of communication behaviours among puma
sex and age classes (hypotheses for each behaviour noted in Table 2). We
next set out to determine if puma sex and age classes spent different durationsof time displaying producing (scraping, body rubbing, and caterwauling behaviours) and consuming (investigating and flehmen response behaviours)
behaviours at scrapes (hypotheses noted in Table 2).
2. Materials and methods
2.1. Study area
We conducted our study in a 17 000 km2 study area in the Santa Cruz Mountains, including parts of Santa Cruz, San Mateo, and Santa Clara counties ofCalifornia (Figure 1). The puma population is not hunted and was considered to be at high density, with most mortality caused by humans (e.g., killed
due to livestock depredations or through vehicle collisions). The study area
was bounded by the Pacific Ocean to the west, the cities of San Francisco
and San Jose to the north, and Highway 101 to the east. A major highway(Highway 17) bisects the study area. Major habitat types in the study area

Definition

Where the puma scraped in
substrate with their hind feetand sometimes urinated and/or
defecated on the scrape

Where the puma is using its
olfactory sense to investigate
cues and signals, noted by thepumas nose within 15 cm of ascrape or other cue

Where the puma rubs its cheekor shoulder on the ground, astump, or tree branch, or rolls
back and forth on the ground

Where the puma gives a loudand reverberating callcharacterized by multiplechanges in pitch

Behaviour

Scraping

Olfactory investigation

Body rubbing

Caterwauling

Mature females will caterwaul
at higher rates than otherclassesMature males will body rub at
higher rates than other classes

Investigation rates will besimilar among all three classes

Mature males will scrape athigher rates than other classes

Hypothesis

Females are thought to caterwaul to attract
prospective mates when they are in oestrus;
this behaviour has not been recorded inmales

Due to female mate choice and maleterritoriality, we expect males to advertise
their presence most frequently

Because scraping behaviour is the mostcommon form of intraspecificcommunication, we would expect allclasses of pumas to be investigating at
equal rates

Due to female mate choice and maleterritoriality, we expect males to advertise
their fitness most often, and expect females
to advertise only when in oestrus

Rationale

Table 2.
Definitions of puma communication behaviours, and our hypotheses regarding differences in the proportion and duration of communication
behaviours among puma sex and age classes.
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Where the puma picked up its
head and curled back its upper
lip, sometimes arching its neckbackwards, in order to expose
its vomeronasal organ

The communication behavioursof scraping, body rubbing, andcaterwauling

The communication behavioursof investigating and flehmen
responses

Flehmen response

ProducingConsuming
Mature females would spend
longer durations on consuming
behaviours than other classes

Mature males would spend
longer durations on producing
behaviours than other classes

Mature female flehmen
response rates will be higher
than other classes

Hypothesis

If female puma strategy is based on
assessment they would be motivated toassess the status of all possible mates andspend longer durations consuming signals
than other classes

If male strategy is based on advertisement
they would be motivated to spend longer
durations producing signals for prospective
mates to find than other classes

Because the flehmen response is used toassess potential mates, females will use
flehmen response at higher rates based onclassic female choice theory

Rationale

Puma classes include mature males and females (2.5 years) and immature pumas (<2.5 years). The behaviour hypotheses regard the
proportion of visits where pumas of each class would exhibit the five behaviours, while the producing and consuming hypotheses regard thedifferences in duration between puma classes.

Definition

Behaviour

Table 2.
(Continued.)

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825

Figure 1. A map of the study area, which included areas in Santa Cruz, San Mateo and Santa
Clara Counties in California. The study area is outlined by the thick black line, within thegreater context of major highways and the cities of Santa Cruz and San Jose, and the locationof each camera is noted.

changed with distance from the coast, and included: coastal scrub, coastal
oak woodland, annual grassland, redwood (Sequoia sempervirens), montane
hardwood–conifer, montane riparian, mixed chaparral, montane chaparral,montane hardwood, ponderosa pine (Pinus ponderosa), eucalyptus, valley
foothill riparian, and valley oak woodland (Mayer & Laundenslayer, 1988).
Elevation ranged from sea level to 1155 m, and the climate is best describedas mild Mediterranean. Historical average daily high temperatures ranged
from 15.5–24.4°C and average daily low temperatures ranged from 3.9–
11.1°C. The annual rainfall varied from 58–121 cm, the majority of which
occurred from November to April (Wilmers et al., 2013).
2.2. Definitions and field methods
Among puma biologists there has arisen a unique and dispersed terminology
regarding scraping behaviour; for the purposes of this study, we differentiated between what we termed ‘individual scrapes’ and ‘community scrapes’.
Individual scrapes are the outcome of scraping behaviour — at its most simple, a scrape. Community scrapes are defined as scrape areas used regularly
to communicate with conspecifics, and are therefore used by more than one
puma. These areas were previously described by Logan & Sweanor (2001)

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Puma communication use and variation

as shared scrape sites, and by Harmsen et al. (2010) as scrape clusters. Community scrapes were identified by an abundance of scrapes in a concentrated
area (roughly 3 scrapes within 9 m2 , though this can vary depending on
substrate and visitation), which had no association with either kill or bedding sites.
Our first step was to find and document individual and community scrapes.
We initially found community scrapes by searching dominant landscape features, areas commonly used by pumas, and by following puma tracks acrossthe landscape. As the study progressed, we used a modification of a custom program we had developed for identifying kill sites through GPS data,
and used it to locate potential community scrapes based on clusters of GPS
locations more than 7 days apart from each other in time (Wilmers et al.,2013). We used the data from our first 9 males (ages 2.5–9 years) and thenvisited these sites and searched the area for the presence of scrapes. We took
measurements of width and length of individual scrapes and accompanying
tracks to confirm the scrapes were created by pumas (Elbroch, 2003). We
set up motion-triggered video cameras with infrared flash (Bushnell TrophyCam, Overland Park, KS, USA) at 26 spatially independent community
scrapes for the experimental treatments (see below), with each community
scrape being at least, 200 m from each other. We then added additional cameras for monitoring communication behaviours, though not always spatiallyindependent, for a total of 45 community scrapes monitored. The cameras
were programmed for maximum recording and viewing, with a set-up torecord a 60 s video every time motion was detected with a 1 s delay before
triggering again.
We concurrently captured 36 pumas from 2008–2012 using trailinghounds, cage traps, or leg-hold snares. Upon capture pumas were anesthetized with Telazol (Fort Dodge Animal Health, Fort Dodge, IA, USA).
Once anesthetized, pumas were sexed, weighed and measured, and thenfit with an ear tag and a combined GPS/radio telemetry collar (Vectronics Aerospace, Berlin, Germany). The Independent Animal Care and Use
Committee at the University of California, Santa Cruz approved all animalhandling procedures. When possible, individual collared pumas detected on
cameras were identified by unique collar identifiers and/or ear tags, whilepumas without collars were identified by the spotting patterns on the insideof the upper leg and other unique features including scarring, kinks in theirtail, and old injuries (Kelly et al., 2008). During captures age was deter-M.L. Allen et al. / Behaviour 151 (2014) 819–840

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mined through measurements of gum line recession (Laundré et al., 2000)
for each individual. When possible, we determined the sex and age classes(mature > 2.5 years old, immature < 2.5 years old) for individuals without
collars through the position of genitals and external physical characteristics(Ashman et al., 1983; Currier, 1983).
2.3. Experimental treatments design
After community scrapes were located, we created a series of experimental
treatments at 26 community scrapes, to determine the roles of the visualand olfactory cues in puma individual scrapes. We created the experimental
treatments based on a crossover design (Table 1), and distributed the paired
experimental treatments in a random design. Each community scrape wasgiven a numeric label, and each treatment variable pair was assigned to anumbered community scrape, before rotating to the next sequential number
the following month. Each community scrape had a most common routeof travel for the pumas (though the pumas were as likely to enter or exitfrom either direction). We determined the most likely route of travel, andcreated the treatment variables on either side of this route to allow equal
probability of detection. This was accounted for in the random design witheach treatment variable pair switching sides (from left to right from thecameras perspective) in the sequential pairs. The experimental treatments
involved 6 different pairs of scrape variables; the designs each involve thepresence or absence of male puma urine (a), a physical scrape (b) and control(0). We used the first visit by a puma to each experimental treatment set as
our samples for analyses.
All experimental treatments were created by the same person to control
for reliability and variation. Physical scrape components were created byhand using scent-free latex gloves, and we administered 0.5 ml of puma
urine from a glass eyedropper for the urine components. For the control, we
did not use either a physical scrape or urine, and instead patted the groundwith gloved hands three times to control for human presence or any novel
scents created at the community scrape. We purchased the un-neutered malepuma urine from a captive facility (InHeatScents, Troy, AL, USA) where
they collected the urine from live pumas. The set of experimental treatments
were monitored for 3–4 weeks, and then at the end of the monitoring period
we raked the community scrape and created the new set of experimental
treatments based on our random design.

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Puma communication use and variation

We viewed each video for puma activity and reaction to the experimental
treatments, and quantified 3 olfaction responses: first investigation, investigation rate, and the investigation duration. We defined olfactory investigation as
when a puma was actively sniffing one of the components of the experimental treatment with its nose within 15 cm of it. We defined first investigation
as the treatment variable which the puma olfactory investigated first during
its visit. Investigation rate was determined as the proportion of each treatment variable which was olfactory investigated by the pumas during visits.
We determined the investigation duration by recording the duration of time
the puma olfactory investigated each of the experimental treatments.
2.4. Communication behaviour design
We attempted to determine whether scraping and associated behaviours wereused differently by pumas of different sex and age classes. We first removed any videos where pumas were reacting to the experimental scrape
treatments we had created, in case our experiments caused changes in thepuma’s behaviour, and then analysed the remaining videos of puma visits.
When possible, we identified the individual puma (either collared pumas or
pumas without collars with distinctive markings), and categorized the puma
as mature male, mature female, immature male, or immature female, withimmature pumas either independent or traveling with their mother. We censured any videos where we were unable to determine the class of pumas
without collars. We watched each video which recorded a puma visiting
a community scrape from February 2010–December 2012, and quantified
the different behaviours it displayed while at the community scrape. In each
video we recorded the duration of the overall visit to the closest second;
and we then noted the occurrence of 5 behaviours and recorded the durationof each behaviour to the closest second. The behaviours included: scraping,olfactory investigation, body rubbing, flehmen response, and caterwauling(with definitions in Table 2). We then grouped scraping, body rubbing, andcaterwauling into the category of producing behaviours, and grouped olfactory investigation and flehmen responses into consuming behaviours.
2.5. Statistical analyses
We used program R version 3.0.0 (R Core Team, 2013) for all statisticalanalyses. Following R guidelines (R Core Team, 2013), we cite any associated packages used in the analyses. Before performing statistical analyses wetested each continuous variable data set for normality with a Shapiro–Wilk

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test and for variance equality with a Levene’s test (Sokal & Rohlf, 1987). In
each analysis, we considered p < 0.05 significant.
2.5.1. Experimental treatment statistical analyses
We analysed the experimental treatments based on the paired design of theexperiments, with each statistical test between the variables present at an experimental treatment set (Table 1). We tested three different sets of hypotheses (Table 1) for each experimental treatment: which variable was investigated first, the investigation rate for each variable, and the duration of timeeach variable was investigated. For example, we first tested the experimental treatment set of puma urine versus the control, and tested for differencesin the two treatment variables in first investigation, investigation rate, duration of investigation (using the analyses below), and then progressed througheach experimental treatment set in turn.
For first investigation, we first removed samples where no variable was investigated, and then used a binomial probability test (Sokal & Rohlf, 1987) todetermine if the treatment variables were different in their rate of being investigated first. For investigation rate, we used a z-test of proportions between
two populations (Sokal & Rohlf, 1987) to determine if treatment variables
were investigated in a different proportion of puma visits. For duration of
investigation, because of a lack of homoscedasticity we used a two-way
Student’s t-test with unequal variances (Sokal & Rohlf, 1987) to test fordifferences between the treatment variables. After testing our hypotheses,
we created post-hoc effect sizes based on Cohen’s d score (Cohen, 1992) forvalues with significant differences, and we considered scores of 0.20 small
effects, 0.50 medium effects, and 0.80 large effects (Cohen, 1992).
2.5.2. Communication behaviours statistical analyses
We used a series of analyses to determine if pumas of different sex andage classes varied in their use of communication behaviours at community
scrape sites (Table 2). To account for malfunctions of cameras and ensure werecorded the majority of a visit we removed samples with substandard quality
and videos where we recorded less than 8 s of a puma visit. We initially had
5 puma age and sex classes: mature males (N = 535), mature females alone(N = 152), mature females with cubs (N = 14), immature males (N = 40),and immature females (N = 11). We first did pre-tests for each behaviour,
first testing for differences between females with cubs against females without cubs, and then testing immature males against immature females. We did
not find any statistical significant differences in the pre-tests, and we there-

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Puma communication use and variation

fore pooled the visits for females with and without cubs, and also pooled all
immature pumas together. In each analysis we then tested among 3 puma
classes: mature males, mature females, and immature pumas. Because themajority of visits were by mature male pumas, we only used the first 10
visits by each individual mature male puma to each monitored community
scrape in order to control for the large sample size of males in comparison tofemales and immature pumas.
First, we tested for differences in the duration of visits to community
scrapes among each puma class (mature males, mature females, and immature pumas). We determined duration of time for each visit to the closest
second, and then used a mixed-model Analysis of Variance (ANOVA) to testfor differences among puma classes using the nlme package (Pinheiro et al.,2013). We used the visit duration as our dependent variable, puma class asa fixed independent variable, and known individual pumas as a random independent variable (to account for the variable number of samples amongindividual pumas).
Second, we tested if puma classes displayed each communication behaviour (scraping, olfactory investigation, caterwauling, flehmen response
and body rubbing) in a different proportion of visits using a chi-square test
(Sokal & Rohlf, 1987). In some cases, because of very low proportions of
behaviours, we used a Fisher’s exact test instead of a chi-square test (Sokal& Rohlf, 1987); in these cases we just report the degrees of freedom andp-values. We then calculated post hoc effect sizes for behaviours with significant statistical differences by calculating phi coefficients (Yule, 1912), using
the vcd package (Meyer et al., 2013), and we considered scores of 0.10 small
effects, 0.30 medium effects, and 0.50 large effects (Cohen, 1992).
Third, we determined the duration of time pumas displayed each type of
behaviour during visits to the closest second, and then tested for differencesin the duration of time puma classes spent displaying producing and consuming behaviours (Table 2). Due to the lack of linearity and homoscedasticity,
we performed a logarithmic transformation (Sokal & Rohlf, 1987) in order
to meet the assumptions of the ANOVA. We then used two mixed-model
ANOVAs in the nlme package (Pinheiro et al., 2013), with the first model
used for producing behaviours and the second model used for consuming behaviours. We used the duration spent on the behaviour during a visit as ourdependent variable, puma class as a fixed independent variable, and known
individual pumas as a random independent variable (to account for the variable number of samples among individual pumas).

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3. Results
3.1. Experimental treatments
Our analyses revealed that when compared to the control the puma urine was
not investigated first more frequently, nor investigated at a higher rate, or investigated for longer durations of time (Tables 3 and 4). In contrast, whencompared to the control, the physical scrape and the physical scrape withurine were investigated first more frequently (pb = 0.0414, pab = 0.0015),
investigated at a higher rate (pb = 0.0011, pab = 0.0004), and investigated for longer durations of time (pb = 0.0004, db = 1.29, pab < 0.0001,
dab = 1.74). When compared to the puma urine, the physical scrape and thephysical scrape with urine were investigated first more often (pb = 0.0146,
pab = 0.0001), investigated at a higher rate (pb = 0.0013, pab < 0.0001),
and investigated for longer durations of time (pb = 0.0024, db = 0.80,
pab = 0.0006, dab = 1.14). In addition, we found that when compared tothe physical scrape the physical scrape with puma urine was not investigatedfirst more frequently, or investigated at a higher rate, but was investigated for
longer durations of time (p = 0.0465, d = 0.53).
3.2. Communication behaviours
We recorded 762 visits by pumas of known age classes, including 37 632 s ofpuma activity, and a minimum of 25 individuals. Mature male pumas wereTable 3.
Differences in first detection and probabilities of detection between variables in the experimental treatments.
Variable pair

0 vs a0 vs b0 vs aba vs ba vs abb vs abFirst investigation

Investigation rate

N

Percentage offirst detectionpdfPercentage
investigatedz-score

p

33
20
21
25
22
28

0.61 vs 0.39
0.25 vs 0.75
0.14 vs 0.86
0.24 vs 0.76
0.09 vs 0.91
0.50 vs 0.50

0.29620.04140.00150.01460.00011.0000

118
40
40
64
44
58

0.40 vs 0.32
0.43 vs 0.91
0.38 vs 0.91
0.27 vs 0.67
0.22 vs 0.96
0.70 vs 0.77

0.9519−3.2733−3.5423−3.2063−5.0906−0.58390.34120.00110.00040.0013<0.0001
0.5593The percentage of visits where a variable was investigated first is noted along with theirp-values. Probability of detections between the variables are represented as percentages
together with z-scores and p-values.

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Puma communication use and variation

Table 4.
Differences in investigation duration between paired treatment variables in the experimental
treatments.
Variable pairdf

Mean ± SEp

0 vs a0 vs b0 vs aba vs ba vs abb vs ab

118
40
40
64
44
58

0.5 ± 0.1 vs 0.8 ± 0.2
0.7 ± 0.2 vs 4.8 ± 1.0
0.5 ± 0.2 vs 6.8 ± 1.1
0.4 ± 0.1 vs 2.0 ± 0.5
0.9 ± 0.5 vs 5.3 ± 1.1
1.9 ± 0.4 vs 3.7 ± 0.8

0.27280.0004<0.0001
0.00240.0006
0.0465The average duration of investigation in seconds and their standard error are noted, alongwith the pairwise p-values between the variables.

the most common visitor to community scrapes, with 73.1% of visits, incomparison to 22.1% for mature females and 3.4% for immature pumas,
while 1.4% were visits by a mature male and female traveling together.
Our analysis of the duration of visits to community scrapes did not find asignificant difference among classes (F2,522 = 1.59, p = 0.2040), with anaverage visit duration of 57.6 s (95% CI = 52.2–63.1).
Our analyses of communication behaviours revealed significant differences among puma classes in the proportion of visits for each behaviour.
Mature males exhibited scraping at 78.5% of visits, a significantly higher
proportion of visits than the 13.6% for mature females (χ 2 = 202.67, df1,637 ,p < 0.0001, ϕ = 0.57) and the 12.8% for immature pumas (χ 2 = 76.84,
df1,529 , p < 0.0001, ϕ = 0.39) (Figure 2), while mature females and immature pumas did not differ significantly. Mature males exhibited olfactory
investigation at 89.6% of visits, a significantly higher proportion than the
76.9% for immature pumas (χ 2 = 4.63, df1,529 , p = 0.0301, ϕ = 0.11). Mature females exhibited olfactory investigation at 85.7% of visits, and were
not significantly different than mature males or immature pumas.
Mature males exhibited body rubbing at 12.4% of visits, a significantly
higher proportion of visits than the 2.7% for mature females (χ 2 = 10.57,
df1,637 , p = 0.0012, ϕ = 0.14) and the 0.0% for immature pumas (df1,529 ,p = 0.0153, ϕ = 0.10), while mature females and immature pumas did not
differ significantly. Mature females exhibited flehmen responses at 30.6% ofvisits, a significantly higher proportion of visits than the 6.5% for mature
males (χ 2 = 59.82, df1,637 , p < 0.0001, ϕ = 0.31) and the 7.7% for immature pumas (χ 2 = 7.30, df1,184 , p = 0.0069, ϕ = 0.21), while mature males

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Figure 2. Proportion of visits where scraping and communication behaviours occurred forpuma class. Behaviours include scraping, olfactory investigation, body rubbing, caterwaulingand flehmen responses.

Figure 3. Mean duration in seconds of producing and consuming behaviours during visits
to community scrapes by each class of pumas. The error bars represent the standard error.
Producing behaviours include scraping, body rubbing and caterwauling, while consuming
behaviours include investigating and flehmen responses.

834

Puma communication use and variationand immature pumas did not differ significantly. Mature females exhibitedcaterwauling at 9.3% of visits, a significantly higher proportion of visits thanthe 0.4% for mature males (df1,612 , p < 0.0001, ϕ = 0.24) and the 0.0% for
immature pumas (df1,177 , p = 0.0401, ϕ = 0.39), while mature males andimmature pumas did not differ significantly.
The duration of producing behaviours was significantly different among
puma classes (F2,522 = 41.38, p < 0.0001) (Figure 3). Our post hoc analysis
revealed that mature males spent longer durations (x ± SE = 22.1 ± 1.5 s)
on producing behaviours than mature females (x ± SE = 3.3 ± 1.0 s, p <0.0001) or immature pumas (x ± SE = 2.7 ± 1.4 s, p < 0.0001), but there
was not a significant difference between immature pumas and mature females. The duration of consuming behaviours was significantly different
among puma classes (F2,522 = 14.31, p < 0.0001). Our post hoc analysis
revealed that mature females spent longer durations (x ± SE = 30.4 ± 3.0 s)
on consuming behaviours than mature males (x ± SE = 13.7 ± 1.0 s, p =0.0001) or immature pumas (x ± SE = 17.5 ± 5.2 s, p < 0.0001), butthere was not a significant difference between immature pumas and mature
males.
4. Discussion
Our results suggest that pumas exhibit strong sexually dimorphic differencesin their scrape communication behaviours, and pumas appear to be a goodstudy species for further study of sexually dimorphic behaviours including
mate selection. Male and female pumas exhibited differences in their duration of producing and consuming behaviours, as well as the proportion ofcommunication behaviours used during visits. Our results support the hypothesis of Logan & Sweanor (2001, 2010) that the differences in use ofcommunication behaviours at community scrapes can be explained throughdifferent life history patterns and evolutionary reproductive strategies of thesexes. Male strategy appears to be based on regular visitation and the production of signals for potential mates to find. In contrast, female visitation
is infrequent, in order to limit potentially dangerous encounters with males
which could lead to infanticide. Female strategy is apparently to limit risk,
and then visit community scrapes for short time periods just before and during oestrus, and use these visits to assess potential mates.
We found that mature males spent longer durations exhibiting producing
behaviours than mature females, and also exhibited scraping and body rub-

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835

bing behaviours at a higher proportion of visits than mature females. Mature
males have large home ranges, and need to leave sign for potential matesto find as well as for territorial defence. Dominance has been linked to frequency of scent-marking in mice (Hurst & Benyon, 2004; Thonhauser et al.,2013), and male strategy may be based on trying to produce as many signals
as possible for potential mates to find. The bi-functional role of scraping for
territorial maintenance and advertisement for mates suggests male strategy isbased on production of signals for others to find. However, although scraping
behaviour was frequently used during visits by mature males, there appeared
to be variation in both the duration of visits and the number of scrapes created. We hypothesize that when males detect recent visits by female pumas
they increase the duration of their visits and the number of scrapes theycreate. Similar to Logan & Sweanor (2001), we never recorded pumas spraying urine, while in contrast to Harmsen (2010), we never recorded pumas
scraping with their front feet, and we are doubtful that pumas exhibit thesebehaviours in our study area. We found body rubbing behaviour to be used at
a higher proportion of visits by mature males, and while we are unclear what
triggers body rubbing behaviours in pumas, we hypothesise that it is used as
an additional form of communication attempts for potential mates.
Mature females were less frequent visitors to community scrapes, andspent less time using producing behaviours. Although there are more mature females than mature males in any given puma population (Sunquist &Sunquist, 2002), mature females were less frequent visitors, accounting for22.1% of visits. The simplest explanation is that mature females visit for
short bouts of temporally clustered visits while in oestrus, as hypothesized
by Logan & Sweanor (2001, 2010). However, females may not just appear
when ready to mate, and their visits to community scrapes may instead occur in a progression, from investigation and assessment to advertising their
receptive status, and eventually to mating. Logan & Sweanor (2001) rarely
documented scraping behaviour in females, and believed that females squatted and urinated on scrapes made by males more frequently than making
scrapes themselves. Through the use of video cameras we also documented
female pumas both scraping and urinating on top of scrapes made by malepumas, but found that among females scraping was actually more common
than urinating on the scrapes of males (13.6% to 2.2%, respectively). We
found that caterwauling behaviour was more frequently used by mature females, only being used by mature males at 0.4% of visits. Caterwauling in836

Puma communication use and variationsome instances is likely more effective than scraping to advertise for potential mates, for instance, caterwauling can be used for immediate attraction
and to advertise from a distance (Logan & Sweanor, 2001).
We found that mature females spent longer durations exhibiting consuming behaviours than mature males, while also exhibiting flehmen response
behaviour at a higher proportion of visits. Mellen (1993) found that the useof the flehmen response behaviour by felid species was common at each investigation of urine; however we found flehmen response behaviour to beless frequently used by wild pumas (it occurred at 11.8% of visits). Rather
than being a difference between pumas and other felid species, Mellen’s(1993) findings may have been a by-product of studying felids in captivity,
where the usually solitary felids come in contact with scent-markings more
often than in the wild. For example, de Boer (1977) found that urine lessthan 4 h old triggered a flehmen response significantly more often than urine
which was over 24 h old. Mellen (1993) also found that flehmen response behaviour was more common in male felids, which contradicted our findings
with wild pumas. We hypothesize that the longer durations of consuming behaviours and the higher rate of flehmen response behaviour by females is due
to females using visits to assess potential mates. In contrast, male pumas apparently spend shorter durations investigating competitors, and instead may
only use flehmen response behaviour to investigate scent left by females or
unknown individuals, both of whom are less frequent visitors to community
scrapes.
The scraping and associated communication behaviours appear to develop
with age, and to only be used by mature females when traveling without cubs.
Intraspecific strife is a frequent source of mortality in juvenile pumas, withmature males killing cubs and sub-adult males (Logan & Sweanor, 2001,2010). Logan & Sweanor (2001) also documented that over 25% of encounters between mature males and females which were not in oestrus were
violent. For this reason, it increases survival and hence fitness for both immature pumas and females with cubs to not openly advertise their presenceat community scrapes. We were unable to find a significant difference between females with and without cubs, possibly due to our low sample sizeof females with cubs visiting community scrapes, however females may use
community scrapes differently based on whether they are with or without
cubs. For example, females with cubs were never recorded displaying either
scraping or caterwauling behaviours, and we hypothesise that females with

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cubs are more closely aligned to immature pumas in regards to being ‘nonparticipants’ in behaviours at community scrapes.
Our experimental treatments showed that the physical scrape and urine
components had different roles, and were both necessary to scrape communications. Experimental components with a physical scrape were detected first
more often and at a higher proportion of visits than urine alone, while urine
alone was not significantly different than the control. Additionally, pumas
did not show difference in first investigation or proportion of investigation
for just physical scrape in comparison to physical scrape with puma urine.
However, there was a significant difference between the two variables in regards to duration of investigation with the physical scrape with urine being
investigated for a significantly longer duration than just the physical scrape.
These results show that pumas rely on the physical scrape to locate communication attempts by other pumas, and then use the urine to convey andinterpret the communication itself.
Scrapes are the most obvious signals pumas leave on the landscape, andmales appear to use scrapes to compete against each other. The scrapes created appear to compete against each other, as the more stimuli available theless experimental treatments were detected and investigated. For example,
the proportion of visits where urine was investigated steadily decreased in response to stimuli, from 32% against control to 27% against a physical scrapeand 22% against a physical scrape with urine; and the duration of investigation of physical scrapes with urine decreased from 6.7 s against control to
5.3 s against urine and 3.7 s against the physical scrape. Some male pumas
may use this to their advantage to create dishonest signals in order to increase
their attractiveness to females. For example, some individual males may create an excess of scrapes in order to overwhelm females with stimuli andincrease the probability that their scrapes are detected over that of competitors. Pumas intentionally leave scrapes as signals for other pumas, however
scrapes are made in areas frequented by other species, and they may also
be using scrape communications as cues. For example, numerous scavengers
have been noted at puma kills (Ruth & Murphy, 2010), and it is possible thatthe mammalian scavengers are using puma scent communications to find andtrack the pumas to their kills.
The importance of the visual component of physical scrapes reinforces
the importance of community scrapes, and could be applied to puma census
efforts. Each individual scrape is an attempt at communication, and if pumas
created scrapes in random areas they would be much more difficult for the838

Puma communication use and variation

signals to be received by other pumas. This is especially true in species withspatially dispersed populations, such as pumas or other solitary carnivores,
where having regular areas for communication (i.e., community scrapes) increases their likelihood of being found. Puma populations have historically
been difficult to census, and many wildlife professionals believe the only
truly accurate way to census puma populations is through long-term study ofthe population with known individuals through radio-telemetry or GPS collars (Cougar Management Working Group, 2005). However, many attempts
are still made to develop accurate census techniques for puma populations(Cougar Management Working Group, 2005; Choate et al., 2006), and using
census techniques involving camera traps (see Kelly et al., 2008) at community scrapes rather than random areas would likely increase the rate ofcapture and hence success. In addition, there are numerous efforts, either for
population census or study capture, to detect pumas through various typesof scent lures often without great success (Long et al., 2003; Choate et al.,2006; Walker & Novaro, 2010). However, the findings of this study showthat the use of scent lures is not the best strategy for pumas and possibly
other felids, and instead, the use of visual lures (possibly in conjunction withauditory lures) would be more effective.
Acknowledgements
Funding was provided by the California Department of Fish and Wildlife, theUniversity of California at Santa Cruz, the University of California at Davis,
NSF grant No. 0963022, and the Gordon and Betty Moore Foundation. M.A.
was supported by a Victoria University of Wellington tuition scholarship.
We thank W. Linklater and K. Burns for comments on the study design,and L. Sweanor, J. Munsi-South and an anonymous reviewer for comments
on earlier drafts which greatly improved the quality of the manuscript. We
also thank C. Wylie and D. Tichenor for their significant support in helping to capture pumas with hounds, K. Cripe Fien for ArcGIS support, and
D. Casady, P. Houghtaling and Y. Shakeri and numerous field technicians fortheir help on the project.
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