Research Note
Effects of Novel and Historic Predator Urines on
Semi-Wild Western Grey Kangaroos
MICHAEL H. PARSONS,1 Centre for Ecosystem Diversity and Dynamics, Department of Environmental Biology, Curtin University,
GPO Box U1987, Perth, WA 6845, Australia
BYRON B. LAMONT, Centre for Ecosystem Diversity and Dynamics, Department of Environmental Biology, Curtin University,
GPO Box U1987, Perth, WA 6845, Australia
BENJAMIN R. KOVACS, Department of Biological Sciences, University of Plymouth, Seale-Hayne, Newton Abbot, Devon TQ12 6NQ, United Kingdom
STEPHEN J. J. F. DAVIES, Centre for Ecosystem Diversity and Dynamics, Department of Environmental Biology, Curtin University,
GPO Box U1987, Perth, WA 6845, Australia
ABSTRACT Classic studies in fear ecology have been inconclusive regarding whether predator waste products repel herbivores and whether
the deterrent effect, if any, is based on repulsion or fear. Other studies imply that the predator must have co-evolved with prey to maximize the
efficacy of response. We used chemosensory cues from the urine of native and nonnative canines to manipulate the behavior of the western grey
kangaroo (Macropus fuliginosus). One-choice feeding trials were located along a distance gradient, and administered to 28 free-ranging, semiwild, western grey kangaroos. Foods closer to the chemical source (within 12 m) were less likely to be eaten than those further from the source
when the urine came from a native predator, the dingo (Canis dingo). Flight behavior was more likely to be observed on occasions when the
dingo urine had been presented. A lesser effect occurred (to within 6 m) when urine was presented from the nonnative canid (coyote [Canis
latrans]), while the flight behavior occurred once. Neither human urine, nor tap-water control, had any effect. We offer the first evidence that
native predator-based chemical cues affect patch selection, while increasing fear, for this herbivore. (JOURNAL OF WILDLIFE
MANAGEMENT 71(4):1225–1228; 2007)
DOI: 10.2193/2006-096
KEY WORDS deterrents, dingo, flight behavior, kairomones, kangaroos, Macropus fuliginosus, olfactory, predator–prey, sensory
modality, vigilance.
Scent-marking among mammals may indicate identity,
competitive ability, sexual attractiveness (Wolf 2004),
location, time, and movement patterns (Rosell et al.
1998). Scents from urine and feces also help define
territorial boundaries (Asa et al. 1990). The selective
pressure to produce a chemical message that cannot be
intercepted by potential prey is demonstrated by the cheetah
(Acinonyx jubatus). The cheetah produces an invisible urine
composed of elemental sulfur, rather than the usual aromatic
compounds produced in most animal urines (Burger et al.
2006). For social predators like canids there has been a
historical game of ‘cat and mouse,’ with time of relaxed
pressure (Blumstein and Daniel 2002), distance from cover
(While and McArthur 2005), and context of presentation
(Apfelbach et al. 2005) all affecting the extent to which prey
detect and respond to the presence of a predator.
For 4,000 years, the dingo (Canis dingo) has been the
primary predator for all kangaroo species (Whitehouse
1977). The intense pressure from this predator is demonstrated by a dog fence that separates the far north-west of
New South Wales from Queensland and South Australia
(Pople et al. 2000). The density of kangaroos inside the dog
fence is 100 times the density outside (Dawson 1995; but see
Newsome et al. 2001). Consequently, western grey kangaroos (Macropus fuliginosus; henceforth, kangaroos) are group
foragers that demonstrate a high degree of vigilance.
The sensory modality by which an herbivore detects the
presence of a predator is species specific (Apfelbach et al.
1
E-mail: [email protected]
Parsons et al.
Effects of Predator Urines on Western Grey Kangaroos
2005) and is unknown among macropods. Optical and
auditory cues may warn of imminent danger, whereas
chemosensory signals may indicate past predator presence
(Pusenius and Ostfeld 2002). Some mammals will not
respond as readily to the threat of chemosensory predator
cues (kairomones) if they live in open areas where sight
would be more effective. Hearing sometimes plays an
important role alongside olfaction in alerting herbivores to a
potential threat (Bender 2003); this is the case among small
mammals and some ungulates (Chabot et al. 1996).
A number of animal species have been observed to respond
to predator odors (Boag and Mlotkiewicz 1994, Banks
1998). The level of response varies by species: urine
compounds (isopentenyl methyl-sulphide) from the red
fox (Vulpes vulpes) are as effective as a highly sought after
commercially available egg-based repellent for deterring
brush-tailed possums (Trichosurus vulpecula) (Woolhouse
and Morgan 1995). Likewise, Wapiti (Cervus elaphus) have
an elevated heart rate following exposure to predator odors
(Chabot et al. 1996). Smell is not important for predator
detection among some animals; meadow voles (Microtus
pennsylvanicus) commonly forage close to cover and have
little reaction to native or novel predator odors (Pusenius
and Ostfeld 2002).
In Australia, bush rats (Rattus fucipes; Powell and Banks
2004) and brush-tailed possums (Pickett et al. 2005) have
been observed to respond to predator cues, though microhabitat played a role in the significance of the effect in the
latter (Pickett et al. 2005). Olfaction is highly sensitive
among red kangaroo (Macropus rufus; Hunt et al. 1999).
1225
Figure 2. Interval plot giving up density (GUD; food dry mass remaining)
by treatment type at the Roo Gully Wildlife Sanctuary, Perth, Australia,
March 2005; 1 ¼ source, 2 ¼ 6 m from source, 3 ¼ 12 m, 4 ¼ 18 m.
Figure 1. Aerial photo of Roo Gully Wildlife Sanctuary, Perth, Australia
(36 ha); arrow represents feeding trial placement, scale: 1:72,000 (a) Mob of
28 free-ranging western grey kangaroos pictured during feeding interval,
March 2005 (b).
This sensory modality may serve as one of several indicators
that help alert macropods to the presence of predators.
An herbivore’s response to a predator is often lost or
minimised where predators and prey are ‘mismatched’ by not
sharing a common natural history (Apfelbach et al. 2005). A
less specific, general response referred to as leitmotif may be
observed when mammals detect the presence of a predator
to which they have not historically been exposed. Thus, we
assessed kairomones from the native dingo and the novel
coyote (Canis latrans). We also tested the effect of human
urine as a native predator threat; herbivores respond to
disturbance stimuli from humans similarly to that of natural
predators (Frid and Dill 2002).
Our study had the following objectives: 1) to establish
whether semi-captive kangaroos are deterred from food
sources using chemosensory cues from a historic predator
(dingo), 2) to establish whether semi-captive kangaroos are
deterred from food sources using chemosensory cues from
nonhistoric predator urines (coyote), and 3) to establish
whether semi-captive kangaroos are deterred from food
sources using chemosensory cues from human urine.
STUDY AREA
We carried out trials at Roo Gully Wildlife Sanctuary
(RGWS), 270 km SE of Perth, Australia. The study area
comprised a large grass paddock through which a creek
flowed during winter. The region had a Mediterranean
climate with cool, wet winters and hot, dry summers.
1226
Average annual rainfall was 800 mm. Average summer
monthly maximum temperatures were 268 C while average
winter minima were 58 C. The soils are ferruginous gravels
with sandy clay subsoils at depth (Churchwood and
Dimmock 1989). Dominant flora at RGWS included river
red gum (Eucalyptus camaldulensis), Tasmanian blue gum (E.
globulus), bottlebrush (Callistemon sp.), wattle (Acacia spp.)
swamp paperbark (Melaleuca raphiophylla), Dryandra sp.,
and a variety of native and introduced grasses and forbs.
METHODS
We performed trials for the primary study from 15 February
2005 to 28 March 2005. Average temperature was 238 C
during feeding time and rainfall was negligible. Twentyeight semi-wild western grey kangaroos had free range of
the 36-ha property (Fig. 1) and were free to choose or
decline human interaction. The kangaroos had free access to
water, herbage, and shrubs. We offered supplemental pellets
and grains daily at the northwest corner of the property. We
did not previously deprive kangaroos of any dietary
substances, and an onsite veterinarian saw any individual
that displayed symptoms of sickness. We conducted all
experiments in compliance with the National Health and
Medical Research Council of Australia’s code of practice for
protecting animal welfare during research (no. N 05 06,
Curtin University).
We obtained dingo urine from the Australian Dingo
Conservation Association (ADCA). We purchased preserved coyote urine from Leg-Up Enterprises (Lovelle,
ME). A nonvegetarian staff member of RGWS provided
human urine. We used evaporative urine dispensers
(Gemplers Inc., Madison, WI) to present the volatile source
near the food. We assessed these treatments along with a
tap-water control for 16 days within a Latin square design
(LSD), where each night we presented a single random
treatment. We set up feeding stations longitudinally at
varying intervals (0 m, 6 m, 12 m, and 18 m) from a single
odor source, 2 containers filled with either 12 ml of the test
urine or control. In order to control for handedness (S.
Davies, Whiteman Park, personal communication), we
The Journal of Wildlife Management
71(4)
alternated between applying treatments on the far right and
far left sides. We deviated from the manufacturer’s
recommendation of suspending the source from trees. We
buried the lower third of the containers into the ground
where urine would naturally occur. At each feeding trough
(Fig. 2), we placed 400 g of commercially available grain
(Boyup Brook Co-op, Boyup Brook, WA, Australia) in
hardware storage containers and partly buried in the ground.
In order to assess daytime proclivities, we tested prior to
nightfall. We performed one trial per day according to when
the animals typically returned to the Northwest sector for
artificial feeds (1700–1900 hr). We halted individual trials
while measurable material remained in the most frequently
chosen dish. Following each feeding session, we collected
remaining pellets, dried them for 48 hours at 758 C, and
weighed the remainder. We quantified quitting harvest rates
from artificial food patches as giving up densities (Brown
1988). We measured difference between treatments using 2way analysis of variance of the means performed via
MINITAB v14 (Minitab Inc, State College, PA). We
made pair-wise comparisons using Tukey’s b post hoc
method. Weather conditions were estimated using wind
vane and anemometer.
We chose to measure vigilance following a pilot where the
owner presented dingo urine by hand to individual
kangaroos. The kangaroos often fled the vicinity. We
recorded the incidents of flight, which took place during
each feeding period.
RESULTS
Climate conditions were stable through all recorded periods,
though heavy rain postponed feeding trials for 3 days. Wind
was mild throughout the trials (0.2–2.3 km/hr). The
kangaroos’ responses to treatments differed with distance
from the source of dingo urine (F3,15 ¼ 8.20, P ¼ 0.003; Fig.
2), while significant differences were observed between 0-m
and 6-m, and 6-m and 12-m, but not between 12-m and 18m points (Tukey’s b). The kangaroos’ response to coyote
urine also differed with distance from the source between 0m and 6-m treatments for the coyote urine (F3,15 ¼ 9.66, P ¼
0.02); however, treatment effects were not significantly
different between 6-m and 12-m or between 12-m and 18m positions. Neither human urine nor the tap-water control
had any effect (P . 0.1). The flight behavior (Fig. 3)
occurred 6 times during the dingo urine treatment and once
each during the coyote and human urine treatments. This
behavior did not occur at any stage during the tap-water
treatment.
DISCUSSION
Flight and avoidance behaviors were observed when
kangaroos were exposed to kairomones from historic, but
less so for nonhistoric, predators. The level of response was
not expected. We hypothesized that olfactory cues might
not be of interest to an animal that spends time in the open
field (Pusenius and Ostfeld 2002). The differences between
the 2 canid sources were evident before data had been
Parsons et al.
Effects of Predator Urines on Western Grey Kangaroos
Figure 3. Scoring of flight behavior occurs when western grey kangaroos
flee from the treatment source at the Roo Gully Wildlife Sanctuary, Perth,
Australia, March 2005, scale 1:15
collected: when the owner approached the mobs with coyote
urine, by hand, they became interested in the new smell and
approached it. When the owner presented the dingo urine
they were startled and fled. The marginal treatment effect of
coyote urine may have been due to the leitmotif effect,
where nonhistorically matched predators may elicit a
marginal response on prey (Apfelbach et al. 2005).
We were surprised that human urine did not have an effect
on behavior; human urine has been mildly effective for
deterring some herbivores from domestic gardens (S.
Davies, personal communication). The lack of response to
human urine may be due to association of the odor cue with
nonthreatening humans, including the landowner who
hand-reared many of them. Griffin and Evans (2003) have
shown harmless encounters with a potential predator may
decrease natural aversion.
An avoidance behavior usually requires a heritable
predisposition (Riechert and Hedrick 1990) reinforced
through experience (Brown et al. 1997). We questioned
whether the relatively short natural history shared between
dingoes and kangaroos was sufficient to allow for evolutionary adaptation. Due to strong selective pressure (Pople
et al. 2000, Griffin and Evans 2003) we cannot rule this
possibility out. Most of the kangaroos in this mob have not
been exposed to dingoes, while domestic dogs (Canis
familiaris) live on the property and harmlessly interact with
the kangaroos.
Vigilance is an expensive behavior, yet is typically
quantified in simple means, such as visual scanning beyond
the animal’s reach while ears are erect (Dumont and Boissy
2000, Treves 2000). Increased vigilance may indicate an
increase in fear but does not necessarily decrease time
feeding (Fortin et al. 2004). Vigilance among this semi-wild
population has not been previously observed during feeding
periods; thus, flight from the trial feeding area gave more
confidence in the deterrence value of the treatments. The
startled response of the kangaroos was obvious in all cases.
We suggest the dingo urine contains a unique fingerprint
that the kangaroos are able to identify.
Follow-up work should investigate whether kangaroos
become habituated to odor cues, and whether this possible
acclimation limits its usefulness in plant protection strat1227
egies. A comparative efficacy study should be undertaken in
the wild. We might expect wild kangaroos to be deterred to
a greater extent than tame animals.
MANAGEMENT IMPLICATIONS
Land managers may wish to take advantage of native
predator kairomones when attempting to deter kangaroos
from particular food patches. Predator urines may be applied
directly as nonlethal deterrent mechanisms in target areas. If
chemosensory signals are to be used, they may prove more
effective when placed at ground level where they are
naturally deposited. It will be necessary to determine how
long kangaroos will be deterred by urine before acclimating
to the signal. It is possible that habituation can be delayed
until target seedlings have sufficient time to mature and
produce self protective mechanisms. Additional challenges
include identifying and synthesizing all active chemicals in
the predator urine, and determining whether these are
appropriate for practical application of deterring kangaroos
from areas prone to roadside hazards, or agricultural areas.
Its usefulness may be targeted to areas where seedling death
is a common outcome in rehabilitation sites, and rapid
return of vegetation is paramount.
ACKNOWLEDGMENTS
This is contribution CEDD03-2007 to the Centre for
Ecosystem Diversity and Dynamics. Thanks to C. Lander
and volunteers of the Roo Gully Wildlife Sanctuary, H.
Robertson of the Perth Zoo, D. Thorne, Sr., and D.
Thorne, Jr., of Caversham Wildlife Park, D. Jenkins
(Australian Hydatid Control and Epidemiology), and B.
Oakman of the Australian Dingo Conservation Society.
This study was supported by the Minerals and Energy
Research Institute of Western Australia, Alcoa World
Alumina (J. Koch), Worsley Alumina Pty. Ltd. (S. Vlahos),
Whiteman Park (S. Davies), Western Australia Chemistry
Centre (K. Dods), and Specialty Feeds Pty. Ltd. (W. Potts).
We thank 2 anonymous reviewers for many helpful comments on an early draft.
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Associate Editor: Hudson.
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