Download Know thy enemy: Behavioural response of a native mammal ( coexistence histories

Austral Ecology (2008) 33, 922–931
Know thy enemy: Behavioural response of a native
mammal (Rattus lutreolus velutinus) to predators of different
coexistence histories
JOANNE MCEVOY, DAVID L. SINN AND ERIK WAPSTRA*
School of Zoology, Private Bag 05, University of Tasmania, Hobart, Tas. 7001, Australia (Email:
[email protected])
Abstract Predation is recognized as a major selective pressure influencing population dynamics and evolutionary
processes. Prey species have developed a variety of predator avoidance strategies, not least of which is olfactory
recognition. However, within Australia, European settlement has brought with it a number of introduced predators,
perhaps most notably the red fox (Vulpes vulpes) and domestic cat (Felis catus), which native prey species may be
unable to recognize and thus avoid due to a lack of coexistence history. This study examined the response of native
Tasmanian swamp rats (Rattus lutreolus velutinus) to predators of different coexistence history (native predatorspotted-tail quoll (Dasyurus maculatus), domestic cats and the recently introduced red fox). We used an aggregate
behavioural response of R. l. velutinus to predator integumental odour in order to assess an overall behavioural
response to predation risk. Rattus lutreolus velutinus recognized the integumental odour of the native quoll (compared with control odours) but did not respond to either cat or fox scent (compared with control odur). In contrast,
analyses of singular behaviours resulted in the conclusion that rats did not respond differentially to either native or
introduced predators, as other studies have concluded.Therefore, measuring risk assessment behaviours at the level
of overall aggregate response may be more beneficial in understanding and analysing complex behavioural patterns
such as predator detection and recognition. These results suggest that fox and cat introductions (and their
interactive effects) may have detrimental impacts upon small native Tasmanian mammals due to lack of recognition
and thus appropriate responses.
Key words: behavioural response, introduced predator, olfactory recognition, predator odour, predator-prey
interaction.
INTRODUCTION
Predation is a strong selective force leading to behavioural modifications in prey species and it is well documented that animals take risk of predation into account
when making decisions about how to behave in their
environment (Kats & Dill 1998; Krupa & Sih 1998).
Numerous studies have examined the responses of
prey species to possible predation risk in the context
of cost–benefit decision making; that is, how animals
make decisions regarding trade-offs between predation
risk and for example, foraging or mating opportunities
(Dickman 1992; Abrams 1993; Jedrzejewski et al.
1993; Jacob & Brown 2000; Sih & McCarthy 2002;
Mohr et al. 2003; Powell & Banks 2004; Devereux et al.
2006; Wohlfahrt et al. 2006).
Selection is likely to lead to those mechanisms in prey
which allow the detection of predators prior to their
attack, thereby increasing the probability of escaping or
*Corresponding author.
Accepted for publication November 2007.
© 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
avoiding encounters. The major behavioural mechanism by which prey species detect predators is an
activity pattern labelled ‘vigilance’ or ‘risk assessment’
(Apfelbach et al. 2005). It involves a number of behaviours (which may be species or taxon-specific) which
facilitate the detection, localization and identification of
predators through the use of particular sensory modes
(Apfelbach et al. 2005). While visual or acoustic cues
may provide direct information on the presence of
predators, olfactory cues may be especially important
because they provide information on predation risk
even when the predator is absent at the time of detection or is difficult to see (especially in dense undergrowth and physically complex habitats). Rattus
norvegicus and Rattus rattus, for example, have been
shown to display innate behavioural responses to the
odours of predators such as cats or the red fox (Burwash
et al. 1998; Laska et al. 2005).
Use of specific predator odour cues may be particularly important for mammals that have a well-developed
chemical sense, such as those that are mainly nocturnal
or live in physically complex habitats (Monclus et al.
2005). For example, in order for prey species to
doi:10.1111/j.1442-9993.2008.01863.x
N AT I V E A N D I N T R O D U C E D P R E DATO R R E C O G N I T I O N
successfully extract information from predator odours,
scent information needs to be a reliable indicator of
predator presence and/or activity. Faeces from predators that use latrine sites (such as quolls, Kruuk &
Jarman 1995) may be less indicative of their typical
movement patterns than those of a predator that
deposits its faeces more widely (Dickman 1992;
Hayes et al. 2006). On the other hand, scent-marking
for the purpose of territory establishment and to convey information about reproductive state or identity
is a common practice among all carnivore families
(Oakwood 2002; Belcher & Darrant 2004; Rostain
et al. 2004; Laska et al. 2005), and this information can
be exploited by prey species to provide cues as to
possible focal areas of predator activity and hence, risk
of predation (Dickman 1992; Powell & Banks 2004;
Russell & Banks 2007). Similarly, predator odours
derived from integumental odours or scent glands can
provide instant information to prey species regarding
predator presence, provided prey can determine how
long ago predator scent marks were laid down.
It has been suggested that prey species should have a
generalized predator response when confronted with
carnivore scent, as there are similarities in the scent
compounds as a result of a carnivorous diet (Nolte et al.
1994; Kats & Dill 1998). However, the ability of prey
species to detect and avoid predators should depend in
part on the life history, ecology and evolutionary history
of both predator and prey, as such, the decision-making
process with regards to risk assessment becomes problematic when prey are faced with introduced (and thus,
possibly unknown) predators (e.g., Jones et al. 2004;
Russell & Banks 2005). Prey species may be better
equipped to recognize coevolved and/or sympatric
predators than recently introduced and/or allopatric
ones (Hayes et al. 2006) and thus native species will be
unable to respond appropriately to predation threat of
introduced species due to the lack of co-evolutionary/
existence history (Banks 1998, 1999; Blumstein et al.
2002; Russell & Banks 2005). Evolutionarily novel
predators, such as the red fox (Vulpes vulpes) and feral
cats (Felis catus) in Australia may therefore have devastating impacts upon native prey species because of this
lack of appropriate response (Banks 1998, 1999; Jones
et al. 2004). Despite these predictions, there are surprisingly few quantitative tests of prey responses to
native versus evolutionarily novel predators (but see
Banks 1998, 1999; Russell & Banks 2005, 2007), and
even fewer where the differences in length of evolutionary association between predator and prey has been
explicitly considered (but see Jones et al. 2004; Russell
& Banks 2007).
The evidence thus far is equivocal on the ability of
prey to recognize or respond to predator odour. For
example, many species from the northern hemisphere
show consistent avoidance of areas tainted with scent
marks of co-evolved predator species only (Murray
© 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
923
et al. 2004; Apfelbach et al. 2005), while some native
Australian mammals show little response to, and avoidance of, the faecal or urine odours of native or introduced predators (Banks 1998; Blumstein et al. 2002;
Banks et al. 2003; Russell & Banks 2005). Importantly,
a recent paper by Russell and Banks (2007) is the first
to demonstrate native Australian mammal avoidance
of predator odour. In their study, in which Elliot traps
were treated with fox faeces and quoll faeces, or left
untreated, native rodents showed avoidance of both
native (quoll) and introduced (fox) predators.There are
at least two potential reasons for the apparent equivocality in the results of these previous studies.The first of
these is the manner in which a ‘predator’ is presented
to potential prey.Visual, acoustic, olfactory or physical
threat presence may all result in a different prey
response, and the response (or lack thereof ) may be
ecologically irrelevant depending on the animal’s environment and primary sensory mode. The second
reason is the manner in which the prey response to
predation risk is assessed. The question here refers to
how prey response to predation threat is examined, for
example, is a singular behavioural variable sufficient, or
is an aggregate score made up of a number of predator
avoidance/detection behaviours more appropriate?
This study examines the risk assessment response of
native rats, Rattus lutreolus velutinus, to the integumental odours of predators of different coexistence history.
Spotted-tailed quolls (Dasyurus maculatus) are a native
predator of R. l. velutinus (Glen & Dickman 2006; D.
Moyle, pers. comm. 2006) and it may be predicted
that rats will respond to the cues of the presence of
quolls. Feral cats (F. catus) and red foxes (V. vulpes) are
two introduced predators to which R. l. velutinus are
relatively naïve. Feral cats have been present in Tasmania for the last 200+ years and are a known predator of
rodents ( Jones & Coman 1981), and are specifically a
threat to the R. l. velutinus population trapped for this
study (Wellington Park Manangement Trust 2006).
Foxes are a recently introduced species with less than
10 years history in the state (Department of Primary
Industries and Water 2006), and pose a major threat to
a number of native small mammal species (Banks
1998; Banks et al. 1998; Short et al. 2002; Jones et al.
2004), including R. lutreolus (Department of Primary
Industries and Water 2006; Russell & Banks 2007).
MATERIALS AND METHODS
Study species, capture and maintenance
The velvet-furred rat, R. l. velutinus (Rodentia:
Muridae) is a moderately sized (ca. 150 g) endemic
subspecies found throughout the state of Tasmania,
Australia, but is especially prevalent in south-west
doi:10.1111/j.1442-9993.2008.01863.x
924
J. M C E VOY ET AL.
Tasmania. Although rarely observed, they are one of
the most abundant and widely distributed mammal
species, occurring at altitudes from sea level to 1600 m
(Rounsevell et al. 1991; Hocking & Driessen 2000)
and are found in a variety of habitats (wet and dry
sclerophyll, coastal heath, button grass sedge and
moorlands). Rattus lutreolus velutinus are predominantly herbivorous, with a highly varied diet (Driessen
1998). Rattus lutreolus velutinus are wholly protected
under the Tasmanian National Parks and Wildlife Act
of 1973, but they are nevertheless under some threat
due to range constriction imposed by encroaching
farmland and cattle grazing, as well as the recent introduction of the fox (V. vulpes) (Department of Primary
Industries and Water 2006).
Rattus lutreolus velutinus were trapped in an area of
heterogeneous forest near Shoobridge Bend inWellington Park, near Hobart, Tasmania (42°56′S, 147°15′E)
and in which quolls and cats are present (foxes have not
yet been reported in Wellington Park). Sixteen female
and 21 male R. l. velutinus were trapped during late
January and early March 2006. Elliot traps (33 ¥
10 ¥ 9 cm, Elliot Scientific, Upway,Victoria, Australia)
were placed near discernable runs in the undergrowth
along a 500 m straight line transect. Traps were set
before dusk each evening (five nights/week), and
checked each morning before 10 . Upon capture, all
animals were micro-chipped (Allfelx ISO implants,
8 ¥ 2 mm) for unambiguous identification before being
housed in the small mammal rooms in the School of
Zoology, University of Tasmania.
Rattus lutreolus velutinus were maintained in captivity in individual plastic cages (90 ¥ 40 ¥ 40 cm),
with wire mesh lids and paper-pellet substrate. Each
cage was provided with shredded paper for nest construction, leaf litter, bark and rocks for environmental
enrichment. Water was available ad libitum. A mix of
food consisting of standard small mammal pellets
(rabbit food), fresh fruit and vegetables, a fruit/nut
mix, crickets, meal worms and dog food biscuits was
provided once a day. Light was kept constant at 11:13
hours light/dark photoperiod, and the temperature
was kept at a relatively constant 10°C (!3°C). We
attempted to minimize disturbance of rats while in
captivity, therefore human interaction with rats was
restricted to daily feeding and fortnightly cleaning of
cages. All animals experienced the same conditions
and handling experience while in captivity (a total of 3
months prior to these experiments).
RESPONSE TO PREDATOR SCENT
Integument odours from spotted tailed quolls
(D. maculatus), cats (F. catus) and red foxes (V. vulpes)
provided a coexistence predator-prey time scale with
which to assess behavioural responses of R. l. velutinus.
doi:10.1111/j.1442-9993.2008.01863.x
A number of studies have found that the greatest behavioural, neurological and endocrinological responses
elicited from prey species have been from integument
odours (Blanchard et al. 2003; Apfelbach et al. 2005;
Masini et al. 2005). It is thought that, especially in
highly complex habitat (such as experienced by the
population of R. l. velutinus where the individuals in
this study were sourced), integument odours should
provide vital cues to predator presence. While the
chemical stimulus from integument of predator species
may be a preferred scent stimulus for use by researchers, it is rarely used. This can be due to a number of
reasons, perhaps most notably the difficulty involved in
obtaining integument cues as opposed to the relative
ease of using faeces and urine.Arguably however, faeces
and urine may provide relatively less information to the
prey species about the range of the predator, or the
temporal nature of predator presence.
Quoll (Dasyurus maculatus) scent was obtained from
captive quolls at Bonorong Wildlife Park (Brighton,
Tasmania, Australia) by rubbing each animal with
cotton wool, concentrating on the back of the neck
where there is a concentration of sebaceous glands
(Oakwood 2002). Fresh samples were sealed in plastic
bags and frozen (at -20°C) until use (e.g. Masini et al.
2005; Hayes et al. 2006). Similarly, cotton wool swabs
were rubbed under the chin area of male and female
domestic cats (F. catus). Cats have a scent region under
their chin (sub-mandibular gland) and around the
mouth (peri-oral glands) which they use to rub against
surfaces to mark their territory (Feldman 1994). Fox
(V. vulpes) scent was obtained by swabbing cotton
wool on the anal glands (obtained from the Department of Sustainability and Environment in Victoria).
Foxes, like other canids, use integument scent (as well
as urine) in order to mark territory (Laska et al. 2005;
Wood et al. 2005). As with quoll scent, cat and fox
swabs were frozen (-20°C) until use.
Assessment of behavioural responses
In each predator scent test, a control (distilled water)
and predator odour test were run concurrently, and
individuals were randomly assigned to predator or
control on day one, with the opposite test conducted at
the same time on the following day (order of presentation was included as a factor in data analysis). A total
of six trials were run for each individual: three controls, and one predator odour for quoll, cat and fox (in
that order). Due to space limitations and the fact that
scent compounds can infiltrate surrounding materials
(e.g. wood, paper pellets), two isolated rooms (a
control room and a scent room) were used and predator treatments were temporally separated rather than
randomized. Both rooms had the same temperatures
and lighting conditions over the course of the testing
© 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
N AT I V E A N D I N T R O D U C E D P R E DATO R R E C O G N I T I O N
925
period. Each different predator/control trial was conducted at least 5 days apart, allowing all rooms to air
out and scent to dissipate between trials.
In order to standardize individuals’ reaction to conspecific smell, paper pellet from all individual’s home
cages were used to line the base of each test arena.
Tests were conducted in a 1.2 ¥ 0.6 m wooden arena,
under dark conditions (50W red light/test arena)
which is ecologically relevant as R. l. velutinus and all
three predators are primarily nocturnally active
( Jones & Coman 1981; Jones & Dayan 2000; Glen &
Dickman 2006) and each trial lasted for 10 min plus
a pre-test acclimation time of 2 min. Each test arena
had a familiar shelter at one end (similar to those in
home cages and used in previous trials), and a feeding
and scent dish at the opposite end. To eliminate the
confounding effects of scent and taste being integrally
linked (Chabot et al. 1996), scent (four cotton wool
swabs) was placed on a separate dish to food ( Jones &
Dayan 2000; Monclus et al. 2005). Each trial was
videorecorded (B&W Bullet CCD Cameras, each
camera connected to a Panasonic video Cassette
Recorder, Series NV-FJ630) with tapes analysed at a
later date.
In order to quantify individuals’ behavioural
response to each predator scent, nine discrete behavioural variables were recorded in each test (Table 1).
These nine behaviours were chosen on the basis of
previous studies (Thor et al. 1988; Burwash et al. 1998;
Kats & Dill 1998; Campbell et al. 2003; Takahashi et al.
2005; Engh et al. 2006) and preliminary pilot observations. Frequency and duration of behaviours were measured, and during video analysis, the arena was divided
into thirds on the monitor to calculate time spent in
each third (shelter end, middle or food/scent end), and
number of thirds moved. An a priori 5-s rule was used
for all frequency counts, in which a behaviour was
scored as a multiple frequency only if there was at least
a 5-s break between occurrences (Martin & Bateson
1993; Sinn & Moltschaniwskyj 2005).
While it is possible to assess response to predator
scent for each specific behaviour (e.g., feeding, grooming, contact events with scent, and this method was also
used, see below), the use of an aggregate behavioural
score provides an alternative way to assess an overall,
integrated and arguably more realistic, behavioural response (Epstein 1983; Sih et al. 2004a,b). Many behaviours within each test were highly inter-correlated. In
order to reduce the number of variables used in subsequent analyses and to facilitate use of a reliable single
score (see Ray & Hansen 2005) representative of ‘risk
assessment behaviour’ (Apfelbach et al. 2005), we subjected the nine behavioural variables to principal components analysis (PCA).We first summed the observed
behaviours (total number of times each behaviour was
performed) from each rat in each test (three from
predator scent, three from control) and subjected these
summed behaviours to PCA with orthogonal varimax
rotation (Tabachnick & Fidell 1996). The number of
components interpreted was based on a scree test
(Cattell 1966), and the interpretability of the components themselves (Zwick & Velicer 1986). For component interpretation, behaviours with a loading of at least
0.40 were considered to contribute to the meaning of a
component (Tabachnick & Fidell 1996). The majority
of the measured behaviours tended to load strongly on
a single component in PCA analysis (Table 2) . Because
PCA loadings (and therefore PCA scores) are often not
replicable across studies, we used PCA to inform our
choice of variables for inclusion in aggregate scores
(Tabachnick & Fidell 1996).Therefore, for each predator and control test, we computed scale scores by
summing the normalized variables measured in each
test which loaded highly on PCA1 (activity, groom,
food, scent, shelter third, final third and shelter – see
Table 1 for behavioural definitions). This method
Table 1. Behavioural variables of Rattus lutreolus velutinus
recorded in the predator response context.Variables in italics
were used to create the behavioural score
Table 2. The solution matrix obtained from the principal
components analysis ( Varimax rotation) of the nine behaviours recorded from the predator test (n = 32)
Behavioural
variable
Time shelter
Activity
Groom
Apple
Food
Scent
Shelter third
Final third
Shelter
Description
Time spent in shelter
Thirds crossed; measure of distance moved
Number of grooming events, involved five
second rule
Amount of apple consumed during the test
period
Number of contact events with food dish
Number of contact events with scent dish
Proportion of time spent in shelter third
Proportion of time spent in final third
(where food and scent is)
Number of times entered the shelter
© 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
Time in shelter
Thirds moved
Groom events
Apple eaten
Contact food
Contact scent
Shelter third
Final third
Shelter
% variance explained
% variance total
Component one
Component two
-0.802
0.599
0.702
-0.0900
0.704
0.848
-0.720
0.818
0.198
53.315
67.281
0.090
0.700
-0.022
0.625
0.539
0.428
-0.260
0.185
0.804
13.966
The highest factor loadings on each component are indicated by boldface type.
doi:10.1111/j.1442-9993.2008.01863.x
J. M C E VOY ET AL.
resulted in aggregate scores which were highly correlated with PCA scores (r = 0.796, P < 0.001, n = 31).
We computed separate risk assessment scores for
each rat in each predator test and its corresponding
control test, resulting in six unique scores per rat
(three predator scent tests, three controls). In each
test, higher scores describe an individual which spends
less time in the shelter and less time in the shelter
third, spends more time in the final third (where the
food and scent is located), moves a greater number of
thirds, has more groom events and initiates a greater
number of contact events with both the scent and food
dishes. A high score indicates an increase in the level of
risk assessment, while a lower score indicates the
reverse (Genaro & Schmidek 2000; Whishaw et al.
2006). It is worth noting here that while groom behaviour is not a risk assessment behaviour per se, it is a
displacement behaviour that rodents typically display
when they are in unfamiliar environments, are unsure
of their surroundings, or are presented with unfamiliar
and possibly threatening stimuli (Thor et al. 1988). It
is used as a measure of an individual’s distress (Thor
et al. 1988; Engh et al. 2006). In this situation, when
considered in conjunction with the other behaviours
that make up the risk assessment behaviours, it represents an individual’s recognition of new and possibly
threatening stimuli in the form of predator scent.
We used repeated-measures  to determine if
R. l. velutinus react to the presence of predator scent
(as opposed to a control odour). As predator trials
were temporally separated, risk assessment scores of
rats were first analysed using three separate one-way
repeated-measures ’s (one  for each predator scent against its concurrent control, e.g. quoll vs.
quoll control, cat vs. cat control and fox vs. fox control).
In addition to using aggregate scores, we examined
two singular behaviours, to determine whether there
was a difference in our interpretation of risk assessment behaviour due to the method of measurement
(aggregate score vs. singular behaviour). These two
behaviours (amount of apple eaten and number of
thirds crossed) were chosen a priori (based on previous
studies). Amount of apple eaten was not included in
the risk assessment scores because it did not load on
PCA1; the other behaviour (number of thirds crossed)
was a variable which contributed to aggregate scores.
Apple eaten was used because a food variable is often
used in assessing prey response to predation threat
(e.g. Jones & Dayan 2000; Blumstein et al. 2002), as is
an activity measure (i.e. number of thirds crossed)
(Kats & Dill 1998; Monclus et al. 2005). The two
singular behaviours were subjected to three separate
one-way repeated-measures  analyses to determine if there was a difference in behavioural response
to predator versus control scents.
Risk assessment scores and singular behaviours
were distributed normally, so no transformations were
doi:10.1111/j.1442-9993.2008.01863.x
required prior to analyses. Analyses on risk assessment
scores and singular behaviours were first conducted
with sex and order of presentation as between-subjects
factors for all repeated-measures s. In all cases,
neither sex nor order of presentation was significant
(P > 0.05), and so these are not considered further. All
data were analysed with SPSS 14.0 for Windows.
RESULTS
Rattus lutreolus velutinus differed significantly in their
response to quoll scent as opposed to control scent
(F(1,29) = 0.425, P = 0.034; Fig. 1A), increasing their
a
0.40
0.30
0.20
0.10
0.00
-0.10
-0.20
-0.30
-0.40
Mean Behavioural score
926
-0.50
b
Quoll
Control - Quoll
Cat
Control - Cat
0.40
0.30
0.20
0.10
0.00
-0.10
-0.20
-0.30
-0.40
-0.50
c
0.40
0.30
0.20
0.10
0.00
-0.10
-0.20
-0.30
-0.40
-0.50
Fox
Control - Fox
Scent situation
Fig. 1. Mean behavioural scores of Rattus lutreolus velutinus
to scent of (a) quoll, (b) cat and (c) fox, associated responses
under control conditions are also presented. Higher scores
indicate individuals which spend less time in the shelter and
less time in the shelter third, spends more time in the final
third (where the food and scent is located), moves a greater
number of thirds, has more groom events and initiates a
greater number of contact events with both the scent and
food dishes. Error bars represent standard error of the mean,
n = 28.
© 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
N AT I V E A N D I N T R O D U C E D P R E DATO R R E C O G N I T I O N
risk assessment behaviour when in the presence of
quoll scent. However, there was no mean level behavioural response to either cat scent or fox scent compared with controls (cat scent to control: F(1,30) =
0.585, P = 0.450; fox scent to control: F(1,28) = 1.067,
P = 0.310, Fig. 1B and 1C).
We were also initially interested in comparing predator scents directly, however, mean risk assessment
scores in controls differed across the 3 weeks of study
(repeated-measures : F(2,26) = 3.72; P = 0.03,
Fig. 1). Risk assessment scores in each of the predator
trials were corrected for the difference in mean response
to controls (Dingemanse et al. 2002), on the assumption that predator and control responses co-vary, and
were then analysed with repeated-measures .
Using the corrected scores to compare directly between
predator scents, there was a significant mean-level
shift in response to the scent of the different predators
(repeated-measures : F(2,27) = 5.533, P = 0.01).
Simple contrasts revealed that there was no significant
difference in behavioural response of R. l. velutinus to
cat and fox scent (F(1,28) = 1.924, P = 0.18), but that
R. l. velutinus differed behaviourally in their response to
quoll scent compared with both cat and fox scent (quoll
to cat scent response: F(1,28) = 4.893, P = 0.035; quoll to
fox scent response: F(1,28) = 9.393, P = 0.005; supporting the conclusion that R. l. velutinus respond to quolls
differently to control, and that they do not respond to
either of the introduced predators). These results
confirm our above results that R. l. velutinus do not
respond to introduced predators. However, due to the
confounding nature of the change in controls, these
results are not discussed further.
Using the single behavioural variable ‘amount of
apple eaten’ there was no significant difference in how
R. l. velutinus responded to any of the three predator
scents, analysed against their concurrent controls
(repeated-measures ; quoll to quoll control:
F(1,30) = 0.012, P = 0.913; cat to cat control: F(1,30) =
2.625, P = 0.116; and fox to fox control: F(1,28) = 0.041,
P = 0.842). Similarly, using the singular behavioural
variable ‘number of thirds crossed’ showed that there
was no significant difference in how R. l. velutinus
behaved with respect to predator scents (repeatedmeasures ; quoll to quoll control: F(1,30) = 0.975,
P = 0.331; cat to cat control: F(1,30) = 1.877, P = 0.181;
and fox to fox control: F(1,28) = 0.288, P = 0.596).
DISCUSSION
Olfactory senses are commonly used by prey species to
detect the presence of predators, and prey individuals
may display a behavioural recognition of, and response
to, predator odour (Banks 1998; Blumstein et al. 2002;
Powell & Banks 2004; Russell & Banks 2007). A ‘risk
assessment’ behavioural response is frequently used by
© 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
927
prey individuals in recognition of predator scent
(Apfelbach et al. 2005), and there is a suggestion that
recognition of predator scent is an innate response
which should exist against the majority of carnivorous
species (Nolte et al. 1994; Burwash et al. 1998; Kats
& Dill 1998). However, the evidence regarding the
response of native prey species to introduced predators
is conflicting. In this study, R. l. velutinus responded
to quoll scent (as opposed to control) but did not
respond to either cat or fox scent (as opposed to
control). This indicates that R. l. velutinus is clearly
capable of behavioural responses to predator scent,
and respond behaviourally to the predator scent cues
of its native, sympatric predators, the spotted tailed
quoll (D. maculatus). Rattus lutreolus velutinus do not
respond to the introduced predator species, cats
(F. catus) or red foxes (V. vulpes), indicating behavioural recognition of native predators only. Such lack
of responses by prey to evolutionarily novel predators
may explain the devastating impacts these predators
have had within Australia; prey appear to lack the
co-evolutionary history required to have developed the
appropriate responses (Coss 1999).
However, there is an alternative explanation of our
results which relates to R. l. velutinus behaviour in
response to predator and control scent as an artefact
of the experimental design. We used a fixed order
of presentation, rather than a randomized approach
(for reasons outlined in the Materials and methods).
However, because of the experimental design, rat
response to odour may reflect habituation to trials, as is
indicated by changes in rat response to control scent
over time. The lack of a significant response in overall
risk assessment behaviour when R. l. velutinus were
confronted with the scent of introduced predators may
simply reflect their familiarization with trials.We do not
believe that this is the case however, as discussed below.
There is evidence from odour recognition trials with
rodents to suggest that they do not habituate to scent
based stimuli, especially when scent trials are temporally separated by long periods of time (Wallace &
Rosen 2000; Blanchard et al. 2003; Burman & Mendl
2006). With R. norvegicus, the odour recognition
memory for individuals that had been housed together
for 18 days was between 48–96 h (Burman & Mendl
2006). After 96 h, rats investigated unfamiliar odours
and the odours of former cage mates equally. Similarly,
a study examining the fear response of rats to trimethylthiazoline (TMT), a component of fox faeces, found
no within-sessions or between-sessions habituation to
TMT, nor did TMT produce contextual conditioning
(Wallace & Rosen 2000; Blanchard et al. 2003). Furthermore, Blanchard et al. (1998) found that after 20
days of 60 min visual exposure per day to cats, rats had
minimal behavioural habituation to the threat, and had
reliably higher basal corticosterone concentrations,
indicating no habituation of the endocrine system (i.e.,
doi:10.1111/j.1442-9993.2008.01863.x
928
J. M C E VOY ET AL.
they were still responding with a stress-based endocrine
response to cat presence). Similarly, experimentation
by File et al. (1993) showed that rats exposed to cat
odour showed no behavioural habituation to the threat
after repeated exposures; they continued to avoid the
odour cloth. Given the above experiments that indicate
little or no behavioural habituation to predator threats,
the length of time our rats were exposed to each predator threat (<35 min per scent), the length of time
between predator presentation (>5 days) and the fact
that the effect of order of presentation (within trials) of
scents was non-significant, we believe that the results
may reasonably be interpreted as R. l. velutinus
responding to the odours from its native predators
(quolls, D. maculatus) but not to that of either of the
introduced predators. Thus, our experimental design,
where response to potential predation risk (quoll, cat or
fox) was measured against a concurrent control (even
though each predator scent trial was separated by a time
period), was suitably designed to test recognition of,
and response to, native versus introduced predation risk.
The fact that R. l. velutinus did not alter their behaviour
in response to fox or cat scent (compared with their
concurrent controls) strongly suggests that they did not
perceive or respond to this risk.
Interpretation of our results that R. l. velutinus
responded to their native predator and not to either of
the introduced predators contrasts with suggestions
that prey species should respond to novel predators
because of common odour constituents reflecting a
generalized carnivore diet (including sulphurous
metabolites of protein digestion: Jedrzejewski et al.
1993; Nolte et al. 1994; Kats and Dill 1998; Apfelbach
et al. 2005; Hayes et al. 2006). While anti-predator
behaviours and predator avoidance strategies are
highly beneficial when there is a real and significant
predation threat, they may also be costly to the individual. Anti-predator behaviours may include the flight
or fight response which is facilitated by an increase in
corticosterone (Dufty & Crandall 2005). Corticosterone can be costly over a long-term period (Marquez
et al. 2004), and it can thus be detrimental for prey
species to respond physiologically to predation threat
unnecessarily. Similarly, predator avoidance strategies
can involve decreased activity patterns and restricted
movement, resulting (in some cases) in a lack of foraging or mating opportunity (Mohr et al. 2003; Devereux
et al. 2006); these effects constitute sub-lethal impacts
of predation (Powell & Banks 2004).Thus, response to
predator odours may be expected to be finely tuned to
those risks associated with sympatric predator species
due to these detrimental effects (Agrawal et al. 1999;
Jones et al. 2004). Our results support these suggestions; in this study, R. l. velutinus displayed a risk
assessment behavioural response to their native predators only, perhaps because of the costs associated with
using a generalized predator response, or because they
doi:10.1111/j.1442-9993.2008.01863.x
do not recognize the threat as the constituents of the
scent are not common enough.
Results on Australian prey species responding to
potential predation threats have not been consistent.
A recent study (Russell & Banks 2007) demonstrated native rodents (Rattus fuscipes, R. lutreolus and
Pseudomys gracilicaudatus) tended to avoid traps scented
with both native quoll (D. maculatus) and introduced
fox (V. vulpes) odour. These responses clearly differ
from our own study (differential responses to quoll and
fox/cat) as they do from earlier work by the same
authors (Banks 1998; Russell & Banks 2005) where
prey showed no response to evolutionarily novel predators using similar methods. The discrepancy between
the results of previous studies and our own may lie in
how responses were assessed. In our study, we used an
aggregate score composed of a number of discrete,
observable investigatory, displacement and locomotory
behaviours (see Table 1) which was representative of
an overall risk assessment response (Apfelbach et al.
2005). Rattus lutreolus velutinus displayed an increase in
risk-assessment behaviours in response to quoll scent,
characterizing an active search and evaluation of the
potential predation risk associated with the scent. This
is similar to the response seen to a decrease in habitat
complexity (and thus increased perceived predation
risk) in which R. l. velutinus increased activity patterns
( J. McEvoy et al. unpubl. data 2006), thus supporting a
specific stimuli-based response. The use of an integrated approach to the measurement of behavioural
responses of R. l. velutinus to predators, unlike singular
measures such as trap avoidance (e.g. Banks 1998) or
food consumption (e.g. Jacob & Brown 2000), provides
an alternative (and not yet widely used) method to
assess prey response to predation. Using two examples
of singular behavioural measures in this study (apple
consumption and activity, commonly used to assess
prey response to predation risk (Kats & Dill 1998; Jones
& Dayan 2000; Blumstein et al. 2002; Monclus et al.
2005)) indicated that there was no differential behavioural response of R. l. velutinus to native or introduced
predators. The conclusion from these results would be
that R. l. velutinus do not respond to olfactory cues
from either native or introduced predators; however,
the use of an aggregate behavioural score provides a
different result, and is (in our opinion) a more accurate
and holistic representation of prey response to predation threat.
In our study, the use of predator integumental
odours (as opposed to urine or faeces) and the
response by R. l. velutinus to the odours of native
predators suggests that they are used as an indicator
of predation risk, perhaps conveying realistic information about predator presence, habitat boundaries and
frequently used travelling routes (Blanchard et al.
2003; Apfelbach et al. 2005; Masini et al. 2005).
Faecal predator cues may be poor predictors of pos© 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
N AT I V E A N D I N T R O D U C E D P R E DATO R R E C O G N I T I O N
sible predation risk (Banks et al. 2003; Blanchard
et al. 2003), especially for predators that use latrine
sites (such as quolls, Kruuk & Jarman 1995) because
they convey little information on typical movement
patterns compared with predators that deposits its
faeces more widely (Dickman 1992; Hayes et al.
2006). The ability of prey to detect predator presence
through the use of scent is likely to be related to both
predator and prey life history and ecology (Jedrzejewski et al. 1993), and further study is needed to test
differential prey responses to alternative scent types
(e.g., integumental vs. urinary/faecal) from the same
predators.
Even though R. l. velutinus has coexisted with cats
for over 200 years, our results suggest that they have
yet to evolve a risk assessment response to cat integumental odour (see also Griffin et al. 2001; Blumstein
et al. 2002). This, coupled with the fact that they also
did not respond to a recently introduced predator, the
red fox, suggests that native fauna may be highly vulnerable to interactive effects induced by multiple evolutionarily novel predator species. Given the equivocal
results on the response of prey to their native and
introduced predators, clarifying the response of native
species to these predators will provide vital knowledge
for assessing the level of risk introduced predators pose
to native wildlife.
ACKNOWLEDGEMENTS
This study was carried out under the University of
Tasmania Animal Ethics Permit numbers of A0008756,
A0008627, and the Department of Primary Industries
and Water permit number FA05257. Thanks to the
Behavioural Ecology and Evolutionary Research
Group for assistance in rat catching and maintenance,
as well as stimulating discussions and feedback on
earlier versions of this manuscript. The authors also
appreciate the efforts of Dan Purdey,TorraneVergis and
Tom Sloane in particular in obtaining predator scent.
The authors also wish to thank the anonymous reviewers for valuable feedback and comments on earlier
versions of this manuscript.
REFERENCES
Abrams P. A. (1993) Optimal ‘traits’ when there are several costs
– the interaction of mortality and energy costs in determining foraging behavior. Behav. Ecol. 4, 246–53.
Agrawal A. A., Laforsch C. & Tollrian R. (1999) Transgenerational induction of defences in animals and plants. Nature
401, 60–3.
Apfelbach R., Blanchard C. D., Blanchard R. J., Hayes R. A. &
McGregor I. S. (2005) The effects of predator odours in
mammalian prey species: a review of field and laboratory
studies. Neurosci. Biobehav. Rev. 29, 1123–44.
© 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
929
Banks P. B. (1998) Responses of Australian bush rats, Rattus
fuscipes, to the odour of introduced Vulpes vulpes. J. Mammal.
79, 1260–4.
Banks P. B. (1999) Predation by introduced foxes on native bush
rats in Australia: do foxes take the doomed surplus? J. Appl.
Ecol. 36, 1063–71.
Banks P. B., Dickman C. R. & Newsome A. E. (1998) Ecological
costs of feral predator control: foxes and rabbits. J.Wildlife
Manage. 62, 762–72.
Banks P. B., Hughes N. K. & Rose T. A. (2003) Do Australian
native small mammals avoid faeces of domestic dogs? Aust.
Zool. 32, 406–9.
Belcher C. A. & Darrant J. P. (2004) Home range and spatial
organization of the marsupial carnivore, Dasyurus maculatus
maculatus (Marsupialia: Dasyuridae) in south-eastern
Australia. J. Zool. 262, 271–80.
Blanchard D. C., Markham C., Yang M., Hubbard D., Madarang
E. & Blanchard R. J. (2003) Failure to produce conditioning
with low-dose trimethylthiazoline or cat feces as unconditioned stimuli. Behav. Neurosci. 117, 360–8.
Blanchard R. J., Nikulina J. N., Sakai R. R., McKittrick C.,
McEwen B. & Blanchard D. C. (1998) Behavioral and
endocrine change following chronic predatory stress.
Physiol. Behav. 63, 561–69.
Blumstein D. T., Mari M., Daniel J. C., Ardron J. G., Griffin
A. S. & Evans C. S. (2002) Olfactory predator recognition:
wallabies may have to learn to be wary. Anim. Conserv. 5,
87–93.
Burman O. H. P. & Mendl M. (2006) Long term social memory
in the laboratory rat (Rattus norvegicus). Anim Welfare. 15,
379–82.
Burwash M. D., Tobin M. E., Woolhouse A. D. & Sullivan T. P.
(1998) Laboratory evaluation of predator odors for eliciting
an avoidance response in roof rats (Rattus rattus). J. Chem.
Ecol. 24, 49–66.
Campbell T., Lin S., DeVries C. & Lambert K. (2003) Coping
strategies in male and female rats exposed to multiple
stressors. Physiol. Behav. 78, 495–504.
Cattell R. B. (1966) The scree test for the number of factors.
Sociol. Methods Res. 1, 245–76.
Chabot D., Gagnon P. & Dixon E. A. (1996) Effect of
predator odours on heart rate and metabolic rate of
wapiti (Cervus elaphus canadensis). J. Chem. Ecol. 22, 839–
68.
Coss R. G. (1999) Effects of relaxed natural selection on the
evolution of behaviour. In: GeographicVariation of Behaviour:
An Evolutionary Perspective (eds S. A. Foster & J. A. Endler)
pp. 180–208. Oxford University Press, Oxford.
Department of Primary Industries and Water (2006) Natural
Environment:Weeds, Pests and Diseases. [Cited 3 July 2006.]
Available from URL: http://www.dpiw.tas.gov.au
Devereux C. L., Whittingham M. J., Fernandez-Juricic E.,
Vickery J. A. & Krebs J. R. (2006) Predator detection and
avoidance by starlings under differing scenarios of predation
risk. Behav. Ecol. 17, 303–9.
Dickman C. R. (1992) Predation and habitat shift in the house
mouse, Mus-Domesticus. Ecology. 73, 313–22.
Dingemanse N. J., Both C., Drent P. J., van Oers K. & Noordwijk
A. J. (2002) Repeatability and heritability of exploratory
behaviour of great tits from the wild. Anim. Behav. 64,
929–38.
Driessen M. M. (1998) Observations on the diets of the longtailed mouse, Pseudomys higginsi, and the velvet-furred rat,
Rattus lutreolus velutinus, in southern Tasmania. Aust.
Mammal. 21, 121–30.
doi:10.1111/j.1442-9993.2008.01863.x
930
J. M C E VOY ET AL.
Dufty A. M. & Crandall M. B. (2005) Corticosterone secretion
in response to adult alarm calls in American Kestrels. J. Field
Ornithol. 76, 319–25.
Engh A. L., Beehner J. C., Bergman T. J. et al. (2006) Behavioural and hormonal responses to predation in female
chacma baboons (Papio hamadryas ursinus). Proc. Roy. Soc. B
273, 707–12.
Epstein S. (1983) Aggregation and beyond: some basic issues on
the prediction of behavior. J. Pers. 51, 360–92.
Feldman H. N. (1994) Methods of scent marking in the domestic cat. Can. J. Zool. 72, 1093–9.
File S. E., Zangrossi H., Sanders F. L. & Mabbutt P. S. (1993)
Dissociation between behavioural and corticosterone
responses on repeated exposures to cat odor. Physiol. Behav.
54, 1109–11.
Genaro G. & Schmidek W. R. (2000) Exploratory activity of
rats in three different environments. Ethology 106, 849–
59.
Glen A. S. & Dickman C. R. (2006) Diet of the spotted-tailed
quoll (Dasyurus maculatus) in eastern Australia: effects of
season, sex and size. J. Zool. 269, 241–8.
Griffin A. S., Evans C. S. & Blumstein D. T. (2001) Learning
specificity in acquired predator recognition. Anim. Behav.
62, 577–89.
Hayes R. A., Nahrung H. F. & Wilson J. C. (2006) The response
of native Australian rodents to predator odours varies seasonally: a by-product of life history variation? Anim. Behav.
71, 1307–14.
Hocking G. J. & Driessen M. M. (2000) Status and conservation
of the rodents of Tasmania. Wildl. Res. 27, 371–7.
Jacob J. & Brown J. S. (2000) Microhabitat use, giving-up densities and temporal activity as short- and long-term antipredator behaviors in common voles. Oikos 91, 131–8.
Jedrzejewski W., Rychlik L. & Jedrzejewski B. (1993) Responses
of bank voles to odours of seven species of predators: experimental data and their relevance to natural predator-vole
relationships. Oikos 68, 251–7.
Jones E. & Coman B. J. (1981) Ecology of the feral cat, Felis catus
(L), in southeastern Australia. 1. Diet. Aust. Wildl. Res. 8,
537–47.
Jones M. & Dayan T. (2000) Foraging behaviour and microhabitat use by spiny mice, Acomys cahirinus and A. russatus, in
the presence of blanford’s fox (Vulpes cana) odor. J. Chem.
Ecol. 26, 455–69.
Jones M. E., Smith G. C. & Jones S. M. (2004) Is anti-predator
behaviour in tasmanian eastern quolls (Dasyurus viverrinus)
effective against introduced predators? Anim. Conserv. 7,
155–60.
Kats L. B. & Dill L. M. (1998) The scent of death: chemosensory
assessment of predation risk by prey animals. Ecoscience. 5,
361–94.
Krupa J. J. & Sih A. (1998) Fishing spiders, green sunfish, and a
stream-dwelling water strider: male-female conflict and prey
responses to single versus multiple predator environments.
Oecologia 117, 258–65.
Kruuk H. & Jarman P. J. (1995) Latrine use by the spotted-tailed
quoll (Dasyurus maculatus: Dasyuridae, Marsupialia) in its
natural habitat. J. Zool. 236, 345–9.
Laska M., Fendt M., Wieser A., Endres T., Salazar L. T. H. &
Apfelbach R. (2005) Detecting danger-or just another
odorant? Olfactory sensitivity for the fox odour component
2,4,5-trimethylthiazoline in four species of mammals.
Physiol. Behav. 84, 211–5.
Marquez C., Nadal R. & Armario A. (2004) The hypothalamicpituitary-adrenal and glucose responses to daily repeated
doi:10.1111/j.1442-9993.2008.01863.x
immobilisation stress in rats: individual differences. Neuroscience 123, 601–12.
Martin P. & Bateson P. (1993) Measuring Behaviour: An Introductory Guide. Cambridge University Press, Cambridge.
Masini C. V., Sauer S. & Campeau S. (2005) Ferret odour as a
processive stress model in rats: neurochernical, behavioral,
and endocrine evidence. Behav. Neurosci. 119, 280–92.
Mohr K., Vibe-Petersen S., Jeppesen L. L., Bildsoe M. & Leirs
H. (2003) Foraging of multimammate mice, Mastomys
natalensis, under different predation pressure: cover, patchdependent decisions and density-dependent GUDs. Oikos
100, 459–68.
Monclus R., Rodel H. G., Von Holst D. & De Miguel J. (2005)
Behavioural and physiological responses of naive European
rabbits to predator odour. Anim. Behav. 70, 753–61.
Murray D. L., Roth J. D. & Wirsing A. J. (2004) Predation risk
avoidance by terrestrial amphibians: the role of prey experience and vulnerability to native and exotic predators.
Ethology 110, 635–47.
Nolte D. L., Mason J. R., Epple G., Aronov E. & Campbell D. L.
(1994) Why are predator urines aversive to prey. J. Chem.
Ecol. 20, 1505–16.
Oakwood M. (2002) Spatial and social organization of a carnivorous marsupial Dasyurus hallucatus (Marsupialia:
Dasyuridae). J. Zool. 257, 237–48.
Powell F. & Banks P. B. (2004) Do house mice modify their
foraging behaviour in response to predator odours and
habitat? Anim. Behav. 67, 753–9.
Ray J. & Hansen S. (2005) Temperamental development in the
rat: the first year. Dev. Psychobiol. 47, 136–44.
Rostain R. R., Ben-David M., Groves P. & Randall J. A. (2004)
Why do river otters scent-mark? An experimental test of
several hypotheses. Anim. Behav. 68, 703–11.
Rounsevell D. E., Taylor R. J. & Hocking G. J. (1991) Distribution records of native terrestrial mammals in Tasmania.
Wildl. Res. 18, 699–717.
Russell B. G. & Banks P. B. (2005) Response of four Critical
Weight Range (CWR) marsupials to the odours of native
and introduced predators. Aust. Zool. 33, 217–22.
Russell B. G. & Banks P. B. (2007) Do Australian small
mammals respond to native and introduced predator
odours? Austral Ecol. 32, 277–86.
Short J., Turner B. & Risbey D. (2002) Control of feral cats for
nature conservation III. Trapping. Wildl. Res. 29, 475–87.
Sih A. & McCarthy T. M. (2002) Prey responses to pulses of risk
and safety: testing the risk allocation hypothesis. Anim.
Behav. 63, 437–43.
Sih A., Bell A. & Johnson J. C. (2004a) Behavioural syndromes:
and ecological and evolutionary overview. Trends Ecol. E. 19,
372–8.
Sih A., Bell A. M., Johnson J. C. & Ziemba R. E. (2004b)
Behavioural syndromes: an integrative overview. Q. Rev.
Biol. 79, 241–77.
Sinn D. L. & Moltschaniwskyj N. A. (2005) Personality traits in
dumpling squid (Euprymna tasmanica): context-specific
traits and their correlation with biological characteristics.
J. Comp. Psych. 119, 99–110.
Tabachnick G. & Fidell L. S. (1996) Using Multivariate Statistics.
HarperCollins, New York.
Takahashi L. K., Nakashima B. R., Hong H. C. & Watanabe K.
(2005) The smell of danger: a behavioral and neural analysis
of predator odour-induced fear. Neurosci. Behav. Rev. 29,
1157–67.
Thor D. H., Harrison R. J., Schneider S. R. & Carr W. J. (1988)
Sex-differences in investigatory and grooming behaviors of
© 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
N AT I V E A N D I N T R O D U C E D P R E DATO R R E C O G N I T I O N
laboratory rats (Rattus norvegicus) following exposure to
novelty. J. Comp. Psych. 102, 188–92.
Wallace K. J. & Rosen J. B. (2000) Predator odor as an unconditioned fear stimulus in rats: elicitation of freezing by trimethylthiazoline, a component of fox feces. Behav. Neurosci.
114, 912–22.
Wellington Park Manangement Trust (2006) Environment.
[Cited 3 July 2006.] Available form URL: http://www.
wellingtonpark.tas.gov.au/environmentnatureindex.php
Whishaw I. Q., Gharbawie O. A., Clark B. J. & Lehmann H.
(2006) The exploratory behaviour of rats in an open
© 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
931
environment optimizes security. Behav. Brain. Res. 171, 230–
39.
Wohlfahrt B., Mikolajewski D. J., Joop G. & Suhling F. (2006)
Are behavioural traits in prey sensitive to the risk imposed
by predatory fish? Freshwater Biol. 51, 76–84.
Wood W. F., Terwilliger M. N. & Copeland J. P. (2005) Volatile
compounds from anal glands of the wolverine, Gulo gulo. J
Chem Ecol. 31, 2111–17.
Zwick W. R. & Velicer W. F. (1986) Comparison of five rules for
determining the number of components to retain. Psychol.
Bull. 99, 432–42.
doi:10.1111/j.1442-9993.2008.01863.x