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Discrimination of introduced predators by ontogenetically naïve prey scales with duration of shared evolutionary history


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Hypotheses on the discrimination and recognition of predators by prey are divided as to whether the prey species' ability to recognize and avoid predators is proportionate to the duration of evolutionary exposure to specific predators or is a result of more generalized discrimination processes. Moreover, understanding of the timeframes necessary for prey species to maintain or acquire appropriate responses to introduced predators is poorly understood. We studied a population of wild, ontogenetically predator naïve greater bilbies, Macrotis lagotis, living within a large (60 km²) predator-free exclosure, to determine whether they modified their burrow-emergence behaviour in response to olfactory stimuli from introduced predators, dogs, Canis familiaris, and cats, Felis catus. Greater bilbies have shared over 3000 years of coevolutionary history with dogs but less than 200 years with cats. Bilbies spent more time only partially emerged (with at most head and shoulders out) as opposed to fully emerged (standing quadrupedally or bipedally) from their burrows when dog faeces were present, in comparison to faeces of cats, rabbits and an unscented control. Our results were consistent with the ‘ghosts of predator past’ hypothesis, which postulates that prey species' abilities to respond to the odours of predators scales with their period of coexistence. Our study supports the notion that introduced predators should be regarded as naturalized if prey possess an innate ability to detect their cues and respond accordingly.
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Discrimination of introduced predators by ontogenetically naïve prey
scales with duration of shared evolutionary history
Lisa A. Steindler
, Daniel T. Blumstein
, Rebecca West
, Katherine E. Moseby
Mike Letnic
Centre for Ecosystem Science, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, Australia
Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA
Arid Recovery Ltd., Roxby Downs, Australia
article info
Article history:
Received 14 August 2017
Initial acceptance 6 November 2017
Final acceptance 27 December 2017
MS. number: 17-00652
antipredator behaviour
evolutionary history
greater bilby
ontogenetic naïvet
predator odour discrimination
prey naivet
e hypothesis
Hypotheses on the discrimination and recognition of predators by prey are divided as to whether the
prey species' ability to recognize and avoid predators is proportionate to the duration of evolutionary
exposure to specic predators or is a result of more generalized discrimination processes. Moreover,
understanding of the timeframes necessary for prey species to maintain or acquire appropriate responses
to introduced predators is poorly understood. We studied a population of wild, ontogenetically predator
naïve greater bilbies, Macrotis lagotis, living within a large (60 km
) predator-free exclosure, to determine
whether they modied their burrow-emergence behaviour in response to olfactory stimuli from intro-
duced predators, dogs, Canis familiaris, and cats, Felis catus. Greater bilbies have shared over 3000 years
of coevolutionary history with dogs but less than 200 years with cats. Bilbies spent more time only
partially emerged (with at most head and shoulders out) as opposed to fully emerged (standing quad-
rupedally or bipedally) from their burrows when dog faeces were present, in comparison to faeces of
cats, rabbits and an unscented control. Our results were consistent with the ghosts of predator past
hypothesis, which postulates that prey species' abilities to respond to the odours of predators scales with
their period of coexistence. Our study supports the notion that introduced predators should be regarded
as naturalized if prey possess an innate ability to detect their cues and respond accordingly.
©2018 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Hypotheses on the discrimination and recognition of predators
by prey are divided as to whether a prey's ability is proportionate to
the duration of coevolution (Banks &Dickman, 2007; Blumstein,
2002) or a result of ontogenetic experience (Berger, 1998) with
specic predators, or whether prey simply generalize their response
to all predators based on characteristics shared among predators
(Apfelbach, Parsons, Soini, &Novotny, 2015; Cox &Lima, 2006). The
ghosts of predators pasthypothesis (Peckarsky &Penton, 1988)
suggests that species that have had a long period of coevolutionwith
a predator may possess hard-wiredantipredator responses. Prey
may exhibit innate abilities to recognize and respond to the
scents and images of coevolved predators (Apfelbach, Blanchard,
Blanchard, Hayes, &McGregor, 2005; Blumstein, Daniel, Schnell,
Ardron, &Evans, 2002; Monclús, R
odel, Von Holst, &De Miguel,
2005). In contrast, prey species that have not been evolutionarily
exposed to predators may learn through ontogenetic experience to
recognize and respond to predators' olfactory cues (Anson &
Dickman, 2013; Berger, Swenson, &Persson, 2001) or to their vi-
sual cues (Atkins et al., 2016).
The predator archetypehypothesis suggests that for many prey
species, their capacity to recognize and respond to cues associated
with predators may be generalized and not be limited to specic
predators (Cox &Lima, 2006). As a result, prey may exhibit anti-
predator responses towards cues that share characteristics with
those with which they have coevolved or cohabited (Cox &Lima,
2006). For example, the common constituentshypothesis posits
that odours from predators share common compounds that prey
should respond to regardless of the predator that produced it
(Apfelbach et al., 2015; Nolte, Mason, Epple, Aronov, &Campbell,
1994). It has also been suggested that a prey's ability to discrimi-
nate between predator odours is inuenced by its body size
(Apfelbach et al., 2015; Woolhouse &Morgan, 1995). Small prey are
more likely to encounter predators at close quarters and thus may
have little opportunity to assess the threat posed by different
*Correspondence: M. Letnic, Centre for Ecosystem Science, School of Biological,
Earth and Environmental Sciences, University of New South Wales, 2035, Sydney,
E-mail address: (M. Letnic).
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0003-3472/©2018 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Animal Behaviour 137 (2018) 133e139
predators (Apfelbach et al., 2015). Hence smaller, less mobile prey
species are predicted to fear almost any carnivore odour (McEvoy,
Sinn, &Wapstra, 2008; Nolte et al., 1994).
In situations where the risk of predation is low or nonexistent,
the benets of expressing antipredator behaviours may be out-
weighed by the costs of missed opportunities to obtain food re-
sources or mates. Consequently, relaxed selection by predators on
both ontogenetic and evolutionary timescales may result in prey
e, whereby species may have diminished antipredator
behaviour and/or fail to recognize and/or mount effective re-
sponses against novel predators (Banks, 1998; Blumstein, 2006;
Blumstein, Daniel, &Springett, 2004; Goldthwaite, Coss, &
Owings, 1990).
Understanding of the factors that dictate prey species' abilities
to recognize and respond to predators is an important theoretical
issue (Cox &Lima, 2006; Ferrari, Messier, &Chivers, 2008;
Parsons, Apfelbach, Banks, Cameron, Dickman, Frank et al.,
2017),as well as an important applied topic. Evolutionary prey
e towards introduced predators has been hypothesized to be
a major factor contributing to population declines of native prey
species and failed attempts to reintroduce locally extinct species
(Moseby et al., 2011; Salo, Korpim
aki, Banks, Nordstr
om, &
Dickman, 2007). However, our understanding of the evolu-
tionary timeframes necessary for prey species to maintain or ac-
quire appropriate responses to introduced predators is poorly
known. Many of the studies that have investigated the evolved
abilities of wild prey to recognize cues associated with coevolved
and novel predator species did not control for variation in onto-
genetic exposure to predators (Anson &Dickman, 2013; Carthey &
Banks, 2012, 2016). Thus, it remains possible that responses of
prey species to predator cues reported in many studies were, to
some extent, shaped by generalization (Dickman &Doncaster,
1984)orreect a result of both an individual's lifetime experi-
ence and the history of evolutionary exposure to predators
(Blumstein, 2006; Hettena, Munoz, &Blumstein, 2014).
Knowledge of the extent to which prey species' responses to
predators are the result of coevolution or learning and the time-
frames required for appropriate antipredator responses to be lost
or develop has direct application to the development of pro-
grammes that attempt to overcome the problem of prey naïvet
(Moseby, Blumstein, &Letnic, 2016; West, Letnic, Blumstein, &
Moseby, 2017). Indeed, if prey species can adequately recognize
and appropriately respond to introduced predators, then it may no
longer be necessary to classify them as introduced but instead
naturalized (Carthey &Banks, 2012).
Prey are able to detect and respond to the presence of predators
through the useof sight, sound and smell (Banks, Bytheway, Carthey,
Hughes, &Price,2014;Parsons, Apfelbach,Banks, Cameron, Dickman,
Frank et al., 2017). In coevolved predatoreprey systems, prey often
use predator odours as cues to detect predators, gauge risk and
respond accordingly (Anson &Dickman,2013; Apfelbach et al., 2005;
Apfelbach et al.,2015; Parsons, Apfelbach, Banks, Cameron,Dickman,
Frank et al., 2017). Prey use refuges, such as burrows, to avoid pre-
dation (Martín &L
opez, 1999; Sih, Petranka, &Kats, 1988). Since
predatorscan move through landscapes, the riskof predation outside
burrows uctuates through time. Consequently, prey must decide
when it is safe to move in and out of a refuge (Martín &L
opez, 2015;
Parsons, Apfelbach, Banks, Cameron, Dickman, Frank et al., 2017; Sih,
1997). We predicted that if a prey species is able to detecta predator
rst, then it will optimize the avoidance of predators through
appropriate risk assessment strategies (e.g. Lima &Dill, 1990).
However, this relies on a prey's ability to rapidly recognize and
discriminate between predator cues.
Here we evaluated the ideas that a prey's ability to respond to
predator odours is inuenced by the duration of coevolution, as
opposed to a generalized response to shared characteristics of
predator cues. We did this by quantifying the behavioural re-
sponses of an ontogenetically predator naïve population of wild-
living greater bilbies, Macrotis lagotis, to faecal samples from two
introduced predators (dog, Canis familiaris, and cat, Felis catus), a
herbivore (rabbit, Oryctolagus cuniculus) and a procedural control
(no odour). Bilbies have shared varying periods of coevolution with
these predators and rabbits. Dingoes/dogs and feral cats are both
known to predate on bilbies, and have been implicated in previous
reintroduction failures of bilbies beyond predator-free fenced re-
serves (Moseby et al., 2011; Southgate &Possingham, 1995). Since
many mammalian predators scent mark features in the landscape,
such as the burrows of prey species, by depositing urinary and
faecal odours (Corbett, 1995; Gorman &Trowbridge, 1989), we
deployed faeces at the entrance of bilbies' burrows. The decision to
emerge from a refuge, such as a burrow, requires prey to estimate
predation risk outside the shelter versus the benets of potential
rewards (Martín &L
opez, 1999; Sih, 1997).
If the duration of coevolution with predators inuenced bilbies'
ability to respond to predators, we would expect that bilbies should
be more wary when emerging from burrows when dog rather than
cat faeces are present. Bilbies have had more than 3000 years of
coevolution with dogs/dingoes (Savolainen, Leitner, Wilton,
Matisoo-Smith, &Lundeberg, 2004), but less than 200 years of
coevolution with cats (Abbott, 2002). If bilbies generalized their
response to placental predators, we expected that bilbies would
respond similarly to dogs and cats, but not respond to rabbits or the
control (no faeces). Rabbits are an introduced herbivore, harmless
to bilbies, with which bilbies have had less than 160 years historical
exposure (Zenger, Richardson, &Vachot-Grifn, 2003). We
restricted our test to introduced predators to which the source
populations would have been exposed in the 20th century and did
not include the scent of a marsupial predator, the western quoll,
Dasyurus geoffroii, with which they would have had a longer period
of evolutionary coexistence. The reasons for not including quoll
scent were twofold. First, quolls and bilbies have not coexisted in
the wild for over 100 years (Morris et al., 2003) and second, it was
not possible for us to obtain scent samples from captive quolls at
the time the study was conducted. Even though we did not have
scents of a marsupial predator, we are condent that our test of the
hypothesis, that the duration of coevolution with a predator in-
uences predator recognition, was not confounded by ontogenetic
experience, as the population of bilbies within our study site have
not been exposed to placental predators for more than 16 years.
Study Area
We studied bilbies within the 60 km
fenced exclosure at Arid
Recovery Reserve, South Australia (12 300 ha, 30
S, 136
Arid Recovery Reserve is in the aridzone, with an average rainfall of
149.4 mm (from 1997 and 2015; Bureau of Meteorology, 2015). A
1.8 m high predator-proof fence surrounds the reserve. Dingoes,
foxes, cats and rabbits are absent from the fenced exclosures where
the study was undertaken. Locally extinct mammals, including bil-
bies, were reintroduced to the Arid Recovery Reserve in 2000
following the eradication of predators and introduced feral herbi-
vores, such as rabbits (Moseby, Hill, &Read, 2009). All the mammals
reintroduced to Arid Recovery are wild, as they are not given sup-
plementary food and are exposed to avian and reptilian predators.
L. A. Steindler et al. / Animal Behaviour 137 (2018) 133e139134
Study Species
Greater bilbies are an omnivorous, burrowing, nocturnal and
largely solitary marsupial (Moseby, Cameron, &Crisp, 2012). Male
bilbies weigh 800e2500 g and females weigh 600e1200 g
(Southgate, Christie, &Bellchambers, 2000). The distribution of
bilbies has contracted markedly since European settlement of
Australia in 1788 and they now occupy just 20% of their former
range (Southgate, 1990). This decline has been attributed primarily
to predation by introduced red foxes, Vulpes vulpes, and feral cats
(Moseby &O'Donnell, 2003; Southgate, 1990), as well as dingoes/
wild dogs (Pavey, 2006). Naïvet
e towards introduced predators
(such as feral cats and red foxes) has been implicated in the decline
of many Australian mammals (Moseby et al., 2012). Bilbies have
been successfully reintroduced to some areas and islands within
their former range where feral cats and foxes are absent, intensively
controlled or eradicated (Moseby &O'Donnell, 2003).
The reintroduced population of bilbies at Arid Recovery Reserve
were sourced from captive stock from Monarto Zoo (Moseby &
O'Donnell, 2003), which descended from wild individuals
captured from deserts in Western Australia and the Northern Ter-
ritory (Moseby et al., 2011). Bilbies can produce a litter of one to
three young, four times a year, and have a captive longevity of 5e9
years (Southgate et al., 2000). Based on the reproductive rate of the
bilby and historical source of the population of bilbies at Arid Re-
covery, we assumed that this population, in the wild, has gone
through ve predator-naïve generations over the past 16 years.
Sources and Storage of Treatment Odours
We used faeces from three species: domestic dogs, domestic
cats and wild rabbits along with a procedural control, which was no
faeces present. We used domestic dog scats as previous studies
have shown that they are chemically indistinguishable from those
of dingoes (Carthey, 2013). To overcome the issue of decomposition
of faecal odours after deposition, domestic dog and cat faecal
samples were collected immediately from private pet owners and
local veterinary hospitals, stored and sealed in airtight zip lock
bags, and frozen at minus 20
C(Carthey, 2013). Wild rabbit faecal
samples were collected fresh from rabbit warrens. Disposable
gloves were always worn when handling faeces to prevent cross
contamination of odours. As faecal samples were collected from
private pet owners and local veterinary hospitals, from multiple
individual sources, the total number of donor individuals was un-
known; however, it may be approximated that samples were
sourced from between two and 10 separate individuals of each
species. As rabbit faeces were collected from a wild population, the
number of source individuals is unknown. To take potential donor
effects into account, faeces allocation was randomized. Since the
diets of domestic pets were consistent between individuals and
were made up of a mix of raw meats and pet foods, we did not
consider diet to be a potential confounding source in analysis
(Carthey, 2013).
Bilby Burrow Emergence Behaviour
A total of 18 wild individual bilbies (10 females, eight males)
were caught and tted with a 9 g core tail mount with whip an-
tenna radiotransmitter (Sirtrack, Havelock North, New Zealand)
between August and October 2015. Transmitters were attached
according to the protocol of the South Australian National Parks and
Wildlife Service (Moseby &O'Donnell, 2003). Individuals were
radiotracked daily to their diurnal burrows for 2e8 weeks, with
experiments commencing at least 2 nights after transmitter
We used a repeated measures design in which each individual
was presented with each odour treatment once according to a
predetermined balanced order. We controlled for order effects
experimentally and assessed these effects statistically.
Odour treatments were presented on every third night of
tracking, for a single night. There were two baselinenights, where
no odour was presented, to ensure that there was no residual odour
from the previous treatment. Faeces were presented on the surface
of the ground, within 20 cm of the burrow entrance. If there were
multiple burrow entrances, faeces were placed at the burrow
entrance that recorded the strongest VHF transmitter signal. One
piece of cat and dog faeces of similar size and weight (approxi-
mately 25e30 g) and 20 pellets of rabbit faeces were presented
outside the burrow accordingly.
At each burrow entrance on treatment and baselinenights a
metal post was positioned approximately 1e2 m from the burrow
entrance, supporting either a Bushnell Trophy Cam (Bushnell,
Overland Park, KS, U.S.A.), Scoutguard SG550V or Scoutguard
Zeroglow (Scoutguard, Molendinar, Australia), infrared motion
sensor video camera. Cameras were mounted 20e100 cm off the
ground and were programmed to take 60 s of video, when trig-
gered, to enable species identication and observe burrow emer-
gence and behavioural responses to the odour treatments (Fig. 1),
with a 0 s inter val between possible triggers, from dusk until dawn
(1700e0700 hours).
Behavioural Scoring
We constructed an ethogram of behaviours (Table 1) based upon
the initial observations of experimental videos. All behaviours were
treated as mutually exclusive (Blumstein &Daniel, 2007). We
scored video recordings 60 s using the event recorder JWatcher
(Blumstein &Daniel, 2007). We focused on quantifying only the
rst 60 s video footage of each bilby at the burrow entrance. We did
this because our study focused on quantifying bilbies' initial
Figure 1. Experimental set-up for the bilby predator odour discrimination study. The
photo shows the infrared motion sensor video camera mounted on a metal post
outside the burrow entrance of a radiotracked bilby.
L. A. Steindler et al. / Animal Behaviour 137 (2018) 133e139 135
behavioural responses to the presence of predators' scats and we
wanted to eliminate the potential for our observations to be
inuenced by habituation to the presence of scats. We calculated
the proportion of time in sight allocated to each behaviour. We
quantied the behaviour of both identied bilbies (i.e. those with a
tail transmitter), as well as other individuals that shared the bur-
rows with marked subjects. Behavioural scoring of the videos
commenced at the start of each 60 s video, with comparisons only
made between treatmentnights. The inclusion of no odour
treatments ensured we were able to compare behavioural re-
sponses to the different odour treatments and as such we did not
compare baselineand treatmentnights.
For analysis we combined behaviours in which the bilby was
fully emerged from the burrow to create a new category fully
emerged(Table 1). It was not possible to record data blind because
our study involved focal animals in the eld and it was possible to
visually identify the odour treatments.
Analysis of Behavioural Data
We tted a series of linear mixed-effects models in SPSS-22
(IBM Corp., Armonk, NY, U.S.A.) with diagonal error structure to
test bilby burrow emergence behaviour in response to treatment.
We had two xed effects in our models: treatment and presenta-
tion order. To account for the possibility of nonindependence be-
tween observations, we included individuals as a random effect. In
preliminary analyses, we also tested for the effects of moon phase;
as this was never signicant, however, we did not include it as a
predictor variable in our nal model. In no case was presentation
order signicant; we retained it as a blocking factor in the analysis,
however, to control for its effect statistically (Quinn &Keough,
2002). In instances where the treatment effect was signicant
(P<0.05), we used Fisher's least signicant difference (LSD) post
hoc test to examine planned comparisons for differences in
response to each odour.
Ethical Note
Work was conducted under animal ethics APEC Approval
Number 1/2014 Tackling Prey Naivety in Australia's Threatened
Mammals' and in accordance with the South Australian Wildlife
Ethics Committee.
Bilbies were captured with either cage traps (45 20 cm and
20 cm high), baited with a combination of peanut butter and rolled
oats, or hand-held shing nets as described by Moseby et al. (2012).
As bilbies did not readily enter the cage traps, 17 of 18 bilbies were
captured with nets. Bilbies that were netted were located during
night-time searches conducted with spotlights from a vehicle. When
sighted, they were approached and netted with a hand-held net. On
capture, bilbies were transferred from the net to a dark nylon eece
bag for processing and transmitter attachment. Bilbies were securely
restrained within the processing bag, rather than anaesthetized
during the attachment of the radiotransmitter. The transmitter
weighed 1.25% of an 800 g female and 0.07% of a 1400 g male bilby.
For transmitter attachment, hair on the tail of the bilby was
removed using scissors and disposable razors, and a transmitter
attached using Leukoplast adhesive tape. To prevent the formation
of tail ulcers, extra care was taken to ensure that the transmitter
was not rmly pressed to the tail (Moseby &O'Donnell, 2003). Only
trained personnel were responsible for transmitter attachment.
To ensure that animal movements were not hindered by the
capture and processing procedure, daily radiotracking of individuals
commenced immediately after transmitter attachment. For 15 bil-
bies, the tail transmitters fell off after approximately 2e3 months.
For three bilbies, the transmitters did not fall off and were manually
removed. These bilbies were captured by placing cage traps near
their burrows within a temporary pen constructed of wire netting
(Southgate, McRae, &Atherton,1995). The bilbies were restrained as
described above and the transmitters removed by cutting the tape
with scissors. Each of the bilbies was deemed healthy on release;
however, further checks were not possible because we could not
locate individual bilbies without transmitters.
There was no effect of treatment on the proportion of time that
bilbies spent out of sight in the burrow (F
3, 29.836
¼0.036, P¼0.991;
Fig. 2a), walking (F
3, 34.225
¼0.634, P¼0.598; Fig. 2b) and running
3, 11.195
¼1.054, P¼0.407; Fig. 2c).
There was a signicant effect of treatment on the proportion of
time that bilbies spent partially emerged from their burrows, with at
most their head and shoulders exposed (F
3, 34.389
Fig. 2d). Planned comparisons (Fig. 2d) revealed that bilbies spent
more time partially emerged when dog faeces were present
compared to cat faeces (Fisher's LSD, dog versus cat: P¼0.013),
rabbit faeces (Fisher's LSD, dog versus rabbit: P¼0.015) and the
control (no faeces; Fisher's LSD, dog versus control: P0.001).
There were no signicant differences in time spent partially
emerged when cat and rabbit faeces (Fisher's LSD, cat versus rabbit:
P¼0.922), cat faeces and the control (Fisher's LSD, cat versus con-
trol: P¼0.135), and rabbit faeces and the control were present
(Fisher's LSD, rabbit versus control: P¼0.213; Fig. 2d).
There was a signicant effect of treatment on the combined
proportion of time spent fully emerged (F
3, 32.283
¼3.134, P¼0.039;
Fig. 2e). Bilbies spent less time fully emerged from the burrow when
dog faeces were present compared to the control (nofaeces; Fisher's
LSD, dog versus control: P¼0.006; Fig. 2e). There was no signicant
difference between time spent fully emerged when dog faeces were
present compared to cat faeces (Fisher's LSD, dog versus cat:
P¼0.180) and rabbit faeces (Fisher's LSD, dog versus rabbit:
P¼0.078). There were no differences in the time spent fully
emerged when cat and rabbit faeces (Fisher's LSD, cat versus rabbit:
P¼0.676), cat faeces and the control (Fisher's LSD, cat versus con-
trol: P¼0.184), and rabbit faeces and the control were present
(Fisher's LSD, rabbit versus control: P¼0.407; Fig. 2e).
Table 1
Ethogram of greater bilby, M. lagotis, burrow emergence behaviour
Behaviour Description of behaviour
Partially emerged Individual at burrow entrance, with at most head and shoulders out. Head xated, potentially looking or
snifng or looking and snifng
Fully emerged Individual standing quadrupedally or bipedally, fully emerged from burrow. Head xated, potentially
looking or snifng, or looking and snifng
Walk Animal moving slowly when exiting and fully emerged from burrow
Run Animal moving rapidly when exiting and fully emerged from burrow
Out of sight in burrow Individual seen on camera and retreated out of sight into burrow
L. A. Steindler et al. / Animal Behaviour 137 (2018) 133e139136
Our results provide support for the ghosts of predators past
hypothesis (Peckarsky &Penton, 1988) which posits that prey
species' ability to respond to predator cues scales with the dura-
tion of their coevolution. This nding was evidenced by the
greater proportion of time that bilbies spent partially emerged
from the burrow as opposed to fully emerged, when dog faeces
were present. In contrast, bilbies spent proportionately more time
fully emerged from their burrows when cat (an introduced pred-
ator) and rabbit faeces (an introduced herbivore) and the proce-
dural control (no odour) were presented. Despite complete
ontogenetic naïvet
e and at least 16 years of evolutionary isolation,
bilbies at the Arid Recovery Reserve appear to have retained
specic antipredator respons es towards the olfactory cues of dogs /
dingoes, but have a negligible response to cats. Bilbies have shared
over 3000 years of evolutionary history with dogs/dingoes,
compared to cats with which they have had less than 200 years of
evolutionary exposure. Our results support the idea that in
coevolved predatoreprey systems, prey may possess innate
abilities to detect the risk associated with predator cues and
respond accordingly, but lack this form of recognition when
predators are novel (Banks et al., 2014; Zhang, Zhao, Zhang,
Messenger, &Wang, 2015).
Our results showed that, while partially emerged, bilbies
appeared to discriminate between the odours of dogs and cats.
They similarly showed a weak response to the odours of cats,
harmless rabbits and the unscented control, while partially
emerged. These results contradict the predator archetypehy-
pothesis, which suggests prey may exhibit a generalized response
towards predator cues that share characteristics with their
coevolved predators (Cox &Lima, 2006). Our results further
contradict the common constituentshypothesis, which suggests
that odours from placental predators share common sulphur- and
nitrogen-rich compounds that prey should respond to regardless
of the predator that produced it (Apfelbach et al., 2015; Nolte et al.,
1994). These ndings further suggest that bilbies responded most
to the predator with which they have shared the longest period of
coevolution, rather than displaying a generalized response to
predator odours.
0.25 (a) (b)
Cat Control Dog Rabbit
Out of sight in burrow (PIS)
Cat Control Dog Rabbit
Walk - slow locomotion (PIS)
Cat Control Dog Rabbit
Run - fast locomotion (PIS)
Cat Control Dog Rabbit
Fully emerged (PIS)
Partially emerged (PIS)
Control Dog
Figure 2. The mean (±1 SEM) proportion of time in sight (PIS) that bilbies allocated to burrow emergence behaviours (a) out of sight in burrow, (b) walk, i.e. slow locomotion, (c)
run, i.e. fast locomotion, (d) partially emerged and (e) fully emerged. Similar letters above bars identify pairwise differences that are not statistically distinguishable (P>0.05).
L. A. Steindler et al. / Animal Behaviour 137 (2018) 133e139 137
Bilbies spent the greatest proportion of time partially emerged
and the least amount of time fully emerged from the burrow
when dog faeces were present. This nding may be due to bilbies
making a trade-off between costs and benets of staying within
or leaving their refuges. Predator evasion is often costly in terms
of time and energy. Thus, theory predicts that prey individuals
should not ee or seek shelter immediately when they detect a
predator, but instead should adjust their response according to
the level of threat perceived (Ydenberg &Dill, 1986). Many ani-
mals modify their refuge use and burrow emergence behaviour
according to the estimated levels of predation risk (Martín &
opez, 1999; Sih et al., 1988; Sparrow, Parsons, &Blumstein,
2016). However, animals require information to make such de-
cisions (Bouskila &Blumstein, 1992). As such, by allocating more
time to assessing the potential risks associated with the presence
of dog faeces, while in the safety of their burrow entrances, bilbies
may have reduced the potential for lethal encounters with a dog/
dingo outside their burrow.
Our certainty regarding lifetime predator experiences in this
study gave us unique insight into the inuence of selection pressure
in the retention and development of antipredator behaviours. We
know the evolutionary history of predator exposure of the bilby
population at Arid Recovery Reserve. We also know that these
bilbies have had no ontogenetic exposure to mammalian predators.
This is in contrast to most other studies of free-ranging wildlife in
which history of predator exposure is unknown. A study of wild
bush rats, Rattus fuscipes, a species suspected to coexist with free-
ranging dogs, showed they had no aversion to dog faecal odours;
however, it was acknowledged that the risk posed to rodents by
feral dogs in the study area was unknown (Banks, Nelika, Hughes, &
Rose, 2002).
There has been little research into when an introduced pred-
ator may be considered naturalized. Carthey and Banks (2012)
proposed that introduced predators should be considered native
predators when their prey species are no longer naïve towards
them. That bilbies with no lifetime exposure to mammalian
predators appear to possess an innate ability to discriminate and
respond to dog/dingo scent by being more reluctant to leave their
burrows thus supports the idea that dingoes should be regarded
as naturalized (Carthey &Banks, 2012; Frank, Carthey, &Banks,
2016). In contrast to their response to dog faeces, bilbies spent
more time fully emerged and less time partially emerged from
their burrows in the presence of cat faeces, rabbit faeces and the
unscented control. This nding implies that bilbies are naïve to-
wards cats and that less than 200 years of evolutionary exposure
to cats may not be long enough for bilbies to develop and retain
appropriate predator discrimination abilities (Frank et al., 2016).
Like the study by Frank et al. (2016), our study raises the question
of how long is long enough before a novel predator, such as a feral
cat, may be considered naturalized? In theory, this question could
be answered by evaluating the magnitude of native prey's re-
sponses to introduced predator cues at many different locations
and using time since predator arrival as a predictor variable.
Finally, our nding that bilbies have limited ability to discrimi-
nate cat scent is also of great applied interest as it better denes
the problem that reintroduction programmes of predator-naïve
populations face. That is, native Australian mammals in the crit-
ical weight range (Burbidge &McKenzie, 1989) facing entirely
novel predators may not be able to identify them as a threat.
Data are available from the Dryad Digital Repository: https://
We thank local pet owners and the Roxby Downs Vet
CliniceWhyalla Vet for the supply of odours and the Arid Recovery
staff and many volunteers for their assistance with the study. This
research was funded by the Australian Research Council (ARC-Link-
age Grant (no. LP130100173) to M.L., K.M. and D.T.B.) and Holsworth
Wildlife Research Endowment (RG152215) (to L.S and M.L).
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... In many species of mammals (Owings and Owings 1979;Fendt 2006), birds (Göth 2001) and fish (Berejikian et al. 2003), predator recognition is an innate trait. Despite years, decades or even thousands of years of isolation from predators, some prey species retain predator recognition skills of their ancestral predators (Blumstein et al. 2008;Li et al. 2011;Steindler et al. 2018). However, for many other prey species, learning and experience are necessary to properly develop and perform appropriate anti-predator behaviours (Griffin et al. 2000). ...
... In the last 150 years, bilbies have undergone a severe range decline which has been attributed in part to naiveté towards introduced predators, the red fox (Vulpes vulpes) and feral cat (Felis catus) (Burbidge and Woinarski 2016). A study of wild bilbies living within the 'Arid Recovery' predator-free fenced reserve in South Australia found that bilbies with no ontogenetic exposure to mammalian predators recognised the scent of a native predator, the dingo (Canis familiaris), which they have shared over 8000 years of co-evolutionary history (Zhang et al. 2020), but did not recognise the scent of a recently introduced predator, the feral cat (Steindler et al. 2018). The bilbies inhabiting the Arid Recovery safe-haven were considered to be wild, because they were not supplementary fed and were exposed to avian and reptilian predators (Steindler et al. 2018). ...
... A study of wild bilbies living within the 'Arid Recovery' predator-free fenced reserve in South Australia found that bilbies with no ontogenetic exposure to mammalian predators recognised the scent of a native predator, the dingo (Canis familiaris), which they have shared over 8000 years of co-evolutionary history (Zhang et al. 2020), but did not recognise the scent of a recently introduced predator, the feral cat (Steindler et al. 2018). The bilbies inhabiting the Arid Recovery safe-haven were considered to be wild, because they were not supplementary fed and were exposed to avian and reptilian predators (Steindler et al. 2018). These findings suggest that bilbies have innate recognition of dingoes, but not feral cats, and that a prey species' ability to respond to the odour of their predators scales with the duration of their evolutionary coexistence (Peckarsky and Penton 1988). ...
Full-text available
Inability to recognise and/or express effective anti-predator behaviour against novel predators as a result of ontogenetic and/or evolutionary isolation is known as ‘prey naiveté’. Natural selection favours prey species that are able to successfully detect, identify and appropriately respond to predators prior to their attack, increasing their probability of escape and/or avoidance of a predator. However, for many prey species, learning and experience are necessary to develop and perform appropriate anti-predator behaviours. Here, we investigate how a remnant population of bilbies (Macrotis lagotis) in south-west Queensland responded to the scents of two predators, native dingoes (Canis familiaris) and introduced feral cats (Felis catus); a procedural control (rabbits; Oryctolagus cuniculus); and an experimental control (no scent). Bilbies in Queensland have shared more than 8000 years of co-evolutionary history with dingoes and less than 140 years with feral cats and less than 130 years with rabbits. Bilbies spent the greatest proportion of time investigating and the least amount of time digging when cat and dingo/dog faeces were present. Our results show that wild-living bilbies displayed anti-predator responses towards the olfactory cues of both a long-term predator (dingoes) and an evolutionary novel predator (cats). Our findings suggest that native species can develop anti-predator responses towards introduced predators, providing support for the idea that predator naiveté can be overcome through learning and natural selection as a result of exposure to introduced predators. Significance statement Not so naïve—As a result of lifetime and/or evolutionary isolation from predators, some prey species appear to be naïve towards introduced predators. This is particularly the case in Australia, where native mammalian species appear to be naïve towards recently introduced predators such as the feral cat and European red fox. In a study of wild-living bilbies, we found that 150 years of co-evolutionary experience is enough to develop predator recognition.
... However, this usually occurred after several months of attachment. With the success of the attachment technique, training was provided to other researchers involved in the reintroduction of the species at Arid Recovery (Moseby and O'Donnell 2003), and it has since been used and adapted for several studies of bilbies at Arid Recovery (Moseby et al. 2012;Steindler et al. 2018;Ross et al. 2019a) and at Scotia Sanctuary (Finlayson et al. 2008), and adapted for multiple studies on Peramelidae spp (e.g. Groenewegen et al. 2017;Robinson et al. 2018;Maclagan et al. 2020). ...
... For trap-shy animals, and species prone to capture myopathy, a low number of recaptures and ABD reattachments is preferred, and may be ethically preferable (Kenward 2001;Hawkins 2004;Matthews et al. 2013;Latham et al. 2015). Tail-mount attachments to bilbies are known to last for up to 2-3 months or longer in the field, and individuals have had successive transmitters attached for over a year (Moseby and O'Donnell 2003;Moseby et al. 2012;Steindler et al. 2018). The longevity of attachments, however, can be affected by extrinsic (e.g. ...
... Tail-mount attachment of ABDs to bilbies lasted over 3 months in the field, with reattachments possible over a semicontinuous period of ~25 months. This supports findings by Moseby et al. (2012) and Steindler et al. (2018), with attachments lasting 2-3 months or more, and by Moseby and O'Donnell (2003), with reattachments possible for extended periods of time of over 12 months without injury. This is much longer -and less variable -than what is possible by gluing ABDs directly to the skin (Kenward 2001; Coetsee et al. 2016). ...
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Context. Continued miniaturisation of tracking technology increases its utility in animal applications. However, species morphology often dictates the type of animal-borne device (ABD) that can be used, and how it is attached. The morphology of species within Peramelemorphia preclude them from the standard collar attachment of ABDs for terrestrial mammals. Aims. This paper describes a method for the tail-mount attachment of ABDs, and deployment results for Peramelemorphia across arid, semi-arid and temperate Australia to (a) test the performance of attachments and ABDs in the field and (b) discuss the animal welfare considerations for this attachment method. Methods. Tail-mount attachment of ABDs were field-tested on a total of 80 greater bilbies (Macrotis lagotis), and 14 long-nosed bandicoots (Perameles nasuta). Key results. Time to natural detachment (TTND) was between 2 and 52 days, with 65.74% (142 of 216) remaining on until manual removal. For ABDs that were manually removed, attachments were retained for up to 94 days. The method used for tail-mount attachment of ABDs to long-nosed bandicoots resulted in significantly shorter TTND compared with the method used for bilbies, and environmental factors (high temperatures and rainfall) had a negative effect on TTND. Tail-mount attached global positioning system (GPS) sensors collected large quantities of accurate data, with a maximum fix success rate of 83.38%. Damage to GPS (antenna breakage and water ingress) during deployment, however, impacted performance. In environments with frequent rainfall and waterlogged soils, the tape on a small proportion (6.25%) of (n = 192) attachments to bilbies caused tail injury. All injuries were resolvable, with most requiring minimal to no veterinary intervention. Key conclusions. Attachment longevity can be affected by how the ABD is mounted to the tail, the species and the deployment environment. The environment can also affect which adhesive tapes are suitable for ABD attachment. However, this method is highly modifiable, practical for field application and can have long retention times relative to other temporary methods. Implications. This ABD tail-mount attachment method adds another tool to the telemetry tool-kit, with all the benefits of a low-tech, low-cost, passive drop-off type attachment. This method has demonstrated practicality for Peramelemorphia, with potential application to other suitable small vertebrates.
... Bilbies have been recorded frequently moving burrows, modifying their burrow emergence behaviour and seeking the shelter of shrubs more often in response to predator exposure (Moseby et al. 2012;Steindler et al. 2018;Ross et al. 2019). Early observations of bilbies in South Australia suggest they rapidly retreated to their burrows to avoid predation (Wood Jones 1924). ...
... Possible reasons for facing burrow entrances in a certain direction could be to take advantage of the natural wind patterns or sunlight to maximise microclimatic benefits in burrows, or possibly to maximise scent detection of predators when bilbies emerge from burrows. Bilbies have been found to alter their burrow emergence behaviour in response to predator odour near the entrance of burrows (Steindler et al. 2018), therefore scent detection of predators is likely an important predator avoidance strategy. An area of interesting future research could be to determine the effect of wind direction and burrow orientation on both burrow microclimatic conditions and scent detection in bilbies emerging from burrows. ...
Remnant natural populations of greater bilbies (Macrotis lagotis) are confined to the Australian arid zone where bilbies construct and shelter in multiple burrows within their home range. We investigated burrow use behaviour of bilbies in a translocated population in temperate southern Australia to determine if behaviour differed in this climatic zone. Over a 12 month period, 43 adult bilbies at Venus Bay Conservation Park were spool-and-line tracked to 118 burrows. Active burrow density was 0.55 per ha, and bilbies at the site used multiple burrows (up to 13 for males and 8 for females) and regularly moved between diurnal burrows. Male bilbies had significantly larger burrow ranges (10.2 � 5.8 ha, MCP100, mean � s.d.) than females (2.6 � 1.8 ha), and were similar in size to those recorded in an arid zone population. Males’ burrow ranges tended to overlap with the burrow range of multiple other males and females. The density of burrows in the current study suggests that bilby burrows were likely to have been a common landscape feature within the southern parts of the species range prior to their local extinction. Further research is needed to determine the impact of the loss of bilby burrows from southern Australia on other burrow commensal species.
... LTKs have had at least 3000 years of co-occurrence with dingoes (Smith and Savolainen 2015) whose odours have been shown to trigger fear responses in marsupials (Parsons et al. 2007;Parsons and Blumstein 2010;Sparrow et al. 2016;Steindler et al. 2018). Due to phylogenetic relationships between dingoes and dogs (Elledge et al. 2006;Carthey and Banks 2012), it seems reasonable to expect that LTKs would also recognise faecal odours from feral dogs as a threat. ...
... Significant changes in the duration of 'comfort' and 'vigilance' and in the frequency of 'vigilance' behaviours when odours from the Tasmanian devil were presented may be attributable to co-evolutionary links between tree-kangaroos and the ancestors of the Tasmanian devil. It has been shown that predator recognition by prey species is shaped by evolutionary experiences of prey with its native predators and their various cues (Atkins et al. 2016;Carthey and Banks 2016;Carthey et al. 2017;Steindler et al. 2018), and can persist despite the loss of the predator as long as predator pressure is present (Blumstein 2006). At this stage it can only be speculated that changes in our subjects' 'comfort' and 'vigilance' behaviours in response to odours from Tasmanian devils could be an expression of the 'ghost of predation past' (Calder and Gorman 1991). ...
... The responses of native animals to the odours of introduced animals have been well studied in predator-prey contexts, particularly for vertebrates (Anton et al. 2020;Steindler et al 2018;Webster et al. 2018). For example, the failure of prey to detect or avoid the odour cues of novel mammalian predators is thought to be a key driver of native species population decline (Spencer 2002;Anton et al 2020). ...
Full-text available
Many animals deposit odours in their environment, either intentionally or unintentionally, that remain at a site after the animal itself has left. These odours may be exploited by other species as social information, and thus have a significant role in structuring species interactions, even where the species involved rarely interact directly. Here we show that three species of Australian social stingless bees (Meliponini) not only detect the odours left behind by conspecifics, but also those of an abundant introduced competitor, the honey bee Apis mellifera (Apini). Foraging bees deposit pheromones that assist nestmates in locating profitable food sources (signals) and/or involuntary olfactory “footprints” (cues), both of which are vulnerable to exploitation by the foragers of other colonies. Using choice trials, we find that foragers of Tetragonula carbonaria, Tetragonula clypearis and Austroplebeia australis were more attracted to feeders recently used by, and thus carrying the odours of, their own species (both nestmates and non-nestmates) or honey bees, than to clean unused feeders. Australia’s stingless bees may learn to associate honey bee odours with food and exploit this to their advantage, or they may mistake honey bee odours for some other attractant and be misdirected. Our results suggest that introduced social insects could have a previously overlooked impact on resident communities, by modifying the olfactory landscape of shared resources in ways that alter native species’ foraging behaviour.
... Animal management can have unintended evolutionary consequences (Shefferson et al. 2018). Refuge naïveté is one of them, and there has been important recent work exploring the challenges and solutions that prey naïveté poses for reintroductions (Moseby et al. 2016Jolly et al. 2018;Steindler et al. 2018;West et al. 2018). ...
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A large component of the anthropogenic biodiversity crisis is the loss of animal species. In response, there has been significant investment in reintroductions of species to their historical ranges. Predation by native and exotic predators, however, remains a barrier to success. Over the past 200 years, Australia has seen the highest rate of mammal extinction on earth, with mammals within a critical weight range (CWR: 35 g–5.5 kg) most affected due to predation by exotic predators. Populations of some threatened species now exist only in Tasmania, offshore islands, or predator-proof sanctuaries. The next critical step is to return native populations outside of predator-free areas, ‘beyond-the-fence’, on the continental mainland. Given our current inability to completely remove exotic predators from mainland ecosystems, how can we achieve successful mammal reintroductions? A potential solution is to drive adaptation of reintroduced animals towards predator-resistance by exposing them to low levels of predation. We propose the concept of a ‘Goldilocks Zone’—the ‘just right’ levels of predation needed to drive selection for predator-resistant native species, while ensuring population viability. We experimentally reintroduced a mammal, the eastern bettong (Bettongia gaimardi), to mainland Australia, 100 years after its local extinction. Using an intense baiting regime, we reduced the population density of the red fox (Vulpes vulpes), the main factor behind the eastern bettong’s extirpation from the continent. Reducing bait take to 15% of previous levels allowed differential survival among bettongs; some surviving under 100 days and others over 450 (~ 4 times longer than some similar trials with related species). Surviving individuals were generally larger at release than those that died earlier, implying selection for larger bettongs. Our results suggest that reducing predation could establish a Goldilocks Zone that could drive selection for bettongs with predator-resistant traits. Our work contributes to a growing body of literature that explores a shift towards harnessing evolutionary principles to combat the challenges posed by animal management and conservation.
... A standard test for neophobia is to introduce novel objects to a famil- Wariness behavior is a response to a potentially threatening stimulus, such as predator odors, particularly those of predators with a long history of coevolution (Steindler et al., 2018;Valcarcel & Fernández-Juricic, 2009). We used garden twine soaked in commercially available wolf urine (Wolf Urine Lure 32 oz., DeerBusters) because it was commercially available and wolves have a long history of coevolution with foxes (Wikenros et al., 2017). ...
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Human–wildlife interactions are believed to be increasing in urban areas. In Britain, numerous media reports have stated that urban foxes (Vulpes vulpes) are becoming “bolder,” thereby posing a risk to public safety. However, such claims overlook how an individual's personality might influence urban fox behavior. Personality determines multiple aspects of an animal's interactions with both conspecifics and its environment, and can have a significant impact on how people perceive wildlife. Furthermore, describing urban foxes as “bold” confounds two different but inter‐related behaviors, both of which influence an animal's propensity to take risks. Neophobia affects an animal's reaction to novelty, wariness its reaction to potential threats. Since urban wildlife frequently encounters both novel and threatening stimuli, a highly adaptable species such as the red fox might be predicted to exhibit reduced neophobia and wariness. We investigated how social status influenced both behaviors in Bristol's fox population. Dominant foxes were significantly more neophobic and warier than subordinates, which adopt a more exploratory and risk‐taking lifestyle to meet their energetic and other needs. We found no seasonal effect on neophobia and wariness, although this may be due to sample size. The presence of conspecifics decreased neophobia for dominants, and wariness for both dominants and subordinates. We highlight the importance of considering animal social status and personality when planning management protocols, since interventions that destabilize fox social groups are likely to increase the number of subordinate foxes in the population, thereby increasing rather than decreasing the number of interactions between humans and urban foxes.
... Although dogs have been living with native species long enough that some have evolved an innate antipredator response (Steindler et al. 2018), introduced predators and increased food and breeding opportunities due to modified land management practices may be affecting the way dogs now interact with their environment. In an Australia-wide study of dog diets, Doherty et al. (2019) found that rabbits (Oryctolagus cuniculus), reptiles and arthropods were encountered more frequently in the arid and semiarid zones compared with other areas. ...
The ecological role of canids in arid Australia is unresolved. Some argue they play a role regulating populations of herbivores and introduced mesopredators such as feral cats (Felis catus) and foxes (Vulpes vulpes). However, evidence also suggests they pose a threat to native species populations. The aims of this study were to determine the extent of canid predation on the bilby population at Astrebla Downs National Park, Queensland, to improve our understanding of the ecological role that canids serve in the park and to determine whether seasonal changes in the canid diet can be used to predict if and when management should intervene. Canid scats (n=723) were collected over seven years and their content examined. The percentage of bilby remains in the canid scats varied from 13 to 85% (mean=43%) and was 20–100% by volume. In total, 23 vertebrate species were identified in canid scats. The percentage of cat remains was 0–44% (mean=11%), peaking in 2013 during a cat plague and coinciding with canids actively hunting cats. Fox remains were not detected in dog scats. These results indicate that canids had a varied diet and at times threatened the bilby population at Astrebla.
... Camera traps can be a powerful tool for many ecological questions, like occupancy, species distribution and many other aspects (Rovero and Zimmermann, 2016), but they have been rarely used in behavioural biology, e.g. to measure behavioral responses. Saxon- Mills et al. (2018) and Steindler et al. (2018) used similar camera traps in their behavioral analysis of two different burrowing, nocturnal and largely solitary marsupials. In such cases, the presence of an observer may disturb and influence the behavior of the animals. ...
Animals trade-off predation risk against feeding opportunities and prey species may use signals or cues of predators to assess predation risk. We analyzed the mesopredators pine and stone marten (Martes martes, M. foina) and nocturnal and diurnal rodents (Glis glis, Apodemus spp., Sciurus vulgaris). The non-experimental approach used camera traps at feeders which were visited by both, predator and prey. As prey species can eavesdrop on predator signals/cues, there should show some avoidance behavior. The study was conducted on a small mountain in Germany, largely covered by wood, between 29.6.2018 and 5.10.2018. Camera traps were placed 0.6 m near a feeder. Food was replenished regularly to provide a continuous food supply. 34 camera traps provided data for an analysis; total trap nights were 513 (12,312 h). Martens detected the food sources first in 10 instances, and prey species Apodemus/G. glis in 24 instances. G. glis seemed to generally avoid places where martens were feeding while Apodemus and Sciurus did not. The visitations of G. glis depended on whether martens were the first visitors and it significantly avoided such places. Similarly, Apodemus appeared less often at a feeder when martens have been present as a first visitor. The time interval to resume feeding to a monitored feeder after a marten visit was significantly longer compared to a control in G. glis, but not in Apodemus and S. vulgaris. The study shows different responses, with the weakest in the diurnal rodent, and the highest in G. glis. Thus, if a food resource was known by prey species before a predator occurred, the trade-off was shifted towards feeding, but when the predators detect the food source first, the trade-off was shifted to predator avoidance.
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Conservation translocations, which involve the intentional movement and release of organisms for conservation benefit, are increasingly required to recover species of conservation concern. In order to maximize post-release survival, and to accomplish conservation translocation objectives, animals must exhibit behaviors that facilitate survival in the wild. The Vancouver Island marmot (Marmota vancouverensis) is a critically endangered endemic in Canada which has been captive-bred for 24 years for reintroductions and reinforcements that have increased the wild population from ~30 to more than 200 individuals. Despite this success many marmots are killed by predators after release and predation represents a major hurdle to full marmot recovery. To better understand if captive-bred marmots are prepared for the novel environment into which they will be released, and to determine whether such suitability changes over time, we presented taxidermy mounts of mammalian predators and non-predators to marmots that were wild-caught, and captive born for between one and five generations. We also examined mortality of offspring from marmots we tested that had been released to the wild. A minimum of 43% of offspring were killed by predators in the wild over 17 years, most by cougars. Marmots in captivity generally responded to taxidermy mounts by decreasing foraging and increasing vigilance, and overall responded more strongly to predators than non-predators, especially wolves. However, marmots in captivity for more than two generations lacked discrimination between cougars, non-predators, and controls, suggesting a rapid loss of predator recognition. This study was only possible because predator-recognition trials were initiated early in the conservation translocation program, and could then be repeated after a number of generations. The finding that changes occurred relatively rapidly (within five generations during which changes in genetic diversity were negligible) suggests that behavioral suitability may deteriorate more rapidly than genetics would suggest. Strategies addressing potential behavior loss should be considered, including sourcing additional wild individuals or pre-release training of captive-born individuals. Subsequently, post-release survival should be monitored to determine the efficacy of behavior-optimization strategies.
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Incorporating an understanding of animal behaviour into conservation programmes can influence conservation outcomes. Exotic predators can have devastating impacts on native prey species and thwart reintroduction efforts, in part due to prey naïveté caused by an absence of co-evolution between predators and prey. Attempts have been made to improve the anti-predator behaviours of reintroduced native prey by conducting laboratory-based predator recognition training but results have been varied and have rarely led to improved survival in reintroduction programmes. We investigated whether in situ predator exposure could improve anti-predator responses of a predator-naïve mammal by exposing prey populations to low densities of introduced predators under controlled conditions. We reintroduced 352 burrowing bettongs to a 26-km² fenced exclosure at the Arid Recovery Reserve in South Australia and exposed them to feral cats (density 0.03-0.15 cats/km²) over an 18-month period. At the same time, we translocated a different group of bettongs into an exclosure free of introduced predators, as a control. We compared three behaviours (flight initiation distances, trap docility and behaviour at feeding trays) of cat-exposed and control bettongs before the translocations, then at 6, 12 and 18 months post-translocation. Cat-exposed bettongs displayed changes in behaviour that suggested increased wariness, relative to control bettongs. At 18 months post-reintroduction, cat-exposed bettongs had greater flight initiation distances and approached feed trays more slowly than control bettongs. Cat-exposed bettongs also increased their trap docility over time. Synthesis and applications. Translocation is recommended as a conservation tool for many threatened species yet success rates are generally low. We demonstrate that controlled levels of in situ predator exposure can increase wariness in the behaviour of naïve prey. Our findings provide support for the hypothesis that in situ predator exposure could be used as a method to improve the anti-predator responses of predator-naïve threatened species populations.
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Fear of predation is a universal motivator. Because predators hunt using stealth and surprise, there is a widespread ability among prey to assess risk from chemical information - scents - in their environment. Consequently, scents often act as particularly strong modulators of memory and emotions. Recent advances in ecological research and analytical technology are leading to novel ways to use this chemical information to create effective attractants, repellents and anti-anxiolytic compounds for wildlife managers, conservation biologists and health practitioners. However, there is extensive variation in the design, results, and interpretation of studies of olfactory-based risk discrimination. To understand the highly variable literature in this area, we adopt a multi-disciplinary approach and synthesize the latest findings from neurobiology, chemical ecology, and ethology to propose a contemporary framework that accounts for such disparate factors as the time-limited stability of chemicals, highly canalized mechanisms that influence prey responses, and the context within which these scents are detected (e.g. availability of alternative resources, perceived shelter, and ambient physical parameters). This framework helps to account for the wide range of reported responses by prey to predator scents, and explains, paradoxically, how the same individual predator scent can be interpreted as either safe or dangerous to a prey animal depending on how, when and where the cue was deposited. We provide a hypothetical example to illustrate the most common factors that influence how a predator scent (from dingoes, Canis dingo) may both attract and repel the same target organism (kangaroos, Macropus spp.). This framework identifies the catalysts that enable dynamic scents, odours or odorants to be used as attractants as well as deterrents. Because effective scent tools often relate to traumatic memories (fear and/or anxiety) that cause future avoidance, this information may also guide the development of appeasement, enrichment and anti-anxiolytic compounds, and help explain the observed variation in post-traumatic-related behaviours (including post-traumatic stress disorder, PTSD) among diverse terrestrial taxa, including humans.
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Alien predators have devastating impacts on native prey in invaded ecosystems worldwide, a fact commonly attributed to ecological naiveté or the failure of native prey to defend themselves against a novel predator due to a lack of experience. Despite this, few studies have convincingly demonstrated naiveté in native prey. Ecological naiveté is of particular relevance in Australia, where eighteen endemic mammal species have gone extinct, and many more are in decline, since the introduction of alien placental dogs (Canis lupus dingo and Canis lupus familiaris), red foxes (Vulpes vulpes) and feral cats (Felis catus). The role of naiveté in the vulnerability of Australia’s native mammal species remains unresolved. More generally, the naiveté of native species towards novel enemies in all types of antagonistic interactions is an important predictor of the outcomes of future introductions and conservation efforts in invaded ecosystems. In this thesis, I used theoretical, experimental and chemical approaches to investigate ecological naiveté in Australian predator-prey interactions and its implications for the persistence of native prey. I reviewed classic predator-prey theory to show how alien species disrupt predator-prey interactions at every stage of the predation sequence, from detection, to capture, and escape or consumption. Rather than adopting the longheld view of naiveté as an all-or-nothing status, I expand upon and argue the recent theory that naiveté is best viewed as a process through which native prey can progress towards predator wariness. Using a broad-scale survey approach, I demonstrated that native vulnerable marsupial bandicoots recognise and avoid pet dogs, but not cats, when choosing where to forage. I attributed this finding to the approximately 4000 years’ experience that bandicoots have with dingoes, which are very closely related to dogs. I extended this line of reasoning to argue that naiveté of local native prey provides an objective criterion for determining the native status of an introduced predator with a long history in a particular ecosystem. I developed a two-pronged experimental approach to test for naiveté in small to medium size free-living mammals, by combining giving-up density (GUD) methodology with remote-sensing night vision cameras to enable direct observation of behavioural changes in response to predator odours. Despite the prevalent use of scats or urine to represent risk in previous studies of olfactory predator recognition, here I used ‘whole animal’ body odour because it represents imminent danger through proximity or likely revisitation of the predator at a den site or resting place. GUDs revealed that native bush rats (Rattus fuscipes) recognise and respond strongly to dog odour, while subtle changes in vigilance behaviour detected by the analysis of camera footage showed that they also increased vigilance in the presence of cat, fox and native quoll (Dasyurus maculatus) odour. In contrast, the same experimental methodology showed that alien black rats (Rattus rattus) increased investigation of alien predator odours over controls or native quoll odour, but did not respond with increased GUDs or vigilance. This highly successful invasive species may exhibit a behavioural invasion syndrome that makes it bolder to forage under predation risk and potentially more aggressive. Native bush rats left low GUDs in the presence of cat odour, and since rats are an intermediate host of the parasite Toxoplasma gondii that has been shown to reduce riskaversion and increase attraction to cat odours in rats (increasing their vulnerability to cat predation so that T. gondii can return to its definitive host) I tested for the presence of T. gondii in the population. Seroprevalence of immune response to T. gondii was found to be relatively low (at 4.10 %), but the role of parasites and pathogens in increasing vulnerability of native species to alien predators deserves further research attention. This is because they may effectively ‘override’ the native species’ preadaptations or any progress made due to learning or adaptation. Using solid phase micro-extraction and gas chromatography-mass spectrometry (SPME GC-MS), I then showed significant differences in the chemical composition of scats, urine and body odours from marsupial and placental predators. The odours of individual predator species also differed from one another with the following exceptions: the compositions of placental body odours overlapped, and the scats, urine and body odours of dingoes and dogs were chemically indistinguishable. If differentiation of social cues has been a major cause of vertebrate evolutionary divergence, the importance of olfaction in social communication between mammals predicts that this difference between species and higher taxonomic groups should occur. The chemical similarity of dog and dingo odour confirms that these two closely related predators probably smell very similar when encountered by native prey, and supports my conclusion that native prey species recognise and respond to dogs due to their considerable experience with dingoes. In Australia, where native mammalian predators are almost exclusively marsupial and alien predators eutherian, differences in odour cues of these two taxonomic groups may have resulted in native prey failing to recognise foxes and cats when they first arrived. This probably played a very important role in Australia’s recent mammal extinctions. Nevertheless, it is clear from this research that native species that survive today, including bush rats and bandicoots, are currently not entirely naïve towards introduced predators. Whether this is due to preadaptations or experience, it has positive implications for their continued persistence.
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Introduced predators have a global reputation for causing declines and extinctions of native species. Native prey naiveté towards novel predators is thought to be a key reason for predator impacts. However, naiveté is not necessarily forever: where coexistence establishes, it is likely that naiveté will be reduced through adaptation, and the once alien predator will eventually become recognised by prey. For example, native marsupial bandicoots in Sydney avoid backyards with domestic dogs (C. lupus familiaris), but not domestic cats (Felis catus), even though cats and dogs were both introduced about 200 years ago (Carthey and Banks 2012). The authors attributed bandicoots' recognition of dogs to long-term exposure to a close relative of dogs, dingoes that arrived in Australia 4000 years ago. Here, we test a prediction of this hypothesis by taking the study to Tasmania, where dingoes have never been present but where domestic dogs also arrived about 200 years ago. We use a similar survey design to that of Carthey and Banks (2012): asking Hobart residents to report on pet-ownership, bandicoot sightings and scats within their backyards, as well as an array of yard characteristic control variables. We predicted that if long term experience with dingoes enabled mainland bandicoots to recognise domestic dogs, then Tasmanian bandicoots, which are inexperienced with dingoes, would not recognise domestic dogs. Our results indicate that Tasmanian bandicoots are naïve to both dogs and cats after only 200 years of coexistence, supporting our hypothesis and the notion that naiveté in native prey towards alien predators (as observed on the mainland) may eventually be overcome.
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Southern hairy-nosed wombats (Lasiorhinus latifrons) are fossorial marsupials that live in large burrow systems where their digging behaviour brings them into conflict with agriculture. In the absence of any available control options, non-selective culling is the primary mode of wombat management. This approach is contentious and has unknown implications for long-term wombat conservation. Predator scents, however, have been effective in altering behaviours of some herbivores and may offer a non-lethal alternative to culling if they discourage wombats from burrowing in perceived problem areas. Therefore, we trialled two dingo scents (faeces, urine) over 75 days to determine whether these scents would deter wombats from repopulating collapsed burrows. Ten inhabited single-entrance burrows were excavated over three days (to allow time for inhabitants to exit), collapsed and then filled in. Five burrows, separated by at least 200 m, were used for dingo scent treatments (three urine; two faeces) and three burrows, separated by the same distance, served as negative controls (unscented), along with two ‘farmer-monitored’ active controls (dog urine and a dingo carcass). We used a rank-sum score to assess wombat activity: scratching was scored with a value of (1), digging (2), and recolonisation (5), with each value reflecting total energy and time spent in the vicinity of the treatment. We fitted Generalised Estimating Equations (repeated-measures, Fisher Method) to explain variation within, and across, treatment and control burrows. Within 20 days, all 10 sites had signs of wombat activity that ranged from fresh digging, to fully functional burrows. Among the five treatment sites, scratching and tracks identified wombats as being present, but they did not dig. After 75 days, the five sites treated with dingo scents had minimal activity and no new burrows, while wombats recolonised all control burrows. Though we used only 10 burrows for this preliminary study, our findings suggest the need for further testing of dingo scents as a tool for dissuading wombats from digging and recolonisation of collapsed burrows. This represents a novel use for a predator scent, in that prey may remain in the vicinity near the deterrent, but curb problematic behaviours of economic consequence.
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Prey may have ontogenetic experience, evolutionary experience, or both types of experiences with their predators and how such experiences influences their ability to identify their predators is of great theoretical and applied interest. We capitalized on predator-free exclosures containing populations of native burrowing bettongs (Bettongia lesueur) and introduced rabbits (Oryctolagus cuniculus) that ensured we had knowledge of our subjects’ ontogenetic experiences with predators and asked whether evolutionary experience influenced their visual predator discrimination abilities. Rabbits evolved with red foxes (Vulpes vulpes) and wolves (Canis lupus) but had less than 200 years of prior exposure to dingoes. The rabbit population we studied had been exposed to dingoes (Canis dingo) and foxes 8 months prior to our study and had heightened responses to red fox models, but not dingo/dog (Canis dingo/Canis familiaris) models. The insular burrowing bettong population had no ontogenetic exposure to mammalian predators, brief evolutionary exposure to domestic dogs and possibly dingoes, and a deeper evolutionary history of exposure to thylacines (Thylacinus cynocephalus)—another large mammalian predator with convergent body morphology to dingoes/dogs but no evolutionary or ontogenetic exposure to foxes. Bettongs showed a modest response to the dingo/dog model and no response to the fox model. These results are consistent with the hypothesis that deep evolutionary history plays an essential role in predator discrimination and provides support for the multipredator hypothesis that predicts the presence of any predators can maintain antipredator behavior for other absent predators. Significance statement Prey may have ontogenetic experience and or evolutionary experience with their predators. How such experiences influence prey species’ ability to identify their predators is of significance to theory on the evolution of antipredator response and to improve the success of translocations and reintroductions for conservation purposes which often fail because of predation on predator naïve prey. Here, we show that prey recognition for two prey species with limited or no ontogenetic exposure to predators, rabbits, and burrowing bettongs was greatest toward the predator to which they had the longest period of coevolution. The results are consistent with the hypothesis that evolutionary history plays an essential role in predator discrimination and provides support for the multipredator hypothesis that predicts the presence of any predators can maintain antipredator behavior for other absent predators.
Greater bilby was once widely distributed throughout arid and semiarid Australia. It has suffered a rapid decline since European settlement and is now restricted to parts of the Tanami, Great Sandy and Gibson Deserts with outlying populations in SW Queensland and N of Alice Springs, Northern Territory. Its distribution is examined in relation to historic and scientific records, climatic and soil features, land use and the distribution of rabbits Oryctolagus cuniculus and foxes Vulpes vulpes. -from Author