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Individual traits influence survival of a reintroduced marsupial only at low predator densities

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Predation is a key factor contributing to the failure of reintroductions of vertebrates but there is variation in predation risk between individuals. Understanding the traits that render some animals less susceptible to predation, and selecting for these traits, may help improve reintroduction success. Here, we test whether prior exposure to predators or specific morphological and/or behavioural attributes explained variation in post‐reintroduction survival in a moderate and low predator density environment. We exposed a population of the threatened burrowing bettong (Bettongia lesueur) to controlled densities of feral cats (Felis catus) for ≥3 years. We then conducted two translocations of cat‐exposed and control populations that had no exposure to predators to a new site where cats were present at moderate, then low density. Variation in survival of burrowing bettongs was not explained by prior predator exposure to predators or measured individual traits at moderate cat density. At lower cat densities, males died sooner and burrowing bettongs with larger hind feet survived longer. Although prior cat‐exposure did not confer a survival advantage at low cat densities, the cat‐exposed burrowing bettong population had larger hind feet (n = 44) compared to the control population (n = 45) suggesting that trait divergence between cat‐exposed and non‐cat‐exposed burrowing bettongs may not yet be sufficient for improved survival. Alternatively, prior predator exposure may not confer a survival advantage because they are “outgunned” by evolutionarily novel cats. Predation is a major problem thwarting successful reintroductions world‐wide. Exposing populations to predators over longer time periods and periodically testing survival will be required to determine whether pre‐release predator exposure prepares animals for life with novel predators. Our study highlights the importance of reducing predator activity at release sites prior to reintroduction to enable any benefits from intraspecific variation in survival traits to be realised. We tested whether prior exposure to predators or specific morphological attributes explained variation in post‐reintroduction survival of burrowing bettongs in a moderate and low predator density environment. Variation in survival was not explained by prior exposure to predators or measured individual traits at moderate cat density, but at lower cat densities males died sooner and burrowing bettongs with larger hind feet survived longer. Predation is a major problem thwarting successful reintroductions world‐wide, and exposing populations to predators over longer time periods and periodically testing survival is required to determine whether pre‐release predator exposure prepares animals for life with novel predators.
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Individual traits influence survival of a reintroduced
marsupial only at low predator densities
H. L. Bannister
1,2
, M. Letnic
1
, D. T. Blumstein
3
& K. E. Moseby
1,4
1 Centre for Ecosystem Science, The University of New South Wales, Sydney, NSW, Australia
2 South Coast Natural Resource Management Inc., Albany, WA, Australia
3 Department of Ecology and Evolutionary Biology, The University of California, Los Angeles, CA, USA
4 Arid Recovery, SA, Australia
Keywords
marsupial; predation; prey naivety;
reintroductions; threatened species;
translocations; post-release survival;
burrowing bettong.
Correspondence
Hannah L. Bannister, 28 Gerdes Way,
Mckail, WA 6330, Australia.
Email: hannah_bannister@outlook.com
Editor: John Ewen
Associate Editor: Elissa Cameron
Received 26 June 2020; accepted 05 March
2021
doi:10.1111/acv.12690
Abstract
Predation is a key factor contributing to the failure of reintroductions of vertebrates
but there is variation in predation risk between individuals. Understanding the traits
that render some animals less susceptible to predation, and selecting for these
traits, may help improve reintroduction success. Here, we test whether prior expo-
sure to predators or specic morphological and/or behavioural attributes explained
variation in post-reintroduction survival in a moderate and low predator density
environment. We exposed a population of the threatened burrowing bettong (Bet-
tongia lesueur) to controlled densities of feral cats (Felis catus) for 3 years. We
then conducted two translocations of cat-exposed and control populations that had
no exposure to predators to a new site where cats were present at moderate, then
low density. Variation in survival of burrowing bettongs was not explained by
prior predator exposure to predators or measured individual traits at moderate cat
density. At lower cat densities, males died sooner and burrowing bettongs with lar-
ger hind feet survived longer. Although prior cat-exposure did not confer a survival
advantage at low cat densities, the cat-exposed burrowing bettong population had
larger hind feet (n=44) compared to the control population (n=45) suggesting
that trait divergence between cat-exposed and non-cat-exposed burrowing bettongs
may not yet be sufcient for improved survival. Alternatively, prior predator expo-
sure may not confer a survival advantage because they are outgunnedby evolu-
tionarily novel cats. Predation is a major problem thwarting successful
reintroductions world-wide. Exposing populations to predators over longer time
periods and periodically testing survival will be required to determine whether pre-
release predator exposure prepares animals for life with novel predators. Our study
highlights the importance of reducing predator activity at release sites prior to rein-
troduction to enable any benets from intraspecic variation in survival traits to be
realised.
Introduction
Many conservation translocations and reintroductions fail
(Short 2009; Wolf et al. 1996) and it is essential to under-
stand why. Intraspecic variation in survival after reintroduc-
tion has been attributed to a variety of factors including
body mass (Hamilton et al. 2010), boldness (Bremner-Har-
rison et al. 2004), prior exposure to predators (Ross et al.
2019) and social groupings (Shier 2006). In many cases,
predation is the primary reason for reintroduction failure.
Controlling or excluding introduced predators is usually a
pre-requisite for reintroduction success where introduced
predators are present (Fischer and Lindenmayer 2000;
Moseby et al. 2011; Short 2009). This is particularly evident
in Australia, where even native predators are susceptible to
predation by introduced predators (Moseby et al. 2015;
Radford et al. 2018). Introduced predators are thought to
have a greater impact on native species than native predators
because of the absence of a shared evolutionary history (Saul
and Jeschke 2015). Traits that improve an individuals ability
to avoid or deter predators in the initial post-release period
may therefore lead to increased survival. Studies have shown
that predation risk can vary between individuals of the same
species based on body mass (MacLeod et al. 2006), age
(Wright et al. 2006), personality (Bremner-Harrison et al.
2004) and sex (Fitzgibbon 1990). Prey facing novel preda-
tors typically have low post-release survival (Moseby et al.
2011; Short 2009), most likely due to prey naivety caused
by evolutionary or ontogenetic isolation from predators
(Banks and Dickman 2007; Carthey and Blumstein 2018).
With introduced predators unlikely to be eradicated from
Australia in the foreseeable future, developing strategies to
Animal Conservation  (2021)  ª2021 The Zoological Society of London 1
Animal Conservation. Print ISSN 1367-9430
permit native species to co-exist with them will lead to
improved reintroduction outcomes. One potential way to
improve reintroduced animalsprospects of survival post-
release in areas where introduced predators remain present
(but subject to control) is to provide them with anti-predator
training prior to release. Such pre-release training generally
occurs in captivity and typically involves exposure to preda-
tors or their cues coupled with an unpleasant experience
(Grifn et al. 2000; van Heezik et al. 1999; McLean et al.
1996). Whilst some studies have reported shifts in the beha-
viour of individuals subject to anti-predator training (H
olzer
et al., 1995; Miller et al. 1990), in many cases post-release
survival was not measured or improved (McLean et al.
2000; Moseby et al. 2012). This could be because the train-
ing used simulations or indirect cues, which may not induce
learning of behavioural traits required to avoid or escape real
predators, or because post-release survival of captive-reared
animals is generally lower than for wild-to-wild transloca-
tions (Grifth et al. 1989).
An alternative way to provide animals with anti-predator
training prior to reintroduction is in situ predator exposure,
whereby populations of na
ıve prey are exposed to novel preda-
tors under real-life conditions prior to reintroduction (Moseby
et al. 2016). The rationale behind this approach is that encoun-
ters with predators will prompt learning and selection for traits
that enhance individualscapacity to avoid fatal encounters
with predators (Moseby et al. 2016). In situ predator exposure
has been trialled at the Arid Recovery Reserve in South Aus-
tralia (Blumstein et al. 2019; Moseby et al. 2018; West et al.
2018b). Populations of endangered marsupials (greater bilbies
Macrotis lagotis, and burrowing bettongsBettongia
lesueur) have been established in a large (26 km
2
) paddock
with feral cats (Felis catus). In support of the in situ predation
concept, a release of cat-exposed and cat-na
ıve bilbies found
that cat-exposed bilbies had signicantly enhanced short-term
survival after reintroduction into an environment where cats
were present (Ross et al. 2019).
Here we extend our knowledge of the factors inuencing
mortality from predation after release by testing the relative
contribution of individual attributes and the efcacy of pre-
release exposure to predators by comparing the survival of
cat-exposed and cat-na
ıve populations following translocation
to an area that contained feral cats. Previous research
showed that bettongs exposed to cats in large, fenced, exclo-
sures for several years were more wary than cat-na
ıve bet-
tongs (Saxon-Mills et al. 2018; West et al. 2018b) and had
longer hind feet (Moseby et al. 2018). Because these traits
might be expected to inuence bettongsability to avoid or
escape predation by cats, they may also improve post-release
survival of reintroduced bettongs. Furthermore, one previous
study showed that post-reintroduction success of burrowing
bettongs is related to movement patterns, with bettongs that
forage closer to their warrens exhibiting increased survival
than more wide-ranging individuals (West et al. 2018a).
Building on this knowledge, we hypothesised that individuals
exposed to cats prior to release would show improved sur-
vival compared to control animals, and that in particular ani-
mals with larger feet and those that used fewer warrens post
release (a metric of movement) would survive longer than
other individuals. The results of this study provide insights
into co-existence thresholds for threatened mammals.
Materials and methods
Study species
Burrowing bettongs (hereafter bettongs) are bipedal, noctur-
nal marsupials that live communally in burrows (Sander
et al. 1997). Once widespread across Australia, they became
extinct on mainland Australia in the 20
th
century, but per-
sisted on three feral predator-free islands in Western Aus-
tralia. Bettongs have since been successfully reintroduced to
cat- and fox-free fenced sanctuaries on mainland Australia
(Moseby et al. 2011; Short and Turner 2000). Bettongs are
considered to be highly susceptible to predation by intro-
duced predators such as cats and foxes (Vulpes vulpes; Rad-
ford et al. 2018) and attempts to release them into areas
with predators on mainland Australia have failed due to cat
predation (Christensen and Burrows 1995) or a combination
of cat, fox and dingo (Canis lupus dingo) predation (Bannis-
ter et al. 2016; Moseby et al. 2011).
Study site
We studied bettongs in the Arid Recovery Reserve (30°29S,
136°53E), a private conservation reserve situated approxi-
mately 20 km north of Roxby Downs, in arid South Aus-
tralia. Average annual rainfall is 148 mm (www.bom.gov.a
u). Habitat consists of dunes dominated by Acacia ligulata,
Dodonaea viscosa and Zygochloa paradoxa, interspersed
with swales of predominantly Maireana astrotricha and Atri-
plex vesicaria, with some Acacia aneura. The 123 km
2
reserve is surrounded by a 1.8 m oppy-top fence (Moseby
and Read 2006) and is divided into six paddocks (exclo-
sures) (Fig. 1), four of which are free of introduced mam-
malian predators (feral cats, foxes and dingoes) and rabbits
(Oryctolagus cuniculus), an introduced herbivore. Feral cats
and rabbits, but not foxes or dingoes, are present in the
Predator Paddock(24 km
2
) and the Release Paddock
(37 km
2
, Fig. 1). We also used bettongs living in two of the
Cat-Free Paddocks(First Expansion8km
2
and Main
Exclosure14 km
2
). The experiment involved releasing bet-
tongs from the Cat-Free Paddocks and Predator Paddock into
the Release Paddock.
Predator treatments and monitoring
To obtain a population of cat-exposed bettongs, bettongs
were originally reintroduced to the Predator Paddock in
October 2014 from Cat-Free Paddocks (Fig. 2). Cats were
removed beforehand but after a settling period were gradu-
ally added back in, where they were to co-exist with bet-
tongsdetailed methods are given by West et al. (2018b).
Cats were known to subsequently interact with or predate on
bettongs (Moseby et al. 2019, K. Moseby unpub. data). In
the current study, cat-exposed and cat-na
ıve (control)
2Animal Conservation  (2021)  ª2021 The Zoological Society of London
Individual traits vs. predator densities in reintroductions H. L. Bannister et al.
bettongs were translocated to the Release Paddock for two
releases, in November 2017 (Release One) and November
2018 (Release Two). Cat-na
ıve bettongs were sourced from
the First Expansion (2017) or Main Exclosure (2018) and
cat-exposed bettongs were sourced from the Predator Pad-
dock after 3 years of cat exposure (ca. 4 generations). In
addition to cats, rabbits were present in both the Predator
Paddock and Release Paddock. Rabbits and small mammals
are regularly consumed by feral cats (Read and Bowen
2001) and thus represent alternative prey for cats than bet-
tongs. Feral cat, bettong, rabbit and small mammal activity
was monitored in the Release Paddock using remote cameras
and monthly track counts. An array of 20 remote cameras
(Bushnell Trophy Cam HD Aggressor) was established in
September 2017. Detections at least 10 minutes apart were
considered independent. Photos were not clear enough to be
able to reliably identify individual cats. In October 2017, we
established three 1 km track transects along dunes (see
Moseby et al. (2011) for methods) and counted tracks of bet-
tongs, cats, rabbits and small mammals. Camera and track
monitoring also occurred in the Predator Paddock, and track
monitoring occurred in Cat-Free Paddocks.
Release one
In August 2017, 39 bettongs weighing >1200 g from the
Cat-Free Paddock (8F, 12M) or the Predator Paddock (9F,
10M) were tted with VHF radio-collars (brass band 25 g,
Sirtrack, Havelock North, New Zealand). Three months later,
in November 2017, these bettongs were translocated to the
Release Paddock (Table 1), where the cat density was esti-
mated to be 0.41/km
2
within the 95% condence interval
for the average density of cats in Australia in an average
year (0.180.45/km
2
(Legge et al. 2017)). One uncollared
female from the Predator Paddock was also translocated. Cat
density was estimated using a combination of remote camera
detections combined with subsequent removal of cats. None
of the radio-collared bettongs from the Predator Paddock
(cats present) died during the three months prior to transloca-
tion. Bettongs were captured in treadle-operated cage traps
baited with peanut butter and rolled oat balls, following stan-
dard operating procedures (Petit and Waudby 2012). Cap-
tured bettongs were weighed and had hind foot (pes) length,
head length and testes width/pouch status recorded (Table 2).
Body measurements were taken to the nearest 0.1 mm using
Figure 1 Arid Recovery Reserve, divided into six separate paddocks of 837 km
2
. The four paddocks relevant to this study are named.
Animal Conservation  (2021)  ª2021 The Zoological Society of London 3
H. L. Bannister et al. Individual traits vs. predator densities in reintroductions
steel callipers. Each bettong was given a uniquely numbered
ear tag. Bettongs were either released directly into rabbit
warrens (in pairs) in the Release Paddock if released in the
early morning, or were released near rabbit warrens if
released in the evening. Where possible, for releases into
warrens, two bettongs from one source (1M, 1F, where pos-
sible) were released into a single warren, with two bettongs
from the opposite source released into an adjacent warren
(100 m away). Two of the females had small pouch young
at the time of translocation.
Release two
Once radio-collars were removed from the remaining four
bettongs in the Release Paddock after Release One, no tracks
were detected two months later and no bettongs were seen
on remote camera six months laterpresumably they died
either from natural causes or, more likely, from cat preda-
tion. We therefore elected to reduce the number of cats in
the Release Paddock to a point where the camera detection
rates were less than half that recorded at the time of the rst
release. Six cats (5 adults, 1 juvenile) were removed while
bettongs from Release One persisted (adaptive management
in response to high bettong mortality rates), and another 6
adult cats were removed after bettong activity ceased in the
Release Paddock, leaving an estimated density of 0.11/km
2
(cats were identied on camera and/or when later removed,
estimating four cats remaining for Release Two). Following
cat control, in November 2018 we again translocated bet-
tongs from the Predator Paddock and a Cat-free Paddock to
the Release Paddock (Table 1). Twenty from each source
(10F, 10M) were tted with VHF collars and another ve
females from each source were tted with GPS collars (Lite-
track 30, 35 g, Sirtrack Havelock North, New Zealand) at
the time of release. No females had pouch young. Bettongs
were released at two release sites either at night or into war-
rens in the morning (as per Release One), with half from
each source at each.
Monitoring
Bettongs were radio-tracked to their warrens, where possible,
twice in the rst week after release and weekly thereafter. If
a collar emitted a mortality signal, the individual was tracked
(a)
(b)
Figure 2 Burrowing bettong and feral cat activity in the Release Paddock (a) and Predator Paddock (b) monitored by remote camera and
track counts (secondary y-axis). Vertical lines represent bettong releases in the Release Paddock, and removals in the Predator Paddock. A
large number of cats (>40) were deliberately removed from the Predator Paddock in January 2018 (Moseby et al. 2020).
4Animal Conservation  (2021)  ª2021 The Zoological Society of London
Individual traits vs. predator densities in reintroductions H. L. Bannister et al.
to its location where we took photographs, recorded evidence
of predation and collected DNA swabs of the collar and/or
carcass. Swabs were sent to Helix Molecular Solutions
(Crawley, Western Australia) for predator species identica-
tion; detailed methods are given by Moseby et al. (2015).
Bettongs that survived the monitoring period were captured
and their collars were removed.
Data analysis
A multivariate analysis of variance (MANOVA) was used to
compare physical traits (body mass, hind foot length, head
length and body condition index [(weight
1/3
)/hind foot length]
of released animals by sex, release year and treatment (includ-
ing interactions). Assumptions of normality were met. Survival
analysis was conducted separately for each release because of
dramatically different survival periods for the two releases, the
difference in cat activity recorded during each release, and dif-
ferences in physical traits between release years. We analysed
survival in both experiments by tting a Cox Proportional
Hazards regression (Cox 1972) to investigate how treatment as
well as sex, hind foot length, head length and, for Release
Two in 2018, the proportion of unique warrens used (number
of unique warrens used divided by number of times radio-
tracked to a warren) inuenced survival. Proportion of unique
warrens used was not included in the analysis of Release One
because many animals were killed soon after release, skewing
the data. The Cox Proportional Hazards regression allows for
censored data and the hazard function produces a conditional
likelihood providing inferences about the unknown regression
coefcients (Cox 1972). We calculated correlation coefcients
prior to analysis to screen for multicollinearity (correlation val-
ues were <0.3). We veried assumptions of the model by
checking Rho values; none were signicant.
Results
Although there were no signicant differences in traits
between the cat exposed and cat naive bettongs in 2014
when they were initially separated into two treatment groups,
cat-exposed bettongs gradually changed over time with cat
exposure (Moseby et al. 2018). At the start of the present
experiment in 2017 there were signicant differences in
physical traits; on average, cat-exposed bettongs were signi-
cantly heavier, had longer feet, longer heads and better body
condition than cat-na
ıve bettongs (Tables 2 and 3). In addi-
tion to differences between treatments, bettongs in Release
One were signicantly heavier, had longer heads and better
body condition than bettongs in Release Two. On average,
male bettongs were heavier and had better body condition
than female bettongs.
In the month prior to Release One, cat activity on tran-
sects was 7.6 tracks/km (camera detections 16.4/100 trap
nights). Cat activity was reduced to 0 on track counts (cam-
era detections 0.3/100 trap nights) prior to Release Two
(Fig. 2). Rabbit activity in the Release Paddock was more
than twice as high during the rst release (136 tracks/km)
compared to the second release (55 tracks/km), while small
mammal activity uctuated throughout.
Survival (to collar removal) for both releases was ulti-
mately poor with 27.9 % of cat-exposed bettongs and 25 %
of cat-na
ıve bettongs surviving to collar removal, but over
different time periods. In Release One, 15.8 % of cat-
exposed bettongs (3 of 19) and 5.0 % of cat-na
ıve bettongs
(1 of 20) survived to collar removal around 100 days after
release [Kaplan Meier probability of survival at day
100 =0.10 (95% CI 0.030.22)]. Collars were removed at
this stage because we felt the cost and logistic effort required
to monitor a such small number of animals (4) over a longer
Table 1 Burrowing bettong translocations
Release Year Cat exposed No. translocated
Bettong activity
at source (tracks/km)
Cat activity
at source (tracks/km)
Cat activity at
release site (tracks/km)
One 2017 Yes 20 (10F, 10M) 122 15 13.3 7.6
One 2017 No 20 (8F, 12M) 245 56 0 7.6
Two 2018 Yes 25 (15F, 10M) 19 3 0.3 0*
Two 2018 No 25 (15F, 10M) 149 58 0 0*
Bettong activity at each source was averaged over the 6 months prior to translocation. Cat activity was recorded in the month prior to
translocation.
*Despite cat activity (tracks/km) being 0 prior to release, cats were known to be present based on remote camera data.
Table 2 Physical traits for bettongs at the time of release (mean 1SE). BCI =body condition index ((body mass
1/3
)/hind foot length)
2017
Cat-exposed
2017
Cat-na
ıve
2018
Cat-exposed
2018
Cat-na
ıve
Female Male Female Male Female Male Female Male
No. released 10 10 8 12 15 10 15 10
Body mass (g) 1554 36 1777 28 1444 56 1642 42 1558 35 1711 54 1428 33 1398 51
Hind foot length (mm) 105.4 0.5 106.6 1.1 103.9 1.6 104.4 1.0 104.6 0.7 105.3 0.9 102.6 0.6 103.9 0.7
Head length (mm) 77.8 0.8 78.4 0.8 76.6 0.7 76.7 0.9 80.7 0.8 81.3 0.5 77.2 0.6 78.5 0.7
BCI 4.91 0.10 5.56 0.07 4.63 0.16 5.24 0.11 4.96 0.10 5.42 0.16 4.64 0.09 4.48 0.15
Animal Conservation  (2021)  ª2021 The Zoological Society of London 5
H. L. Bannister et al. Individual traits vs. predator densities in reintroductions
period was not of benet considering the remote nature of
the eld site. Cats were conrmed killers of 88 % of dead
radio-collared bettongs based on DNA results, even when
wedge-tailed eagles had interfered with carcasses. Because
no DNA was able to be extracted from the remaining swabs,
cause of death remained unclear. In Release Two, 37.5 % (9
of 24) of cat-exposed bettongs and 41.7 % of cat-na
ıve bet-
tongs (10 of 24) survived to collar removal around 250 days
after release (Table 4), with a 0.96 probability of survival to
day 100 (95% CI 0.840.99). The probability of survival to
100 days for bettongs released at low cat density (Release
Two) was higher (0.96) than at moderate cat density (0.10)
(Release One). When the two releases were pooled, there
was no difference in the probability of survival to day 100
based on treatment, with a probability of 0.58 (95% CI
0.430.73) for cat-exposed bettongs, and a probability of
0.55 (95% CI 0.390.68) for cat-na
ıve bettongs.
Patterns of decline differed between the two releases; dur-
ing Release One, survival rapidly declined following the
release. For Release Two, post-release survival was much
higher until 200 days post-release, when there was a rapid
decline in survival (Fig. 3).
No signicant variation in survival duration was explained
by our measured variables for Release One (Table 5). By
contrast, in Release Two, we found that having a large hind
foot decreased the risk of mortality and there were trends
towards males dying sooner than females, and those with
smaller heads surviving longer (Table 5).
Discussion
Despite the experimental burrowing bettong population being
exposed to feral cats for at least three years, prior exposure
to this predator did not confer a survival advantage to bet-
tongs at moderate or low cat densities. A lower cat density
permitted a longer survival time for both treatments, but
even the lower cat density of 0.11/km
2
was too high to per-
mit co-existence of a newly reintroduced population, with
the population ultimately declining prior to intervention (cat
removal). It is important to note that these cat densities were
much lower than those recorded in the cat-exposed source
population (Predator Paddock) where cat density was 1.84/
km
2
in January 2019, reduced (articially) to 0.64/km
2
two
months later (Moseby et al. 2020). A key difference between
the Predator and Release Paddocks is that cats were not pre-
sent when bettongs were initially translocated to the Predator
Paddock but were added in shortly afterwards (West et al.
2018b) suggesting that a period of low or no predator den-
sity prior to exposure to cats may be benecial. Intensive
pre-release predator control to allow released animals a set-
tling period may thus be advantageous. However, most
deaths in the low cat density experiment occurred more than
200 days after release which does not support this sugges-
tion.
At moderate cat densities both cat-exposed and cat-na
ıve
bettongs had low survival during the ca. 100 day tracking
period in the Release Paddock and no bettongs were
recorded on camera after nine months. This high mortality
of both groups after release mirrors the ndings of previous
reintroductions of bettongs into areas with introduced preda-
tors (Bannister et al. 2016; Christensen and Burrows 1995;
Moseby et al. 2011), but is at odds with a reintroduction of
greater bilbies into the same area where cat exposed individ-
uals survived for longer that cat-na
ıve individuals (Ross
et al. 2019). In the present study, none of the measured
physical traits conferred a survival advantage for bettongs at
moderate cat densities suggesting that when predation rates
Table 3 Results of a MANOVA, investigating pre-existing
differences in body mass, hind foot length, head length and body
condition index (BCI) for burrowing bettongs by release year,
treatment (cat-exposed and cat-na
ıve), sex, release year 9sex and
release year 9treatment
Dependent
variable Factor F-value df P-value
Body mass Release year 11.9 1 0.0009*
Sex 14.7 1 0.0002*
Treatment 29.3 1 <0.0001*
Release year
9treatment
1.8 1 0.19
Release year 9sex 6.6 1 0.012*
Hind foot length Release year 3.3 1 0.072
Sex 1.5 1 0.23
Treatment 8.4 1 0.0048*
Release year
9treatment
0.03 1 0.87
Release year 9sex 0.005 1 0.95
Head length Release year 13.6 1 0.0004*
Sex 1.3 1 0.26
Treatment 21.5 1 <0.0001*
Release year
9treatment
2.6 1 0.11
Release year 9sex 0.3 1 0.59
BCI Release year 10.1 1 0.0021*
Sex 14.4 1 0.0003*
Treatment 25.1 1 <0.0001*
Release year
9treatment
2.5 1 0.12
Release year 9sex 7.9 1 0.0062*
Measurements were taken at the time of translocation.
*Indicates significance (P<0.05).
Table 4 Survival (to collar removal) of translocated burrowing
bettongs
Cat-exposed Cat-na
ıve
Survived Died Survived Died
Release one (2017)
Female 2 7 1 7
Male 1 9 0 12
Release two (2018)
Female 6 8 8 6
Male 3 7 2 8
Total (%) 27.9% 72.1% 25% 75%
Collar removal occurred around 100 days after release for release
one, and around 250 days after release for release two.
6Animal Conservation  (2021)  ª2021 The Zoological Society of London
Individual traits vs. predator densities in reintroductions H. L. Bannister et al.
are high, all individuals are at a similar risk irrespective of
their physical traits.
In contrast to Release One, bettong sex had a weak inu-
ence (P=0.08) on survival during Release Two, with males
tending to die sooner. Males may have been at higher risk
of encountering a cat during Release Two, when there was
lower cat activity, because they undertake longer movements
(Sander et al. 1997) and engage more actively in agonistic
intra-specic interactions than females (Stodart 1966). In
Release One, cat densities were higher and less mobile indi-
viduals (females) were possibly equally as likely to encoun-
ter cats.
During Release Two, when cat activity was lower, bettong
survival was high until 200 days post-release. However, after
200 days, mortality increased sharply over a period of one
month despite cat activity remaining stable over the post
release period. This spike in predation could reect a reduc-
tion in the availability of alternative prey leading to cats
prey switching (Doherty et al. 2015) and targeting bettongs.
Although there was no obvious reduction in rabbit activity,
reptile activity was not monitored and the timing of the
decline coincides with the onset of winter, while small mam-
mal activity was slightly higher in the summer months
immediately following the release, before declining in
autumn. Alternatively, there may have been an incursion of
cat(s) into the paddock, or cats (present within the Release
Paddock) may have learned to hunt bettongs over time or
reached an age and size where they could catch bettongs,
which are at the upper end of the prey size range of cats
(Doherty et al. 2017). Previous studies have found that male
cats (Marlow et al. 2015) or large male cats (>4 kg)
(Moseby et al. 2015) are more likely to kill difcult or large
prey and can increase their hunting rate over time. Increas-
ingly dry conditions, owing to drought, may also have led to
bettongs foraging further from their warrens (e.g. Dickman
et al. 2010), and thus increasing their exposure to predators.
However, bettongs in Release Two began breeding almost
immediately after release, suggesting conditions were not
unfavourable. The delayed spike in mortalities is interesting
for reintroduction biology in the broader context because the
critical period for most releases is the period immediately
following reintroduction (Armstrong et al. 2017). Our nding
that predation rates can increase sharply 200 days after rein-
troduction highlights and supports other studies showing pre-
dation rates on reintroduced prey can change dramatically
over short time periods (Hardman et al. 2016).
Although West et al. (2018b) and Moseby et al. (2018)
found physical and behavioural differences between popula-
tions of cat exposed and cat-na
ıve bettongs after only
18 months of cat-exposure, three years of cat exposure did
not confer a survival advantage for reintroduced bettongs in
this study. However, the results of Release Two, when cat
activity was low, showed that hind foot length was a predic-
tor of bettong survival and that individuals with longer feet
survived for longer. Despite cat-exposed bettongs having
longer hind feet on average, there was overlap with cat-na
ıve
bettongs (Release Two hind foot length (range), cat-
Figure 3 Burrowing bettong survival by release treatment and year.
Table 5 Results of Cox proportional hazard regression analysis for
experimental burrowing bettong releases conducted in 2017
(n=39, Concordance =0.57 (SE =0.06), Wald test =1.79, 4 df,
P=0.78, R
2
=0.05), and 2018 (n=45, Concordance =0.70
(SE =0.06), Wald test =12.45, 5 df,P=0.03, R
2
=0.24)
Release Coefficient SE P-value
2017 (Release one)
Treatment (cat-na
ıve) 0.05 0.37 0.89
Sex (male) 0.46 0.37 0.22
Hind foot length (mm) 0.03 0.06 0.57
Head length (mm) 0.01 0.07 0.87
2018 (Release two)
Treatment (cat-na
ıve) 0.05 0.53 0.93
Sex (male) 0.71 0.41 0.08
Hind foot length (mm) 0.26 0.09 0.004*
Head length (mm) 0.19 0.10 0.07
Proportion unique warren use 0.20 0.76 0.80
Significant (*) negative coefficients indicate that a variable
decreased hazard, and hence increased longevity.
Animal Conservation  (2021)  ª2021 The Zoological Society of London 7
H. L. Bannister et al. Individual traits vs. predator densities in reintroductions
exposed =100.3109.3 mm, cat-na
ıve =99.1106.9 mm;
Table 2) which may explain why hind foot length, rather
than treatment per se, signicantly increased survival. Larger
hind foot length may confer a survival advantage by giving
bettongs a locomotor advantage during escape. A previous
study with a larger sample size found a signicant difference
in hind foot length between cat-exposed and cat-na
ıve bet-
tongs (Moseby et al. 2018), however the difference in hind
foot length in the much smaller sample size of the current
study may explain why a signicant effect of treatment on
survival was not also found. West et al. (2018a) found that
smaller bettongs foraged further from their warren and were
more likely to die after release suggesting there may also be
a link between size and movement, which could affect pre-
dation risk.
There may be several reasons why we recorded no post-
release survival difference between the cat-exposed and cat
na
ıve bettongs despite a survival difference being previously
recorded in predator exposed bilbies at the same study site
(Ross et al. 2019). First, although strong selection by preda-
tors can trigger rapid evolutionary changes (R
eale and Festa-
Bianchet 2003), the magnitude of the trait differences
between our two populations may have been too small to
have a tness effect. Related to this, because the effect size
on survival may be small, our sample size of 2025 individ-
uals in each treatment in each release may have been insuf-
cient to detect signicant differences. Either larger release
groups and/or longer cat exposure may be required to enable
survival differences to be detected.
Second, bettongs may simply be outgunned(Banks and
Dickman 2007) and, despite signicant trait changes, are
unable to effectively respond to threats imposed by cats and
other novel predators. Support for the outgunnedhypothe-
sis is provided by the fact that burrowing bettongs became
extinct from mainland Australia, due primarily to predation
by introduced foxes and feral cats (Short and Turner 1993).
Further support for this explanation comes from the original
source of our animalsan island where their populations
had no exposure to terrestrial predators following the cre-
ation of these islands by rising sea-levels approximately
7000 years ago (Lewis et al. 2013). Indeed, it may be that
three years of cat exposure is not long enough to counteract
the effects of 7000 years of isolation and relaxed selection
for anti-predator traits (Blumstein and Daniel 2005). Bilbies,
in contrast, still exist in the wild in a number of places
which suggests that they have developed anti-predator
responses that allow them to co-exist with introduced preda-
tors (Steindler and Letnic 2021).
Third, behavioural differences between bettongs and bil-
bies may also contribute to the increased vulnerability of bet-
tongs to introduced predators, because bettongs are highly
social and live in permanent shared warrens (Sander et al.
1997), while bilbies tend to live alone in burrows (Russell
1984) and move burrows regularly (Moseby and ODonnell
2003). These differences between bilbies and bettongs may
increase the conspicuousness of bettongs, thus increasing the
chance of cats detecting and then preying on them. A previ-
ous study found that bettongs which stayed closer to their
warrens were less docile and had a greater chance of sur-
vival (West et al. 2018a), thus it is possible that individual
personality traits play a role in post-release survival. Finally,
bettong density was higher in the Cat-free Paddock than the
Predator Paddock, a result that is to be expected due to the
cat predation impacts within the Predator Paddock regulating
the bettong population. This difference in bettong density
may have contributed to the differences in morphology
reported during the study, but separating out the effects of
density-dependence (non-direct effects) and predation is dif-
cult (Creel and Christianson 2008). However, the shifts in
behaviour and morphology we report are consistent with
responses to predation. Controlled experiments such as com-
mon garden experiments, where density, predation and
maternal effects can be controlled for, are required and rec-
ommended in order to condently identify predation effects.
In summary, our results show that 3 years of prior expo-
sure to predators had no measurable effect on the survival of
reintroduced bettongs and that individual attributes may not
be important for survival when predator densities are too
high, but that at low predator densities intraspecic differ-
ences are more apparent. Moreover, the contrasting effects of
prior predator exposure on the fates of reintroduced bettongs
(no effect, this study) and greater bilbies (signicant positive
effect, see Ross et al. 2019) highlights that prior predator
exposure has the potential to improve anti-predator responses
of reintroduced prey, but also that the efcacy or time of
exposure required may vary between species, or that the co-
existence thresholds of some species with introduced preda-
tors may be too low to be sustained in the wild. We used
bettongs that were exposed to feral cats under natural condi-
tions, thus our results are likely to be applicable to wild situ-
ations and relevant to a range of circumstances. We suggest
that exposing populations to predators over longer time peri-
ods, monitoring divergence in traits and testing survival is
required to determine whether pre-release predator exposure
prepares animals with prolonged relaxation of predation pres-
sure, like bettongs, for life with predators. Furthermore, the
rapid failure of the reintroduction of bettongs at a moderate
cat density and eventual failure of the reintroduction con-
ducted at low cat density demonstrates that it is likely that
some level of predator control will always be required prior
to reintroduction including in situations where in situ expo-
sure to predators has been conducted prior to release, in
order for benets of intraspecic variation in anti-predator
traits to be realised.
Acknowledgements
This project was supported by ARC Linkage Grants
(LP130100173 and LP160100270), with extensive in-kind
support provided by our partner Arid Recovery. Arid Recov-
ery is a conservation and research organisation supported by
BHP Billiton, The University of Adelaide, The SA Depart-
ment for Environment and Water, and Bush Heritage Aus-
tralia. We thank Rebecca West for her assistance developing
the cat-exposed bettong population, Katherine Tuft for logis-
tical support, Louise Falls, Pat Hodgens, Anna Rogers and
8Animal Conservation  (2021)  ª2021 The Zoological Society of London
Individual traits vs. predator densities in reintroductions H. L. Bannister et al.
Melissa Jensen for assistance with radio-tracking and trap-
ping bettongs, and Frank Bernhardt, Hugh McGregor and
Mark Young for assistance with cat control. We thank sev-
eral anonymous reviewers for their constructive feedback.
This research was conducted with ethics approval from the
South Australian Wildlife Ethics Committee permit no. 9/
2017.
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Individual traits vs. predator densities in reintroductions H. L. Bannister et al.
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Context: Over the last 230 years, the Australian terrestrial mammal fauna has suffered a very high rate of decline and extinction relative to other continents. Predation by the introduced red fox (Vulpes vulpes) and feral cat (Felis catus) is implicated in many of these extinctions, and in the ongoing decline of many extant species. Aims: To assess the degree to which Australian terrestrial non-volant mammal species are susceptible at the population level to predation by the red fox and feral cat, and to allocate each species to a category of predator susceptibility. Methods: We collated the available evidence and complemented this with expert opinion to categorise each Australian terrestrial non-volant mammal species (extinct and extant) into one of four classes of population-level susceptibility to introduced predators (i.e. 'extreme', 'high', 'low' or 'not susceptible'). We then compared predator susceptibility with conservation status, body size and extent of arboreality; and assessed changes in the occurrence of species in different predator-susceptibility categories between 1788 and 2017. Key results: Of 246 Australian terrestrial non-volant mammal species (including extinct species), we conclude that 37 species are (or were) extremely predator-susceptible; 52 species are highly predator-susceptible; 112 species are of low susceptibility; and 42 species are not susceptible to predators. Confidence in assigning species to predator-susceptibility categories was strongest for extant threatened mammal species and for extremely predator-susceptible species. Extinct and threatened mammal species are more likely to be predator-susceptible than Least Concern species; arboreal species are less predator-susceptible than ground-dwelling species; and medium-sized species (35 g-3.5 kg) are more predator-susceptible than smaller or larger species. Conclusions: The effective control of foxes and cats over large areas is likely to assist the population-level recovery of ∼63 species-the number of extant species with extreme or high predator susceptibility-which represents ∼29% of the extant Australian terrestrial non-volant mammal fauna. Implications: Categorisation of predator susceptibility is an important tool for conservation management, because the persistence of species with extreme susceptibility will require intensive management (e.g. predator-proof exclosures or predator-free islands), whereas species of lower predator susceptibility can be managed through effective landscape-level suppression of introduced predators.
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Individuals often respond to threatening situations in consistently different ways and these differences may predict later translocation success. Thus, the ability to easily identify these differences prior to translocation may assist in improving conservation outcomes. We asked whether burrowing bettongs (Bettongia lesueur), a marsupial species that has undergone significant decline since the introduction of exotic predators to Australia, responded in consistently different ways to capture in traps, and if so, whether this was related to anti-predator behaviour, ranging behaviour and survival following translocation. Behavioural responses of 40 bettongs were measured and included response to removal from traps (trap docility), latency to leave a trap or bag and escape behaviour upon release. We used flight initiation distance to measure escape behaviour, and distance moved from diurnal refuges during nocturnal foraging to measure ranging behaviour. Survival was measured through radiotracking after release. Behaviours scored during removal from a trap were consistent and repeatable, and formed a behavioural syndrome with anti-predator and ranging behaviour. Less docile bettongs foraged closer to refuges and had longer flight initiation distances. Less docile bettongs were also more likely to survive after release, although the sample size of mortalities was small. Our results suggest that behaviours scored during trapping could be a useful metric for pre-release screening in translocation programs to enhance the chances of individual survival post-release.
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Prey may recognize and respond to predatory cues based on a period of co-evolution or life experience with a predator. When faced with a novel predator, prey may be naïve to the threat posed and/or unable to respond effectively, making them highly susceptible to predation. Burrowing bettongs (Bettongia lesueur) are one such species whose naïveté towards introduced predators has contributed to their extinction from mainland Australia. Here, we asked whether bettongs that were predator-naïve and bettongs which had been exposed to feral cats (Felis catus) for up to 2 years could discriminate between odors of a predator with which they shared no evolutionary history (feral cats), a predator with which they share a deep evolutionary history (Tasmanian devil—Sarcophilus harrisii), a novel herbivore (guinea pig—Cavia porcellus), and procedural control (a towel moistened with deionized water). We deployed scents at foraging trays and filmed bettongs’ behavior at the trays. Predator-naïve bettongs’ latency to approach foraging trays and behavior did not differ between scents. Cat-exposed bettongs increased their latency to approach in the presence of animal scents compared with control, and approached predatory scents slowly and cautiously more often than herbivore and procedural control scents. Taken together, these results suggest that bettongs have not retained anti-predator responses to Tasmanian devils after 8000 years of isolation from mammalian predators but nevertheless show that bettongs exposed to predators are more wary and may be able to generalize predator response using olfactory cues. Significance statement When prey encounter a novel predator, they are often naïve to the threat posed and employ ineffective anti-predator responses, because they lack either evolutionary or ontogenetic experience with the predator. Determining how prey identify novel predators is important to improve the success of translocations and reintroductions. Here, we examine how exposure of predator-naïve individual burrowing bettongs to predators influences anti-predator responses. By quantifying bettong responses to odors, we show that those experimentally exposed to cats increased their vigilance in response to odors from cats and Tasmanian devils. The results are consistent with the idea that prey generalize anti-predator responses based on non-specific compounds found in predatory odors, and that exposure to novel predators can improve anti-predator responses.
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ContextFeral cats pose a significant threat to wildlife in Australia and internationally. Controlling feral cats can be problematic because of their tendency to hunt live prey rather than be attracted to food-based lures. The Felixer grooming trap was developed as a targeted and automated poisoning device that sprays poison onto the fur of a passing cat, relying on compulsive grooming for ingestion. AimsWe conducted a field trial to test the effectiveness of Felixers in the control of feral cats in northern South Australia where feral cats were present within a 2600-ha predator-proof fenced paddock. Methods Twenty Felixers were set to fire across vehicle tracks and dune crossings for 6 weeks. Cat activity was recorded using track counts and grids of remote camera traps set within the Felixer Paddock and an adjacent 3700-ha Control Paddock where feral cats were not controlled. Radio-collars were placed on six cats and spatial mark–resight models were used to estimate population density before and after Felixer deployment. Key resultsNone of the 1024 non-target objects (bettongs, bilbies, birds, lizards, humans, vehicles) that passed a Felixer during the trial was fired on, confirming high target specificity. Thirty-three Felixer firings were recorded over the 6-week trial, all being triggered by feral cats. The only two radio-collared cats that triggered Felixers during the trial, died. Two other radio-collared cats appeared to avoid Felixer traps possibly as a reaction to previous catching and handling rendering them neophobic. None of the 22 individually distinguishable cats targeted by Felixers was subsequently observed on cameras, suggesting death after firing. Felixer data, activity and density estimates consistently indicated that nearly two-thirds of the cat population was killed by the Felixers during the 6-week trial. Conclusions Results suggest that Felixers are an effective, target-specific method of controlling feral cats, at least in areas in which immigration is prevented. The firing rate of Felixers did not decline significantly over time, suggesting that a longer trial would have resulted in a higher number of kills. ImplicationsFuture studies should aim to determine the trade-off between Felixer density and the efficacy relative to reinvasion.
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Many translocations and introductions to recover threatened populations fail because predators kill prey soon after release; a problem exacerbated for predator-naive prey. While pre-release training has been shown to work in some situations, it is time consuming and relies on using inferred predator cues and treating small groups. We review a relatively new and very promising management tool: in situ , pre-release predator conditioning. Here, the goal is to allow prey in large enclosures to live with low densities of predators to accelerate selection for antipredator traits (in an evolutionary sense) or provide prey essential experience with predators that they will later encounter. We review the published results of a large-scale, controlled experiment where we have permitted burrowing bettongs ( Bettongia lesueur ) and greater bilblies ( Macrotis lagotis ) to live with low densities of feral cats ( Felis catus ), a species implicated in their widespread decline and localized extinction. We found that both species could persist with cats, suggesting that future work should define coexistence thresholds—which will require knowledge of prey behaviour as well as the structure of the ecological community. Compared to control populations, predator-naive prey exposed to cats has a suite of morphological and behavioural responses that seemingly have increased their antipredator abilities. Results suggest that predator-conditioned bilbies survive better when released into a large enclosure with an established cat population; future work will determine whether this increased survival extends to the wild. This article is part of the theme issue ‘Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation’.
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Prey naïveté is thought to be a significant factor contributing to the failure of native prey to re-establish in the presence of introduced predators. We tested whether exposing naïve prey to low levels of in situ predation pressure from introduced predators could cause accelerated selection for certain physical or behaviour traits. Such selection could improve the chance of future coexistence between introduced predators and native prey. In 2014, we reintroduced 352 burrowing bettongs (Bettongia lesueur) into a 26 km 2 fenced paddock where pre-dation levels could be carefully controlled. Four feral cats (Felis catus) were introduced to the paddock several months after bettong reintroduction and predation events were subsequently recorded. We measured a suite of physical and behavioural traits on the bettongs prior to release and compared these between individuals that survived or were assumed to have died. Population level parameters were also compared between the reintroduced population and the predator-free source population. No a priori measured physical or behavioural traits were significant predictors of individual survival after release and the high survival rate of radio-collared bettongs and the positive population growth rate suggests that the predation pressure from the introduced feral cats may not have been sufficiently high to cause strong selection over a short time period. However, population level comparisons found cat-exposed male bettongs had significantly longer hind feet than the source population at 18-22 months after release. Hind foot length was consistently longer in both older released animals and younger recruits and thus may be an indicator of selection and/or phenotypic change in response to the presence of predators. Our study suggests that predation may cause phenotypic change over short time periods but that higher cat predation pressure may be required to enable the benefits of accelerated natural selection to be adequately assessed.
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Through natural as well as anthropogenic processes, prey can lose historically important predators and gain novel ones. Both predator gain and loss frequently have deleterious consequences. While numerous hypotheses explain the response of individuals to novel and familiar predators, we lack a unifying conceptual model that predicts the fate of prey following the introduction of a novel or a familiar (reintroduced) predator. Using the concept of eco-evolutionary experience, we create a new framework that allows us to predict whether prey will recognize and be able to discriminate predator cues from non-predator cues and, moreover, the likely persistence outcomes for 11 different predator-prey interaction scenarios. This framework generates useful and testable predictions for ecologists, conservation scientists, and decision-makers.