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Prey naïveté and the anti-predator responses of a vulnerable marsupial prey to known and novel predators

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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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ORIGINAL ARTICLE
Prey naïveté and the anti-predator responses of a vulnerable marsupial
prey to known and novel predators
Eleanor C. Saxon-Mills
1
&Katherine Moseby
1,2
&Daniel T. Blumstein
3
&Mike Letnic
1
Received: 2 February 2018 / Revised: 20 August 2018 / Accepted: 20 August 2018
#Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract
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 devilSarcophilus harrisii), a novel herbivore (guinea
pigCavia porcellus), and procedural control (a towel moistened with deionized water). We deployed scents at foraging
trays and filmed bettongsbehavior at the trays. Predator-naïve bettongslatency 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 re-
sponses 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.
Keywords Prey naïveté .Anti-predator responses .Olfactory recognition .Generalization .Acquired predator recognition
Introduction
An individuals ability to recognize and respond to predator
cues may require periods of co-evolution or ontogeny (life
experience) with a predator (Carthey and Blumstein 2018;
Parsons et al. 2018). As a result, when a prey encounters a
novel predator species, they are often naïve to the threat posed
and are unable to recognize or respond effectively (Moseby
et al. 2011). Prey naïveté can occur due to isolation from one
or more types of predators and this isolation relaxes selection
pressure (Blumstein and Daniel 2005). It is also conceivable
Communicated by A. I. Schulte-Hostedde
*Eleanor C. Saxon-Mills
eleanorcsaxon@gmail.com
1
Centre for Ecosystem Science, School of Biological, Earth and
Environmental Sciences, University of New South Wales,
Sydney,NSW,Australia
2
Arid Recovery Ltd., Roxby Downs, SA, Australia
3
Department of Ecology and Evolutionary Biology, University of
California, Los Angeles, CA, USA
Behavioral Ecology and Sociobiology (2018) 72:151
https://doi.org/10.1007/s00265-018-2568-5
that anti-predator responses could be actively selected against,
because the missed opportunity costs to foraging and repro-
ducing from employing anti-predator responses can be high
(Brown and Kotler 2004). The loss of anti-predator responses
after isolation from predators can occur over very short time
periods of time (e.g., as few as 130 years in tammar wal-
labiesMacropus eugenii, Blumstein et al. 2004) and has
been attributed to a combination of relaxed selection on anti-
predator behaviors and benefits accrued from reducing the
energetic costs associated with employing anti-predator be-
haviors (Caro 2005). However, some species can retain anti-
predator responses after extended periods of isolation (e.g.,
quokkasSetonix brachyurus, after 7000 years of isolation,
Blumstein et al. 2001).
Interestingly, the loss of anti-predator responses can be re-
versed (Griffin et al. 2000). Indeed, prey species have been
observed to relearn predatory cues in as little as one generation
(mooseAlces alces,Bergeretal.2001). Prey may not only
relearn lost behaviors, but may also learn to discriminate and
respond to novel predators after short periods of coexistence
(e.g., 130 years for ringtail possumsPseudocheirus
peregrinus,AnsonandDickman2013; 30 years for Iberian
waterfrogsPelophylax perezi, Nunes et al. 2014).
Whether, and the degree to which, prey are able to learn
about their predators is of particular importance when native
prey have suffered dramatic declines as a result of predation
by introduced predators. For instance, Australia has one of the
worlds worst mammalian extinction records, with 30 mam-
mals becoming extinct since European settlement (Woinarski
et al. 2015). Predation by introduced predators, red foxes and
feral cats (Felis catus), is cited as one the major factors driving
declines of mammal populations (Short and Smith 1994), due
in part to prey naïveté. Naïveté towards introduced predators
is thought to make native mammals particularly susceptible to
predation, given the long history of predator absence during
evolution (Moseby et al. 2015a).
Conservation managers have employed various tactics to
address the issue of predation by introduced predators. This
includes manipulating the environment of prey species by
eradicating introduced predators and moving at-risk popula-
tions onto predator-free islands and into predator-proof fenced
exclosures (Short 2009). However, these methods often are
short-term solutions, because predator removal is costly
(Parks et al. 2012), and an incursion by a few individual pred-
ators can decimate an entire population (Christensen and
Burrows 1995). Additionally, this very isolation from preda-
tory threats may exacerbate the problem of prey naïveté, be-
cause the removal of predatory threats relaxes selection pres-
sures (Moseby et al. 2015a). Exacerbation of prey naïveté
brought about by isolation from predators may be a key factor
why many reintroductions, which often use animals from
predator-free areas, fail to establish self-sustaining popula-
tions (Moseby et al. 2015a).
To combat the problem of prey naïveté, some researchers
have attempted to manipulate the traits of prey individuals by
training naïve or captive-bred animals to recognize and re-
spond to novel predatory threats prior to reintroduction. In
some instances, wildlife managers have used Pavlovian con-
ditioning by pairing predatory cues with an aversive event to
stimulate prey learning (McLean et al. 2000; Griffin et al.
2001) Predator learning after training has been demonstrated
in a variety of fishes (Ferrari et al. 2007; Brown et al. 2011)
and mammals (Griffin et al. 2001). However, few studies have
tested whether pre-release training actually improves post-
release survival (houbara bustardsChlamydotis [undulata]
macqueenii, Van Heezik et al. 1999; Puerto Rican parrots
Amazona vittata, White et al. 2005). Moseby et al. (2015b)
suggest that pairing predatory cues with non-dangerous aver-
sive events in training assays, such as stimulated capture
(Griffin et al. 2001), or being shot at by water pistols
(Mclean et al. 1996), may not stimulate the appropriate anti-
predator responses to the threat of actual predation. Instead,
they propose that in situ exposure to low densities of intro-
duced predators may facilitate prey learning and it may permit
natural selection to occur in response to predation.
Another foundational issue in applied predator recognition
is the degree to which prey are able to generalize their anti-
predator responses from a known predator to an unknown
predator (Ferrari et al. 2007). The ability to generalize anti-
predator responses from a known to an unknown predator
would be particularly advantageous and may reduce prey mor-
tality and enhance survival in environments with novel pred-
ators (Ferrari et al. 2007). Generalized responses towards
predators have been reported in a variety of taxa, including
fish (Brown et al. 2011; Ferrari et al. 2016), reptiles (Webb
et al. 2009), and mammals (Griffin et al. 2001; Blumstein et al.
2008).
The archetype hypothesis (Cox and Lima 2006)suggests
one mechanism for generalization, where prey can recognize
unknown predators that have a close phylogenetic relationship
to known predators, and which share similar traits (life history,
hunting style, physical appearance). True generalization, how-
ever, does not require predators to be of the same archetype;
instead, learning about one potential threat heightens re-
sponses to other threats (Ferrari et al. 2007). One mechanism
for true generalization is the use of chemical compounds to
identify predatory odors regardless of previous exposure,
termed the common constituents hypothesis (Nolte et al.
1994; Ferrero et al. 2011; Osada et al. 2015).
In this study, we test two hypotheses. First, do burrowing
bettongs (Bettongia lesueur) with up to 2-year experience liv-
ing with a novel, introduced predator (feral cats) exhibit wary
anti-predator responses in the presence of this predatory odor?
Second, do cat-exposed bettongs respond with increased war-
iness in the presence of unknown predator odors? We tested
our hypotheses by exposing cat-exposed and non-cat-exposed
151 Page 2 of 10 Behav Ecol Sociobiol (2018) 72:151
bettongs to the scents of two predators, Tasmanian devils
(Sarcophilus harrisii) and cats, guinea pigs (Cavia porcellus)
and a procedural control (a towel moistened with deionized
water) and analyzing their behavioral responses.
Methods
Study site
We conducted the study at Arid Recovery (30° 29S, 136° 53
E), a 123-km
2
fenced reserve located approximately 20 km
north of Roxby Downs, South Australia. Arid Recovery was
established in 1997, and currently consists of six separate
fenced exclosures, in which introduced predators foxes, cats,
and dingoes were systematically removed between 1999 and
2001. Locally extinct mammals were reintroduced between
1998 and 2008, including greater stick-nest rats (Leporillus
conditor), greater bilbies (Macrotis lagotis), burrowing
bettongs, and western barred bandicoots (Perameles
bougainville) (Moseby et al. 2011). We conducted our study
in May 2017; at this time, five of the exclosures were predator-
free and one, the Red Lake exclosure, had feral cats introduced
in 2014 to examine the effects of living with predators on prey
behavior and population biology (West et al. 2018). In this
study, we used the Red Lake Exclosure (26 km
2
) as our pred-
ator treatment site and the Northern Expansion (30 km
2
)asa
control predator-free site.
Study species
Bettongs are social, medium-sized marsupials (11.5 kg) that
once occupied the widest geographical range of any
Australian mammal species. They now occur naturally on
only three predator-free offshore islands: Bernier, Dorre, and
Barrow Islands (Short and Turner 2000). Bettongsinability to
avoid predation by introduced cats and foxes has been impli-
cated as one of the major causes of their decline (Christensen
and Burrows 1995;Mosebyetal.2015b). Three
reintroductions to fenced mainland sites have occurred in ef-
forts to conserve the species: Heirisson Prong in 1992 (failed),
Arid Recovery in 19992001, and Scotia Wildlife Sanctuary
in 2008.
The bettongs at Arid Recovery were sourced from the
Bernier Island and Heirisson Prong (originally Dorre Island)
populations (Moseby et al. 2011). Bernier and Dorre Islands
have been almost entirely predator-free since their isolation
from the mainland approximately 8000 years ago
(Shortridge 1910;Gale2009), which occurred due to rising
sea levels (Lewis et al. 2013). Before this isolation, the range
of the bettong overlapped with that of native marsupial pred-
ators, including Tasmanian devils, thylacine (Thylacinus
cynocephalus) (Gale 2009), and western quolls (Dasyurus
geoffroii) (Shortridge 1910).
There is no documented evidence that Indigenous people
lived permanently on these islands, but it is possible that they
visited with dingoes during the Holocene (Abbott 1979).
Domestic dogs and cats were brought to Dorre and Bernier
Islands in the late nineteenth century, when pastoral operations
were established, and between 1908 and 1918, when the
islands operated as hospitals for Aboriginal people
(Shortridge 1910). During this time, dogs were used for mus-
tering livestock, companion pets, and likely helped
Aborigines in the hunting of mammals (Stingemore 2010).
During the early twentieth century, cats were believed to have
hunted mammals on the islands and were thought to be a
factor contributing to the rarity of the western barred bandi-
coot on the islands (Shortridge 1910).
The islands could have been predator-free from as early as
1918, at the closure of the hospital. The islands were consid-
ered to be free of mammalian predators in 1959 when a sci-
entific expedition conducted an inventory of the islandsbiota
(Ride et al. 1962). Thus, the bettongs introduced to Arid
Recovery had 8000 years with no exposure to native mamma-
lian predators and only a relatively brief period (maximum
60 years) of co-occurrence with introduced predators (domes-
tic dogs and cats) in modern times, which ended at least
60 years ago.
Experimental rationale
We aimed to examine the response of bettongs to predatory
odors that they have ontogenetic experience with and those
that are entirely novel, and whether experience with predators
leads to an increased wariness around predator odors in gen-
eral. To do so, we video recorded the behavior of bettongs
with different histories of predator exposure at stations where
food baits were paired with either a predator or control scent.
The olfactory stimuli were sourced from an evolutionary nov-
el introduced predatorcats, a predator with which they share
a deep evolutionary historyTasmanian devils, a novel her-
bivore scentguinea pigs, and a control scent (a towel moist-
ened with deionized water).
We chose to test cat stimuli to examine whether bettongs
could respond to an evolutionary novel predator after 3-year
ontogenetic exposure with the predator. Importantly, from an
applied perspective, predation by cats is implicated in the de-
cline of bettongs and the failure of previous reintroductions
(Short and Turner 2000). The Tasmanian devil scent was cho-
sen to examine if bettongs can generalize anti-predator re-
sponses to an unknown predator after ontogenetic exposure.
This is complicated by the shared deep evolutionary history of
bettongs and Tasmanian devils. However, if we find that
bettongs lost anti-predator responses to Tasmanian devils,
Behav Ecol Sociobiol (2018) 72:151 Page 3 of 10 151
then we can examine their ability to generalize anti-predator
responses.
To examine prey learning and generalization abilities, we
made the following predictions:
If ontogenetic experience influences bettongsability to
discriminate amongst predators and non-predators, we
expect that cat-exposed bettongs display a heightened
anti-predator response to cats compared to herbivore
and control scents, and that control bettongs would not
discriminate between scents.
If bettongs have lost anti-predator responses to
Tasmanian devils after 8000 years of isolation, we would
expect that control bettongs do not discriminate between
Tasmanian devil and control scents.
If bettongs have lost anti-predator responses to
Tasmanian devils, then any heightened response to devil
scent in cat-exposed bettongs implies generalization has
occurred due to ontogenetic exposure to cats. If bettongs
can generalize, we expect that cat-exposed bettongs dis-
play a heightened anti-predator response to both cats and
devils, and that control bettongs do not discriminate be-
tween predator and control scents.
Experimental design
Foraging stations consisted of 100 g of oats evenly distributed
in 500-g soil, and then partially buried, since bettongs dig for
food (Short and Turner 1993). Scent treatments were attached
to stakes and positioned directly behind the food at a distance
of 20 cm. The stations were located every 200 m along vehicle
tracks, 2 m from the tracks. Bettongs have large home ranges,
between 29 and 35 ha dependent on population density
(Finlayson and Moseby 2004), so the placement of stations
along vehicle tracks should collect videos from a representa-
tive sample of the bettong population. The population density
of bettongs in 2016 was estimated to be 19.8/km
2
and 61.7/
km
2
in Red Lake Exclosure and Northern exclosure respec-
tively (Moseby et al. 2018a,b). A random number generator
determined the scent treatment deployed at each station. At
each station, a motion sensor, night-vision camera (Bushnell
BNatureView^, Bushnell BTrophy Cam^, or Scoutguard
BZeroGlow^) was positioned 1 m high on a stake positioned
2 m away from the food bait. Cameras had a 60° field of view;
cameras could monitor the bait from approximately 1 m to the
left or right of the station, 1.5 m in front of the bait station, and
2 m behind the bait, depending on visibility. Bettongsbehav-
ior was recorded from when bettong was within 1 m of the
station. Cameras were programmed to record 60-s length
videos. To reduce the amount of nontarget videos recorded,
motion-triggered recording was set to begin 30 min before
sunset. A lapse of between 0 and 1 s occurred between
consecutive videos, depending on capabilities of the camera
model deployed.
To avoid the effects of habituation to foraging stations,
each station was setup for one night only. A total of 157
stations in Red Lake Exclosure and 122 stations in Northern
Expansion were deployed across nine nights in May 2017.
Not all videos were usable because cameras often failed due
to insufficient battery life, nontarget species consuming the
food before bettongs could forage and/or human error in cam-
era positioning and camera programming. A total of 59 sta-
tions in Red Lake Exclosure and 48 stations in Northern
Expansion were usable and analyzed by Saxon-Mills.
Stimulus preparation
We used cotton towels imbued with body odor because pre-
vious studies have shown that odors sourced from fur and skin
presented a more immediate risk of predation compared to
odors sourced from feces or urine (Apfelbach et al. 2005;
Parsons et al. 2018). Animals used cotton towels as a bedding
material for 2 weeks; after which, we cut the towels into 10×
10-cm pieces, placed them in airtight containers and froze
them at 18 °C until use. We collected guinea pig scents from
four different household pets (two male, two female), cat
scents from five different household pets (three male, two
female), Tasmanian devil scents from two captive bred ani-
mals (both male) and a procedural control treatment (control
scent): a towel moistened with deionized water before
freezing.
Data analysis
In the following data analysis, the two predator-exposure
treatments, cat-exposed bettongs, and control group bettongs
were analyzed separately. This is because we only had one
example of each predator-exposure treatment (our large pad-
docks). Thus, while individuals with a paddock were replicat-
ed, treatments were not formally replicated.
Foraging station avoidance
We compared the number of foraging stations visited and
those that were not visited between scent treatments to ask
whether bettongs avoided stations based on scent treatment.
We used a contingency table to test this hypothesis.
Latency to approach
We calculated the latency to first approach the scent treatment
as the duration of time after sunset that the first bettong visited
the foraging station. Burrowing bettongs are nocturnal, and
are thus active almost exclusively following sunset (Short
and Turner 1993), so time after sunset was deemed an
151 Page 4 of 10 Behav Ecol Sociobiol (2018) 72:151
appropriate analog for latency to investigate. Longer durations
before bettongs investigated predatory scents may indicate
recognition of a potential threat, or increased wariness or
avoidance behaviors (Caro 2005). For latency to approach
calculations, we obtained the time of sunset on each day of
the experiment at Roxby Downs using an online calculator
(Geoscience Australia 2017). We fitted a generalized linear
model for each predatory exposure treatment, with scent type
as a fixed factor, to test if the latency to approach a foraging
station differed between predator and control scents. Because
the response variable (duration of time after sunset) was not
normally distributed, we log10(x) transformed the variable
prior to analysis. Pairwise comparisons were used to analyze
differencesinresponsetoscentsinpredator-exposedandcon-
trol groups.
Approach events
We scored videos using the event recorder BORIS (Friard and
Gamba 2016). To minimize observer bias, blinded methods
were used when behavioral data were scored and analyzed.
Videos with multiple bettongs present were removed from
analysis, to control for the effect that the presence of conspe-
cifics may have on behavior. An ethogram was developed that
focused on movement, foraging, and sniffing (Table 1). We
scored bettongsapproach behavior as events, either fast ap-
proaching or slow approaching. BFast approach^was defined
as when a bettong bipedally hopped towards bait without
pausing. BSlow approach^was categorized as slow
pentapedal movement towards stations, while pausing and
looking around because bettongs, like other macropodids,
use their tail and all four limbs when Bwalking^slowly. We
fitted a binomial logistic distribution to investigate if bettongs
performed approach behaviors as a function of scent
treatment, as bettongs performed either fast or slow approach.
Pairwise comparisons were used to analyze differences be-
tween responses to scents in predator-exposed and control
groups separately. In some instances, approach style was not
captured due to delays in camera recording. Recordings that
showed neither fast nor slow approaches were removed from
this analysis, meaning sample sizes differ from other statistical
tests.
Behavioral response to stimuli
After scoring the behaviors of the first minute of a bettong in
sight, we calculated the proportion of time in sight allocated to
behaviors and combined them into three categories (Table 1).
BOlfactory investigation^was comprised of any sniffing be-
havior, including quadrupedal and bipedal sniffing and olfac-
tory investigation of scent. BForaging^included both foraging
with head raised and foraging with head down. BMovement^
included locomotion that occurred following the initial ap-
proach, which includes fast lateral movement, fast escape,
and slow retreat.
We fitted generalized linear mixed models to investigate if
bettongs allocated different amounts of time (proportion of
time in sight) to behaviors as a function of scent treatment in
each of the two paddocks, separately. We fitted models for the
dependent variables, proportion of time in sight engaged in
olfactory investigation, foraging, and movement. Because the
response variables were not normally distributed and the
dataset contained many zero values, we log10(x+ 1) trans-
formed each variable prior to analysis. Pairwise comparisons
were used to analyze differences between bettongsresponses
towards scents in predator-exposed and control groups.
Statistical analysis was conducted using IBM SPSS Statistics
(IBM corp 2014). We set our alpha to 0.05 for all tests.
Table 1 Ethogram of burrowing bettongs visiting food baits, indicating the type of behavior and the categories used for analysis
Type Behavior Description Category Vigilance category
Event Fast approach Rapidly hop bipedally towards bait without pausing Fast approach Low vigilance
Event Slow approach Slow pentapedal movement towards bait, while pausing
and looking around
Slow approach High vigilance
State Fast escape Run quickly away from bait Movement High vigilance
State Slow retreat Move slowly away from bait Movement Low vigilance
State Fast lateral movement Rapid movement neither towards nor away from bait Movement Low vigilance
State Quadrupedal sniff On all fours sniffing Olfactory investigation High vigilance
State Bipedal sniff Stand on back legs sniffing Olfactory investigation High vigilance
State Foraging head down Head down and feeding Foraging Low vigilance
State Foraging head up Head up while chewing Foraging High vigilance
State Vigilant interaction with scent Interacting with scent while sniffing and looking Olfactory investigation High vigilance
State Relaxed interaction with scent Interacting with scent without sniffing and looking, includes
consuming the scent bait
Olfactory investigation Low vigilance
State Out of sight Out of camera range Other Other
Behav Ecol Sociobiol (2018) 72:151 Page 5 of 10 151
Data availability The datasets generated during and analyzed
during the current study are available in the Figshare reposi-
tory, https://doi.org/10.6084/m9.figshare.5649247.v1.
Results
Foraging station avoidance
Neither control group bettongs (χ
2
=1.941,df=3,P=0.585)
nor cat-exposed bettongs (χ
2
= 2.402, df = 3, P= 0.493)
avoided foraging stations based on scent treatment type
(Table 2).
Latency to approach
Control bettongs did not modify their latency to approach as a
function of scent type (F=0.198, df=3,P= 0.978; Fig. 1a).
Cat-exposed bettongs modified their latency to approach sta-
tions as a function of scent type (F= 8.112, df = 3, P=0.044;
Fig. 1b). Pairwise comparisons revealed that the latency to
approach the unscented control treatment was significantly
different from that of cat (FishersLSD,P= 0.006), guinea
pig (Fishers LSD, P=0.045), and Tasmanian devil (Fishers
LSD, P=0.040) scents, with control scents having a shorter
period of latency (Fig. 1b).
Approach behavior
Control group bettongs did not differ in their use of fast and
slow approaches across scent treatments (χ
2
=3.683, df=3,
P= 0.298; Fig. 2a). Cat-exposed bettongs showed differences
in the proportion of animals engaging in fast or slow ap-
proaches between scent treatments (χ
2
= 24.583, df = 3,
P< 0.001; Fig. 2b). Pairwise comparisons revealed that re-
sponses to cat and Tasmanian devil scents differed from con-
trol (FishersLSD,P< 0.001) and guinea pig (FishersLSD,
P= 0.001) scents. A higher proportion of cat-exposed
bettongs approached cat and Tasmanian devil scents slowly
compared to control and guinea pig scent. Additionally, cat-
exposed bettongs only fast approached in the presence of con-
trol and guinea pig scent treatments (Fig. 2b).
Behavioral response to stimuli
Both control and cat-exposed bettongs ate from all scent treat-
ments. Control group bettongs did not allocate time differently
as a function of scent treatment for olfactory investigation
(F= 0.499, df = 3, P= 0919; Fig. 3a), foraging (F= 0.671,
df = 3, P= 0.890; Fig. 3c), or movement after approach (F=
2.525, df = 3, P= 0.471; Fig. 3e). Similarly, cat-exposed
bettongs showed no difference in the proportion of time spent
in olfactory investigation (F=1.962, df=3, P=0.580;
Fig. 3b), foraging (F=0.040,df=3,P= 0.998; Fig. 3d), and
movement after approach (F= 0.105, df = 3, P= 0.991;
Fig. 3f) across treatments.
Discussion
Bettongs with no ontogenetic experience with mammalian
predators did not discriminate between stations with odors of
predators and either stations with odors of herbivores or with
the procedural control. These results suggest that predator-
naïve bettongs do not respond to predator odors. In contrast,
cat-exposed bettongs increased their latency to approach in the
presence of predator and herbivore odors but not a procedural
control. Bettongs also approached stations slowly and cau-
tiously more often in the presence of predatory odors than
the odors of a novel herbivore or a procedural control. These
results suggest that cat-exposed bettongs were more wary in
the presence of novel odors and assess the odors of predators
as threatening. Interestingly, cat-exposed bettongs responded
similarly to a predator with which they have exposure too,
cats, and one that they have no experience with for the past
8000 years, Tasmanian devils. The employment of anti-
predator responses to both cat and Tasmanian devil odors
suggests that bettongs have the ability to generalize anti-
predator responses amongst at least a subset of their predators.
Cat-exposed bettongs took longer to approach in the pres-
ence of animal scents, whereas control bettongs did not alter
latency to approach as a function of scent treatment. Greater
latency to approach foraging stations with animal scents sug-
gests that cat-exposed bettongs avoid areas with a novel odor,
which may be adaptive because it reduces that potential for
encountering a high-risk situation. Avoiding areas of risk
Table 2 Counts of foraging
stations that were visited and not
visited in control and cat-exposed
groups. Counts of visited stations
reflect stations where videos of
bettongs were recorded, and
counts of stations not visited
represent stations where no
videos of bettongs were recorded
Control group Cat-exposed group
Scent treatment Approached station No visitation Approached station No visitation
Cat 15 3 14 3
Control 20 3 10 7
Guinea pig 13 4 15 6
Tasmanian devil 11 4 9 3
151 Page 6 of 10 Behav Ecol Sociobiol (2018) 72:151
should have the greatest influence on the outcome of predator-
prey interactions, because avoiding predators before direct
contact reduces the number of encounters with predators
(Lima and Dill 1990).
Many animal species exhibit heightened vigilance in re-
sponse to predator odors and allocate more time towards
sniffing, scanning, and escaping behaviors at the expense of
foraging (Caro 2005). Our results provide no evidence that
bettongs allocated more time to vigilance activities in re-
sponse to encountering predator scents once they approached
the foraging station. However, cat-exposed bettongs were
more likely to approach foraging trays slowly and cautiously
in the presence of predatorsscents, and only approached
quickly in the presence of herbivore and control scents. Such
cautious approach may provide bettongs with more time to
assess the true risk of predation (FitzGibbon 1994).
Inspecting predatory cues appears counterintuitive for prey,
as the risk of predation increases as prey approach predatory
threats (Fishman 1999). However, predator inspection can
provide benefits to prey species which may include acquiring
more information on the nature of the potential threat,
informing conspecifics of the potential threat, deterring pred-
ator attack, and advertising quality to mates (Parsons et al.
2018). Prey can minimize costs due to lost opportunities to
forage and reproduce by inspecting predator cues before
employing anti-predator behaviors (Fishman 1999). Our re-
sults are consistent with the theory that prey recognize preda-
tory odors and inspect them to acquire more information on
the nature of the potential threat (Parsons et al. 2018).
Control bettongs did not inspect or employ other anti-
predator responses in the presence of predatory odors includ-
ing Tasmanian devils, a predator with which they share deep
evolutionary history but have been isolated from for
8000 years. These findings suggest that bettongsisolation
from predators has resulted in the loss of anti-predator behav-
ior. Such loss of anti-predatory behavior could be lost due to
the absence of selection by predators or indeed be selected
against (Blumstein 2002). Populations that occur in
predator-free environments often occur at high densities and
are limited the availability of food resources (Alder and
Levins 1994). In such environments, with intense intra-
specific competition for food resources, it is conceivable that
anti-predator behaviors may be lost due to strong selection
against missed opportunity costs arising from engaging in
unnecessary anti-predator behavior (Novosolov et al. 2013).
Cat-exposed bettongs seemingly identified both cats and
Tasmanian devils as predatory threats and responded similarly
to their odors. Taken together, these findings suggest that the
Fig. 1 Average latency to approach stations (minutes after sunset) (±
1 SE) in acontrol (cats n= 10, procedural control n= 14, guinea pig
n= 9, and Tasmanian devil n=5) and bcat-exposed (cats n= 14,
procedural control n= 9, guinea pig n= 11, and Tasmanian devil n=8)
bettongs. Similar letters above bars identify statistically indistinguishable
(P> 0.05) pairwise differences
Fig. 2 Proportion of acontrol (cats n= 9, procedural control n= 10,
guinea pig n= 4, and Tasmanian devil n=3) and bcat-exposed (cats
n= 11, procedural control n= 8, guinea pig n= 9, and Tasmanian devil
n= 5) bettongs engaged in fast and slow approach behaviors in response
to the deployment of predatory and control olfactory stimuli. Similar
letters (e.g., a and b) above bars identify statistically indistinguishable
(P> 0.05) pairwise differences
Behav Ecol Sociobiol (2018) 72:151 Page 7 of 10 151
responses of cat-exposed bettongs to Tasmanian devil scent
were due to the generalization of responses from cats to
Tasmanian devils, as a result of cat exposure. At a proximate
level, this observation is consistent with the Bcommon constit-
uents hypothesis,^whereby chemical compounds that are
commonly present in predator odors cause prey to respond
similarly to known and novel predatory scents (Nolte et al.
1994; Ferrero et al. 2011; Osada et al. 2015). However, the
common constituents hypothesis implicitly assumes that this
recognition of predatory odors, based on these common con-
stituents, is innate, but control group bettongs did not innately
discriminate amongst predatory odors. Therefore, the com-
mon constituents hypothesis does not account for the apparent
recognition of predatory cues demonstrated by cat-exposed
bettongs, as control group bettongs did not innately recognize
predatory odors.
Our study has implications for reintroduction of threatened
vertebrates because it demonstrates that pre-release exposure
to low levels of controlled predation can alter the expression
of anti-predator behaviors in predator-naïve prey (Moseby
et al. 2015a). Previous studies have shown that development
of observable anti-predator behaviors was associated with im-
proved post-release survival of houbara bustards (Van Heezik
et al. 1999) but not black-footed ferrets (Mustela nigripes,
Biggins et al. 1999). However, it is important to note, that
our study focused on behavioral responses in the face of
Fig. 3 Average proportion of time (± 1 SE) control (cats n=15,
procedural control n= 20, guinea pig n= 13, and Tasmanian devil n=
11) and cat-exposed (cats n= 14, procedural control n= 10, guinea pig
n= 15, and Tasmanian devil n= 9) bettongs spent engaged in a,b
olfactory investigation, c,dforaging, and e,fmovement after approach
in response to the deployment of predatory and control olfactory stimuli.
Similar letters above bars identify statistically indistinguishable
(P> 0.05) pairwise differences
151 Page 8 of 10 Behav Ecol Sociobiol (2018) 72:151
potential predatory threats, and thus does not show that expo-
sure to cats actually improves the survival of bettongs
reintroduced to predator-rich environments. To do the latter
would require conducting releases of cat-exposed and preda-
tor-naïve bettongs into a common environment with predators
and monitoring their survival. We recommend that further
research is conducted to determine if behavioral responses
towards predators brought about by predator exposure trans-
late to enhanced survival of reintroduced prey.
Acknowledgments We thank the Arid Recovery staff and volunteers for
their help with this study. We thank the two anonymous reviewers whose
comments and suggestions helped improve and clarify this manuscript.
Funding Funding for this project was provided by the Australian
Research Council.
Compliance with ethical standards
Conflict of interest The authors declare that they have no competing
interests.
Ethical approval All applicable international, national, and/or institu-
tional guidelines for the care and use of animals were followed. The work
was conducted under the UNSWanimal ethics (APEC Approval 15/19A)
and in accordance with The Australian Code of Practice for the Care and
Use of Animals for Scientific Purposes (1997).
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Background Mammals, globally, are facing population declines. Strategies increasingly employed to recover threatened mammal populations include protecting populations inside predator-free havens, and translocating animals from one site to another, or from a captive breeding program. These approaches can expose predator-naïve animals to predators they have never encountered and as a result, many conservation projects have failed due to the predation of individuals that lacked appropriate anti-predator responses. Hence robust ways to measure anti-predator responses are urgently needed to help identify naïve populations at risk, to select appropriate animals for translocation, and to monitor managed populations for trait change. Here, we outline a protocol for a systematic review that collates existing behavioural assays developed for the purpose of quantifying anti-predator responses, and identifies assay types and predator cues that provoke the greatest behavioural responses. Methods We will retrieve articles from academic bibliographic databases and grey literature sources (such as government and conservation management reports), using a Boolean search string. Each article will be screened for the satisfaction of eligibility criteria determined using the PICO (Population—Intervention—Comparator—Outcome) framework, to yield the final article pool. Using metadata extracted from each article, we will map all known behavioural assays for quantifying anti-predator responses in mammals and will then examine the context in which each assay has been implemented (e.g. species tested, predator cue characteristics). Finally, with mixed effects modelling, we will determine which of these assays and predator cue types elicit the greatest behavioural responses (standardised difference in response between treatment and control groups). The final review will highlight the most robust methodology, will reveal promising techniques on which to focus future assay development, and will collate relevant information for conservation managers.
... Here we extend our knowledge of the factors influencing mortality from predation after release by testing the relative contribution of individual attributes and the efficacy of prerelease 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, exclosures for several years were more wary than cat-na€ ıve bettongs (Saxon-Mills et al. 2018;West et al. 2018b) and had longer hind feet . Because these traits might be expected to influence bettongs' ability to avoid or escape predation by cats, they may also improve post-release survival of reintroduced bettongs. ...
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... Predator-proof fencing may be required until the releases develop appropriate fear/avoidance responses. Before wild release, MPPs could also undergo training to enhance fear of carnivores, a strategy that appears to be at least partially successful in relation to translocation of other marsupials [73]. ...
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The fossil record provides important information about changes in species diversity, distribution, habitat and abundance through time. As we understand more about these changes, it becomes possible to envisage a wider range of options for translocations in a world where sustainability of habitats is under increasing threat. The Critically Endangered alpine/subalpine mountain pygmy-possum, Burramys parvus (Marsupialia, Burramyidae), is threatened by global heating. Using conventional strategies, there would be no viable pathway for stopping this iconic marsupial from becoming extinct. The fossil record, however, has inspired an innovative strategy for saving this species. This lineage has been represented over 25 Myr by a series of species always inhabiting lowland, wet forest palaeocommunities. These fossil deposits have been found in what is now the Tirari Desert, South Australia (24 Ma), savannah woodlands of the Riversleigh World Heritage Area, Queensland (approx. 24–15 Ma) and savannah grasslands of Hamilton, Victoria (approx. 4 Ma). This palaeoecological record has led to the proposal overviewed here to construct a lowland breeding facility with the goal of monitoring the outcome of introducing this possum back into the pre-Quaternary core habitat for the lineage. If this project succeeds, similar approaches could be considered for other climate-change-threatened Australian species such as the southern corroboree frog ( Pseudophryne corroboree ) and the western swamp tortoise ( Pseudemydura umbrina ). This article is part of a discussion meeting issue ‘The past is a foreign country: how much can the fossil record actually inform conservation?’
... The introduction of a novel predator in an area can have a significant impact on prey species, particularly if prey species do not respond appropriately to novel predator cues, or if there is a learning period (Dunlop-Hayden and Rehage, 2011; Polo-Cavia and Gomez-Mestre, 2014; Carthey et al., 2017). Given that in a previous study (submitted) in the same system novel predator visual cues influenced the incidence of prey species (incidence was more strongly predicted by familiar predator cue presence), we predicted that ungulates might similarly respond less strongly behaviourally to cues from a novel predator (Amur tiger) than to cues from a familiar one (brown bear) (Smith et al., 2008;Saxon-Mills et al., 2018). However, our results show no difference in the amount of time spent vigilant or feeding between the two predator cues treatments (tiger and bear visual cues), i.e., ungulates showed the same lack of response to both novel and familiar predator cues. ...
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With an increasing human population and expansion of urban settlements, wild animals are often exposed to humans. As humans may be a threat, a neutral presence or a source of food, animals will benefit from continuously assessing the potential risk they pose in order to respond appropriately. Herring gulls, Larus argentatus, are increasingly breeding and foraging in urban areas, and thus have many opportunities to interact with humans. We recently found that herring gulls take longer to approach food when being watched by a human. However, it is not known whether aversion to human gaze arises from experience with humans, and whether individual differences in responsiveness are a result of differential exposure. Here, we tested whether herring gulls' responses to human gaze differ according to their age class and urbanization of their habitat. We measured the gulls' flight initiation distance when an experimenter approached with either a direct or an averted gaze. Neither gull age class nor urbanization significantly influenced the effect of human gaze on flight initiation distance. However, as recently fledged juveniles responded strongly to the experimenter's gaze, aversion to human gaze may not require extensive exposure to humans to develop. Gulls in urban areas could be approached more closely than those in rural areas, consistent with findings in other species. These results indicate that gaze aversion is present early in development and that exposure to humans may influence gulls' responses to perceived risk from humans. Investigating the processes generating individual differences in responses to humans will provide further insights into human–wildlife interactions and the effects of urbanization.
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We report first-year survival for 34 captive-reared Puerto Rican Parrots (Amazona vittata) released in the Caribbean National Forest, Puerto Rico between 2000 and 2002. The purpose of the releases were to increase population size and the potential number of breeding individuals of the sole extant wild population, and to refine release protocols for eventual reintroduction of a second wild population elsewhere on the island. After extensive prerelease training, we released 10 parrots in 2000, 16 parrots in 2001, and eight parrots in 2002 ranging in age from 1–4 years old. All birds were equipped with radio-transmitters to monitor survival. The overall first-year survival estimate for the 34 parrots was 41% (CI = 22%–61%). Only one parrot died within the first week postrelease, with most (94%) surviving for at least eight weeks after release. Most (54%) documented mortalities were due to raptor predation, which claimed 21% of all released parrots. A captive-reared bird (male, age one), released in 2001, paired with a wild female and fledged two young in 2004. We also calculated survival based on 0% and 50% of observed predation losses and found hypothetical survival rates of 72% and 54%, respectively. Rigorous prerelease training and acclimation was believed to have improved initial postrelease parrot survival, and releasing mixed age-class groups suggests the potential for shortening the time to recruitment. Supervivencia de Individuos de Amazona vittata Criados en Cautiverio y Liberados en el Bosque Nacional del Caribe Resumen. Determinamos la supervivencia de 34 individuos de cotorras Amazona vittata criados en cautiverio y liberados en el Bosque Nacional del Caribe, Puerto Rico entre el 2000 y el 2002. El propósito de las liberaciones era aumentar el tamaño de la población y el número potencial de individuos reproductores en la única población silvestre remanente, y refinar los protocolos de liberación para eventualmente establecer una segunda población silvestre en la isla. Después de un adiestramiento extensivo, liberamos 10 cotorras en el 2000, 16 cotorras en el 2001, y ocho cotorras en el 2002 fluctuando en edades entre uno y cuatro años. Cada individuo se liberó con un radio transmisor para determinar su supervivencia. La tasa general de supervivencia para 34 cotorras después de un año fue de 41% (IC = 22–61%). Sólo una cotorra murió durante la primera semana post-liberación, con la mayoría (94%) sobreviviendo por lo menos ocho semanas después de liberadas. La mayoría (54%) de la mortandad se debió a la depredación por aves rapaces, la que reclamó 21% de todas las cotorras liberadas. Una cotorra criada en cautiverio (macho, un año de edad), y liberada en el 2001, se apareó con una hembra silvestre y produjeron dos volantones en el 2004. Reduciendo la mortandad por aves rapaces informada en este estudio en un 100%, o en un 50%, resultó en tasas hipotéticas de supervivencia del 72% y 54%, respectivamente. Creemos que el adiestramiento y la aclimatación rigurosa pre-liberación mejoraron la supervivencia inicial post-liberación, y que la liberación de grupos de cotorras de edades mixtas sugiere el potencial de acortar el tiempo de reclutamiento.
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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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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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Burrowing bettings Bettongia lesueur and golden bandicoots Isoodon auratus were reintroduced from an island off the NW coast of Western Australia to the Gibson Desert on the Australian mainland. Both species quickly adapted to their new mainland habitat and had gained weight within a few weeks. The golden bandicoots also bred well. Measures to control introduced predators successfully reduced dingo Canis familiaris dingo and fox Vulpes vulpes numbers but resulted in increased numbers of feral cats Felis catus. The reintroduced species showed different biological and behavioural traits affecting their vulnerability to predation. Betongs were highly vulnerable to predation by feral cats so it will be difficult to establish this species, and others with similar traits, in the presence of anything but extremely low densities of introduced predators. Golden bandicoots were less vulnerable to predation so it should be possible to establish viable populations of this species in the arid zone, providing introduced predator numbers are significantly reduced and animals are released into areas of optimum habitat. -from Authors
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The failure of broadscale management to protect some threatened species has led to an increase in the use of islands and fenced reserves as translocation sites or foci for intensive threat mitigation. Although highly successful at excluding some threats, these sites may be prone to ecosystem imbalance due to the absence or removal of predators and competitors. We documented population trends and environmental impacts of the burrowing bettong, (Bettongia lesueur), a threatened herbivorous macropod reintroduced to a 1400 ha fenced reserve in arid Australia for 17 years after release. The population increased from 30 individuals to an estimated 1532 individuals (1.09 per ha), a density up to ten times higher than wild populations. There was little evidence that population growth was density dependent, the average intrinsic rate of increase (r) was 0.125 and population size was unrelated to rainfall, body condition or reproductive output. Browse damage on palatable plant species increased, and cover of palatable shrub species decreased, with increased abundance of bettongs. Activity of another reintroduced herbivore, the greater stick-nest rat, (Leporillus conditor), declined as bettong abundance increased while a reintroduced species not reliant on herbage was unaffected. The burrowing bettong has been successfully reintroduced to the Arid Recovery fenced reserve but the positive average intrinsic rate of increase, inflated population density and impacts to resident plant and animal species suggests the population is now overabundant. This is the first documented case of overpopulation of a reintroduced species at a restricted site in Australia, highlighting the importance of preparing overpopulation management plans and considering reintroductions of species from all trophic levels including native predators.
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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.