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\begin{document}

\title{Trophic cascade driven by behavioural fine-tuning as na\selectlanguage{ngerman}ïve prey rapidly
adjust to a novel predator\selectlanguage{english}}



\author[1]{Chris Jolly}%
\author[2]{Adam Smart}%
\author[3]{John Moreen}%
\author[4]{Jonathan Webb}%
\author[5]{Graeme Gillespie}%
\author[6,6]{Ben Phillips}%
\affil[1]{University of Melbourne School of BioSciences}%
\affil[2]{The University of Melbourne}%
\affil[3]{Kenbi Rangers}%
\affil[4]{University of Technology Sydney}%
\affil[5]{Northern Territory Government of Australia}%
\affil[6]{University of Melbourne}%


\vspace{-1em}



  
  \date{May 25, 2024}


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\selectlanguage{english}
\begin{abstract}
The arrival of novel predators can trigger trophic cascades driven by
shifts in prey numbers. Predators also elicit behavioural change in prey
populations, and this may also contribute to trophic cascades. We
document rapid demographic and behavioural changes in rodent populations
(grassland melomys) following the introduction of an ecologically novel
predator (northern quoll). Within months, melomys from quoll-invaded
populations suffered reduced survival relative to quoll-free
populations. They also exhibited increased shyness which became
fine-tuned to more threat-specific antipredator behaviour. These
behavioural shifts were associated with lower per-capita seed take, and
avoidance of quoll-scented seeds. These behavioural shifts could reflect
phenotypic plasticity or may be adaptive responses to selection imposed
by predation. Overall, our study reveals rapid numerical and behavioural
shifts in response to a novel predator and shows that both behavioural
and numerical responses can drive trophic cascades.%
\end{abstract}%



\sloppy


\textbf{}

\textbf{}

\textbf{INTRODUCTION}

Predation is one of the most pervasive and powerful forces acting on
populations. Not only does predation directly impact a population's
demography (Schoener \& Spiller 1996), it also imposes natural selection
(Abrams 2000). The pressure that predators impose on populations will
vary through time and space for many reasons, including tightly coupled
predator-prey dynamics, predator movement, prey switching, or stochastic
processes (Lima \& Dill 1990; Sih 1992). The fact that predation is not
constant, and that antipredator defences may be costly, suggests that
flexible responses to predation pressure will often be favoured
(Sih\emph{et al.} 2000; Berger \emph{et al.} 2001). There is, in fact, a
great deal of empirical evidence that flexible responses to predation
are common and vary with the perceived risk of predation (e.g. Relyea
2003; Brown \emph{et al.} 2013; Cunningham \emph{et al.} 2019).

Predators also play a powerful role in structuring communities
(Estes\emph{et al.} 2011). Some of our best evidence for this comes from
the introduction of novel predators. Invasive predators can cause
extinctions (Medina \emph{et al.} 2011; Woinarski \emph{et al.} 2015;
Doherty \emph{et al.} 2016), and alter trophic structures and ecosystem
function within recipient communities (Courchamp \emph{et al.} 2003;
Simberloff \emph{et al.} 2013). These cascading outcomes are often
treated as purely numeric effects: predators depress the size of prey
populations, and the altered numbers of prey can cause cascading
numerical changes down trophic levels (Ripple \emph{et al.} 2001). These
numerical effects are undeniably important, but the fact that predators
can also elicit phenotypic change in prey populations---through
phenotypic plasticity and natural selection---means that subtler
ecological effects may also manifest. Prey species living alongside
predators may forage at different times, or in different places compared
with the same species in a predator-free environment (Laundre \emph{et
al.} 2010). Such behavioural shifts can alter downstream species
interactions in potentially complex ways (Fortin \emph{et al.} 2005;
Suraci \emph{et al.} 2016).

Because predator invasions are rarely intentional or anticipated, there
is a scarcity of controlled empirical work on the effects of novel
predators on recipient communities and the mechanisms via which these
effects play out (but see Lapiedra \emph{et al.} 2018; Pringle \emph{et
al.} 2019). Such tests are needed, however, if we are to predict
invasive species impacts, and improve both conservation management
(Sih\emph{et al.} 2010a) and our understanding of how communities are
structured (Sax \emph{et al.} 2007).

Northern quolls (\emph{Dasyurus hallucatus} ) were, until recently, a
common predator across northern Australia. They have declined over the
last several decades, following the general decline in northern
Australian mammals (Woinarski \emph{et al.} 2015)(Braithwaite \&
Griffiths 1994). More recently, the invasion of toxic invasive prey
(cane toads, \emph{Rhinella marina} ) has resulted in dramatic,
range-wide population declines in northern quolls (Shine 2010;
Oakwood\emph{et al.} 2016)(Moore \emph{et al.} 2019). For their
conservation, northern quolls have recently been introduced to a number
of offshore islands where they have never previously existed.

In 2017, a population of 54 northern quolls were introduced to a
25km\textsuperscript{2} island off the coast of north-western Northern
Territory, Australia (Kelly 2019). Prior to this introduction, Indian
Island (Kabarl) lacked mammalian predators, and large native reptilian
predators had recently been reduced to near extinction by the invasion
of cane toads. We take advantage of the introduction of northern quolls
to a new island to directly test the effects of quolls as a novel
predator on an island ecosystem and observe how native prey populations
adjust to mitigate the impacts of their arrival. Since quolls are an
ecologically novel predator on this island, we predict that this
introduction may result in demographic effects (reduced survival and
abundance) in invaded prey populations. If behavioural adjustments are
able to reduce the demographic effects of a novel predator, we predict
rapid behavioural changes in quoll-exposed melomys populations, such as
changes in personality composition, foraging behaviour and responses to
predator-scent, may manifest through time.

\textbf{METHODS}

\emph{Introduction of northern quolls}

In May 2017, 54 adult northern quolls were introduced to the
north-eastern tip of Indian Island, Bynoe Harbor, Northern Territory,
Australia (12\selectlanguage{ngerman}°37'24.60''S, 130°30'0.72''E) to field test the
conservation strategy of targeted gene flow (Kelly \& Phillips 2016).
Quolls are a voracious, opportunistic generalist predator (\textless{}
1.5k g; Oakwood 1997), and their introduction presented an opportunity
to monitor the behavioural and demographic impacts on grassland melomys
(\emph{Melomys burtoni} ), a native mammalian granivorous prey species
(mean body mass 56 g, 5.6--103.7 g). Logistical challenges prevented us
from implementing a Before-After Impact-Control study design (see
Supporting Information). Here, we present data from before the
introduction of quolls from one invaded site only. Most of our data
compare quoll-invaded (impact) versus quoll-free (control) sites over
time, commencing within a few months of quoll arrival.

\emph{Melomys population monitoring}

To determine whether the arrival of a novel predator resulted in
demographic impacts (population size and survival) to a native prey
species, we monitored four ``impact'', quoll-invaded sites established
in the north of Indian island in the vicinity of where quolls were
released and three ``control'', quoll-free sites established in the
south of the island (Fig. 1). Populations of melomys on Indian Island
were monitored during four trips occurring immediately prior to the
introduction of quolls in May (site 1) 2017, and after the introduction
of quolls August 2017 (sites 2--7), April 2018 (sites 1--7), and May
2019 (sites 1--7).

\textbf{Hosted file}

\verb`image1.emf`  available at \url{https://authorea.com/users/349935/articles/474906-trophic-cascade-driven-by-behavioural-fine-tuning-as-na%C3%AFve-prey-rapidly-adjust-to-a-novel-predator}

\textbf{Figure 1.} Map showing the arrangement of grassland melomys
(Melomys burtoni) monitoring sites on Indian Island, Northern Territory,
Australia. Quolls were present at the four monitoring sites in the north
of the island and quolls were absent from the three monitoring sites in
the south of the island for the duration of the study.

Melomys were monitored at seven independent 1ha (100 m x 100 m) plots
(sites 1--7) spread out across Indian Island using a standard
mark-recapture trapping regime designed for a monitoring project
(Begg\emph{et al.} 1983; Kemper \emph{et al.} 1987). Sites in the north
(quoll-invaded) and south (quoll-free) of the island were between 8.7
and 9.8km apart (Fig. 1; Table S1) and were composed of similar habitat
types. The northern and southern sections of Indian Island are divided
by mangrove habitat which is inundated at high tide. Cage and camera
trapping as well as track surveys confirmed that quolls were present at
the ``impact'' sites and absent from the ``control'' sites for the
duration of the study (Jolly \emph{et al.} unpub. data).

Each of the seven monitoring sites consisted of 100 Elliott traps
(Elliott Scientific Equipment, Upwey, Victoria) spaced at 10 m intervals
in a 10 x 10 grid. Most trapping grids were open for four nights,
however, the first trapping grid (site 1, May 2017) was open for six
nights. After four trap nights, the majority of the melomys population
had been captured at least once (Jolly \emph{et al.} 2019). Traps were
baited with balls of peanut butter, rolled oats and honey. These baits
were replaced daily for the duration of each trapping session. Traps
were checked for captures early each morning and all traps were cleared
within two hours of sunrise.

Captured melomys were weighed (g) and sexed. Before release, each
melomys was implanted with a microchip (Trovan Unique ID100). On
successive mornings, all melomys were scanned (Trovan LID575 Handheld
Reader), and any new individuals were microchipped. On the last morning
of each trapping session, all melomys caught were retained for
behavioural assays. Throughout the study 439 individual melomys were
captured and given microchips (melomys caught per site: site 1 = 83;
site 2 = 52; site 3 = 63; site 4 = 59; site 5 = 69; site 6 = 59; and
site 7 = 54). Of these, 146 (33\%) were caught on the final night of
trapping and were retained for behavioural trials. Only large, healthy
juveniles (\emph{n} = 11), adult males (\emph{n} = 58), and adult
non-visibly pregnant females (\emph{n} = 77) were retained for
behavioural experiments. Melomys were retained in their respective
Elliott traps and taken to the field station for diurnal husbandry. They
were provided food and water \emph{ad libitum} until 2 hours prior to
testing. At this point, in an attempt to standardise hunger levels,
access to food and water was removed. Indian Island is remote and
uninhabited by humans, so all behavioural experiments were conducted in
the field under near natural conditions (see Jolly \emph{et al.} 2019
for detailed experimental procedures).

\emph{Modified open field tests}

We employed modified open field tests (also referred to as emergence
tests: see Brown \& Braithwaite 2004; López \emph{et al.} 2005;
Carter\emph{et al.} 2013; Jolly \emph{et al.} 2019) to assess boldness
in grassland melomys and whether the arrival of a novel predator
resulted in behavioural shifts in invaded populations. All open field
tests were conducted on the night after the last trap night (night 5)
and in opaque-walled experimental arenas (540mm x 340mm x 370mm).
Experimental arenas were modified plastic boxes that had an inverted
Elliott trap sized hole cut in one end and were illuminated by strings
of red LED lights (Jolly \emph{et al.} 2019). Each experimental arena
had natural sand as substrate, and a rolled ball of universal bait
(peanut butter, oats and honey) located both in the centre and along one
wall of the arena (Jolly \emph{et al.} 2019). After dark, Elliott traps
containing a melomys were inserted into the hole in the side of each
experimental arena and melomys were allowed to habituate for 10 min. At
the start of each trial, Elliott trap doors were locked open---the
inverted orientation of the trap prevented them from being triggered
closed. Melomys were given 10 min to explore the open field arena. After
10 min, individuals were rounded back into their retreat (the Elliott
trap) and a novel object (standard red, plastic disposable bowl) was
placed at the end of the arena opposite the Elliott trap (Jolly \emph{et
al.} 2019). Melomys were then given a further 10 min to explore the
arena and interact with the novel object. Elliott traps remained open
during the open field tests and melomys could shelter and emerge from
them under their own volition. All trials were recorded using a GoPro
HERO 3. A previous study in this system determined that melomys showed
repeatable behaviour between trials (boldness: \emph{R} {[}± 95\%CI{]} =
0.67 {[}0.47, 0.80{]}, \emph{P} \textless{} 0.001; emergence time:
\emph{R}{[}± 95\%CI{]} = 0.73 {[}0.53, 0.83{]}, \emph{P} \textless{}
0.001; novel object: \emph{R} {[}± 95\%CI{]} = 0.61 {[}0.209,
0.974{]},\emph{P} \textless{} 0.001; Jolly \emph{et al.} 2019),
therefore the data presented in this study were from a single
behavioural trial of each animal (\emph{n} = 146). Once trials were
complete, each melomys was released at its point of capture.

To measure the boldness of individual melomys, we scored three
behaviours typically associated with boldness and neophobia in rodents
(Dielenberg \& McGregor 2001; McGregor \emph{et al.} 2002; Réale\emph{et
al.} 2007; Cremona \emph{et al.} 2015): whether melomys fully emerged
from their Elliott trap hide and entered the open arena during the 0--10
min period (scored 0 or 1, respectively); whether they fully emerged and
entered the trial arena during the 10--20 min period (scored 0 or 1);
and whether they interacted (touched) with the novel object that was
placed in the arena during the 10--20 min period (scored 0 or 1). Videos
were scored by a single observer who was blind to each melomys' origin
and identity. Because interacting with the novel object was predicated
on a melomys' willingness to emerge from their hide during the 10--20
min period, for analysis we combined their emergence during this period
and interaction with the novel object into a single binary score: 0
(neophobic) = did not emerge or emerged but did not interact with novel
object; or 1 (not neophobic): emerged and interacted with novel object.

\emph{Seed removal plots}

To assess whether the arrival of a novel predator affected the seed
harvesting behaviour of granivorous melomys, we established seed removal
plots at each site and sampled them each trapping session (night 6).
After trapping and open field tests were conducted and melomys had been
returned to their capture location, we set up 81 seed plots at each site
by scraping away leaf litter with a shovel to create bare earth plots.
These bare earth plots were created so that they were located in the
centre between four Elliott traps within the 10x10 trapping grid. All
seed plots were located randomly with respect to ``distances to cover''
but were all located on relatively open patches of ground. Sufficient
within site replication (\emph{n} = 81) significantly reduces the
likelihood of distance to cover biasing population-level responses to
seeds. Just before dark on the night of the seed removal experiment, we
placed a single wheat seed in the centre of each bare earth plot. These
seeds were either unscented, control seeds (\emph{n} = 40) or
predator-scented seeds that had been maintained in a sealed clip-lock
bag filled with freshly collected northern quoll fur (\emph{n} = 41).
The placement of predator-scented and unscented seeds was alternated so
that there was a chequered arrangement of scented and unscented seeds
across the site. To ensure that the predator-scent was strong enough to
be detected by melomys, along with the predator-scented seeds, we also
placed a few strands of quoll fur around the predator-scented seeds.
Before light the next morning, we returned back to each plot and counted
the number of seeds of each scent-type that were removed from the plot.
Melomys are the only nocturnal granivorous animal that occurs on Indian
Island, and to avoid diurnal granivorous birds from removing seeds we
conducted this experiment during the night only.

\emph{Wildfire on northern Indian Island}

Immediately following our monitoring and experiments in August 2017, a
wildlife broke out on northern Indian Island in the vicinity of the four
quoll-invaded sites and burnt through all of the sites. Because of this,
our experimental design is confounded by the fact that all of our
quoll-invaded sites were burnt, and all of our quoll-free sites were
unburnt. Fire is a regular disturbance in this landscape
(Andersen\emph{et al.} 2005), and previous work has shown little effect
of fire on abundance, survival or recruitment of grassland melomys
(Griffiths \& Brook 2015; Liedloff \emph{et al.} 2018). Nonetheless,
this confound exists and we proceed with caution when interpreting the
effects of quolls on population size and survival of melomys.

\emph{Statistical analysis}

During trapping sessions we identified individual melomys that were
captured at each site by their unique microchips. Because melomys on
Indian Island have very small home ranges (tending to be caught in the
same or adjacent traps throughout the trapping period: Jolly \emph{et
al.} unpub. data) and since we never observed captures of melomys marked
at other sites (Jolly \emph{et al.} unpub. data), we treated each site
as independent with regard to demographics and behaviour (Fig. 1; Table
S1).

To estimate between-session survival, we analysed the mark-recapture
data to estimate recapture and survival rates using Cormack-Jolly-Seber
models in program MARK (see Supporting Information for details).

To test whether the presence of quolls impacted melomys population size,
we used a hierarchical model in which population size was made a
function of quoll presence/absence, capture session, and the interaction
between these factors. Population size at each site during each session
is estimated in this process, and we fitted this model in a Bayesian
framework (see Supporting Information for details).

To assess whether the introduction of quolls affected the behaviour of
melomys populations, we divided the responses of melomys in open field
tests into two independent response variables: whether individuals
emerged or not during the 0-10 min period (binomial: 0 or 1); and
whether individuals emerged and interacted with the novel object or not
during the 10-20 min period (binomial: 0 or 1). We used generalised
linear mixed-effects models with binomial errors and a logit link to
test the effect of quoll presence (two levels: quolls present and quolls
absent) and trapping session (continuous), with site included as a
random effect, on the behavioural response variables. \emph{P} -values
were obtained by likelihood ratio tests of the full model with the
effect in question against the model without the effect. This analysis
was performed using R with the \emph{lme4} software package
(Bates\emph{et al.} 2007).

To assess whether the numerical impact of quolls on melomys affected the
seed harvesting rate of invaded melomys populations, we first examined
the relationship between melomys population size (estimated above) and
the total number of control (unscented) seeds harvested from each site.
Here we used a simple linear model with number of seeds harvested as a
linear function of population size, quoll presence/absence and the
interaction between these effects. To test whether there was an
additional effect of quoll presence, beyond their effect on population
size, we defined a new variable, Δ\textsubscript{ks}, as the difference
in seed take between scented and unscented treatments within each
site.session. Here any effect of melomys density is cancelled out
(because density is common to both treatments within each site.session).
Thus, we fitted a model in which Δ\textsubscript{ks} is a function of
quoll presence/absence, session and the interaction between these
effects. All analyses were performed using R version 3.3.2 (R Core Team
2019).

\textbf{RESULTS}

\emph{Effect of novel predator on survival}

When we assessed the impact of quolls on melomys survival between
trapping sessions the best supported model was one in which survival
rates between sessions were lower at quoll-invaded sites than at
quoll-free sites, and recapture rates were session-dependent (see Table
S3). All other models were more than 4 AIC units from this best model,
and so clearly inferior descriptions of the data. From the
best-supported model, estimates of apparent survival (\emph{S} ) for the
intervals between the capture sessions were substantially higher at
quoll-free sites (\emph{S\textsubscript{2017--2018}} =
0.368;\emph{S\textsubscript{2018--2019}} = 0.225) than at quoll-invaded
sites (\emph{S\textsubscript{2017--2018}} =
0.207;\emph{S\textsubscript{2018--2019}} = 0.091; Fig. 2). The differing
survival probability between sessions is largely explained by the time
difference between intervals (2017--2018 = 9 months vs. 2018--2019 = 13
months; Fig. 3).

\textbf{Hosted file}

\verb`image2.emf`  available at \url{https://authorea.com/users/349935/articles/474906-trophic-cascade-driven-by-behavioural-fine-tuning-as-na%C3%AFve-prey-rapidly-adjust-to-a-novel-predator}

\textbf{Figure 2.} Between trapping session survival (± 95\% CI) of
grassland melomys (\emph{Melomys burtoni} ) on Indian Island in
quoll-invaded (\emph{n} = 4) and quoll-free (\emph{n} = 3) populations
on Indian Island, Northern Territory, Australia.

\emph{Effect of novel predator on population size}

Populations of melomys declined dramatically in quoll-invaded sites in
the year following their introduction but not in quoll-free sites (Fig.
3). We observe a strong negative interaction between the presence of
quolls and trapping session in 2018 (mean = -1.194, 95\% credible
interval {[}-1.732, -0.665{]}) and 2019 (mean = -1.097, 95\% confidence
interval {[}-1.652, -0.551{]}; Fig. 3; see Table S2).

\textbf{Hosted file}

\verb`image3.emf`  available at \url{https://authorea.com/users/349935/articles/474906-trophic-cascade-driven-by-behavioural-fine-tuning-as-na%C3%AFve-prey-rapidly-adjust-to-a-novel-predator}

\textbf{Figure 3.} Posterior mean population sizes
(\emph{N\textsubscript{ks}} ± 95\% CI) for quoll-invaded and quoll-free
populations of grassland melomys (\emph{Melomys burtoni} ) on Indian
Island, Northern Territory, Australia. The orange dotted vertical line
denotes the timing of the introduction of quolls. The red dotted
vertical line denotes the timing of an unplanned fire that burnt through
the quoll-invaded sites. In each predator treatment, different sites are
denoted by different shaped points. Estimates assume closure of the
population within each session and detection probability that varies
across sessions.

\emph{Effects of novel predator on prey behaviour}

For the proportion of melomys emerging in open field tests during the
0--10 min period, there was a significant interaction between quoll
presence and trapping session (χ\textsuperscript{2} (5) = 4.386,\emph{P}
= 0.04; Fig. 4). There was no interaction between quoll presence and
trapping session for the proportion of melomys emerging and interacting
with the novel object during 10--20 min period (χ\textsuperscript{2} (5)
= 2.567, \emph{P} = 0.109; Fig. 4). The model without this interaction,
however, revealed a significant effect of quoll presence, with fewer
melomys emerging from hiding and interacting with the novel object
during the 10--20 min period of open field tests from sites where quolls
were present than from sites where quolls were absent
(χ\textsuperscript{2} (5) = -4.696, \emph{P} \textless{} 0.001; Fig. 4).

\textbf{Hosted file}

\verb`image4.emf`  available at \url{https://authorea.com/users/349935/articles/474906-trophic-cascade-driven-by-behavioural-fine-tuning-as-na%C3%AFve-prey-rapidly-adjust-to-a-novel-predator}

\textbf{Figure 4.} Mean proportion (± 95\% CI) of grassland melomys
(\emph{Melomys burtoni} ) emerging from hiding during open field tests
from quoll-invaded sites in 2017 (\emph{n} = 16), 2018 (\emph{n} = 28)
and 2019 (\emph{n} = 29), and quoll-free sites in 2017 (\emph{n} = 14),
2018 (\emph{n} = 35) and 2019 (\emph{n} = 24) on Indian Island, Northern
Territory, Australia.

\emph{Effects of novel predator on seed harvesting and predator-scent
aversion}

Although there was no interaction between melomys density and quoll
presence (\emph{t} \textsubscript{18} = -0.251, \emph{P} = 0.805; Fig.
5a), there was a very clear positive relationship between melomys
density and seed take (\emph{t} \textsubscript{18} = 5.112,
\emph{P}\textless{} 0.001; Fig. 5a) and a clear negative relationship
between quoll presence and seed take (\emph{t} \textsubscript{18} =
-2.344,\emph{P} = 0.031; Fig. 5a). When we looked at the difference in
seed take (Δ\textsubscript{ks}) between scent treatments within
site.session, a striking pattern emerges, in which there is a clear
interaction between the presence of quolls and session (\emph{F}
\textsubscript{3,17}= 18.61, \emph{P} \textless{} 0.001; Fig. 5b).

\textbf{Hosted file}

\verb`image5.emf`  available at \url{https://authorea.com/users/349935/articles/474906-trophic-cascade-driven-by-behavioural-fine-tuning-as-na%C3%AFve-prey-rapidly-adjust-to-a-novel-predator}

\textbf{Figure 5. (a)} Effect of estimated population size on the number
of control, unscented seeds removed from seed plots (\emph{n} = 21) in
quoll-invaded and quolls-free sites. Dotted lines denote the effect of
quoll presence on seed removal rate. (b) Mean (± 95\% CI) difference (Δ)
between the number of predator-scented seeds and control, unscented
seeds removed by melomys from quoll-invaded (\emph{n} = 3; 2017
\&\emph{n} = 4; 2018-19) and quoll-free (\emph{n} = 4; 2017 \& \emph{n}
= 3; 2018-19) sites during each trapping session.

\textbf{DISCUSSION}

The introduction of northern quolls to Indian Island was associated with
lowered survival and an apparent drop in population size in
quoll-invaded melomys populations. This numerical effect on melomys
density had an impact on seed predation rates, because seed take is
strongly associated with the density of melomys in this system. This is
a classic trophic cascade: predation suppresses herbivore density, which
reduces the pressure that herbivores place on primary producers. Our
study, however, also reveals an additional, subtler, cascade effect;
driven by altered prey behaviour rather than by altered prey density.

Within months of quolls appearing on the island, invaded populations of
melomys were measurably shyer than nearby, predator-free populations of
conspecifics. This rapid but generalised response to a novel threat
appears to have had a subtle effect on seed predation rates: when we
examine unscented seeds, per capita seed take is slightly lower in
quoll-invaded populations. This generalised response appears to have
been supplemented over time with more threat-specific antipredator
behaviours. Although the boldness of predator-exposed melomys converged
through time with that of predator-free melomys, predator-exposed
melomys continued to be more neophobic than their predator-free
conspecifics throughout the study. Meanwhile, predator-scent aversion,
as evidenced by seed plots, steadily increased over time. Presumably the
novel predation pressure imposed by quolls resulted in selection on
behaviour and/or learning in impacted rodent populations, allowing them
to fine-tune their behavioural response (decrease general shyness, but
maintain neophobia, and respond to specific cues) as the nature of the
threat became clearer. These changing behavioural responses imply a
generalised reduction in seed take that becomes fine-tuned over time,
with high risk sites (those that smell of predators) ultimately
displaying substantially lower seed take than low risk sites. We see the
emergence of a fine-scaled aversive response (varying on a spatial scale
measured in the tens of metres) and affecting per capita rates of seed
predation.

Although our study documented dramatic population declines in
predator-invaded melomys populations, and we are assigning the primary
cause of these declines to the introduction of quolls, we acknowledge
there is potential for confounding factors to affect our results. We do
not believe these confounds can explain our results, however (see
Supporting Information). The primary confound is the unplanned fire that
burnt through northern Indian Island after completion of our population
monitoring in 2017. Such fires are commonplace in the Australian wet-dry
tropics (Russell-Smith \& Yates 2007); a regular disturbance that is
often rapidly offset by the annual monsoon driven wet season. Grassland
melomys are adapted to fire in this system and populations have been
shown to be very robust to its short- and long-term impacts (Griffiths
\& Brook 2015; Liedloff \emph{et al.} 2018). For these reasons (see
Supporting Information for detailed rationale), we suspect the fire was
unlikely to be directly responsible for the demographic effects we
observed, and fire cannot in any way explain the behavioural response we
observed to quoll-scented seeds. Our interpretation of these changes as
being driven mostly by the addition of a novel predator to the system is
the most parsimonious and globally coherent interpretation of the data.

Predation is a pervasive selective force in most natural systems,
driving evolutionary change in prey morphology, physiology, life history
and behaviour. Unlike morphology and physiology, however, the labile
nature of behaviour makes it a particularly powerful trait for rapid
response in a changing world (Réale \emph{et al.} 2007; Sih \emph{et
al.} 2010b; Dall \& Griffith 2014). Behavioural comparisons of wild
populations exposed to differing predation regimes provides some support
for the prediction that reduced boldness would be selected for under
high predation scenarios (Åbjörnsson \emph{et al.} 2004; Bell 2005;
Brydges \emph{et al.} 2008) and that the appearance of novel predators
can result in bold individuals becoming shyer (Niemelä \emph{et
al.}2012). The opposite pattern or a non-response can also occur,
however (Brown \emph{et al.} 2005; Urban 2007)(Laurila 2000; Carlson \&
Langkilde 2014). Interestingly, a number of studies have demonstrated
that individuals from high-predation areas were quicker to emerge
(Harris \emph{et al.} 2010) and were bolder and more aggressive (Bell \&
Sih 2007; Dingemanse \emph{et al.} 2007) than predator-naïve
conspecifics. Although we found the opposite pattern to this immediately
following the arrival of a novel predator, by the second year after
predator introduction we found the boldness of melomys converging with
that of predator-free populations. Thus, it is clear that the
behavioural composition of these populations is dynamic, and it seems
likely this dynamism (and perhaps the capacity of the prey species to
identify specific threats) may explain some of the variation between
earlier studies.

Although boldness may change over time, neophobia, as a generalised
adaptive response to predation pressure, is now well supported across a
number of studies (Crane \emph{et al.} 2019). Individuals living under
high predation risk scenarios have been shown to typically display
generalized neophobia (Brown \emph{et al.} 2015; Elvidge \emph{et
al.}2016), and neophobia can increase the survival of predator-naïve
individuals in initial encounters with predators (Ferrari \emph{et
al.}2015; Crane \emph{et al.} 2018). Certainly, in our study,
predator-exposed melomys were significantly more neophobic than their
predator-free conspecifics; an effect maintained throughout the study.

Despite reduced survival, significant population declines, and clear
behavioural changes in invaded populations, it is impossible to
determine from our data whether changes in the behaviour of
predator-invaded melomys populations are the result phenotypic
plasticity (learning) or natural selection. The low between trapping
session survival of melomys in quoll-invaded populations means few
individuals survive between sessions, so natural selection is a
possibility, and selection on these behavioural traits is potentially
very strong. Although behavioural changes in predator-invaded
populations have been documented in a few systems where predator
introductions have been staged and experimentally controlled
(Lapiedra\emph{et al.} 2018; Blumstein \emph{et al.} 2019; Cunningham
\emph{et al.} 2019; Pringle \emph{et al.} 2019), elucidating whether
these observed changes arise because of behavioural plasticity or
natural selection can be exceptionally difficult. Rapid behavioural
responses of vulnerable prey to recovered predators has been observed in
a single prey generation, presumably due to behavioural plasticity
(Berger\emph{et al.} 2001; Cunningham \emph{et al.} 2019). Similarly,
behavioural adjustments to an introduced predator have been observed as
a result of natural selection on advantageous behavioural traits
(Lapiedra \emph{et al.} 2018). In our study we had measures of
individual behaviour, but our between session recapture rates of these
individuals was too low to test whether individuals were altering their
behaviour or whether natural selection was resulting in population-level
change. It thus remains possible (and quite likely) that both mechanisms
were in play.

Although northern quolls represent a novel predator to melomys on Indian
Island, the two species' shared evolutionary history on the northern
Australian mainland may provide some explanation as to why this staged
introduction resulted in rapid, finely-tuned behavioural adjustment in
melomys, rather than extinction. Isolation from predators can result in
rapid loss of antipredator behaviours from a prey species' behavioural
repertoire (Blumstein \& Daniel 2005; Jolly \emph{et al.} 2018a),
dramatically increasing an individual's susceptibility to predation
following the introduction of either predator or prey (Carthey \& Banks
2014; Jolly \emph{et al.} 2018b). But such outcomes are not inevitable:
length of isolation, co-evolutionary history, degree of predator
novelty, density-dependent effects, population size, and pre-existing
predator-prey associations (Berger \emph{et al.} 2001; Blumstein 2006;
Banks \& Dickman 2007; Sih \emph{et al.} 2010a; Carthey \& Banks 2014)
are all likely hugely influential in determining whether an invaded
population adjusts to the invader or proceeds towards extinction.
Recently, a conservation introduction of Tasmanian devils to an island
previously lacking them found that their possum prey rapidly adjusted
their foraging behaviour to accommodate this newly arrived predator
(Cunningham \emph{et al.} 2019). Despite possums having lived on the
island in isolation from devils since the 1950s, presumably, their long
evolutionary history together on mainland Tasmania had them primed to
respond to this predatory archetype (Sih \emph{et al.} 2010a; Carthey \&
Banks 2014; Cunningham \emph{et al.} 2019). This shared evolutionary
history is likely responsible for both possums' and melomys' ability to
rapidly mount appropriate antipredator responses. The predators are
novel within an individual's lifetime, but the individual's ancestors
have encountered them before.

Although our results suggest that invaded melomys populations are
beginning to adjust to the presence of northern quolls, there has been
no sign of demographic recovery on the island. Data from our seed
removal experiment clearly demonstrated that the function of melomys as
seed harvesters and dispersers scales with density. Trophic cascades
resulting from the addition and loss of predators from ecosystems has
been observed in a number of systems globally (Ripple \emph{et al.}2001;
Terborgh \emph{et al.} 2001; Estes \emph{et al.} 2011), and the results
can profoundly shape entire systems. As the only rodent and the dominant
granivore in this system, while melomys populations may or may not go
extinct as a result of quoll invasion, their reduced abundance and
weakened ability to harvest and disperse seeds may have yet to be
observed, longer-term consequences for the vegetation structure and
ecosystem function of Indian Island (McConkey \& O'Farrill 2016).
Currently, grass is a rare vegetation feature on Indian island (though
it is a dominant feature of nearby savanna woodlands on the mainland),
and this is quite possibly a result of the high density of melomys on
this (previously) predator-free island. The presence of quolls may well
change that, as both numerical and behaviour responses of melomys
cascade down to the grass community.

Empirical research on the effects of novel predators on recipient
communities under controlled conditions on a landscape-scale is
exceptionally difficult and remains relatively rare. The introduction of
threatened predators to landscapes from which they have been lost
(Cunningham \emph{et al.} 2019) or where they are entirely novel
(Lapiedra \emph{et al.} 2018), however, provides a unique opportunity to
observe how naïve prey can respond to novel predators, and the
mechanisms by which predators can structure communities. Our study
provides empirical support that some impacted prey populations can
adjust rapidly to the arrival of a novel predator via a generalised
behavioural response (decreased boldness) followed by development of a
species-specific antipredator response (behavioural fine-tuning). The
arrival of the novel predator appears to have set off a trophic cascade
that was driven, not only by changed prey density, but also by changed
prey behaviour. Thus, rapid adaptive shift may allow prey populations to
persist, but large-scale, system-wide changes may still follow.

\textbf{ACKNOWLEDGMENTS}

Thanks to Kenbi Traditional Owners (Raylene and Zoe Singh) for land
access permission and Kenbi Rangers for assistance in the field. Special
thanks to Kenbi Rangers (Brett Bigfoot, Rex Edmunds, Jack Gardner, Ian
McFarlane, Dale Singh, and Rex Sing) for continued field assistance
throughout this project. Thanks to Kenbi Ranger Co-ordinator Steven
Brown for logistical support in the field. Thanks to Ella Kelly and
Naomi Indigo for logistical and moral support on the island. Thanks to
Alana de Laive for graphic design of figures. We thank two anonymous
reviewers and Professor Réale for their comments via Peer Community in
Ecology, which greatly improved the manuscript. This research was funded
by an Australian Research Council Linkage Grant (JKW and BLP
LP150100722). Animal ethics approval for this work was provided by the
University of Melbourne (1814518) and Charles Darwin University (A13026)
Animal Ethics Committees. In kind support was provided by Kenbi Rangers
and the Northern Territory Government Department of Environment and
Natural Resources, Flora and Fauna Division (via GRG). CJJ was supported
by an Australian Postgraduate Award, the Holsworth Wildlife Research
Endowment and David Hay Postgraduate Writing Up Award.

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