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 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 et al. 2007; Sih 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 et al. 2004; Bell 2005;
Brydges et al. 2008) and that the appearance of novel predators
can result in bold individuals becoming shyer (Niemelä et al.2012). The opposite pattern or a non-response can also occur, however
(Brown 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 et al. 2010) and were bolder and more aggressive (Bell &
Sih 2007; Dingemanse 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 et al. 2019). Individuals living under
high predation risk scenarios have been shown to typically display
generalized neophobia (Brown et al. 2015; Elvidge et al.2016), and neophobia can increase the survival of predator-naïve
individuals in initial encounters with predators (Ferrari et al.2015; Crane 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 (Lapiedraet al. 2018; Blumstein et al. 2019; Cunningham et
al. 2019; Pringle 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 (Bergeret al. 2001; Cunningham et al. 2019). Similarly,
behavioural adjustments to an introduced predator have been observed as
a result of natural selection on advantageous behavioural traits
(Lapiedra 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 et al. 2018a),
dramatically increasing an individual’s susceptibility to predation
following the introduction of either predator or prey (Carthey & Banks
2014; Jolly 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 et al. 2001; Blumstein 2006;
Banks & Dickman 2007; Sih 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 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 et al. 2010a; Carthey &
Banks 2014; Cunningham 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 et al.2001; Terborgh et al. 2001; Estes 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 et al. 2019) or where they are entirely novel
(Lapiedra 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.