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Novel habitat associations and seasonality in threatened Mitchell’s water monitors (Varanus mitchelli): Implications for conservation

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Abstract

Mitchell’s water monitors (Varanus mitchelli) are a small to medium‐sized (<1 m TL) Australian varanid lizard endemic to northern Western Australia and the Northern Territory, extending just into north‐western Queensland. They are a semi‐aquatic, semi‐arboreal monitor, typically thought of as being associated with freshwater riparian habitats. Following the arrival of cane toads (Rhinella marina) across their distribution, V. mitchelli were observed to have suffered precipitous population declines and local extinctions due to lethal toxic ingestion of toads. Here, we present observations of V. mitchelli from previously unreported saline and brackish habitats, as well as information on the cryptic behaviour and seasonal activity of this threatened species in Darwin, Northern Territory. Currently, because V. mitchelli are undocumented in mangrove and littoral habitats, ecological consultants in northern Australia are considering such habitats unsuitable for this threatened varanid and are not recommending targeted surveys for this species in these habitats. We argue that the niche occupied by V. mitchelli is broader than currently recognised and they should be considered as potentially occurring in most mangrove habitats across their known range. We also suggest species‐appropriate survey techniques to improve detection of this very cryptic threatened species. Concerningly, despite recently being recognised as Critically Endangered by the International Union for Conservation of Nature (IUCN), V. mitchelli are currently not recognised as threatened by the federal Environment Protection and Biodiversity Conservation (EPBC) Act 1999.
Natural History Notes
Novel habitat associations and seasonality in threatened
Mitchells water monitors (Varanus mitchelli): Implications
for conservation
ALANA DE LAIVE,
1
*BRENDAN SCHEMBRI
2
AND CHRIS J. JOLLY
2,3
1
Australian Museum Research Institute, Australian Museum, Sydney, NSW 2010 (Email:
alanahdelaive@gmail.com);
2
Research Institute for the Environment and Livelihoods, Charles Darwin
University, Darwin, NT; and
3
Institute of Land, Water and Society, School of Environmental Science,
Charles Sturt University, Albury, NSW, Australia
Abstract Mitchells water monitors (Varanus mitchelli) are a small to medium-sized (<1 m TL) Australian vara-
nid lizard endemic to northern Western Australia and the Northern Territory, extending just into north-western
Queensland. They are a semi-aquatic, semi-arboreal monitor, typically thought of as being associated with fresh-
water riparian habitats. Following the arrival of cane toads (Rhinella marina) across their distribution, V. mitchelli
were observed to have suffered precipitous population declines and local extinctions due to lethal toxic ingestion
of toads. Here, we present observations of V. mitchelli from previously unreported saline and brackish habitats,
as well as information on the cryptic behaviour and seasonal activity of this threatened species in Darwin, North-
ern Territory. Currently, because V. mitchelli are undocumented in mangrove and littoral habitats, ecological
consultants in northern Australia are considering such habitats unsuitable for this threatened varanid and are not
recommending targeted surveys for this species in these habitats. We argue that the niche occupied by V. mitch-
elli is broader than currently recognised and they should be considered as potentially occurring in most man-
grove habitats across their known range. We also suggest species-appropriate survey techniques to improve
detection of this very cryptic threatened species. Concerningly, despite recently being recognised as Critically
Endangered by the International Union for Conservation of Nature (IUCN), V. mitchelli are currently not recog-
nised as threatened by the federal Environment Protection and Biodiversity Conservation (EPBC) Act 1999.
Key words: cane toad, detection, goanna, reptiles, Rhinella marina, survey methods.
Throughout Australia, varanid lizards, colloquially
known goannas, are recognised as a taxon group that
has suffered some of the most severe impacts of the
arrival of toxic invasive cane toads (Doody et al.
2009; Shine 2010). Australian species that are most
vulnerable to the impacts of toads via lethal toxic
ingestion typically appear to share some similarities.
In general, relatively large, generalist predators that
forage in riparian areas and are willing and able to
attack or consume medium to large toads have suf-
fered most dramatically from their impacts (Shine
2010; Feit & Letnic 2015), and numerous larger
native predators have rapidly disappeared from the
landscape following the arrival of toads (Shine 2010).
An exception to this rule appears to be the Mitchells
water monitor (Varanus mitchelli)a comparatively
small varanid lizard that has suffered dramatic
population-level declines following cane toad inva-
sion (Doody et al. 2009, 2015; Doody et al. 2017),
presumably due to their habit of foraging for prey in
riparian areas. Unfortunately, due to their cryptic
nature and the difculty of working with wild vara-
nids, our understanding of the speciesecology and
natural history remains relatively rudimentary, poten-
tially limiting our ability to conserve them.
Varanus mitchelli are a small to medium-sized
(<1 m TL) varanid lizard endemic to the northwest
Qld, the northern NT and Kimberley region, WA
(Schultz & Doody 2004; Macdonald 2020). They are
a diurnal, semi-aquatic, semi-arboreal monitor and,
like Mertenswater monitors (Varanus mertensi), are
typically thought of as being associated with freshwa-
ter riparian habitats (Shea et al. 2018; EcOz 2019).
The species that warrant the most concern regarding
the impacts of cane toads are those that suffer the
most extreme population-level impacts, and those
which are also restricted to areas where toads have
*Corresponding author.
Accepted for publication February 2021.
© 2021 Ecological Society of Australia doi:10.1111/aec.13029
Austral Ecology (2021) 46, 871875
invaded or are likely to invade. The known distribu-
tion of V. mitchelli is soon to be entirely invaded by
cane toads, and because they have been observed to
decline so rapidly and dramatically upon arrival of
cane toads, they have recently been listed by the
IUCN as Critically Endangered (Shea et al. 2018).
Although many populations of V. mitchelli have suf-
fered dramatic declines as a consequence of the cane
toad invasion (e.g. Doody et al. 2017), it is becoming
increasingly clear that like other native predators
impacted by cane toads (e.g. Fukuda et al. 2016;
Moore et al. 2019), some populations do persist. In
some cases, populations may persist if individuals
possess innate and heritable toad-averse traits that
provide them with some resilience to cane toad
impacts (e.g. Phillips & Shine 2006; Llewelyn et al.
2014; Kelly & Phillips 2017; Indigo et al. 2021), with
probability of persistence potentially mediated by
resource availability (Moore et al. 2019). In others,
features of the landscape may offer some protection
by being less habitable for toads, lessening the impact
on vulnerable natives. For us to better understand
these patterns and conserve natural refuges of persis-
tence, we rst need to identify where they are in the
landscape. Currently, V. mitchelli are thought to be
primarily conned to freshwater riparian areas; how-
ever, here, we provide evidence that some popula-
tions are persisting in saline littoral (coastal
foreshore) and brackish mangrove habitats across the
greater Darwin region, Northern Territory.
Between 20052020, we both opportunistically and
actively observed Varanus mitchelli persisting in lit-
toral and mangrove habitats in numerous areas across
the greater Darwin region, Northern Territory
(Fig. 1). Our (CJJ and BS) rst observation of this
species in a littoral habitat occurred in April 2005,
when we encountered numerous adult V. mitchelli
amongst rocks on the Nightcliff foreshore, NT.
Annually since then, all three authors have consis-
tently observed V. mitchelli along the foreshore of the
Darwin Peninsula, in adjacent mangroves, and even
in gardens of suburban coastal foreshore properties
(Fig. 2). Typically, monitors were encountered in the
mid-morning basking on manmade structures, such
as rock sea walls, slabs of concrete, as well as on
mangrove and Casuarina trees (Fig. 2). Over this 15-
year period, incidental detections and specic search
effort for this species in these areas have suggested
that there is a distinct seasonal activity period for the
species (Fig. 3). We observed them basking and
active on most days during the most humid, wet sea-
sonmonths (November to April). Although they can
be observed active and basking from mid-August to
mid-May, albeit less regularly, there appears to be a
distinct period of signicantly reduced activity during
the coolest dry seasonmonths (June and July;
Fig. 3). It appears, their seasonal activity is strongly
driven by periods of high temperature, rainfall and
humidity. Similar seasonal activity patterns have been
reported for this species in freshwater riparian habi-
tats in the Northern Territory (Shine 1986), and
have also been observed in other tropical varanid spe-
cies (Christian et al. 1995; Christian & Weavers
1996). Although they are active and can be observed
basking and/or foraging through much of the year
around Darwin, this species is exceptionally cryptic
and near impossible to detect. From our observa-
tions, it is apparent that V. mitchelli are highly reliant
on crypsis to avoid detection, making them excep-
tionally hard to detect during active surveys. Once
they are aware that they have been detected, they
tend to slowly and cautiously retreat to nearby shel-
ter, such as rock crevices or tree hollows.
Our observations of persisting populations of
V. mitchelli in the Darwin region warrants considera-
tion into what circumstances may be allowing this
threatened species to persist in these habitats. The
most obvious assumption would be that these saline
habitats are providing refuge from cane toads. Cane
toads have, however, been observed living and breed-
ing abutting the locations where V. mitchelli are per-
sisting (Atlas of Living Australia 2020; C. Jolly
unpub. data 2020). Unlike most anurans, cane toads,
as well as their eggs and tadpoles, are remarkably tol-
erant of salinity (Covacevich & Archer 1975; Liggins
& Grigg 1985; Wijethunga et al. 2016), and are regu-
larly observed in or near littoral and mangrove habi-
tats in the Northern Territory. Despite this, toads do
appear to be less abundant in saline and brackish
habitats than in freshwater systems. Thus, while this
explanation may not completely account for the per-
sistence of V. mitchelli in these habitats, it is poten-
tially having some alleviating effect. If mangrove and
Fig. 1. Locations (blue dots) across the greater Darwin
region, Northern Territory, that the authors have inciden-
tally observed Mitchells water monitors (Varanus mitchelli)
persisting in littoral and mangrove habitats since the arrival
of cane toads (Rhinella marina).
doi:10.1111/aec.13029 © 2021 Ecological Society of Australia
872 A . D E L A I V E ET AL.
Fig. 2. Mitchells water monitors (Varanus mitchelli) photographed in littoral and mangrove habitats in Darwin, Northern
Territory. (a) Adult V. mitchelli in black mangroves (Lumnitzera racemosa) at Rapid Creek, Darwin (Photo: Brendan Schembri).
(bc) Adult V. mitchelli on articial rock sea walls at Nightcliff, Darwin (Photos: B. Schembri & M. Clancy). (d) Adult V. mitchelli
on natural coastal rock at Nightcliff, Darwin (Photo: Chris Jolly).
Fig. 3. Activity period of Varanus mitchelli in Darwin, Northern Territory. Varanus mitchelli appear to be most active and detect-
able during the hot, humid wet seasonmonths of November to April (dark green). Varanus mitchelli activity declines in May as
declining humidity signals the start of the dry season (light green). Varanus mitchelli appear to be inactive and undetectable during
the coolest, driest months of June and July (white). As the humidity increasingly rises between August (light green) and Septem-
berOctober (mid-green), V. mitchelli become increasingly active and detectable. Shades signify activity periods, with the darker
shades indicating increased detectability. Mean climatic conditions for Darwin Airport from a 79-year dataset collected by the
Bureau of Meteorology. The red line connects mean monthly maximum air temperatures, and the blue line shows mean monthly
minimum air temperatures. Histograms show mean monthly rainfall.
© 2021 Ecological Society of Australia doi:10.1111/aec.13029
NOVEL HABITAT FOR MITCHELLS WA T E R M O N I T O R 873
littoral habitats are providing a refuge from the
impacts of toads, the conservation of these habitats
could be critical in supporting the persistence and
recovery of Varanus mitchelli.
Our observations expanding the reported habitat
associations of V. mitchelli are of critical importance to
this threatened species because, until recently, Darwin
was one of Australias most rapidly growing cities (Pop-
ulation Australia 2020). Although it is currently not
well recognised, Darwin is home to one of the few
known remnant populations of Australias only Criti-
cally Endangered varanid. Recently, because published
documentation of this speciesassociation with man-
grove and littoral habitats is lacking, assessments
intending to investigate the potential impact of devel-
opments have not considered this species as a likely
inhabitant of riparian habitats without permanent
freshwater (EcOz 2019). And, for this reason, targeted,
species-specic surveys in these habitats were decient
in the preapproval assessments of recently proposed
developments. Additionally, there are no survey guide-
lines currently available for threatened varanids (EcOz
2019). Due to their supercial similarities and co-oc-
currence in freshwater habitats, V. mitchelli are often
likened to a Mertenswater monitor (Varanus mertensi)
and survey methodologies assume that like V. mertensi,
V. mitchelli are reasonably detectable when present in
an area and can simply be detected by active search
methods (EcOz 2019). This assumption, however, is
not accurate. Varanus mitchelli are a much more cryptic
and arboreal species that is near impossible to detect
via active search without sufcient experience. For this
reason, species-specic survey methodologies, which
account for the speciesecology and do not rely on the
skill level of the observer, should be designed for V.
mitchelli. Remote camera traps baited with sardines
(Moore et al. 2020) and chicken necks (Pettit et al.
2020) have been used successfully to improve detec-
tions of other Australian varanids. In light of our obser-
vations, we suggest this, in combination with active
searches by experts (but see Ward-Fear et al. 2019), as
the most appropriate survey methodology for this spe-
cies. Additionally, for logistical and human comfort
reasons, biodiversity surveys and impact assessments
tend to be conducted in the coolest, driest months in
the Top End. However, surveys conned to the cooler
months have a higher likelihood of encountering false
absences for V. mitchelli (Fig. 3). Future impact assess-
ments must conduct targeted surveys in the warmer
months when this species is most active and must not
assume, as they currently are, that this species will not
be present in mangrove and littoral habitats. We must
endeavour to improve survey methodologies for this
species lest we lose additional populations of this
Critically Endangered species.
Interestingly, recent research has emerged that sug-
gests that both the size (Jolly et al. 2016) and/or
personalitiesof goannas (Ward-Fear et al. 2018,
2019) may inuence their vulnerability to cane toads,
such that larger and/or bolder individuals within the
population may be the rst to die. Smaller and/or shyer
individuals within a population of toad-naive varanids
process their prey with more caution than larger indi-
viduals and may be less likely to consume a lethal dose
of toad toxin (Jolly et al. 2016). Given that V. mitchelli
are notably shyer and more cautious by nature than lar-
ger, toad-vulnerable varanid species, it is possible that
these inherent traits may be particularly advantageous
in some populations. Concerningly, if only the shyest
individuals of an already reticent species remain in the
populations following an impact, they may be even
more difcult to detect and may be assumed to be
absent from areas where they persist (Ward-Fear et al.
2019). Recently, shyer varanids were found less likely
to be detected by ecologists, but not Indigenous obser-
vers, during active surveys (Ward-Fear et al. 2019). As
the impacts of toads may be non-randomly distributed
across individuals within a population, shyer goannas
may avoid the impacts of toads but may still be missed
in active surveys.
As a direct consequence of the cane toad invasion,
numerous varanid species have suffered severe decli-
nes across their Australian range. Being medium to
large carnivorous lizards, some of these species play
vital roles in trophic regulation (e.g. Doody et al.
2013, 2015; Jolly et al. 2015; Feit et al. 2020) and
are important for the Indigenous cultures of northern
Australia. Yet, currently, no varanid species is listed
under the EPBC Act. Although Varanus mitchelli are
listed as Vulnerable in the Northern Territory and
Critically Endangered by the IUCN, they are not
federally listed, and a review of listing status is
urgently required for this species. Without Common-
wealth recognition as a threatened species, V. mitch-
elli is not entitled to National Recovery Plans or
protection for populations outside of national parks,
such as persisting remnant populations across the
Darwin region. Future research should endeavour to
use our recommended survey techniques to assess
where this species is persisting across its Australian
distribution and attempt to determine what mecha-
nisms are allowing remnant populations to persist.
ACKNOWLEDGEMENT
We would like to thank Matt Clancy for allowing us
to use one of his photos and Melanie Elphick for
assistance with gure production.
CONFLICTS OF INTEREST
The authors declare no conicting interests.
doi:10.1111/aec.13029 © 2021 Ecological Society of Australia
874 A . D E L A I V E ET AL.
AUTHOR CONTRIBUTION
Alana de Laive: Conceptualization (equal); Data
curation (equal); Investigation (equal); Methodology
(equal); Project administration (equal); Resources
(equal); Visualization (equal); Writing-original draft
(equal); Writing-review & editing (equal). Brendan
Schembri: Conceptualization (equal); Data curation
(equal); Investigation (equal); Methodology (equal);
Resources (equal); Visualization (equal); Writing-
original draft (equal); Writing-review & editing
(equal). Christopher James Jolly: Conceptualiza-
tion (equal); Data curation (equal); Investigation
(equal); Methodology (equal); Resources (equal);
Visualization (equal); Writing-original draft (equal);
Writing-review & editing (equal).
REFERENCES
Atlas of Living Australia (2020) Rhinella marina. https://bie.ala.
org.au/species/urn:lsid:biodiversity.org.au:afd.taxon:
e79179f8-44bf-46eb-b139-a2e66f6045c1
Christian K. A., Corbett L. K., Green B. & Weavers B. W.
(1995) Seasonal activity and energetics of two species of
varanid lizards in tropical Australia. Oecologia 103,
34957.
Christian K. A. & Weavers B. W. (1996) Thermoregulation of
monitor lizards in Australia: An evaluation of methods in
thermal biology. Ecol. Monogr. 66, 13957.
Covacevich J. & Archer M. (1975) The distribution of the cane
toad, Bufo marinus, in Australia and its effects on
indigenous vertebrates. Mem. Queensl. 17, 30510.
Doody J. S., Castellano C. M., Rhind D. & Green B. (2013)
Indirect facilitation of a native mesopredator by an invasive
species: are cane toads re-shaping tropical riparian
communities? Biol. Invasions 15, 55968.
Doody J. S., Green B., Rhind D., Castellano C. M., Sims R. &
Robinson T. (2009) Population-level declines in Australian
predators caused by an invasive species. Anim. Conserv. 12,
4653.
Doody J. S., Rhind D., Green B., Castellano C., McHenry C.
& Clulow S. (2017) Chronic effects of an invasive species
on an animal community. Ecology 98, 2093101.
Doody J. S., Soanes R., Castellano C. M. et al. (2015) Invasive
toads shift predatorprey densities in animal communities
by removing top predators. Ecology 96, 254454.
EcOz (2019) Kittyhawk Threatened Species Survey. Available at:
https://litchfield.nt.gov.au/sites/default/les/uploads/meeting/
attachments/2020/15.07%20PA2019%200329%20Attachme
nt%20D%20Part%20Development%20Application%20Environ
mental%20Assessment%20Part%202.pdf
Feit B., Dempster T., Jessop T. S., Webb J. K. & Letnic M.
(2020) A trophic cascade initiated by an invasive vertebrate
alters the structure of native reptile communities. Glob.
Change Biol. 26, 282940.
Feit B. & Letnic M. (2015) Species level traits determine
positive and negative population impacts of invasive cane
toads on native squamates. Biodivers. Conserv. 24, 1017
29.
Fukuda Y., Tingley R., Crase B., Webb G. & Saalfeld K.
(2016) Long-term monitoring reveals declines in an
endemic predator following invasion by an exotic prey
species. Anim. Conserv. 19, 7587.
Indigo N. L., Jolly C. J., Kelly E., Smith J., Webb J. K. &
Phillips B. L. (2021) Effects of learning and adaptation on
population viability. Conserv. Biol. https://doi.org/10.1111/
cobi.13691.
Jolly C. J., Shine R. & Greenlees M. J. (2015) The impact of
invasive cane toads on native wildlife in southern Australia.
Ecol. Evol. 5, 387994.
Jolly C. J., Shine R. & Greenlees M. J. (2016) The impacts of
a toxic invasive prey species (the cane toad, Rhinella
marina) on a vulnerable predator (the lace monitor,
Varanus varius). Biol. Invasions 18, 1499509.
Kelly E. & Phillips B. L. (2017) Get smart: native mammal
develops toad-smart behavior in response to a toxic
invader. Behav. Ecol. 28, 8548.
Liggins G. W. & Grigg G. C. (1985) Osmoregulation of the
cane toad, Bufo marinus, in salt water. Comp. Biochem.
Physiol. Part A Mol. Integr. Physiol. 82, 6139.
Llewelyn J., Schwarzkopf L., Phillips B. L. & Shine R. (2014)
After the crash: How do predators adjust following the
invasion of a novel toxic prey type? Austral Ecol. 39, 1907.
Macdonald S. (2020) Australia Reptile Online Database.
Available at: http://www.arod.com.au/arod/
Moore H. A., Dunlop J. A., Valentine L. E. et al. (2019)
Topographic ruggedness and rainfall mediate geographic
range contraction of a threatened marsupial predator.
Divers. Distrib. 25, 181831.
Moore H. A., Valentine L. E., Dunlop J. A. & Nimmo D. G.
(2020) The effect of camera orientation on the
detectability of wildlife: a case study from north-western
Australia. Remote Sens. Ecol. Conserv. 6, 54656.
Pettit L., Ward-Fear G. & Shine R. (2020) Choose your meals
carefully if you need to coexist with a toxic invader. Sci.
Rep. 10, 21866.
Phillips B. L. & Shine R. (2006) An invasive species induces
rapid adaptive change in a native predator: cane toads and
black snakes in Australia. Proc. R. Soc. B 273, 154550.
Population Australia (2020) [online]. Available from: http://
www.population.net.au/darwin-population/
Shea G., Woinarski J. C. Z. & Cogger H. (2018) Varanus
mitchelli. The IUCN Red List of Threatened Species 2018:
e.T83778268A101752345. https://dx.doi.org/10.2305/
IUCN.UK.2018-1.RLTS.T83778268A101752345.en.
Shine R. (1986) Food habits, habitats and reproductive biology
of four sympatric species of varanid lizards in tropical
Australia. Herpetologica 42, 34660.
Shine R. (2010) The ecological impact of invasive cane toads
(Bufo marinus) in Australia. Q. Rev. Biol. 85, 25391.
Shultz T. & Doody J. S. (2004) Varanus mitchelli. In: Varanoid
Lizards of the World (eds E. R. Pianka & D. King) pp.
41622.Indiana University Press, Bloomington and
Indianapolis.
Ward-Fear G., Brown G. P., Pearson D. J., West A., Rollins
L. A. & Shine R. (2018) The ecological and life history
correlates of boldness in free-ranging lizards. Ecosphere 9,
e02125.
Ward-Fear G., Rangers B., Pearson D., Bruton M. & Shine R.
(2019) Sharper eyes see shyer lizards: Collaboration with
Indigenous peoples can alter the outcomes of conservation
research. Conserv. Lett. 12, e12643.
Wijethunga U., Greenlees M. & Shine R. (2016) Living up to
its name? The effect of salinity on development, growth,
and phenotype of the marinetoad (Rhinella marina). J.
Comp. Physiol. B 186, 20513.
© 2021 Ecological Society of Australia doi:10.1111/aec.13029
NOVEL HABITAT FOR MITCHELLS WA T E R M O N I T O R 875
... Ward-Fear, personal observation). Populations of large-bodied species (yellowspotted monitor, Varanus panoptes; Mertens' water monitor, V. mertensi) have declined by >90% following toad invasion (Brown et al., 2013;Doody et al., 2009;Shine, 2010), and Mitchell's water monitor (Varanus mitchelli) may be endangered due to toads (Laive et al., 2021). ...
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Invasive species can trigger trophic cascades in animal communities, but published cases involving their removal of top predators are extremely rare. An exception is the invasive cane toad (Rhinella marina) in Australia, which has caused severe population declines in monitor lizards, triggering trophic cascades that facilitated dramatic and sometimes unexpected increases in several prey of the predators, including smaller lizards, snakes, turtles, crocodiles, and birds. Persistence of isolated populations of these predators with a decades-long sympatry with toads suggests the possibility of recovery, but alternative explanations are possible. Confirming predator recovery requires longer-term study of populations with both baseline and immediate post-invasion densities. Previously, we quantified short-term impacts of invasive cane toads on animal communities over seven years at two sites in tropical Australia. Herein, we test the hypothesis that predators have begun to recover by repeating the study 12 yr after the initial toad invasion. The three predatory lizards that experienced 71–97% declines in the short-term study showed no sign of recovery, and indeed a worse fate: two of the three species were no longer detectable in 630 km of river surveys, suggesting local extirpation. Two mesopredators that had increased markedly in the short term due to these predator losses showed diverse responses in the medium term; a small lizard species increased by ~500%, while populations of a snake species showed little change. Our results indicate a system still in ecological turmoil, having not yet reached a " new equilibrium " more than a decade after the initial invasion; predator losses due to this toxic invasive species, and thus downstream effects, were not transient. Given that cane toads have proven too prolific to eradicate or control, we suggest that recovery of impacted predators must occur unassisted by evolutionary means: dispersal into extinction sites from surviving populations with alleles for toxin resistance or toad avoidance. Evolution and subsequent dispersal may be the only solution for a number of species or communities affected by invasive species for which control is either prohibitively expensive, or not possible.
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Although invasive species can cause major declines in native populations, some individuals in a native population are better equipped to deal with the threat than others. Existing trait variation - especially in highly flexible behavioral traits - may thus buffer populations and allow natural selection to proceed. Cane toads (Rhinella marina) have caused dramatic declines in native Australian predators, which unwittingly attack the poisonous toads. The northern quoll (Dasyurus hallucatus) is one such predator, with declines and local extinction of quoll populations typically occurring rapidly after toads arrive. Despite this, some quoll populations persist in areas where toads have been present for ≥70 years. Here, we compare northern quolls from toad-infested and toad-free areas to test whether this persistence is enabled by behavioral traits. We demonstrate that northern quolls from long-term toad-infested areas have indeed become "toad-smart," spending significantly less time investigating a toad compared with a control prey item, and limiting this investigation time to investigatory rather than attacking behavior. By contrast, quolls from toad-naive populations vary in their response to toads, with many exhibiting attack behavior. These results demonstrate that behavioral variation exists within naive populations and the few persisting northern quoll populations in toad-infested areas have naturally developed toad-smart behavior. Population modeling suggests this behavior likely persists across generations. Although the mechanism is unknown, the observed shift in toad-smart behavior may be due to rapid adaption, and if so could become a vital tool for conserving this endangered species. © The Author 2017. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved.