Behavioral
Ecology
The official journal of the
ISBE
International Society for Behavioral Ecology
Behavioral Ecology (2014), 25(3), 604–611. doi:10.1093/beheco/aru031
Original Article
Wary invaders and clever natives: sympatric
house geckos show disparate responses to
predator scent
Adam Cisterne,a Eric P. Vanderduys,b David A. Pike,c and Lin Schwarzkopfa
aSchool of Marine and Tropical Biology, 1 James Cook Drive, James Cook University, Townsville,
Queensland 4811, Australia, bCSIRO Ecosystem Sciences, Australian Tropical Sciences Innovation Precinct,
1 James Cook Drive, James Cook University, Townsville, Queensland 4811, Australia, and cSchool of
Marine and Tropical Biology and Centre for Tropical Environmental and Sustainability Science, 1 James
Cook Drive, James Cook University, Townsville, Queensland 4811, Australia
Received 27 October 2013; revised 2 February 2014; accepted 12 February 2014; Advance Access publication 12 March 2014.
The ability to detect and avoid potential predators can enhance fitness, but also has costs, and thus many animals respond to potential
predators either in a general (avoid all potential predators) or threat-sensitive (selectively avoid dangerous predators) manner. We used
2-choice trials to investigate strategies used by globally invasive house geckos (Hemidactylus frenatus) and native Australian house
geckos (Gehyra dubia) to avoid chemical cues from potential snake predators (Acanthophis antarcticus, Antaresia maculosa, Boiga
irregularis, and Pseudechis colletti). Invasive geckos did not respond to a novel chemical cue (perfume), but significantly avoided shelters scented by all 4 predatory snake species, and did not discriminate among snake species that occurred within or outside their current geographic range. Thus, the invasive gecko showed generalized predator avoidance. In contrast, native geckos avoided shelters
scented with perfume but did not avoid shelters scented by any of the 4 predatory snake species. We interpret the lack of response by
native geckos as threat sensitive, suggesting that they may require additional cues beyond scent alone (e.g., visual cues) to judge the
situation as threatening. Generalized responses may be costly for native species living in native habitats filled with predators but may
facilitate the rapid establishment of invasive species in novel (especially urban) environments, where general responses to predators
may have relatively low costs and enhance survival.
Key words: Gehyra dubia, generalized response, Hemidactylus frenatus, invasive species, predator–prey overlap, prey, threatsensitive response.
Introduction
Predation is a powerful selective force (Frid et al. 2012) because it
can influence individual fitness and shape characteristics such as
habitat use (Eichholz et al. 2012), time spent foraging (Quinn et al.
2012), duration of courtship (Habrun and Sancho 2012), reproductive frequency (Jochym and Halle 2012), ontogenetic changes
in behavior (Llewelyn et al. 2012), and parental care (Chelini and
Machado 2012). Avoiding predation is clearly beneficial to fitness,
but the act of avoiding predators gives rise to a trade-off between
the costs of avoidance (e.g., time or energy lost for other fitness
enhancing activities) and the costs of an encounter (e.g., possible
injury or death from predatory attacks; Sih et al. 2010). Managing
these trade-offs directly affects an individual’s fitness and thus
Address correspondence to A. Cisterne. E-mail: [email protected].
© The Author 2014. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved. For
permissions, please e-mail: [email protected]
animals should evaluate potential predators and match their antipredator responses to the threat posed by specific predators (i.e.,
the “threat-sensitivity hypothesis”; Sih et al. 2010).
There is widespread empirical support for the threat-sensitivity
hypothesis: animals often avoid potential predators in relation to
the actual risk they pose. For example, scincid lizards selectively
avoid chemical cues from dangerous varanid predators and ignore
those of less dangerous predators (Lloyd et al. 2009). Similarly,
skinks may avoid cues from ambush predators more strongly than
active predators (Head et al. 2002). Antipredator behaviors can
also change ontogenetically to match threats posed to different prey
life stages (Head et al. 2002; Pike et al. 2010). Animals can perceive
these risks at surprisingly fine temporal scales; for example, both
predator diet and activity patterns influence salamander (Plethodon
cinereus) assessment of the danger posed by garter snakes (Thamnophis
sirtalis) (Madison et al. 1999). Conversely, some prey species do not
Cisterne et al. • Disparate responses of geckos to predators
discriminate among potential predators in a threat-sensitive manner, leading to a general wariness of all potential predators (Webb
et al. 2009). Avoiding predators that pose little threat to the prey
is common when the cost of avoidance is low (such as moving a
short distance to avoid encountering a predator or remaining still to
avoid detection); however, when faced with high costs of avoidance,
prey may be more selective about which potential predators they
avoid (Blumstein 2006).
The prey-naivety hypothesis predicts that native prey may be
unable to recognize introduced predators because of a lack of
experience with them (Sih et al. 2010), causing increased predation
by invasive predators. The opposite scenario, in which invasive prey
species are faced with, but unable to identify, novel native predators, is just as plausible. In such cases, introduced species may face
a higher risk of predation than native species of similar body sizes
and ecologies. Traits associated with generalized predator recognition and antipredator behavior may be beneficial, and thus common, in successful invaders. A growing body of evidence suggests
that many introduced prey species display antipredator behaviors
toward novel predators (Gheradi et al. 2002; Pennuto and Keppler
2008; Salo et al. 2008; Grason and Miner 2012). These behavioral
traits may be especially important when invasive prey species are
establishing new populations where a novel suite of predators could
be encountered (Weis 2010). Stronger predator avoidance responses
may improve the relative success of invasive prey species over ecologically similar native prey species (Pennuto and Keppler 2008).
Therefore, antipredator behaviors can influence invasion success
via interactions between invasive prey and native predators and
also by disrupting native predator–prey relationships. Predation,
therefore, can profoundly influence the coexistence of invasive and
native prey species (Palmer and Ricciardi 2005).
The world’s most widespread lizard is the invasive Asian house
gecko (Hemidactylus frenatus; Hoskin 2011). Originating in south and
southeast Asia (Case et al. 1994), this species has been introduced
to Japan, parts of Central America, Mexico, the southern United
States, Madagascar, Kenya, coastal Australia, and many islands in
the Pacific, Indian, and Atlantic Oceans (McKay et al. 2009; Hoskin
2011). Several traits may make Asian house geckos suited to invasion, including a generalist diet composed of invertebrates (Bobrov
1992), eggs that are resistant to saltwater and desiccation (facilitating survival during ocean crossings and on small islands) (Brown and
Alcala 1957; Pike et al. 2012), females that can store sperm, allowing reproduction in the absence of males (Yamamoto and Hidetoshi
2006), and the ability to displace some resident, native geckos using
aggressive exclusion (Bolger and Case 1992) and exploitative competition (Petren and Case 1996). In addition, the ability to occupy
anthropogenically modified habitats may aid invasion success of this
species (Hoskin 2011; Vanderduys and Kutt 2013).
We know very little about why invasive Asian house geckos are
so successful in urban environments although high prey intake rates
and a tolerance of other geckos in close proximity are likely contributors (Petren and Case 1996; Canyon and Hii 1997). Another
potential contributing factor may be that this invasive species can
readily identify and avoid potential predators within the invaded
range. In northeastern Australia, Asian house geckos overlap in
distribution with the ecologically similar native house gecko, Gehyra
dubia (Wilson 2005; McKay et al. 2009; Figure 1): both species use
urban environments, are nocturnal, and shelter by day in crevices
(Canyon and Hii 1997; Hoskin 2011). Nocturnal lizards carefully
select diurnal retreat sites based on physical cues that indicate a
variety of ecological opportunities, including favorable thermal
605
profiles (Kearney 2002), conspecific interactions (Shah et al. 2003),
avoidance of competition (Langkilde and Shine 2007), and avoidance of predators (Webb et al. 2010). We compared diurnal retreatsite selection of invasive Asian house geckos and native Australian
house geckos to determine the influence of chemical cues from
potential predators on these 2 species. We predicted that invasive geckos would show a generalized response to predator cues,
whereas the responses of native geckos would be more finely tuned
to appropriate threat levels posed by individual predators.
Materials and Methods
Native and invasive geckos
The native house gecko G. dubia is a medium-sized (up to 70-mm
snout to vent length, SVL) Australian gecko that occurs across
Cape York and central Queensland and south into the Macquarie
marshes of New South Wales (King 1983; Doughty 1996;
Figure 1). The invasive Asian house gecko H. frenatus is a small- to
medium-sized gecko (up to 60-mm SVL). Its Australian distribution is currently centered around urban areas, suggesting multiple
importations and carriage along domestic transport corridors
(Hoskin 2011; Figure 1).
We collected 117 adult native geckos and 210 adult invasive geckos
from the Townsville campus of James Cook University, Queensland
Australia (−19.330°S, 146.758°E, elevation 37 m) between September
2012 and March 2013. In the 3 h following sunset, we hand-captured
geckos from buildings, gardens, and other areas around campus. We
determined sex of all individuals (and whether females were gravid)
and measured SVL (to 1 mm), tail length (to 1 mm), and body mass
(to 0.1 g). Geckos were housed in a temperature-controlled room at
21 °C, with a night–day light cycle of 12:12 h. Individual plastic cages
(30 cm × 15 cm × 10 cm L × W × H) contained a paper substrate, a
shelter, and a drown-proof water dish. A heating strip beneath one
end of the cage created a gradient ranging from 20 to 35 °C, allowing
geckos to thermoregulate. Geckos were fed live crickets twice weekly
and cages were cleaned at least once weekly.
Snake predators
We obtained chemical cues from 4 different snake species that
vary in their ecology and diet: 1) 1 male and 1 female death adder
(Acanthophis antarcticus; Elapidae), 2) 1 male and 1 female Collett’s
snake (Pseudechis colletti; Elapidae), 3) a female spotted python
(Antaresia maculosa; Pythonidae), and 4) 2 female brown tree snakes
(Boiga irregularis; Colubridae). These predators have diverse foraging
ecologies and distributions and thus should pose different levels of
threat to both invasive and native geckos (Table 1 and Figure 1).
Death adders (Shine 1980), spotted pythons (Shine and Slip
1990), and brown tree snakes (Trembath and Fearn 2008) consume geckos and are sympatric with both the native and invasive
house geckos in northeastern Queensland (Wilson 2005; Figure 1).
Spotted pythons and brown tree snakes are similar in their foraging
strategies, though the former uses more ambush and the latter a
more active foraging mode (Vanderduys E, personal observation).
Death adders are ground-dwelling ambush predators, presumed
to be active at all times (Vanderduys E, personal observation).
The ecology of Collett’s snakes is poorly documented, but they
consume amphibians and mammals in the wild (Shine 1991a).
Collett’s snakes are known to inhabit deep soil cracks in Mitchell
Grass Downs (Wilson 2005), which is a microhabitat rarely utilized
by either of the geckos in this study (Cogger 2000; Wilson 2005;
606
Behavioral Ecology
Figure 1
Approximate distributions of prey and predator study species in northeastern Australia. The native house gecko Gehyra dubia points are derived from Atlas
of Living Australia, clipped to land surfaces on Australia, and CSIRO (unpublished data). The remaining polygons are drawn from Atlas of Living Australia
data clipped to land surfaces and CSIRO (unpublished data). Because there is substantial overlap between brown tree snake (Boiga irregularis; Colubridae),
death adder (Acanthophis antarcticus; Elapidae), and spotted python ranges (Antaresia maculosa; Pythonidae), for clarity, we only show the area of overlap between
these 3 species (“Combined snake species”).
CSIRO, unpublished data). Other Pseudechis spp. are generalist vertebrate predators (Shine 1991a) and it is likely that Collett’s snakes
would consume reptiles, including geckos, if they were available.
The native geckos are likely to encounter spotted pythons and
brown tree snakes because of temporal and spatial overlap in foraging activity. Therefore, we predicted the threat from these species
may be high and native geckos would have antipredator responses
to indirect (i.e., chemosensory) cues from these 2 snakes (Table 1).
Because death adders consume geckos, the threat from this species
is also high, and we predicted that native geckos would avoid areas
scented by death adders (Table 1). Collett’s snakes are largely allopatric with the native gecko species and, therefore, the threat from
this species is low (Table 1). If native geckos behave in accordance
with the threat-sensitivity hypothesis, then native geckos (G. dubia)
should not avoid shelters scented by Collett’s snakes.
It is more difficult to predict the behavior of the invasive house
gecko to native snake predators because it may treat all snakes as
equally dangerous due to naivety or ignore all snakes because it
does not (or cannot) recognize them as a threat. Also, depending on
the rate of evolution, invasive geckos may have evolved responses
Cisterne et al. • Disparate responses of geckos to predators
607
to some snakes (the ones they are more likely to be encountered
and attacked by due to geographic overlap: spotted pythons, brown
snakes, and death adders) but may not respond to the Collett’s
snake because they have never encountered them.
The death adders, spotted pythons, and Collett’s snakes (5
snakes total, N = 2, 1, and 2, respectively) were obtained from
a permanent captive population. Two brown tree snakes were
captured within 10 km of James Cook University and held for
2 weeks, during which time they were not fed. All snakes were
housed in species-appropriate enclosures and provided with water
ad libitum.
Collection of predator scent
Scents were collected from donor snakes onto filter paper (Whatmans
11 cm, GE Healthcare Australia Pty Ltd). To accomplish this, distilled
water was sprayed onto papers, which were placed under each donor
snake for 48 h. We paired scented filters with unscented control filters, which were moistened and left to dry for 48 h. This allowed us
to offer individual geckos 2 microhabitats that were identical in structure, except that one contained a scented and the other contained an
unscented filter paper. To ensure that the geckos were responding to
scents, and thus using chemosensory processes, we also used a novel,
nonbiological scent as a pungency control. Pungency control filters
were moistened with diluted men’s perfume (1:10 dilution with distilled water, 9 IX by ROCA WEAR, EA fragrances Co., New York)
and left to dry for 48 h. All filters were handled with forceps that we
thoroughly cleaned between uses with distilled water; prepared filters
were used within 48 h of scent collection.
Microhabitat selection assays
Each behavioral assay trial took place in a clean plastic box (30 cm
× 11 cm × 11 cm L × W × H, internal space) containing 2 identical tile shelters, each of which was composed of 2 white ceramic tiles
(10 × 10 cm) separated by a 1 cm crevice. This created 2 identical shelters on opposite sides of the container, one of which contained a filter
paper scented by a snake or pungency control scent (perfume) and the
other of which contained a control filter paper (distilled water). Trials
took place in a temperature-controlled room maintained at 25 °C,
and the location of the scented shelter was randomized by cage.
For each trial, a single gecko was placed into a cage no more
than 30 min before the lights went out. Geckos were left to explore
the cages for the remaining light period and during the next 12 h
of darkness. One hour after the lights came on in the morning, we
noted which shelter (scented or control) each gecko had selected as
a diurnal retreat site. Individual geckos and filter papers were used
only once each to maintain statistical independence. All equipment
was cleaned thoroughly between trials by washing cages and lids with
hot soapy water; these were allowed to air dry. Ceramic tiles were
soaked in hot water, then rinsed in fresh hot water, and dried under
a 40-W heat lamp. Clean equipment was handled with new, disposable, nonpowdered latex gloves to prevent scent contamination.
Experimental treatments
Native and invasive geckos were exposed to 3 types of shelters in
3 types of trials: 1) unscented controls, 2) pungency controls, and
3) predator scents (summarized in Table 2). Approximately equal
Table 1
Ecological characteristics of the 4 snake species used as scent donors
Species
Size (m)
Activity and foraging mode
Venom
Distribution overlap with
native and invasive geckos
Consumes
geckos?
Brown tree snake,
Boiga irregularis
Collett’s snake,
Pseudechis colletti
Death adder,
Acanthophis antarcticus
Spotted python,
Antaresia maculosa
1–2
Nocturnal, roaming hunter
Yes
Both
Yes
1.5–2.5
Diurnal, roaming hunter
Yes
Neither
Likely
1
Diurnal and nocturnal,
lure and ambush
Nocturnal, ambush
Yes
Both
Yes
No
Both
Yes
1
Reference
Shine (1991b) and
Trembath and Fearn (2008)
Shine (1987) and
Wilson (2005)
Shine (1980) and
Wilson (2005)
Shine and Slip (1990) and
Wilson (2005)
All snake species include geckos in their diet; however, only brown tree snakes, death adders, and spotted pythons overlap substantially in distribution with the
gecko species used in this study (see Figure 1 for distribution maps).
Table 2
Numbers of native and invasive geckos used in each set of shelter choice trials
Control trials
Gecko species
Native house gecko,
Gehyra dubiaa
Invasive Asian house
gecko, Hemidactylus
frenatusb
Predator trials
Brown tree snake
Collett’s snake
Death adder
Spotted python
Distilled
water
Pungency
(perfume)
Snake #1
Snake #2
Snake #1
Snake #2
Snake #1
Snake #2
Snake #1
17
20
20
—
21
—
18
18
20
20
20
20
20
29
20
30
31
20
native gecko G. dubia was trialed against scents from 2 death adder (Acanthophis antarcticus) individuals and one each of brown tree snakes (Boiga irregularis),
Collett’s snakes (Pseudechis colletti), and spotted pythons (Antaresia maculosa).
bThe invasive gecko H. frenatus was trialed against scents of 2 individuals of each of death adders, Collett’s snakes, and brown tree snakes, and 1 individual
spotted python.
aThe
Behavioral Ecology
608
numbers of male and female geckos were included in each treatment, and each gecko was used only once. On any given night,
individual trials exposed geckos to all scent treatments to avoid temporal confounding effects.
1)
2)
3)
Distilled water control trials—This assay determined whether
geckos would use the crevices we offered them as diurnal shelters and whether geckos showed a preference for 1 side of the
experimental cages. For these trials, a gecko was placed into a
cage with 2 identical shelters, both containing control filters
exposed to distilled water, but no snake or other scent.
Pungency control trials—We used the pungency controls to determine if geckos avoided or selected novel chemical cues that are
unrelated to predation. For these trials, each gecko was offered
the choice between a shelter containing an unscented control
filter and a shelter containing a filter scented with perfume.
Snake scent trials—This assay determined whether the geckos
avoided diurnal shelters that contained scents collected from
potential snake predators. Each gecko was offered the choice
between a shelter containing an unscented control and a
shelter containing a filter scented by a snake (7 individuals
comprising 4 species; Table 1). We examined the responses
of invasive geckos (H. frenatus) to all 7 individual snakes and
native geckos (G. dubia) to one spotted python, one Collett’s
snake, one brown tree snake, and both death adders (Table 2).
Data analysis
Because body size can influence antipredator behaviors (Head et al.
2002; Bohorquez Alonso et al. 2010; Cooper 2011), we first tested
for body size differences between the sexes of native and invasive
geckos, using separate ANCOVAs for each species, with sex as the
factor, SVL as the dependent variable, and body mass as the covariate. Next, we assessed whether body size (SVL and mass) influenced
the choice of shelter site by geckos; that is, whether smaller or larger
geckos of the same species responded differently to predator scents.
To do this, we used a separate logistic regression for the native and
invasive gecko species, using gecko response (i.e., selecting or avoiding snake scent) as the dependent variable and SVL, tail length,
and body mass as independent variables. Due to potential problems
with colinearity among these variables, we performed a stepwise
analysis by removing the body size variable with the highest nonsignificant P value and rerunning the analysis until only one independent variable remained. Sex could not be included in the logistic
regression as an independent variable because in some treatments,
all of the individuals of 1 sex responded in the same manner to the
predator scent. Thus, to examine the effect of sex (male or female)
on diurnal shelter choice (scented or unscented), we used a separate
contingency table analysis for each gecko species.
We tested whether geckos would use the shelters provided and
whether their choice was side biased in the absence of any scents
(unscented controls). We used contingency table analyses, done separately for each gecko species, to compare the number of geckos
choosing shelters at the front or the back of the cage. Next, we
tested whether the shelter choice of native or invasive gecko species was influenced by the presence of the pungency controls in the
same manner.
Earlier work suggests that characteristics of individual scent
donors may influence the prey responses (Stapley 2003). Thus, we
tested whether geckos responded in the same manner to different
individuals of the same predator species (for the species of snakes
for which we had more than 1 individual: death adders, Collett’s
snakes, and brown tree snakes, Table 2). To do this, we compared
the geckos’ responses with the 2 individual snakes of the same species using contingency table analyses.
We also investigated whether the shelter choices of native and
invasive geckos depended on the presence of predator scent. We
used separate contingency table analyses for each gecko species
and predator species combination. Finally, we used contingency
table analyses to determine whether the native and invasive geckos
selected different retreat sites in the presence of predators that differed in their ecology (Table 1). All statistical analyses were conducted using S-plus (TIBCO Software Inc., Palo Alto, CA), and
statistical significance was assumed when P < 0.05.
Results
Effects of body size and sex on gecko responses
The body size of male and female native geckos was 58.4 ± 0.98
and 58.7 ± 0.97 mm, respectively, and the body size of male and
female invasive geckos was 52.4 ± 0.45 and 50.5 ± 0.29 mm, respectively. Mean body mass of male and female native geckos was
4.5 ± 0.23 and 4.6 ± 0.24 g, respectively, and for invasive geckos,
3.1 ± 0.10 and 2.8 ± 0.05 g, respectively. For both native and invasive geckos, mean body size did not differ significantly between the
sexes (ANCOVA with SVL as the dependent variable and mass
as the covariate; native geckos: F1,111 = 0.119, degrees of freedom [df] = 1, P = 0.731; invasive geckos: F1,182 = 1.683, df = 1,
P = 0.196).
Body size (SVL, tail length, and/or body mass) did not significantly influence shelter choices of either gecko species in the presence of predator scents (logistic regression; in all cases, models
produced independent variables with P > 0.15). The shelter choices
of geckos in each treatment were also independent of sex (contingency table analysis, P > 0.05 for both gecko species). These results
indicate that body size and sex did not significantly influence the
responses of these gecko species to the predator scents used in our
experiments, and thus, we excluded these variables from further
analysis.
Effects of distilled water and pungency controls
on gecko responses
When presented with the choice between 2 shelters containing
unscented control filters, all of the native and invasive geckos tested
readily sheltered within one of the available crevices during all trials and showed no preference for a shelter on either side of the
cage (native geckos: χ2 = 0.06, df = 1, P = 0.808; invasive geckos:
χ2 = 0.8, df = 1, P = 0.371; see Table 2 for all sample sizes).
When we presented geckos with pungency controls and scents
collected from predators, some geckos were found outside of shelters in the morning, clinging to the roof of the cage (Figure 2). This
occurred in 18% of trials overall and suggested a strong avoidance
response to the scents that were offered because this behavior never
occurred in trials using unscented controls. Thus, in all remaining
analyses, we classified geckos that were clinging to the roof of the
cage in the same category with those sitting in the shelter containing distilled water; both of these behaviors indicate avoidance of
the predator scent.
The 2 gecko species differed strongly in their response to the
pungency controls. The native gecko strongly and significantly
avoided shelters with filters scented with perfume (χ2 = 9.8, df = 1,
Cisterne et al. • Disparate responses of geckos to predators
609
them in the strength of response (χ2 = 2.41, df = 3, P = 0.49;
Figure 2).
In contrast, the invasive gecko significantly avoided shelters
scented by all 4 predatory snake species (death adder: χ2 = 4.74,
df = 1, P = 0.029; Collett’s snake: χ2 = 10.80, df = 1, P = 0.001;
spotted python: χ2 = 9.8, df = 1, P = 0.002; brown tree snake:
χ2 = 10, df = 1, P = 0.002; see Table 2 for sample sizes and
Figure 2). Overall, then, invasive geckos avoided all 4 snake species
and did not differentiate among them in the strength of response
(χ2 = 3.85, df = 3, P = 0.28; Figure 2).
Discussion
Figure 2
Percentage of native Gehyra dubia (A) and invasive Hemidactylus frenatus (B)
that avoided shelters containing scent from 4 predatory snake species or
diluted perfume (“pungency control”). Snake species included the death
adder (Acanthophis antarcticus), Collett’s snake (Pseudechis colletti), brown tree
snake (Boiga irregularis), and spotted python (Antaresia maculosa). Geckos had
a choice between a shelter containing a scented filter (predatory snake
scent or diluted perfume) and a shelter containing an unscented filter.
Geckos observed in the unscented shelter (black) or on the roof (white) were
combined and scored as avoiding the predator scent. The dashed horizontal
line indicates the point at which 50% of geckos were avoiding the scented
shelter. An asterisk (*) denotes that the proportion of geckos that avoided
the scented shelter was significantly greater than 50%.
P = 0.002; Figure 2), whereas the invasive gecko was equally likely
to shelter in the crevices containing pungency controls as those containing an unscented control filter (χ2 = 0, df = 1, P = 1.0; Figure 2).
Effects of snake scent on gecko responses
In general, chemical cues from individual snakes of the same species elicited similar levels of gecko avoidance. Thus, there was no
significant difference in the responses of native (χ2 = 0.19, df = 1,
P = 0.66) or invasive geckos (χ2 = 1.0, df = 1, P = 0.32) exposed
to scents donated from either of the individual death adders.
Similarly, the responses of invasive geckos to different individual
Collett’s snakes (χ2 = 0.589, df = 1, P = 0.44) and different individual brown tree snakes (χ2 = 0, df = 1, P = 1.0) did not differ
significantly. Thus, we pooled the results from individual snakes of
the same species for the remaining predator avoidance analyses.
The native geckos selected shelter sites independently of whether
the crevice contained a snake scent or a control filter for all snake
species (death adders: χ2 = 0.11, df = 1, P = 0.74; Collett’s snakes:
χ2 = 1.19, df = 1, P = 0.28; spotted python: χ2 = 0.20, df = 1,
P = 0.66; brown tree snakes: χ2 = 0.80, df = 1, P = 0.37; see Table 2
for sample sizes and Figure 2). Overall, then, native geckos did not
avoid scents of the 4 snake species and did not differentiate among
The antipredator behavior of invasive species toward native predators may differ from that of native species, which share a longer
evolutionary history with native predators (Pennuto and Keppler
2008). We examined whether 2 ecologically similar gecko species,
one invasive and the other native, avoided diurnal shelters scented
by predatory snakes. We found that the invasive Asian house gecko
H. frenatus avoided shelters scented by all of the predators we tested
but did not discriminate between shelters scented by perfume from
unscented shelters. In contrast, the native house gecko G. dubia
avoided perfume but did not avoid any of the predator scents we
tested. The consistent avoidance of all snake scents by the invasive
gecko suggests that they have a generalized antipredator response
of wariness because avoidance was equally strong for all sympatric and allopatric predators (Figure 2). Generalized antipredator
behavior that is based on indirect predator cues could be a preadaptation for invaders, potentially reducing dangerous encounters
with numerous novel threats, and therefore assisting with invasion
success (Pennuto and Keppler 2008). Similarly, a willingness to use
novel shelters that smell of perfume suggests that these invaders are
willing to explore novel stimuli, which could also contribute to invasion success. In contrast, the avoidance of perfume by the native
geckos suggests that they may be more wary of novel stimuli.
There are 4 reasons why native geckos may not have shown a
strong avoidance response to predator scents. First, native geckos
may not have detected the scents. Clearly, however, they strongly
avoided shelters scented with perfume, demonstrating that native
geckos can detect some scents and do respond to them (Figure 2).
Second, native geckos may detect the scents but fail to associate the
scent with a threat. This seems unlikely because chemical cues from
predators elicit antipredator responses in other native gecko species (e.g., Oedura lesueurii, Webb et al. 2009) and can influence diurnal shelter selection (Downes and Shine 1998; Webb et al. 2010).
Furthermore, death adders, spotted pythons, and brown tree snakes
consume geckos and likely pose a real threat in nature (Shine 1980;
Shine and Slip 1990; Table 1). Other species of native Australian
geckos can assess the size and shape of retreat sites, their thermal
qualities, and presence of conspecifics (Croak et al. 2008; Webb
et al. 2010). This sophisticated assessment, which relies on a combination of chemical, tactile, and visual cues, may allow native geckos
to avoid shelters scented by a predator (Webb et al. 2010). Thus, it
seems unlikely that native G. dubia are simply unable to recognize
the scents of predators. A third possibility is that the experimental
chamber was too small to offer a real escape from the scent. Thus,
our native geckos may have selected any small shelter that could
offer protection against a roaming snake. In this case, the tendency
for the invasive geckos to cling to the roof of our test chambers
could suggest a propensity for flight in response to predators of this
species compared with a sheltering response. However, our native
Behavioral Ecology
610
geckos nearly always avoided the perfumed controls by sheltering in
the other shelter, suggesting that they could distinguish the location
of origin of scents in our experiments, and avoid them if they chose
to do so. Also, in the trials with invasive geckos, only 18% of individuals clung to the roof; the other individuals avoided the scented
shelter by using the other shelter, again suggesting that geckos accurately distinguish the source of the scent. Finally, a fourth scenario
is most plausible, whereby native geckos can associate the scent of
snakes with predators, but judge the act of avoiding them to be
more costly than not avoiding them, due to lack of any more direct
evidence of predator presence.
Antipredator behaviors may be useless or even counterproductive if there are never any attacks on geckos in shelters (Blumstein
2006) or if geckos frequently encounter the residual scents of predators with no associated danger (i.e., after the snake has left; Webb
et al. 2010). Indirect costs of intimidation to prey can be high and
in some cases can be responsible for mortality rates equal to those
from actual consumption (Preisser et al. 2005). Antipredator behavior can, therefore, be rapidly lost in the absence of a real threat
associated with stimuli (Blumstein 2006). The benefits of predator scent avoidance for geckos could be far outweighed by the cost
of foregoing a quality shelter when predators are common, but
attacks are rare (Lloyd et al. 2009). A study comparing predator
avoidance responses of invasive (Echinogammarus ischnus) and native
amphipods (Gammarus fasciatus) also found that the invasive species
showed stronger avoidance of native predator cues than did native
prey (Pennuto and Keppler 2008). Because of their long evolutionary exposure to native snake predators, native gecko species may
more accurately judge threat levels compared with the invasive
species. Therefore, we propose that the lack of response by native
geckos to the scents of these predators constitutes threat-sensitive
behavior and that the geckos accurately gauged that there was no
real threat from any of these scents. Assessment of predator presence using both visual and chemical cues occurs in the wall lizard
Podarcis muralis (Amo et al. 2004, 2006), and native geckos could
also rely on visual cues (such as detecting predator movement) as
direct evidence of more proximate threats. Further work is needed
to determine whether native house geckos use more immediate or
multiple cues to assess the threat of predation.
Invasive house geckos avoided diurnal shelters scented by all four
of the snake species we used, including Collett’s snakes, which are
mostly allopatric (Table 1 and Figures 1 and 2). Introduced Asian
house geckos share a common Asian biogeographic origin with
Australian elapids, pythons, and colubrids (Shine 1991b; Carranza
and Arnold 2006; Rawlings et al. 2008; Sander and Lee 2008;
Bansal and Karanth 2010) and thus may have a long shared evolutionary history at higher taxonomic levels. Even given the short
ecological history (~50 years) of invasive Asian house geckos in
Australia with these particular predator species, evolutionary exposure may have preadapted this gecko to display caution around any
Australasian snake cues (Llewelyn et al. 2011).
Generalization of antipredator responses should evolve when
ambiguity of signals from multiple predators is high, and the cost of
not responding is much higher than that of responding (Blumstein
2006; Brilot et al. 2012). Invasive house geckos may not distinguish signals from different snake species, and as the cost of an
encounter with any potential predator could be high (i.e., injury or
death), they favor an antipredatory response to all potential threats.
Generalized responses by invasive species may aid in invasion success, but ultimately these responses could be costly once established,
causing them to avoid areas where they could actually live. There
is some evidence that invasive Asian house geckos do not establish
in native vegetation (Vanderduys and Kutt 2013), and this may
be driven in part by their generalist, undiscriminating response to
native predators.
Biological invasion is a multistep process involving movement
(by transportation or natural means), introduction, establishment, and spread; failure in any of these stages results in failure
to expand the range (Chapple et al. 2012). The threat of predation is present at all of these stages, and the ability to detect
indirect predator cues may provide important benefits to prey in
terms of avoiding or reducing encounters with a predator. For
example, a strong response by individual lizards (Lampropholis
guichenoti) to predator scents correlates positively with survival during actual predator–prey encounters (Downes 2002). Avoiding
predators using indirect cues can incur energetic costs (Downes
2001; Preisser et al. 2005) that may ultimately restrict the benefits
derived from generalized antipredator responses to nonthreatening potential predators. We hypothesize that these costs would be
greater for the invasive species because the native species may be
able to use more direct cues (e.g., visual) in conjunction with scent
to better evaluate threats. Understanding the costs, benefits, and
consequences of predator avoidance will advance our ability to
understand how and why some species are more successful invaders than others and how that drives competition with native species within the invaded range.
Funding
Funding was provided by the School of Marine and Tropical
Biology at James Cook University.
We thank N. Phongkangsananan, S. Stiso, M. Vickers, R. Duffy,
A. Wootton, and students in the James Cook University Herpetology class
of 2012 for the help in collecting geckos. Our research was approved by the
James Cook University Animal Ethics Committee (approval A1825) and the
Queensland Department of Environment and Heritage Protection (permit
number WISP12103212).
Handling editor: Johanna Mappes
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