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Austral Ecology (2005) 30, 201–209
Does intraspecific niche partitioning in a native predator
influence its response to an invasion by a toxic prey species?
JONATHAN K. WEBB,1* RICHARD SHINE2 AND KEITH A. CHRISTIAN1
1
School of Science, Charles Darwin University, Darwin, Northern Territory, and 2School of Biological
Sciences, The University of Sydney, New South Wales, Australia
Abstract The introduced and highly toxic cane toad (Bufo marinus) is rapidly spreading across northern Australia
where it may affect populations of large terrestrial vertebrate predators. The ecological impact of cane toads will
depend upon the diets, foraging modes and habitat use of native predators, and their feeding responses to cane
toads. However, intraspecific niche partitioning may influence the degree of vulnerability of predators to toxic
prey, as well as the time course of the impact of alien invaders on native species. We studied the diet of the northern
death adder Acanthophis praelongus and their feeding responses to cane toads. In the laboratory, death adders from
all size classes and sexes readily consumed frogs and cane toads. Diets of free ranging A. praelongus from the
Adelaide River floodplain were more heterogeneous. Juvenile snakes ate mainly frogs (39% of prey items) and
small scincid lizards (43%). Both sexes displayed an ontogenetic dietary shift from lizards to mammals, but adult
males fed on frogs (49%) and mammals (39%) whereas adult females (which grew larger than males) fed mainly
on mammals (91%) and occasionally, frogs (9%). Feeding rates and body condition of adult snakes varied
temporally and tracked fluctuations in prey availability. These results suggest that cane toads may negatively affect
populations of northern death adders in the Darwin region. However, we predict that different size and sex classes
of A. praelongus will experience differential mortality rates over different timescales. The initial invasion of large
toads may affect adult males, but juveniles may be unaffected until juvenile toads appear the following year, and
major affects on adult female death adders may be delayed until annual rainfall fluctuations reduce the availability
of alternative (rodent) prey.
Key words: conservation, population, predation, snake, toxic prey.
INTRODUCTION
The introduction of exotic animals to new environments can have profound effects on native species and
ecological communities (Vitousek et al. 1996; Fritts &
Rodda 1998). Exotic species can negatively affect natural ecosystems by spreading novel diseases, disturbing or destroying habitats, displacing or eliminating
species through competition, predation or herbivory,
and altering native vegetation and fire regimes (Mack
et al. 2000). Given the magnitude of these effects,
predicting the impact of invading species on native
species is an important goal for ecologists and conservation biologists (Ricciardi & Rasmussen 1998; Mack
et al. 2000). However, numerous factors complicate
any such attempt, even in apparently straightforward
cases.
One such case is the introduction of highly toxic
prey species that resemble native prey species. When
*Corresponding author. Present address: School of Biological
Sciences A08, The University of Sydney, NSW 2006, Australia
(Email: [email protected])
Accepted for publication May 2004.
predators are naïve to novel toxins, they may be unable
to detect or detoxify them, so that the effects of toxic
invaders on native predators can be dramatic (Brodie
& Brodie 1999). To survive an invasion of toxic prey,
predators must learn how to avoid toxic prey or they
must evolve an ability to detoxify the novel toxins
(Brodie & Brodie 1999). To predict the ecological
impact of invasion by toxic prey, one needs to know
the probable eventual geographical range of the
invader, the feeding habits of native predators and the
physiological resistance of those predators to the novel
toxin. A recent study on the invasion of the introduced
cane toad (Bufo marinus) into northern Australia provides these data, and predicts that the toad will seriously affect 30% of Australian snake species (Phillips
et al. 2003).
Size-structured interactions between predators and
prey can also influence the impact of an exotic invader
(Werner & Gilliam 1984; Wootton 1994). In many
tropical snake populations, individuals span a wide
range of body sizes, and because the head size of a
snake limits the size of prey that it can ingest, this
body-size variation has strong implications for dietary
composition (Houston & Shine 1993). For example,
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J. K . W E B B E T A L .
juvenile snakes often eat smaller prey, and different
prey species, than do conspecific adults (Webb &
Shine 1993), and males often take different sizes and
kinds of prey than do females (Houston & Shine 1993;
Pearson et al. 2002). The resultant intraspecific niche
partitioning means that the arrival of a novel toxic prey
type may differentially affect different size, age or sex
classes within a population.
The invasion of the highly toxic cane toad
B. marinus across northern Australia offers an opportunity to examine the ways in which size-structured
interactions affect the ecological impact of toxic prey
on native species. Cane toads contain potent toxins
that are unique to toads (Daly et al. 1987), and all life
stages (eggs, tadpoles, metamorphs and adults) are
highly toxic to many invertebrates and vertebrates
(Licht 1968; Covacevich & Archer 1975; Crossland &
Alford 1998). The cane toad is currently spreading
across northern Australia and is predicted eventually
to occupy an area of approximately 2 million km2
(Sutherst et al. 1995). Cane toads have recently
invaded Arnhem Land, Kakadu National Park and the
Mary River floodplain, and based on their current rate
of spread (up to 100 km per year in river catchments),
they will colonize most of the Top End of the Northern
Territory in the next 20 years (Freeland & Martin
1985; van Dam et al. 2002).
In Australia, cane toads occupy a broad range of
habitats, attain high population densities (up to 2138
individuals per hectare, Freeland 1986), and have
much higher fecundity than native frogs (Lever 2001).
To date, most experimental studies on the effects of
toads have focused on fish, frogs and aquatic invertebrates, and several authors have concluded that toads
may not adversely affect these organisms (Freeland &
Kerin 1988; Crossland 1998; Williamson 1999). By
contrast, numerous anecdotal reports suggest that
cane toads have adversely affected populations of large
terrestrial vertebrate predators, particularly quolls,
varanid lizards and snakes (reviewed by Lever 2001).
However, the question of whether cane toads seriously
affect populations of native vertebrate predators
remains controversial (Freeland 1984; Burnett 1997).
Most significantly, two recent experimental studies
suggest that cane toads have contributed to the local
extinction of northern quoll (Dasyurus hallucatus)
populations in Kakadu National Park (Watson &
Woinarski 2003; M. Oakwood, unpubl. data 2003).
Here we investigate the likely impact of cane toads
on populations of the northern death adder Acanthophis praelongus, an ambush-foraging snake that inhabits tropical floodplains and woodlands across northern
Australia. Several authors have predicted that the cane
toad will seriously affect death adder populations in
the Top End (van Dam et al. 2002; Phillips et al.
2003). However, these studies have assumed that a
high proportion of individuals within a population will
eat frogs, and that all frog-eating individuals will eat
cane toads. Testing this assumption is critical for predicting the overall impact of cane toads on tropical
snake faunas (Phillips et al. 2003). Our approach in
this study was twofold. First, we studied a free-ranging
population of A. praelongus on the Adelaide River
floodplain, to determine which snake size classes feed
on frogs, and thus, are likely to experience mortality
from feeding on cane toads. At the same time, we used
pitfall and box traps to estimate the range of prey types
available to snakes, and to establish whether prey
abundance fluctuated temporally. The second part of
our study involved a laboratory experiment to test the
critical assumption that death adders that feed on
frogs would also feed on cane toads. Our data come
from a population of snakes that have not yet encountered cane toads, but will probably contact toads
within one year.
METHODS
Study species and study sites
The northern death adder is a medium-sized (to
90 cm snout–vent length (SVL), 400 g), viviparous,
nocturnal, elapid snake that inhabits a range of habitats (open woodlands, floodplains, rocky hills) across
northern Australia (Cogger 2000). We studied the
feeding ecology of A. praelongus on the Adelaide River
floodplain 70 km east of Darwin, Northern Territory,
Australia. Males and females from this population
grow rapidly and reach sexual maturity at 12 and
18 months, respectively (Webb et al. 2002). Female
death adders attain larger body sizes than do male
conspecifics (mean adult SVL of 612 vs. 457 mm,
respectively, Webb et al. 2002). Males and females
have similar-sized heads at the same body size (Shine
1980). The vegetation on our study sites (east of
Beatrice Hill) has been altered by the construction of
levee banks and the introduction of para grass Brachiaria mutica for buffalo grazing, while the western
floodplain has large stands of introduced Mimosa
pigra. Temperatures are high year-round (monthly
mean maxima 31–34∞C, minima 15–24∞C), but precipitation is highly seasonal with 75% of the annual
rain falling from December to March.
Field sampling
From November 1996 to November 1999, we captured death adders by slowly driving the Arnhem
Highway (4 km either side of Adelaide River) and the
Beatrice Hill road. We searched for snakes from
15 min before sunset until 1 h after dusk (when snakes
E F F E C T S O F C A N E TOA D S O N D E AT H A D D E R S
were most active) on 16 nights each month. Within
16 h of capture, we weighed (to the nearest gram),
measured (SVL and tail length, to the nearest millimetre) and determined the sex (by manual eversion of
hemipenes) of all snakes (see Webb et al. 2002 for
details). We palpated stomachs for prey but did not
force snakes to regurgitate prey items. Snakes with
large prey items in stomachs were kept at ambient
temperature until they defecated (usually within 2–
3 days). We recorded whether snakes defecated during
handling and placed any fecal samples in vials with
70% ethanol for subsequent prey identification. Prey
were identified to species where possible using hair
analysis (Brunner & Coman 1974) and by microscopic
comparison of scales and hair with those from our
reference collection. Except for gravid females or
snakes with large prey in their stomachs, we released
each snake at the point of capture within 24 h.
We used pitfall-traps and Elliott traps to estimate
prey availability during the wet and dry seasons. To
sample small lizards and ground-dwelling frogs, we
placed 29 pitfall traps (20 L plastic buckets) in three
lines of 10, 10 and 9 traps (each trap 10 m apart, each
trap line 20 m apart) on the Adelaide River floodplain
adjacent to Beatrice Hill. We opened pitfall-traps for
4–6 consecutive nights during the 1997 early wet season (20 October-6 November 1997, 116 trap nights),
1998 dry season (10 June-14 August, 155 trap nights)
and 1999 dry season (21 July-2 August 1999, 174 trap
nights). We were unable to open pitfall-traps during
the wet seasons of 1997 or 1998 because of cyclonic
flooding in both years. We used Elliott traps baited
with a mixture of peanut butter and oats to capture
small mammals. We placed traps on two transects of
25 traps (each trap spaced 10 m apart), one transect
in the open floodplain and another adjacent to thick
para grass on the road edge. Radio-tagged death
adders used both habitat types during the study ( J.
Webb, unpubl. data 1999). During each trapping
period, we placed traps in the same locations, opened
them for 3–4 consecutive nights and checked them at
sunrise. Sampling dates and total number of trap
nights were 12–14 August 1998 (150 trap nights), 27–
29 November 1998 (75 trap nights) and 29 July-1
August 1999 (200 trap nights).
For captures of frogs and lizards, we recorded trap
number, SVL and tail length (with a ruler, to the
nearest millimetre) and sex, but we did not individually mark them. For the small marsupial Planigale maculata, we measured body length (SVL, with a ruler, to
the nearest millimetre), mass (to nearest 0.1 g), and
sex, and individually toe-clipped each animal. For
each mammal captured in Elliott traps (Rattus colletti
and Melomys burtoni) we recorded the trap number,
and body length, mass (to the nearest gram), sex, and
reproductive status. Each mammal was marked with a
small individually numbered ear tag.
203
Feeding responses of death adders in the laboratory
The critical assumption underlying predictions of cane
toad impact is that all individuals within a predator
population will treat toads as potential prey items.
However, some size and/or sex classes within a population might not consume toads whereas other size/sex
classes might feed readily upon them. To test this
assumption, we captured 33 snakes (9 females: mean
SVL = 453 mm, range 300–690 mm; 24 males:
mean SVL = 430 mm, range 292–550 mm) from the
Darwin region during the 2002–2003 wet season. We
placed snakes individually in plastic cages measuring
38 cm ¥ 31 cm ¥ 23 cm to 45 cm ¥ 35 cm ¥ 26 cm,
depending on snake body size, in a room maintained
at 28–32∞C, under natural photoperiod. We kept
snakes in captivity for brief periods (<1 month) and
tested their feeding responses to terrestrial frogs and
cane toads. We offered each snake one to eight individual frogs (mean = 4.76) from seven species that
were locally abundant on the Adelaide River floodplain. For each trial, we placed a freshly collected
ingestible-sized frog in each death adder’s cage in the
evening (17.00 hours), and recorded its fate (alive,
ingested or killed but not eaten) the following morning
(08.00 hours). Two days later, we offered the same
snake a different anuran species, and recorded its fate.
The order in which each frog species was presented to
snakes was randomized, but occasionally we made
multiple tests on the same snake with the same prey
species when alternative frog species were unavailable.
Because cane toads are highly toxic to death adders
(Phillips et al. 2003), we only offered cane toads to 19
randomly chosen snakes. To minimize the risk of mortality to these snakes, we vigorously squeezed the
parotid glands of each toad to expel the toxin (Meyer
& Linde 1971) before placing it into the snake’s cage.
The feeding trials allow us to examine the influence of
sex and body size on the propensity of the snakes to
treat anurans and cane toads as prey.
RESULTS
Prey availability on the floodplain
We captured three species of small mammals, three
species of scincid lizards and two species of frogs in
pitfall and Elliott traps (Table 1). Vertebrates captured
most frequently in pitfall-traps included small skinks
(Carlia gracilis), frogs (Limnodynastes convexiusculus),
and small carnivorous marsupials (P. maculata).
Larger skinks (Glaphyromorphus douglasi and Tiliqua
scincoides) were captured less frequently (Table 1).
Two species of rodent, the grassland mouse M. burtoni
and the dusky rat R. colletti were captured in Elliott
204
J. K . W E B B E T A L .
Table 1. Numbers of amphibians, reptiles and small mammals captured in pitfall and Elliott traps during the wet and dry
seasons on the Adelaide River floodplain adjacent to Beatrice Hill
Prey species
Frogs
Limnodynastes convexiusculus
Litoria nasuta
Lizards
Carlia gracilis
Glaphyromorphus douglasi
Tiliqua scincoides
Snakes
Rhinoplocephalus pallidiceps
Mammals
M. burtoni (Elliott traps)
P. maculata
R. colletti (Elliott traps)
Year and season
1998
Wet
Prey size
(SVL or mass)
1997
Wet
1998
Dry
1999
Dry
20–40 mm
35–40 mm
71
2
22
0
–
–
25
0
24–41 mm
50–83 mm
300 mm
4
6
0
22
0
0
–
–
–
17
2
1
220 mm
0
0
–
1
18–50 g
2–20 g
42–200 g
–
–
–
11 (0.07)
16 (0.09)
0 (0)
1 (0.01)
18 (0.15)
35 (0.47)
24 (0.12)
3 (0.02)
39 (0.20)
Numbers of individual Planigale maculata, Melomys burtoni and Rattus colletti captured per trap night (captures/total trap
nights) are shown in parentheses. The symbol ‘–’ denotes that no trapping was carried out in that season due to cyclonic
flooding of the study sites. No Elliott traps were available during the 1997 wet season. SVL, snout–vent length.
Table 2. Prey items recorded from 114 individual northern death adders Acanthophis praelongus from the Adelaide River
floodplain, Northern Territory, Australia
Juveniles
Prey species
Lizards
Carlia gracilis
Glaphyromorphus douglasi
Frogs
Unidentified frogs
Mammals
Melomys burtoni
Planigale maculata
Rattus colletti
Birds
Unidentified bird
Males
SVL < 400 mm
(n = 32)
n
%
F
Adults
Females
SVL < 500 mm
(n = 41)
n
%
F
Males
SVL ≥ 400 mm
(n = 30)
n
%
F
Females
SVL ≥ 500 mm
(n = 11)
n
%
F
11
4
34.4
12.5
34.4
12.5
17
1
37.0
2.2
41.5
2.4
2
2
6.1
6.1
6.7
6.7
0
0
0
0
0
0
13
40.6
40.6
17
37.0
41.5
16
48.5
50.0
1
9.1
9.1
1
3
0
3.1
9.4
0.0
3.1
9.4
0.0
2
7
0
4.3
15.2
0.0
4.9
17.1
0
7
5
1
21.2
15.1
3.0
23.3
16.7
3.3
2
1
7
18.2
9.1
63.6
18.2
9.1
63.6
0
0.0
0.0
1
4.3
2.4
0
0.0
0.0
0
0
0
The table shows the number of individual snakes containing each prey type (n), the percentage of the total numerical diet
(%) and the proportion of individual snakes containing each prey type (F). Numbers in parentheses show the number of
individual snakes that contained identifiable prey items. Note that some snakes had ingested multiple prey types. SVL, snout–
vent length.
traps. The abundance of both of these species varied
temporally at our study site (Table 1). The dusky rat
was not captured on the floodplain in the 1998 dry
season, but was captured in large numbers during
the 1998–99 wet season and the 1999 dry season
(Table 1).
Diets of death adders in the field
Dietary information was obtained from 114 individual
snakes. Northern death adders fed on two species of
scincid lizards and three species of small mammals,
plus unidentified frogs and birds (Table 2). Most death
adders sampled had only ingested a single prey type,
but three juvenile females and one adult male had
ingested skinks and P. maculata, one juvenile female
had eaten M. burtoni and a bird, and another adult male
had ingested M. burtoni and R. colletti (Table 2). The
diet of juvenile snakes consisted mainly of small lizards
(43% of numerical diet) and frogs (39%, Table 2). A
strong ontogenetic shift in prey type from lizards to
mammals occurred in both sexes. Adult males rarely
consumed lizards, and fed mainly on frogs (48% of
E F F E C T S O F C A N E TOA D S O N D E AT H A D D E R S
205
25
20
15
10
5
0
100–200
201–300
301–400
401–500
> 500
Snake snout-vent length (mm)
Fig. 1. Relationship between snake body size (snout–vent
length) and prey type and size for free ranging Acanthophis
praelongus from the Adelaide River floodplain. The figure
shows the number of individual snakes in each 100 mm
snake size class containing ( ) small scincid lizards, ()
unidentified frogs, and small- to medium-sized mammals.
The three mammal species ranged in body size from () the
small Planigale maculata (2–20 g), ( ) the medium-sized
Melomys burtoni (18–50 g), and ( ) the large dusky rat
Rattus colletti (42–200 g).
numerical diet) and mammals (39%). By contrast,
adult females fed almost entirely on small mammals
(91%, Table 2). Based on the mean body size of the five
major prey types (frogs, skinks, M. burtoni, P. maculata
and R. colletti) larger snakes ate larger prey (Fig. 1).
Analysis of variance showed the body size (SVL) of
snakes differed significantly with respect to prey type
(F4,103 = 31.7, P < 0.0001). Post hoc tests (Fisher’s
PLSD) showed that snakes that fed on R. colletti were
significantly larger (mean SVL = 619 mm) than snakes
that fed on frogs, M. burtoni and P. maculata (mean
SVL = 402.6 mm) and snakes that fed on skinks (mean
SVL = 301.5 mm).
Feeding rates of snakes in the field
Of 282 death adders captured over the 3-year period
(November 1996–November 1999), only 3% of
snakes (8 of 282) contained large prey items (as
detected by palpation). Because we kept snakes at
ambient temperature for 12–16 h before processing
them, most snakes would have already digested small
prey items (frogs and lizards) by this time (Bedford
1996). Thus, the proportion of field-collected snakes
that defecate may provide a better estimate of feeding
rates in the wild. In this study, 34% of death adders
(97 of 282 snakes) defecated when we measured them.
Of these animals, a significantly higher proportion of
juveniles (47%) defecated compared to adults (22%,
67 of 143 vs. 30 of 139 adults, c2 = 19.95,
P < 0.0001).
Fig. 2. Feeding rates and relative body condition of juvenile (solid bars) and adult (open bars) northern death adders
captured in successive wet seasons (November–May) during
a 3-year (1996–99) study. The figure shows (a) the relative
body condition of snakes and (b) the proportion of recently
fed snakes. Body condition was estimated using the residuals
from a linear regression of log-transformed snout–vent
length on log-transformed mass, but gravid females were
excluded from this analysis. Note that the body condition of
death adders was lowest during 1997 following cyclonic
flooding of our study sites in December 1996 and January
1997. Error bars denote standard errors.
We examined yearly variation in feeding rates by
comparing the proportions of adults and juveniles that
had recently fed (= those snakes that defecated) during
the wet season (November–May) over the 3-year
study. Proportions were arcsin transformed before statistical analysis (Underwood 1997). A two-factor analysis of variance, with year and snake size as factors,
showed a significant effect of snake size (F1,25 = 6.99,
P = 0.01) but no effect of year (F1,25 = 0.55, P = 0.58)
and no interaction between snake size and year
(F1,25 = 0.86, P = 0.17). Juvenile snakes fed more frequently than did adults and the pattern was consistent
across years (Fig. 2).
We used analysis of covariance (ANCOVA) to test
whether snake body condition varied significantly
among years within each snake size class (adults vs.
juveniles). For each snake size class, we computed the
ANCOVA with year as the factor, log-transformed SVL
as the covariate, and log-transformed mass as the independent variable. For juveniles, the ANCOVA showed
that slopes were parallel (F1,113 = 0.67, P = 0.51), with
no significant effect of year on snake body condition
(F1,115 = 2.17, P = 0.12). For adults, the ANCOVA
showed that slopes were parallel (F2,103 = 1.98,
206
J. K . W E B B E T A L .
P = 0.14), but snake body condition differed significantly among years (F2,105 = 3.55, P = 0.03). Post hoc
tests (Fisher’s PLSD) showed that adult snakes were
in better physical condition (i.e. were heavier relative
to SVL) in 1998–99 than in other years (see Fig. 2).
Adult body condition was highest in the year in which
small mammals were abundant on the floodplain
(Table 1).
Feeding responses of death adders in the laboratory
We tested 33 death adders in 196 feeding trials.
Because of ambiguity in interpreting cases where
snakes killed anurans but did not eat them (perhaps
these were defensive strikes not feeding responses), we
omitted these trials (n = 12) from our analyses. Overall, 91% of death adders that were offered frogs consumed them. Most snakes ate a high proportion of
the frogs that were offered to them (mean = 0.83,
SD = 0.38), and there was no obvious rejection of
particular prey species. Death adders readily consumed individuals of seven species of frog (Cyclorana
australis 78% of 36 offered, Cyclorana longipes 100%
of 13, L. convexiusculus 83% of 23, Limnodynastes
ornatus 78% of 23, Litoria nasuta 81% of 53, Litoria
tornieri 100% of 4 and Uperoleia lithomoda 100% of 5).
We then compared the feeding responses of snakes
offered both frogs and toads (n = 19 snakes) and
snakes offered only frogs (n = 14). The proportion of
individuals that consumed toads (16 of 19 snakes) was
similar to the proportion of snakes that consumed
frogs (11 of 14 snakes, c2 = 0.17, 1 d.f., P = 0.68).
Snakes that were offered both frogs and toads consumed cane toads as readily as frogs (toads were consumed in 78% of trials, frogs in 83% of trials, paired
t-test, t = 0.52, 18 d.f., P = 0.61). Although we
attempted to ‘detoxify’ the cane toads before the feeding trials, six snakes died after ingesting cane toads.
Logistic regression suggested that the willingness of a
snake to consume a toad was not affected by its sex
(c2 = 0.18, 1 d.f., P = 0.67) or body size (c2 = 1.37,
1 d.f., P = 0.24).
DISCUSSION
Predicting the effects of alien invaders on native species is an important goal for ecologists and wildlife
managers, and can help to identify high-risk species
before the invasion (Ricciardi & Rasmussen 1998;
Mack et al. 2000). The short-term impact of cane
toads on predator populations will depend on predator
diets, their propensity to attack and ingest cane toads
and their ability to detoxify cane toad toxins. Our field
data show that frogs are numerically important prey
for northern death adders. Although we could not
determine which frog species were ingested by death
adders in the wild, our feeding trials showed that
A. praelongus consumed seven species of terrestrial
frogs, including one species (C. australis) that superficially resembles cane toads. Most importantly, a high
proportion (84%) of death adders that were offered
cane toads ingested them. Snakes of all size and sex
classes consumed both frogs and cane toads under
laboratory conditions. This is a critical observation,
because it falsifies the alternative possibility that some
individuals within the population might eat frogs but
not cane toads. Thus, our study confirmed an important assumption of previous studies, namely that frogeating snakes will also eat cane toads (van Dam et al.
2002; Phillips et al. 2003). Because A. praelongus cannot detoxify cane toad toxins (Phillips et al. 2003), our
results suggest that cane toads will cause high mortality rates in death adder populations. However, the
interaction between toads and snakes may not be
straightforward because of complications arising from
intraspecific dietary divergence.
In the field, northern death adders displayed a
strong size-based dietary shift, with juveniles feeding
on lizards and frogs, and adult females feeding mainly
on small mammals. Similar ontogenetic shifts in prey
size and type from small ectothermic prey (lizards)
to larger endothermic prey (small mammals) occur
among larger Australian elapids (Webb & Shine 1998),
including the congeneric Acanthophis antarcticus
(Shine 1980). This variation in consumption of frogs
with the size and sex of a snake has strong implications
for the way in which the toad invasion will influence
snake demography. Because juveniles and adult males
feed heavily on frogs, these two life stages will be most
seriously affected by the cane toad invasion. However,
the initial toad invasion is characterized by large toads
(Freeland 1986) that are too bulky for juvenile death
adders to swallow. Thus, we predict that adult males
will suffer high mortality rates (via ingestion of toads)
during the initial invasion, whereas juveniles will experience high toad-induced mortality rates during the
following year when juvenile toads appear in high densities (Freeland 1986). The larger adult female snakes
are likely to remain relatively unaffected so long as
mammalian prey are abundant. As soon as rainfall
patterns result in low rat numbers, a condition which
occurs frequently in this system (Redhead 1979;
Madsen & Shine 1999), adult female snakes are likely
to switch to toads, and would experience high mortality rates as a result. We thus predict that the impact of
the cane toad invasion on populations of northern
death adders will be spread out over several years, and
could involve successive waves of mortality that affect
adult males, then juveniles of both sexes, and then
adult females.
These predictions are based on the assumption that
adult females will eat cane toads when alternative
E F F E C T S O F C A N E TOA D S O N D E AT H A D D E R S
mammalian prey is unavailable. Our laboratory feeding
trials confirmed this assumption, and already there are
reports of large female A. praelongus dying after ingesting cane toads (G.S. Bedford, pers. comm. 2004).
Importantly, two features of cane toad biology make
our laboratory trials relevant to the situation that will
occur after cane toads invade tropical floodplains.
First, cane toads attain massive abundances within
2 years after colonization (Freeland 1986), so that
encounter rates between snakes and toads will be high.
Second, death adders are ambush foragers that utilize
caudal luring to bring prey to within striking distance
(Carpenter et al. 1978). The caudal lure (modified tailtip) of A. praelongus increases in size and changes
colour (from white to black) with increasing snake size
(J. Webb, unpubl. data 1999). Cane toads are strongly
attracted to black, wriggling objects (Ingle & McKinley
1978) and may be attracted to the caudal lure of adult
death adders. We thus anticipate many fatal encounters
between cane toads and adult female death adders as
the toads invade tropical floodplains.
The availability of alternative prey may also influence predator vulnerability during the toad invasion.
Feeding rates and body condition of adult northern
death adders of both sexes varied temporally (Fig. 2),
presumably because cyclonic flooding of our study
sites in the 1996–97 wet season caused substantial
decreases in rodent abundance (Table 1). Previous
studies have found strong links between rainfall patterns and annual changes in rodent abundance on
these floodplains (Redhead 1979; Williams 1987;
Madsen & Shine 1999). Because few large prey were
available to death adders during years with low mammal abundance (Table 1), many snakes were in poor
physical condition (Fig. 2). However, large prey will
be super-abundant once cane toads invade the system.
In years when rodents are scarce, death adders will
likely feed on the most abundant alternative prey (cane
toads). This type of prey switching, with predation on
cane toads and the subsequent death of the predator,
was reported for the carpet python Morelia spilota, a
species that does not usually eat anurans (Covacevich
& Couper 1992). Thus, the timing as well as the
magnitude of the impact of cane toads on the adult
A. praelongus population may depend on the abundance of small mammals. Toads may exert their impact
on adult death adders immediately, if they arrive in a
year when mammals are scarce. Alternatively, there
may be little impact of cane toads for several years if
recent weather conditions have resulted in high rodent
numbers on the floodplain (Madsen & Shine 1999).
In conclusion, our results suggest that cane toads
will cause population declines of death adders from
the Darwin region. However, the persistence of
A. praelongus in northern Australia will depend on the
impact of cane toads on other death adder populations, the nature of the impact (is it short- or long-
207
term?), and on the level of dispersal between populations (Thompson 1994). Predicting the impact of
cane toads on other death adder populations is difficult, particularly if they display geographical variation
in their diets and feeding responses, as occurs in some
snake species (Drummond & Burghardt 1983). If
most individuals from other populations do not attack
cane toads, the direct impacts of toads on such populations may be less severe. Future laboratory studies
are urgently needed to evaluate this possibility. If
our results are applicable to other populations of
A. praelongus, then conservation measures will be
urgently needed to prevent the extinction of this species. We do not advocate the translocation of death
adders to snake-free islands, as this could create serious problems for native predator-naïve animals on
such islands (as occurred on Guam, Savidge 1987;
Fritts & Rodda 1998). An alternative conservation
strategy is to set up toad exclosures or toad quarantine measures on offshore islands that currently
harbour populations of A. praelongus (e.g. on Quail
Island near Darwin). The status of vulnerable (floodplain) populations of A. praelongus could also be
monitored each year by counting death adders on
transects (bitumen roads) in the hour after dusk during the mating season (November, Webb et al. 2002).
Long-term population studies are needed to assess
the ecological impacts of cane toads on tropical snake
faunas, and to test the hypotheses that we have developed within this article.
ACKNOWLEDGEMENTS
We thank Peter Fisher, Jenny Koenig, Thomas
Madsen, Myfanwy Runcie and Tim Schultz for their
assistance in the field, and Gavin Bedford for carrying
out feeding trials in the laboratory. The Northern
Territory Department of Primary Industries and Fisheries and the Parks and Wildlife Commission of the
Northern Territory kindly allowed us to work on the
floodplain adjacent to Beatrice Hill. Martin Whiting,
Mike Bull and two anonymous reviewers provided
critical comments and suggestions that helped to
improve an earlier version of the manuscript. We thank
John Woinarski and Meri Oakwood for kindly allowing
us to cite their recent unpublished work on northern
quoll populations. The work was carried out in accordance with Northern Territory University Animal
Care and Ethics Committee guidelines under the
approval of the Northern Territory Parks and Wildlife
Service (licence #7952 to J. Webb). The research was
supported financially by grants from the Australian
Research Council (to R. Shine and K. Christian) and
an Australian Postdoctoral Fellowship and Northern
Territory University Research Support Grant (to J.
Webb).
208
J. K . W E B B E T A L .
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