Beruflich Dokumente
Kultur Dokumente
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: jwebb@bio.usyd.edu.au)
Accepted for publication May 2004.
202
J. K . W E B B E T A L .
METHODS
Study species and study sites
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
203
RESULTS
Prey availability on the floodplain
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)
Prey size
(SVL or mass)
1997
Wet
1998
Dry
1999
Dry
2040 mm
3540 mm
71
2
22
0
25
0
2441 mm
5083 mm
300 mm
4
6
0
22
0
0
17
2
1
220 mm
1850 g
220 g
42200 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, snoutvent 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
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
4.3
2.4
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.
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
0
100200
201300
301400
401500
> 500
Fig. 2. Feeding rates and relative body condition of juvenile (solid bars) and adult (open bars) northern death adders
captured in successive wet seasons (NovemberMay) during
a 3-year (199699) 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 snoutvent
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.
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 (Fishers PLSD) showed that adult snakes were
in better physical condition (i.e. were heavier relative
to SVL) in 199899 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).
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
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
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-nave 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).
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J. K . W E B B E T A L .
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