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Global Ecology and Biogeography, (Global Ecol. Biogeogr.) (2013) ••, ••–••
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R E S E A RC H
PAPER
The current decline of tropical
marsupials in Australia: is history
repeating?
Diana O. Fisher1*, Chris N. Johnson2, Michael J. Lawes3, Susanne A. Fritz4,
Hamish McCallum5, Simon P. Blomberg1, Jeremy VanDerWal6, Brett Abbott7,
Anke Frank2,8, Sarah Legge9,10, Mike Letnic12, Colette R. Thomas13,
Alaric Fisher8,10, Iain J. Gordon11 and Alex Kutt14†
1
School of Biological Sciences, The University
of Queensland, St Lucia 4072, Queensland,
Australia, 2School of Zoology, University of
Tasmania, Private Bag 5, Hobart, Tasmania
7001, Australia, 3Research Institute for the
Environment and Livelihoods, Charles Darwin
University, Darwin, NT 0909, Australia,
4
Biodiversity and Climate Research Centre
(BiK-F) & Senckenberg Gesellschaft für
Naturforschung, Senckenberganlage 25, 60325
Frankfurt, Germany, 5School of Environment,
Griffith University, Nathan Campus, 170
Kessels Rd, Nathan, Qld 4111, Australia,
6
Centre for Climate Change and Tropical
Biology, School of Marine and Tropical
Biology, James Cook University, Townsville,
Qld 4811, Australia, 7Ecosystem Sciences,
CSIRO, PMB PO, Aitkenvale, Qld 4814,
Australia, 8Northern Territory Department of
Land Resource Management, PO Box 496,
Palmerston, NT 0831, Australia, 9Australian
Wildlife Conservancy, PO Box 8070, Subiaco
East, WA 6008, Australia, 10National
Environmental Research Program Northern
Australia Hub, Charles Darwin University,
Casuarina, NT 0909, Australia, 11James
Hutton Institute, Invergowrie Dundee DD2
5DA, Scotland, UK, 12School of Biological,
Earth and Environmental Sciences, University
of New South Wales, Randwick, NSW 2052,
Australia, 13TropWATER, James Cook University,
Townsville, Qld 4811, Australia, 14School of
Marine and Tropical Biology, James Cook
University, Townsville, Qld 4811, Australia
*Correspondence: Diana O. Fisher, School of
Biological Sciences, Goddard building (8), The
University of Queensland, St Lucia, Qld 4072,
Australia. E-mail [email protected].
†Current address: PO Box 151, Ashburton, Vic
3147, Australia.
© 2013 John Wiley & Sons Ltd
ABSTRACT
Aim A third of all modern (after 1500) mammal extinctions (24/77) are Australian
species. These extinctions have been restricted to southern Australia, predominantly in species of ‘critical weight range’ (35–5500 g) in drier climate zones.
Introduced red foxes (Vulpes vulpes) that prey on species in this range are often
blamed. A new wave of declines is now affecting a globally significant proportion of
marsupial species (19 species) in the fox-free northern tropics. We aim to test
plausible causes of recent declines in range and determine if mechanisms differ
between current tropical declines and past declines, which were in southern (nontropical) regions.
Location Australian continent
Methods We used multiple regression and random forest models to analyse traits
that were associated with declines in species range, and compare variables associated with past extinctions in the southern zones with current tropical (northern)
declines.
Results The same two key variables, body mass and habitat structure, were associated with proportion-of-decline in range throughout the continent, but the form
of relationships differs with latitude. In the south, medium-sized species in open
habitats of lower rainfall were most likely to decline. In the tropics, small species
that occupy open vegetation with moderate rainfall (savanna) are now experiencing
the most severe declines. Throughout the continent, large-bodied species and those
in structurally complex habitats (rainforest) are secure.
Main conclusions Our results indicate that there is no mid-sized ‘critical weight
range’ in the north. Because foxes are absent from the tropics, we suggest that
northern Australian marsupial declines are associated with predation by feral cats
(Felis catus) exacerbated by reduced ground level vegetation in non-rainforest
habitats. To test this, we recommend experiments to remove cats from some locations where tropical mammals are threatened. Our results show that comparative
analysis can help to diagnose potential causes of multi-species decline.
Keywords
Comparative methods, critical weight range, introduced predators, mammal
extinction, marsupials, random forest models, tropical conservation.
DOI: 10.1111/geb.12088
http://wileyonlinelibrary.com/journal/geb
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D. O. Fisher et al.
I N T RO D U C T I O N
Identifying the relative importance of multiple plausible causes
of decline is a critical step in conservation of threatened species
(Murray et al., 2011). When sets of species decline synchronously over a large area, casewise experimental treatment of all
potential causes is impractical and time consuming, or impossible if declines were historical. In these situations comparison
of the characteristics and distributions of declining versus nondeclining taxa can rapidly provide support for or discount the
plausibility of candidate causes (Fisher et al., 2003; Johnson
et al., 2007; Murray et al., 2011). Information on past causes of
decline is important for conservation of both remnant populations and species being newly impacted by a spreading threat.
For example, to minimize reintroduction failures it is crucial to
know if the original causes of extinction have been removed
(Wolf et al., 1998).
Globally, habitat loss and hunting are the major current causes
of population loss in mammals (Schipper et al., 2008), although
small invasive predators such as cats Felis catus, rats Rattus rattus
and R. exulans, and mongoose Herpestes auropunctatus have
caused many extinctions of small mammals on islands (Clavero
& Garcia-Berthou, 2005; Fisher & Blomberg, 2011). Australian
mammals have already declined substantially; in the second half
of the 19th century the geographic ranges of a third of species
(70/208) decreased by > 25%, and 24 species went extinct (Fisher
et al., 2003; Johnson et al., 2007). This wave of extinctions represents a third of all mammal extirpations globally since 1500,
although Australia has only 6% of the world’s mammal species
(IUCN, 2011). Reasons for past declines of continental Australian
mammals have been difficult to identify because the declines
accompanied multiple land use changes (pastoralism, vegetation
clearing, altered fire, grazing by introduced sheep Ovis aries,
cattle Bos taurus, B. indicus and rabbits Oryctolagus cuniculus),
invasion by non-native predators (particularly red foxes Vulpes
vulpes) and wildlife diseases following European occupation
(Fisher et al., 2003; Johnson, 2006; Johnson et al., 2007). Until
recently, it was assumed that tropical species were safe from the
process of decline that affected southern Australian mammals,
but widespread declines are now occurring in tropical marsupials
(Fitzsimons et al., 2010; Woinarski et al., 2011a). The causes are
unknown, but suggested avenues for investigation include
changes in populations of feral cats, dingoes, other feral species
such as cane toads, and changes in grazing, fire or disease
(Woinarski et al., 2011a). Cats are known to threaten declining
marsupials on northern Australian islands, but their effect on the
mainland is unclear. Woinarski et al. (2011b) found that eight of
the most severely declining mammals in northern Australia (up
to 2900 g) became extinct on all or some of a group of islands in
the Northern Territory following the introduction of cats, and
that cat predation best explained the disappearance of seven of
these. Our aim is to use comparative approaches to inform the
next course of action needed to understand and stem the causes
of tropical marsupial declines in general.
Although not as dramatic as pre-1950 population losses in
southern parts of the continent, which affected the majority of
2
Figure 1 Map of Australia showing range centres (location
record centroids) for marsupial species whose range area has
declined. Numbers represent percentage of decline. 1 = 1–24%,
2 = 25–74%, 3 = 75–89%, 4 = 90–100%. These declines were
pre-1950 in southern Australia, and post-1970 for northern
Australia. Northern species are underlined. The dotted line is
latitude -23°26′ (the tropic of Capricorn). Light shading indicates
arid regions (ⱕ 300 mm annual rainfall; primarily grassland and
shrubland), and dark shading indicates high rainfall regions
(ⱖ 1200 mm annual rainfall; variable vegetation composition and
structure including patches of rainforest).
mammal species (52%) (Fig. 1), the magnitude of these tropical
declines is globally significant and investigation of causes is
needed (Fitzsimons et al., 2010; Woinarski et al., 2011a).
Twenty-two tropical marsupial species (30%) have declined
since ~1970, and comparisons of historical and recent trapping
rate and sightings suggest that three species (the northern brush
tailed phascogale Phascogale pirata, northern quoll Dasyurus
hallucatus and fawn antechinus Antechinus bellus) have declined
> 90% in abundance in addition to range declines (Fitzsimons
et al., 2010; Woinarski et al., 2011a). In diagnosing the causes of
these current declines, it is important to distinguish between
two possibilities: (1) a process that began with the spread of
European influence across southern Australia over a hundred
years ago has finally reached the north; or (2) a novel threatening process is now affecting marsupials in northern Australia. If
there is one continent-wide process at work, then it may be
possible to learn from the past to predict the course of current
declines and help prevent further extinctions. If the southern
and northern causes of decline are different, new tactics in marsupial conservation may be needed.
In southern (non-tropical) Australia, a set of morphologically
and ecologically similar mammal species disappeared rapidly
and synchronously in the 19th and early 20th century (Burbidge
& McKenzie, 1989; Johnson, 2006). Analysis of the attributes of
declining versus non-declining species has consistently revealed
Global Ecology and Biogeography, ••, ••–••, © 2013 John Wiley & Sons Ltd
Causes of tropical marsupial decline
an association with body size and climatic region (Burbidge &
McKenzie, 1989; Johnson, 2006). Very small-bodied species and
those in regions with relatively high rainfall and dominated by
forest (where human density is highest) were safe from declines,
whereas medium-sized (‘critical weight range’, Burbidge &
McKenzie, 1989) species and those in relatively arid, grasslanddominated regions declined. The critical weight range concept is
entrenched in Australian conservation biology and policy to the
extent that the term has come to mean ‘threatened Australian
mammal’. Some studies have also identified ground-dwelling
species as the most extinction-prone, and species that are carnivorous or arboreal, or inhabit rock outcrops as least
extinction-prone (Burbidge & McKenzie, 1989; Smith & Quin,
1996; Johnson, 2006; Johnson & Isaac, 2009). A widely held
explanation for these patterns was that changes in primary productivity due to grazing, combined with altered fire regimes and
drought increased the probability of extinction of mediumsized mammals in arid areas (Burbidge & McKenzie, 1989;
Johnson, 2006). Extinctions have also been blamed on exotic
wildlife disease (Abbott, 2006). An introduced predator that is
common in southern Australia but absent from the north (the
red fox) was viewed as a secondary contributor to extinction
after land use change but is now hypothesized to be the major
cause of past marsupial losses in southern Australia by many
authors. This view is based on four lines of evidence: (1) the fox
hunts medium-sized mammals at ground level, and does not
occur in rainforest or in the tropics, where mammals were stable
(Johnson, 2006); (2) studies of the timing of some marsupial
declines show that these coincided with the historical arrival of
foxes in southern Australia (Friend, 1990; Short, 1998; Abbott,
2001); (3) populations of some declining mammals have recovered after foxes were poisoned (Kinnear et al., 2002; Dexter &
Murray, 2009); and (4) comparative analyses of spatial overlap
of potential threats show that high densities of dingoes (Canis
lupus) are correlated with mammal persistence, but high densities of sheep and foxes are correlated with native mammal
declines (Fisher et al., 2003; Johnson et al., 2007). This is likely
to be because dingoes reduce the density of foxes in pastoral
areas of southern Australia (Johnson et al., 2007; Letnic et al.,
2011). Causes of past mammal extinction in Australia remain
substantially unresolved (Johnson, 2006), and there has been no
quantitative analysis of potential causes of recent tropical
declines.
Comparative analysis of extinction risk is popular in conservation biology, but its usefulness for informing specific conservation actions has been questioned (Fisher & Owens, 2004;
Cardillo & Meijaard, 2012). Cardillo & Meijaard (2012) recently
suggested that this method is irrelevant to important conservation questions. Most authors use comparative analysis to suggest
priorities for future conservation and to develop theory
(Cardillo & Meijaard, 2012). However, detailed, regional analyses that incorporate information on extrinsic threats are more
likely to be successful in refining sets of potential causes of
extinction to be urgently addressed (Fisher & Owens, 2004;
Murray et al., 2011). Here, we test if traits and environmental
associations of declining marsupial species in the Australian
tropics (north of the Tropic of Capricorn) differ from those in
the south, and rapidly identify plausible causes of current tropical declines, including putative roles of introduced predators.
METHODS
Data and definitions
We compiled a dataset of ecological and life history traits that
have been used to support explanations for past marsupial
declines (Appendices 1 and 2 in Supporting Information). These
were mean female body mass; pre-decline geographic range size
(based on digitized maps in Van Dyck & Strahan, 2008); mean
litter size; diet rank based on increasing protein and energy
content [1 = grass/leaves, 2 = seeds, forbs, grass, roots and fungi,
3 = nectar, gum and insects (insects < 50% of the diet) or fruit,
leaves and insects (insects < 50% of the diet), 4 = insects or
vertebrates (> 50% of the diet)]; habitat number (number of
categories of vegetation structure in which the species occurs,
with a maximum of 33); mean rank of habitat openness (based
on standard categories of height and structural complexity
of vegetation; Specht, 1970) 0 = grassland or shrubland, 1 =
woodland (e.g. Acacia or open Eucalypt woodland), 2 = both
woodland and forest, 3 = forest (e.g. dry or wet sclerophyll),
4 = rainforest (including subtropical, tropical or monsoon
forest). We also calculated the latitude of the range centroid, and
mean rainfall in the geographic range (modelled using ArcMap
10, with precipitation based on 30-year climate averages and
splined using Anuclim 5.2 (http://fennerschool.anu.edu.au/
research/products/anuclim) and a 1-km DEM), based on location records of each species in the following databases: The
CSIRO Australian National Wildlife Collection, Museum of Victoria, Atlas of NSW Wildlife, NT fauna database, QWILDNET,
Biological Survey of South Australia, South Australian Museum,
Victorian Biodiversity Atlas Fauna Records, Western Australian
Museum specimens database, and the Western Australian DEC
Fauna Survey Database).
We classified species as northern (distributed in the tropics)
or southern (not distributed in the tropics). The response variable, proportional range decline, was based on digitized maps of
original and current ranges in Van Dyck & Strahan (2008) (see
Appendix S1). These data are based on collection records and
recent subfossils. Because maps were published in 2008, and as
an additional source of evidence, we examined the correlation
between proportional range decline and ‘decline rank’ (Appendix S2, Fisher et al., 2003; Johnson et al., 2007), a measure based
on more recent expert opinion of distributional decline and
used in IUCN assessment criteria. For northern marsupials,
decline ranks were derived from sources published in 2010 (see
Appendix S2). These sources include Fitzsimons et al. (2010),
which is based on two workshops on Australian tropical
mammal declines (attended by most authors). The decline rank
and proportional decline metrics were strongly correlated
(F 1,175 = 446, P < 0.0001, r2 = 0.72). Our aim was to compare
historic (19th and early 20th century) southern declines with
recent (post-1950) northern declines. In this paper, we do not
Global Ecology and Biogeography, ••, ••–••, © 2013 John Wiley & Sons Ltd
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D. O. Fisher et al.
compare these two events with a third event of recent southern
declines because recent changes to some southern species ranges
(e.g. the bilby Macrotis lagotis and kowari Dasyuroides byrnei;
IUCN, 2011) have not been enough to move species between
our broad categories, and do not warrant a third level of the
dependent variable. We included all Australian marsupials,
except for nine species for which we had no data on status (black
wallaroo Macropus bernadus, northern and southern marsupial
moles Notoryctes typhlops and N. caurinus, Carpentarian pseudantechinus Pseudantechinus mimulus, Rory’s pseudantechinus
P. roryi, chestnut dunnart Sminthopsis archeri, Kangaroo Island
dunnart S. aitkeni, monjon Petrogale burbidgei and Rothschild’s
rock wallaby P. rothschildi).
Statistical analysis
To test for associations between proportion of range decline and
explanatory variables, we used two modelling approaches:
1. To find if environmental variables and traits associated with
current northern marsupial declines differ from those associated
with past southern declines, we used a multiple regression with
all Australian marsupials, including an interaction between
‘southernness’ (recent northern declines = 1 vs. pre-1950 southern declines = 2) and each independent variable. Twenty-nine
species had ranges including both northern (north of the Tropic
of Capricorn) and southern Australia; for these we included
northern populations in the northern dataset, and southern
populations separately in the southern dataset. Because we
focused on identifying differences between past southern and
recent northern declines, we omitted the northern populations
of three mainly southern species with partial ranges in the
tropics (north) from the Australia-wide dataset. These species
declined in southern Australia before 1950 and were already
known or presumed extinct or had declined to small relict populations on the mainland by 1970 (Onychogalea fraenata, Lasiorhinus krefftii and Bettongia leseur).
For multiple regressions, we tested for multicollinearity using
variance inflation factors, calculated using the ‘car’ package in R
(Fox et al., 2009). After omitting ‘litter size’ (which was correlated with body mass), no values were > 3.2 (indicating no problematic multicollinearity for either dataset). After omitting ‘litter
size’, there were no missing data. We initially used generalized
least squares to account for phylogenetic non-independence
(using the same phylogeny as in Johnson et al., 2007), and ordinary least-squares (OLS) regression models of raw species data
(i.e. without taking account of phylogeny). There was no significant difference between any of the phylogenetic (GLS) and nonphylogenetic (OLS) model results (P > 0.99 in each case), so
there was no significant phylogenetic signal. Our final models,
which we implemented with the R package ‘VGAM’ (Yee & Wild,
1996), were non-phylogenetic, and due to skewed data, we
assumed a beta binomial distribution.
2. We constructed a random forest regression tree using all
Australian marsupials. We used this model to determine the
factors that were associated with whether a species had declined
(Murray et al., 2011). This method builds a model by repeatedly
4
splitting the data based on whether they fall above or below a
threshold value of an explanatory variable (Bielby et al., 2010).
We used this method because it can identify interactions in
which the same variable repeatedly enters a model at different
levels, and it finds threshold values (Davidson et al., 2009; Bielby
et al., 2010). However, unlike multiple regression, this method
cannot account for phylogenetic structure, and the relative
strength of association of covariates with the response variable
can be difficult to interpret because small changes in values of
the covariates can alter their order in the tree (Bielby et al.,
2010). To minimize this possibility and improve classification
accuracy, our random forest approach combined a large number
of regression trees and evaluated the results by a cross-validation
process (Murray et al., 2011). Error is reported as an out-ofsample prediction error rate, in which prediction accuracy is
determined on a subset of the data different from that used to
generate the prediction. We used the package ‘randomForest’ in
R (Liaw & Wiener, 2002). To visualize the results of this analysis,
we used a single conditional inference tree based on the six
variables identified as the most strongly associated with the
response variable by the random forest analysis. The tree was
constructed using the function ‘ctree’ in the R package ‘Party’
(Hothorn et al., 2006).
RESULTS
Our multiple regression and regression tree models both indicate that the proportional range decline of marsupial species was
significantly less in northern than in southern Australia
(Table 1; Figs 1 & 2). Similar to results of past analyses of the
correlates of marsupial decline in southern Australia, results of
our multiple regressions showed that the variables most strongly
associated with proportional range decline in northern Australia
are body mass and vegetation structure or rainfall (Table 1).
Multiple regressions using all species showed that in both northern and southern regions, species in more open and drier
regions are more likely to decline, and the largest species are not
threatened (Table 1). However, the form of associations between
decline and body mass, rainfall, and diet – the key traits used to
develop previous hypotheses to explain Australian mammal
extinction – differ between north and south in both of our
models (Table 1). In particular, marsupials declining in northern Australia are smaller than species that declined in southern
Australia. Marsupials with the most substantial range declines in
the tropics are small, carnivorous species that inhabit the drier
savanna grasslands and woodlands.
The variables most strongly associated with range decline in
random forest models were body mass, vegetation structure,
rainfall, diet, litter size and whether the species occurred in
northern or southern Australia (Fig. 2). A conditional inference
tree with these six traits indicated that the effects of vegetation
structure, body mass, diet and rainfall on decline probability
differ between northern and southern marsupials, and that the
crucial (first) dichotomous split was whether a species was
northern versus southern (Fig. 2). We report the form of associations between covariates and the response variable below.
Global Ecology and Biogeography, ••, ••–••, © 2013 John Wiley & Sons Ltd
Causes of tropical marsupial decline
Table 1 Results of a beta binomial regression testing for
correlates of proportional decline in range and interactions
between southernness (presence in southern and temperate versus
northern and tropical Australia) and other explanatory variables,
using 147 species of marsupials, 29 with both northern and
southern populations. Values that were statistically significant at
alpha = 0.05 are labelled in bold. The response variable
‘proportional decline’ is calculated from maps in Van Dyck &
Strahan (2008). ‘SEM’ is the standard error of the mean.
Predictor
Coefficient
SEM
t-value
P
Intercept
Southernness
Rain
Rain2
Log(mass)
Log(mass)2
Diet
Habitat
Southernness:rain
Southernness:rain2
Southernness:log(mass)
Southernness:log(mass)2
Southernness:diet
Southernness:habitat
-9.77
4.06
-19.41
-16.65
72.94
-26.97
1.53
0.07
4.19
8.55
-25.25
8.86
-0.64
-0.21
1.71
1.00
10.99
7.97
10.71
6.85
0.52
0.46
8.98
7.35
6.19
3.82
0.29
0.27
-5.73
4.02
-1.76
-2.09
6.81
-3.93
2.93
0.16
0.47
1.16
-4.08
2.32
-2.15
0.76
< 0.001
< 0.001
0.08
0.04
< 0.001
< 0.001
0.003
0.87
0.64
0.25
< 0.001
0.02
0.03
0.45
Body size and diet
The regression analysis indicated that in the south, range decline
was greater in larger species than in the north, and range decline
was greater in species of intermediate body mass in the south
than in the north (Table 1; Fig. 3). In contrast, range decline was
greatest in small species in the north (Table 1; Fig. 3). The mean
body mass of species that have declined in the tropics is a third
of that in southern Australia (1014 ⫾ 275 g vs. 3265 ⫾ 883 g
standard error of the mean). Body mass decreased linearly as
severity of decline increased in the north, and there was a
15-fold difference in mean mass between species that had the
greatest declines in range size and species that had stable range
sizes (Fig. 3a, 264 ⫾ 135 g vs. 4025 ⫾ 759 g). These effects are
not confounded by a difference in body size distribution
between northern and southern Australia (north: 3446 ⫾ 650 g,
south: 3155 ⫾ 805 g). The regression tree based on the
Australia-wide dataset also showed that in southern Australia,
body mass was the critical variable associated with declines.
There was a threshold at 40.7 g, below which species were
unlikely to decline (Fig. 2). Species heavier than 6310 g declined
less than those with intermediate body masses (40.7–6310 g).
The regression tree model suggests that medium body mass is
not a critical factor in distinguishing how much species are likely
to decline in the tropics, but among grassland and savanna
dwelling marsupials, herbivorous species (which are relatively
large: 6763 ⫾ 1186 g) declined significantly less than carnivorous or omnivorous species (which are small: 625 ⫾ 156 g).
Tropical species with more carnivorous diets declined more
than species with herbivorous diets (55% of species that
declined were carnivorous vs. 25% of stable species). Relatively
few predators declined in the south (32%) compared with the
north (55%), but the effect of diet was minor compared with
those of body size and rainfall (Table 1).
Rainfall and vegetation structure
Marsupial declines and extinctions are concentrated in moderately dry regions in northern Australia and the driest regions in
southern Australia (Table 1; Fig. 3). The vegetation composition
and structure of both regions varies from sparsely vegetated
desert grassland and shrubland to structurally complex rainforest in zones of high rainfall. Species in regions of high rainfall
throughout Australia declined least (Table 1). The regression
tree indicated that in southern Australia, rainfall was the variable
most strongly associated with decline after body mass (Fig. 2).
All southern marsupials in the intermediate body mass range
(40.7–6310 g) and in a zone with less than 789-mm annual
rainfall declined (Fig. 2). Most species in this size range also
declined in higher rainfall regions in the south (Fig. 2). In contrast, vegetation structure is the critical variable that distinguishes declining marsupials in the tropics. Grassland and
tropical savanna species declined the most, and almost no marsupials in forest or rainforest are declining. Among nonherbivores in the relatively open grassland and savanna, > 90%
of marsupials in regions with more than 911 mm of annual
rainfall are declining (Fig. 2).
DISCUSSION
Associations between mammalian species traits and
causes of extinction
Worldwide comparative studies have concluded that small geographic range size is the most important predictor of extinction
risk in mammals, followed closely by large body size (Fisher &
Owens, 2004; Davidson et al., 2009; Fritz et al., 2009). Ecologically specialized species usually have small range sizes, which
makes them prone to extinction from habitat loss such as deforestation, because all of their habitat is likely to be lost as blocks
of vegetation are progressively eliminated (Pimm et al., 1995;
Hockey & Curtis, 2009). Large-bodied mammals are disproportionately likely to decline in response to activities associated with
high human density, particularly hunting, because they are more
profitable to hunt than smaller species, and have a lower capacity to recover due to their relatively slow reproduction (Fisher &
Owens, 2004; Fritz et al., 2009). Large mammals are more likely
to decline in the tropics than elsewhere, and global analyses
indicate that they have already been eliminated from temperate
regions that have long been settled and subject to high intensity
agriculture (Fritz et al., 2009).
We found a strikingly opposite pattern in recent tropical Australian marsupial declines; small body size signifies high current
extinction risk as measured by proportional decline in range,
and tropical rainforest specialization is associated with low
extinction risk and stable geographic ranges. Our interpretation
Global Ecology and Biogeography, ••, ••–••, © 2013 John Wiley & Sons Ltd
5
D. O. Fisher et al.
Figure 2 Conditional inference tree
based on the six variables most strongly
associated with percentage of range
decline from a random forest model.
Although litter size was included in the
analysis, it did not generate a split.
Shading represents the proportion of
species declining, and n = the number of
species in each of the final groups.
Numbers in boxes represent the node
number at which each split occurred.
Overall out-of-sample prediction error
rate was 21%, with an error rate of 16%
for non-declining species and 27% for
declining species.
of these contrasting threatened species attributes is that the
causes of northern Australian marsupial decline are different
from those in other continental tropical regions. Human population pressure, intensive hunting and accelerating vegetation
clearing such as rainforest removal for agriculture threaten
mammal diversity in most tropical countries. In northern Australia, in contrast, human population density is very low, and
most remaining rainforest (but not most savanna) is effectively
protected in national parks.
We propose that the change in mean body size of declining
marsupials as a function of latitude is pivotal to understanding
the causes of decline. Our comparative results show that body
mass, habitat structure and aridity were strongly associated with
decline throughout Australia but their relative strength and
forms of association differed between the north and south of the
continent. In the south, associations between body mass and
decline were non-linear, and species with mass between ~40 g
and 6300 g were most likely to decline according to the regression tree, particularly in areas with less than 789 mm annual
rainfall. These results are roughly consistent with previously
published estimates of ‘critical weight range’ of 35–5500 g for
southern mammal declines and extinctions generally (Burbidge
& McKenzie, 1989), and 100–5000 g for marsupials (Johnson &
Isaac, 2009). Because foxes can cause extinctions of populations
of marsupials up to ~6000 g (Short, 1998; Kinnear et al., 2002)
and are absent from rainforest (Johnson, 2006), the ‘critical
weight range’ is consistent with the hypothesis that foxes are
responsible for most marsupial declines in southern Australia.
The critical weight range idea is also the basis for other explanations of past Australian mammal extinctions, such as changed
fire regimes and changes in primary productivity due to pastoralism and agriculture (Burbidge & McKenzie, 1989). However,
our regression and random forest analysis both indicated that
6
there is no ‘critical weight range’ (over-representation of declining species at intermediate body masses) in northern Australia.
Why is there no medium-sized ‘critical weight range’
in northern Australia?
Most of the declining northern Australian marsupials are not
medium-sized but small (mean ~1 kg), carnivorous or omnivorous, and widely distributed inhabitants of regions with low to
moderate rainfall and simple vegetation structure. We can think
of no scenario in which altered fire regimes and grazing would
disproportionately affect small carnivorous species unless a
predator is part of the explanation, in addition to changes in
vegetation structure. The fox is absent from tropical Australia –
the only introduced predator of mammals in this region is the
feral cat. We propose that the association of small body size and
open vegetation with marsupials that are declining in the
tropics, combined with the lack of alternative explanations
linked to direct human population pressure or disease, implicates predation by feral cats as a probable major cause of decline
(Fisher et al., 2003; Johnson et al., 2007). The 21st century
spread of toxic cane toads Rhinella marina into and beyond
Kakadu National Park is linked to declines in the ~500 g northern quoll, which eats amphibians, unlike smaller carnivorous
marsupials, which are mainly insectivorous. However, the range
of the northern quoll contracted substantially in the late 20th
century, before toads arrived (Johnson, 2006; Woinarski et al.,
2011a).
Worldwide, severe impacts of feral cats on their mammalian
prey are linked to small prey body size, living on the ground and
open vegetation (Loss et al., 2013). In the period 1921–91, introduced cats caused the extinction of at least five species of small
mammals globally (all rodents < 2000 g), all on islands with
Global Ecology and Biogeography, ••, ••–••, © 2013 John Wiley & Sons Ltd
Causes of tropical marsupial decline
(a)
(b)
prey in southern Australia than cats because cats are suppressed
by foxes (Johnson, 2006). Burbidge & Manly (2002) showed that
the presence of cats is associated with local extinction of
medium-sized mammals on Australian islands with little rainfall
(i.e. relatively open vegetation). Cats have eliminated small
populations of arid zone marsupials such as the ~2 kg rufous
hare wallaby Lagorchestes hirsutus on the mainland (Gibson
et al., 1993).
Consistent with results of previous analyses of Australian
mammal decline (Burbidge & McKenzie, 1989; Johnson, 2006;
Johnson et al., 2007; Johnson & Isaac, 2009), we found that
desert species declined to the greatest extent in the south
(Fig. 1); however, arid zones had fewer marsupial declines than
the savanna region of moderate rainfall in the north. This might
appear to contradict the conclusion that species in open vegetation are more likely to become extinct in the tropics than in
non-tropical regions, but it is consistent with the concept of an
extinction filter (Balmford, 1996), in which marsupials in arid
regions in northern Australia declined earlier. That is, species
were eliminated from the southernmost (i.e. desert) portions of
their ranges during the earlier southern decline event and are
now absent from the tropics.
Why might the influence of cats have increased
recently?
Figure 3 Distribution of mean female body mass (a) and mean
annual rainfall (b) in the range of marsupial species with respect
to proportional range decline category, in southern (N = 97,
including species with partial ranges in the tropics) versus
northern (N = 75, including species with partial ranges in the
south) Australia. Error bars are standard errors. Categories are
0 = no decline, 1 = 1–24%, 2 = 25–74%, 3 = 75–89%, 4 = 90–100%
decline.
sparse and degraded vegetation (Mellink et al., 2002; IUCN,
2011). The feral cat in northern Australia preys predominantly
on small mammals (Kutt, 2012). Cats eat smaller prey species
than do foxes in the same areas in southern Australia (Catling,
1988; Letnic et al., 2009). Risbey et al. (2000) showed experimentally that control of cats and foxes led to a doubling of small
mammal abundance (< 50 g) in open, semi-arid regions.
Control of only foxes allowed cats to increase threefold in abundance, and deplete small mammals that had previously coexisted
with foxes (Risbey et al., 2000), supporting the widely held view
that foxes are likely to have had a greater effect on marsupial
Cats have been present on the coast around Darwin since 1827,
and inland regions of northern Australia since ~1860–1909
(Abbott, 2002), so an obvious question is why would their
impact have increased during the last 50 years? Historical
numbers were not monitored, but it is possible that tropical cat
populations have been released from former suppression as a
result of dingo declines. The control of dingoes (predators of
cats) in northern Australia has progressively intensified since the
introduction of the canid-targeting poison 1080, which was
introduced to northern Australia in the late 1960s (Fleming
et al., 2001; Kennedy et al., 2011). Dingoes may also have
declined since the 1960s due to major increases in diseases such
as heartworm, distemper and canine parvovirus (Fleming et al.,
2001). Alternatively, increasing cat impacts might be linked to
declining ground cover (see below). The pattern of mammalian
extinctions caused by cats on sparsely vegetated islands suggests
that there is a link between decreasing ground cover (density of
fallen timber with hollows, and vegetation such as grass and
shrubs) and increasing impact of cats in the tropics (Johnson,
2006).
Causes of declines in savanna-dependent marsupials
In southern Australia, pastoralism appears to have altered the
habitat of ground-dwelling marsupials in grassland, shrubland
and open woodland habitats, increasing habitat quality for
introduced predators such as foxes, reducing shelter for marsupials and increasing predator hunting success (Fisher et al.,
2003; Johnson et al., 2007; Johnson & Isaac, 2009). Sheep are
absent from northern Australia, but frequent, human-caused
Global Ecology and Biogeography, ••, ••–••, © 2013 John Wiley & Sons Ltd
7
D. O. Fisher et al.
fires and cattle grazing are concentrated in open (savanna) vegetation there and are suspected to be linked to mammal population declines (Legge et al., 2008; Woinarski et al., 2011a; Kutt &
Gordon, 2012). Replicated, large-scale experiments demonstrate
that fire is associated in a frequency-dependent manner with
reduced cover and rapid population declines of grounddwelling small mammals in tropical savanna, apparently
because frequent burning increases predation pressure (Pardon
et al., 2003). Comparisons between burnt, grazed and unburnt
plots in two other Australian tropical savanna regions have concluded that grazing amplifies the detrimental effect of fire on
small mammals, and removal of cattle combined with reduction
of fire frequency promotes mammal recovery (Kutt &
Woinarski, 2007; Legge et al., 2008). In the 1970s, when we
suggest that tropical savanna mammal declines began, cattle
grazing pressure increased because drought-tolerant Bos indicus
and hybrid cattle increasingly replaced B. taurus in northern
Australia, and there was a programme to eradicate brucellosis
and tuberculosis in cattle (McKeon et al., 1990; Redunz, 2006).
We suspect that recent tropical marsupial decline is linked to
open vegetation, small body size and ground-dwelling habits
because species with these traits are particularly susceptible to
predation by cats when grassland cover is reduced by intense
grazing or fire.
CONCLUSIONS
Our interpretation of these correlations between marsupial
ecological, environmental and life history variables and
declines in northern and southern Australia is that a single
overall process is the most likely major contributor to marsupial declines throughout the continent: introduced predators,
probably facilitated by habitat degradation. The form of associations between body mass, vegetation structure and range
decline, in particular the absence of a critical weight range in
the tropics, suggests that the agents differ between northern
and southern Australia, and we argue that that cats are most
likely to be important in recent declines in the tropics. These
results suggest that comparative analysis is not just useful for
indirect priority setting and theory development (Cardillo &
Meijaard, 2012) but also may inform practical conservation
measures when spatially extensive threats affect multiple
species. We recommend that the next course of action should
be experiments that remove cats from fenced habitat of declining marsupials (Woinarski et al., 2011a), restoration of groundlevel shelter in critical habitats of declining tropical Australian
marsupials, particularly through large scale reduction of fire
frequency and removal of cattle, to test whether cats are
responsible for declines and whether landscape scale vegetation
management can be used to reduce the impacts of cats. Given
that three marsupials and three native rodents are at risk of
imminent extinction, and more than twenty other mammals
are declining in northern Australia (Fitzsimons et al., 2010;
Woinarski et al., 2011a), we believe a response is urgently
needed to address these globally important losses.
8
ACKNOWLEDGEMENTS
The workshops that instigated the preparation of this manuscript were supported by the Australian Centre for Ecological
Analysis, a facility of the Terrestrial Ecosystem Research
Network, which is funded by the Australian Government
through the National Collaborative Research Infrastructure
Strategy and the Super Science Initiative. We thank TERN staff
and Linnaeus for funding, accommodation and practical help,
especially Alison Specht. D.O.F., H.I.M., C.N.J. and M.L. were
supported by ARC Fellowships and grants (DP0773920,
FTll0100191, DP110103069 and FT110100057). A.K. and C.R.T.
were supported by funding from the CSIRO Building Resilient
Australian Biodiversity Assets Theme. A. Frank was supported
by an ARC Linkage grant (LP100100033).
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10
SUPPORTING INFORMATION
Additional supporting information may be found in the online
version of this article at the publisher’s web-site.
Appendix S1 Table of marsupial species traits, environmental
and ecological variables.
Appendix S2 Table with sources and detailed justification of the
‘decline rank’ metric of decline severity in northern Australian
marsupials.
BIOSKETCH
The authors have research interests in conservation
ecology of Australian vertebrates and causes of
extinction in mammals, including impacts of
introduced predators, disease, climate and land use
change (http://www.aceas.org.au/). D. Fisher drafted the
manuscript, formatted and analysed data, and collected
data on southern Australian marsupial traits. D. Fisher,
C. Johnson and M. Lawes compiled the data and edited
successive drafts. S. Fritz calculated range centroids and
rainfall metrics in ArcGIS. A. Frank organized access to
databases and meta-data. H. McCallum constructed
regression tree models. J. VanDerWal and B. Abbott
modelled ranges in ArcGIS and calculated proportional
range declines. S. Blomberg constructed multiple
regressions and phylogenetic regression analyses. A.
Kutt and C. Thomas organized support for this work
through the Australian Centre for Ecological Analysis
and Synthesis, a Facility of the Terrestrial Ecosystem
Research Network which is funded by the Australian
Government through the National Collaborative
Research Infrastructure Strategy and the Super Science
Initiative. All authors helped to compile information on
tropical species declines and species traits, and to write
the final manuscript.
Editor: Erica Fleishman
Global Ecology and Biogeography, ••, ••–••, © 2013 John Wiley & Sons Ltd