Biological Conservation 144 (2011) 1472–1480
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Biological Conservation
journal homepage: www.elsevier.com/locate/biocon
The 10 Australian ecosystems most vulnerable to tipping points
William F. Laurance a,⇑, Bernard Dell b, Stephen M. Turton c, Michael J. Lawes d, Lindsay B. Hutley d,
Hamish McCallum e, Patricia Dale e, Michael Bird c, Giles Hardy b, Gavin Prideaux f, Ben Gawne g,
Clive R. McMahon d, Richard Yu h, Jean-Marc Hero i, Lin Schwarzkopf j, Andrew Krockenberger a,
Samantha A. Setterfield d, Michael Douglas d, Ewen Silvester k, Michael Mahony l, Karen Vella m,
Udoy Saikia h, Carl-Henrik Wahren n, Zhihong Xu e, Bradley Smith o, Chris Cocklin o
a
School of Marine and Tropical Biology, James Cook University, Cairns, Queensland 4870, Australia
School of Biological Sciences and Biotechnology, Murdoch University, Murdoch, Western Australia 6150, Australia
c
School of Earth and Environmental Sciences, James Cook University, Cairns, Queensland 4870, Australia
d
Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, Northern Territory 0909, Australia
e
Environmental Futures Centre, School of Environment, Griffith University, Nathan, Queensland 4111, Australia
f
School of Biological Sciences, Flinders University, Bedford Park, South Australia 5042, Australia
g
Murray-Darling Freshwater Research Centre, LaTrobe University, Bundoora, Victoria 3086, Australia
h
School of the Environment, Flinders University, Bedford Park, South Australia 5042, Australia
i
Environmental Futures Centre, School of Environment, Griffith University, Gold Coast Campus, Queensland 4222, Australia
j
School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia
k
Department of Environmental Management and Ecology, LaTrobe University, Bundoora, Victoria 3086, Australia
l
School of Environmental and Life Sciences, University of Newcastle, Newcastle, New South Wales 2300, Australia
m
Griffith School of Environment, Griffith University, Gold Coast Campus, Queensland 4222, Australia
n
Centre for Applied Alpine Ecology, LaTrobe University, Melbourne, Victoria 3086, Australia
o
Research and Innovation, James Cook University, Townsville, Queensland 4811, Australia
b
a r t i c l e
i n f o
Article history:
Received 26 November 2010
Received in revised form 16 January 2011
Accepted 22 January 2011
Available online 21 February 2011
Keywords:
Catastrophes
Climatic change
Ecological resilience
Ecological thresholds
Exotic pests and pathogens
Feral animals
Fire regimes
Global warming
Habitat fragmentation
Invasive species
Salinization
Sea-level rise
Species extinctions
a b s t r a c t
We identify the 10 major terrestrial and marine ecosystems in Australia most vulnerable to tipping
points, in which modest environmental changes can cause disproportionately large changes in ecosystem
properties. To accomplish this we independently surveyed the coauthors of this paper to produce a list of
candidate ecosystems, and then refined this list during a 2-day workshop. The list includes (1) elevationally restricted mountain ecosystems, (2) tropical savannas, (3) coastal floodplains and wetlands, (4) coral
reefs, (5) drier rainforests, (6) wetlands and floodplains in the Murray-Darling Basin, (7) the Mediterranean ecosystems of southwestern Australia, (8) offshore islands, (9) temperate eucalypt forests, and
(10) salt marshes and mangroves. Some of these ecosystems are vulnerable to widespread phase-changes
that could fundamentally alter ecosystem properties such as habitat structure, species composition, fire
regimes, or carbon storage. Others appear susceptible to major changes across only part of their geographic range, whereas yet others are susceptible to a large-scale decline of key biotic components, such
as small mammals or stream-dwelling amphibians. For each ecosystem we consider the intrinsic features
and external drivers that render it susceptible to tipping points, and identify subtypes of the ecosystem
that we deem to be especially vulnerable.
Ó 2011 Elsevier Ltd. All rights reserved.
1. Introduction
Various vulnerability assessments have been carried out for
Australian terrestrial and marine ecosystems. Some have focused
on identifying vulnerable ecological communities (e.g. EPBC,
1999) or species (e.g. Watson et al., 2010), whereas others have assessed particular environmental threats, such as climatic change
⇑ Corresponding author. Tel.: +61 7 4042 1819; fax: +61 7 4042 1213.
E-mail address: bill.laurance@jcu.edu.au (W.F. Laurance).
and its potential impacts on biodiversity (Hennessy et al., 2007;
Johnson and Marshall, 2007; Steffen et al., 2009) and ecosystem
function (Hughes, 2003; Murphy et al., 2010).
To date, however, no assessment of Australian ecosystems has
focused explicitly on their potential vulnerability to tipping points.
Such an exercise is important because these ecosystems will face
important environmental challenges in the future (Beeton et al.,
2006). Current projections of climate change, for instance, suggest
that minimum and maximum temperatures will continue to
increase whereas precipitation will become more seasonal and
W.F. Laurance et al. / Biological Conservation 144 (2011) 1472–1480
sporadic across large swaths of the Australian continent (CSIROAustralian Bureau of Meteorology, 2007). By the end of this
century, much of southern Australia could become drier (Hennessy
et al., 2007), whereas arid and semi-arid zones of northern Australia could experience more heat waves (Tebaldi et al., 2006). Large
expanses of the Australian continent are likely experiencing fire regimes for which their ecosystems are poorly adapted (Ward et al.,
2001; Mooney et al., 2010; Setterfield et al., 2010). In the surrounding oceans, sea levels are rising while sea-surface temperatures
and acidity are both increasing (De’ath et al., 2009; Hughes et al.,
2010). Habitat loss and degradation continue apace in parts of
the continent, and many ecosystems are suffering seriously from
invasions of non-native plants and animals (Rea and Storrs,
1999; Rossiter-Rachor et al., 2009; Setterfield et al., 2010) or from
emerging pests and pathogens (Laurance et al., 1996; Garkaklis
et al., 2004a; Cahill et al., 2008). Key components of the native biota have been lost, and continue to be lost, from many Australian
ecosystems (Hero et al., 2006; Jones et al., 2007; AWC, 2010; Burbidge et al., 2009; Woinarski et al., 2010).
In this paper, we define a tipping point rather loosely as a circumstance by which a relatively modest change in an environmental driver or perturbation can cause a major shift in key ecosystem
properties (Fig. 1), such as habitat structure, species composition,
community dynamics, fire regimes, carbon storage, or other important functions. The tipping point is an ecological threshold beyond
which major change becomes inevitable and is often very difficult
to reverse. Because of ecological feedbacks, many ecosystems seem
relatively stable as they approach a tipping point, but then shift
abruptly to an alternative state once they reach it (see Washington-Allen et al. (2009), Hughes et al. (2010), and references
therein).
In conducting our analysis we found it useful to distinguish
among three broad categories of ecosystems that vary in their geographic extent and severity of their tipping points. ‘Tipping’ ecosystems are likely to experience profound regime changes across
most or all of their geographic range, whereas ‘dipping’ ecosystems
experience similarly profound changes, but these are restricted
geographically, affecting only a portion of the entire ecosystem. Finally, ‘stripping’ ecosystems are being stripped of important ecosystem components, such as their small mammal, amphibian, or
large predator fauna, but such changes are more insidious and less
visually apparent than major regime changes, at least at present.
We present here our ‘top 10’ list of vulnerable Australian terrestrial and near-coastal marine ecosystems. For each we outline
some of the intrinsic features and external drivers that render it
susceptible to tipping points, and identify subtypes of the ecosystem that we consider especially vulnerable. Our emphasis here is
primarily on the physical and biological sciences, and we concede
that a social-science perspective might yield a different list—one
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that considers a range of socioeconomic factors that also affect ecosystem vulnerability. We also emphasize that we regard this exercise as exploratory and thought-provoking, not definitive. Our goal
is to stimulate critical thinking about tipping points while highlighting Australian ecosystems that we believe could—in the absence of effective conservation or management interventions—
change dramatically in the future.
2. Methods
We conducted our assessment in two phases. In early October
2010, the 26 coauthors of this paper were invited to submit independent lists of major terrestrial and marine ecosystem types that
he or she considered vulnerable to tipping points, along with potential intrinsic characteristics or external threats that were
thought to render each nominated ecosystem vulnerable. Many
of these coauthors have long-term research experience in Australia
and the universities with which they are affiliated span all Australian states except Tasmania (and several coauthors have active research programs in Tasmania). These initial data were compiled
into a preliminary list by the lead author, and the nominated ecosystems ranked by the number of investigators that considered
them vulnerable.
In late October 2010, the authors met in Cairns, Queensland for
an intensive 2-day workshop in which we discussed and refined
the initial list. We had five goals: (1) to identify the ‘top 10’ major
Australian ecosystems vulnerable to tipping points, (2) to highlight
key subtypes of each ecosystem type currently at critical risk, (3) to
identify the intrinsic features of each ecosystem that predisposed it
to tipping points, (4) to identify major external threats to each ecosystem, and (5) to cross-tabulate the intrinsic features and external
threats across all 10 vulnerable ecosystems to identify any general
attributes that render them vulnerable to tipping points. To
achieve aims (3) and (4) we devised general schemes to categorize
intrinsic ecosystem features (Table 1) and external threats (Table
2) that predispose ecosystems to tipping points. For all analyses,
we reached a final consensus via a combination of discussion, debate, and formal voting.
3. Results: vulnerable ecosystems
Among a total of 22 nominated Australian ecosystems, the following 10 were judged to be most vulnerable to tipping points.
We begin with the ecosystems for which consensus among our panel of experts was strongest.
Fig. 1. Striking contrast between a natural tropical savanna-woodland near Bachelor, Northern Territory, Australia and similar habitat 300 m away that is heavily invaded by
Gamba grass (Andropogon gayanus), an exotic species. The grass promotes high-intensity fires that dramatically transform the ecosystem (photos by S. Setterfield).
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Table 1
Intrinsic features of 10 Australian ecosystems that can render them vulnerable to tipping points, as perceived by 26 environmental experts. For each ecosystem type, the most
important feature is numbered 1 with those of lesser importance numbered subsequently.
Intrinsic feature
Mountains
Narrow environmental envelope
Near threshold
Geographically restricted
History of fragmentation
Reliance on ecosystem engineers
Reliance on framework species
Reliance on predators or keystone
mutualists
Positive feedback
Proximity to humans
Social vulnerability
1
3
2
Tropical
savannas
Coastal
wetlands
Coral
reefs
Drier
rainforests
4
1
3
1
1
2
2
3
MurrayDarling
1
4
5
3
Temperate
eucalypt
3
4
4
3
5
2
Estuarine
wetlands
1
1
1
2
4
5
Islands
2
1
2
3
2
SW Australia
Mediterranean
2
4
1
4
2
6
5
3
6
3
5
Table 2
Environmental threats to 10 Australian ecosystems that render them vulnerable to tipping points, as perceived by 26 environmental experts. For each ecosystem type, the most
important threat is numbered 1 with those of lesser importance numbered subsequently.
Environmental threat
Mountains
Increased temperatures
Changes in water balance and
hydrology
Extreme weather events
Ocean acidification
Sea-level rise
Changed fire regimes
Habitat reduction
Habitat fragmentation
Invasives
Pests and pathogens
Salinization
1
2
Tropical
savannas
Coastal
wetlands
Coral
reefs
Drier
rainforests
MurrayDarling
SW Australia
Mediterranean
Islands
Temperate
eucalypt
Estuarine
wetlands
1
2
3
4
2
2
1
6
2
3
3
8
3
2
3
3
3
8
5
6
4
7
2
4
1
2
1
8
5
6
4
2
3
9
5
6
4
1
5
6
4
5
6
3
1
3
4
8
9
6
5
7
4
5
1
7
2
1
4
5
4
7
3.1. Elevationally restricted mountain ecosystems
3.2. Tropical savannas
Mountain ecosystems in Australia are most predominant in the
Great Dividing Range, which skirts the country’s eastern seaboard
from western Victoria northward to the Cape York Peninsula in
northern Queensland. Mountains also occur in parts of Tasmania,
South Australia, and the southwest of Western Australia. Many
habitats types in these mountains are elevationally restricted,
including alpine ecosystems of Tasmania and southeastern Australia, and montane rainforests at temperate, subtropical, and tropical
latitudes of northern New South Wales and Queensland. In our
view the most vulnerable habitats are those that rely substantially
on cloud-stripping for moisture inputs during the drier months
(Hutley et al., 1997; McJannet et al., 2007), have seasonal snow
cover (Pickering et al., 2003), or, like many rainforests, sustain high
numbers of restricted endemic species (Fig. 2) (Williams et al.,
1996; Hoskin, 2004).
These ecosystems are considered inherently vulnerable because
of their often-narrow environmental envelopes, their geographically restricted distribution, and the fact that many appear to be
near climatic thresholds (Table 1). We regard global warming (Williams et al., 2003), potential changes in moisture inputs and a rising cloud base (Pounds et al., 1999; Still et al., 1999), and extreme
weather events (Tebaldi et al., 2006) as the most serious future
threats (Table 2). Further perils include invasive plants and fauna,
habitat loss and fragmentation (Laurance, 1991), new pests and
pathogens (such as the chytrid fungus that has decimated many
stream-dwelling amphibian populations; Skerratt et al., 2007),
and, in alpine ecosystems, changing fire regimes (Wahren et al.,
1999; Fairfax et al., 2009) and a reduction in insulating snow cover
in winter (Pickering et al., 2003).
Tropical savanna-woodlands are one of the most extensive
environments in Australia, spanning much of the northern third
of the continent (Mackey et al., 2007). This system is experiencing
severe regime changes in only parts of its geographic range—and
hence is a ‘dipping’ ecosystem. Invasive weeds and animals (Setterfield et al., 2010; Woinarski et al., 2010), changing fire regimes
(Prior et al., 2010; Midgley et al., 2010), and extreme weather
events are seen as the major threats, with habitat fragmentation
and overgrazing by livestock (Kutt and Woinarski, 2007) being further perils (Table 2). In addition, this ecosystem is currently experiencing an apparently widespread decline of its small mammal
fauna—a feature of a ‘stripping’ ecosystem—for reasons that remain
uncertain (AWC, 2010; Woinarski et al., 2010).
A key reason for the high vulnerability of tropical savannas is massive weed invasions (Fig. 1) that profoundly alter fire regimes and
other fundamental ecosystem attributes such as carbon storage and
nitrogen cycling (Rea and Storrs, 1999; Rossiter-Rachor et al., 2009;
Setterfield et al., 2010) (Table 1). We believe that sandstone savannas
and heaths, which have an endemic flora (Woinarski et al., 2006) and
fauna and a highly restricted geographic range, are especially vulnerable habitats, with increasing fire incidence their principal threat
(Russell-Smith et al., 2001; Sharp and Bowman, 2004).
3.3. Coastal floodplains and wetlands
Coastal floodplains and wetlands are freshwater (or only
slightly brackish) ecosystems in coastal areas throughout Australia
(Adam, 1992; Kingsford et al., 2004). They are most widespread in
the vast tropical floodplains of the Northern Territory (Cowie et al.,
2000), Queensland, and Western Australia. Principal threats to
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Fig. 2. Endemic rainforest vertebrates in eastern Australia that are considered exceptionally vulnerable to global warming, and thus could be ‘stripped’ from ecosystems. All
species shown have highly restricted geographic ranges and are confined to montane rainforest. From upper left: Bartle Frere barsided skink (Eulamprus frerei), lemuroid
ringtail possum (Hemibelideus lemuroides), baw baw frog (Philoria pughi), golden bowerbird (Prionodura newtoniana), Daintree River ringtail possum (Pseudochirulus cinereus),
buzzing frog (Cophixalus bombiens) (photos by S. Williams, M. Trenerry, G. Webster, G. Guy, G. Calvert, and S. Williams, respectively).
these systems are rising sea levels caused by global warming, extreme weather events (such as storm surges that cause major saltwater incursions inland), and massive plant invasions (Table 2).
Hydrological changes, habitat loss and fragmentation, pollution,
and changing fire regimes are seen as important localized threats
(Table 2).
In general, coastal floodplains and wetlands are vulnerable to
tipping points because of their restricted and naturally fragmented
geographic distribution, narrow environmental envelopes, and frequently close proximity to land-use pressures in coastal areas (Table 1). Many sustain sensitive wildlife; for instance, coastal wallum
habitats in eastern Australia contain flora and fauna endemic to
their highly acidic waters (e.g. Meyer et al., 2005). We believe
the most susceptible habitats are relatively flat, topographically restricted wetlands, especially those trapped between habitat conversion or topography on the inland side and rising sea levels on
the seaward side. Wetlands adjoining coastal areas with high tidal
amplitudes (5–13 m), which have more physical energy to drive
seawater inland, are also highly vulnerable. They are often connected, at least intermittently, to intertidal wetlands, making them
vulnerable to saltwater intrusions both at the surface and via
groundwater. Salinity is toxic to amphibians and demonstrably alters fish populations (Sheaves and Johnston, 2008; Sheaves, 2009).
3.4. Coral reefs
Coral reefs occur in shallow seas along much of northeastern Australia with smaller, scattered reefs along the Western Australian
coast. These reefs are considered vulnerable to tipping points because of their narrow thermal and water-quality tolerances, heavy
reliance on key ‘framework’ species (reef-building corals), and high
susceptibility to nutrient runoff and eutrophication (Johnson and
Marshall, 2007; Hughes et al., 2010). In our view the most vulnerable
reefs are those near rivers carrying heavy nutrient loads from nearby
farmlands, and those at near-equatorial latitudes off Cape York Peninsula and northern Western Australia (Table 1), which are susceptible to coral bleaching associated with global warming. Isolated reefs,
such as Ningaloo Reef in Western Australia, are also vulnerable because local species declines are not as easily offset by immigration
as occurs in less-isolated reefs (e.g. Underwood, 2009).
The greatest threat to coral reefs in Australian waters is probably rising sea temperatures, followed by extreme weather events
(especially heat waves and destructive storms), ocean acidification,
and pollution. Reef destruction and overharvesting of fish, crustaceans, gastropods, and other reef species are ancillary threats
(Table 2), but are lesser problems in Australia than elsewhere in
the tropics.
3.5. Drier rainforests
Relatively dry rainforest types, including vine thickets, monsoonal vine-thickets, and semi-deciduous rainforest types such as
Mabi forest in far north Queensland, occur in moist, comparatively
fire-proof refugia scattered across much of northern Australia
(Russell-Smith, 1991; Bowman, 2000). Shifts in fire regime, rising
temperatures, changing rainfall regimes, and extreme weather
events (especially droughts and heat waves) are considered their
greatest threats, although many sites are also heavily invaded by
lantana (Lantana camara), rubber vine (Cryptostegia grandiflora),
and other tropical weeds that can suppress tree recruitment, provide fuel for destructive surface fires (Humphries et al., 1991; Russell-Smith and Bowman, 1992; Fensham, 1994), and render the
habitat unsuitable for some native species (e.g., Valentine et al.,
2007). Some are also being degraded by human habitat disruption
and overgrazing by livestock (Table 2).
In broad terms, drier rainforest types are vulnerable to tipping
points because of their narrow environmental tolerances, their
highly restricted and patchy distributions (Bowman and Woinar-
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ski, 1994; Price et al., 1999), and the destabilizing positive feedbacks that occur when heavy weed invasions increase fire incidence, which in turn opens up the forest and makes it more
prone to further weed invasions and fire (Table 1). We believe that
forest patches that are small, near human settlements, in frequently burned areas, and in low-lying areas prone to rising sea
levels are especially vulnerable.
3.6. Wetlands and floodplains of the Murray-Darling Basin
Before flowing into the sea near Adelaide, the waters of the vast
Murray-Darling Basin must traverse some of the most intensively
exploited lands in Australia. Wetlands and floodplains in this basin
and the linked Coorong estuary are threatened by chronic water
overharvesting for agriculture and other human uses (Kingsford,
2000; Frazier and Page, 2006), salinization (Nielsen et al., 2003),
habitat loss (Kingsford and Thomas, 2004), fragmentation (Thoms
et al., 2005; Wedderburn et al., 2008), sedimentation and associated nutrient changes (Davis and Koop, 2006; Gell et al., 2009),
and rising temperatures and sea levels (Table 2).
The Murray-Darling wetlands and floodplains are broadly vulnerable to tipping points because they are heavily fragmented, rely
on vital ‘framework’ species (a limited number of wetland and
floodplain plants) that are approaching environmental thresholds
(Colloff and Baldwin, 2010), occur in close proximity to human
populations, and are affected by intense inter-jurisdictional debates over water rights (Table 1). Southeastern Australia, where
they occur, is also at high risk of a decline in mean rainfall, according to future climatic projections (CSIRO-Australian Bureau of
Meteorology, 2007). In our opinion, the most vulnerable habitats
in the Murray-Darling are those that contain mineral sulfide soils
(Hall et al., 2006), are susceptible to eutrophication, or are prone
to fluctuating water tables. The Coorong estuary is also vulnerable;
threshold modeling suggests rapid transitions to different ecosystem states are possible in the estuary (Fairweather and Lester,
2010).
3.7. Mediterranean ecosystems of southwestern Australia
Recognized as a global biodiversity hotspot because of its megadiverse plant endemism (Myers et al., 2000), the Mediterranean
habitats of southwestern Australia sustain a complex mixture of
relict ancient and modern species. These habitats are intrinsically
vulnerable for several reasons: they are near important thresholds
of temperature and rainfall (Abbott and Le Maitre, 2010), are geographically restricted, rely on vital ‘framework’ species (one or
more locally dominant tree species), have suffered losses of key
fauna (especially mycophagous marsupials; Garkaklis et al.,
2004b), and are prone to positive feedbacks between weed invasions and destructively intense fires (Table 1). In our opinion, the
most vulnerable habitats are the dry sclerophyll forests, woodlands, and heathlands.
The key threats to these Mediterranean ecosystems are current
and future declines in regional precipitation, especially in winter
(Pitman et al., 2004; Yates et al., 2010), rising temperatures, extreme weather events (especially droughts and heat-waves but
also frosts), intensifying fire regimes, emerging pathogens and
pests (Fig. 3), and salinization. Habitat loss from agriculture and
urbanization, fragmentation, timber harvesting, feral animals,
and mining operations also pose important threats (Table 2).
3.8. Offshore islands
Excluding Tasmania, Australia has over 8300 offshore islands,
ranging in size from <1 ha to nearly 580,000 ha (Ecosure, 2009).
In Australia, as elsewhere, islands are considered vulnerable to dramatic changes because of their restricted size, physical isolation,
often-narrow environmental envelopes, and relatively limited
(yet often highly endemic) biodiversity that may facilitate species
invasions (Table 1) (Burbidge and Manly, 2002; Ecosure, 2009). We
believe the most vulnerable are small, species-poor islands with
many vacant ecological niches, which are prone to species invasions; those with large human populations or visitation; those near
ocean-circulation boundaries or with many species that depend on
upwelling; and low-lying islands susceptible to rising sea levels.
Not all Australian islands have suffered invasions; some have provided important refugia for native wildlife that have been extirpated elsewhere by introduced predators and competitors
(Morton et al., 1995; Burbidge, 1999).
The chief threats to Australia’s islands are myriad invading species such as rats, mice, rabbits, foxes, pigs, cats, toads, and fire ants
(Burbidge and Manly, 2002); extreme weather events such as intense storms or droughts that can have disproportionately large
impacts on insular ecosystems; rising sea levels; habitat loss and
degradation; rising sea-surface temperatures that might affect oceanic circulation and the upwelling of nutrient-rich waters; and
emerging pathogens and pests (Table 2).
Fig. 3. Dieback of native vegetation in Fitzgerald River National Park in Western Australia caused by the fungal pathogen Phytophthora cinnamomi. Vegetation in the
foreground has suffered dieback whereas that just behind is still unaffected (photo by G. Hardy). Dieback causes profound changes in vegetation structure and floristic
composition.
W.F. Laurance et al. / Biological Conservation 144 (2011) 1472–1480
3.9. Estuarine wetlands (salt marshes and mangroves)
Salt marshes and mangroves are estuarine ecosystems that play
many important environmental roles. These include stabilizing
coastal sediments, acting as nutrient and pollution traps, providing
protection from storm surges and tsunamis, sustaining wildlife
populations, and functioning as vital ‘nurseries’ for breeding fish
and crustaceans (Beck et al., 2009). Their narrow environmental
tolerances, geographically restricted nature, proximity to dense
human populations in coastal regions, patchy and fragmented distribution (Duke et al., 2007), and reliance on a few key framework
species generally render them vulnerable (Table 1). We believe
that salt marshes and coastal-fringe mangroves (those in narrow
strips along coastlines rather than in estuarine areas) are especially
susceptible, particularly those in densely populated areas.
In the future, increasing storm intensity could be a serious
threat to salt marshes and particularly to mangroves at the seaward edge (e.g. Cahoon et al., 2003). They also are increasingly
likely to be squeezed between human land-uses or topography
on the landward side and rising sea levels on the seaward side
(Eslami-Andargoli et al., 2010). Furthermore, water pollution and
small changes in salinity and hydrology can cause dramatic
changes in estuarine communities (Table 2).
3.10. Temperate eucalypt forests
In our view, temperate eucalypt forests are ‘dippers’—ecosystems that could suffer dramatic future changes but only in part
of their geographic range. In general, habitat loss and fragmentation, a reliance on ‘framework’ species (one or a few dominant
eucalypt species), close proximity to humans, prior losses of key
fauna (mycophagous and excavating marsupials), and synergisms
between weed invasions and fire render them especially vulnerable (Table 1). We believe that habitats with altered fire regimes
(those that deviate from pre-European burning conditions) or suffering from heavy habitat loss and fragmentation are most vulnerable (Lindenmayer and Possingham, 1996; McCarthy et al., 1999;
Gibbons, 2010).
Among the most important future threats to temperate eucalypt forests are changes to fire regimes arising from climate
change. Key determinants of fire regime include fuel moisture
and weather, factors that will be significantly altered by shifts in
temperature, potential evaporation, and the amount and seasonal
distribution of precipitation (Bradstock, 2010). In the future, wet
eucalypt forests are likely to experience elevated levels of fire
activity. Rising atmospheric CO2 levels and the resulting increases
in plant water-use efficiency might offset drought-induced declines in fuel production, although these interactions are complex
and uncertain. Habitat loss, fragmentation, overexploitation of timber, and invasive pathogens (especially Phytophthora dieback;
Weste and Marks, 1987) are important localized threats (Table 2).
4. Discussion
4.1. A focus on tipping points
We emphasize at the outset that our analysis differs from other
assessments of vulnerable ecosystems in Australia. Our list of the
10 ecosystems most vulnerable to tipping points overlaps only
minimally, for instance, with the Australian government’s list of
‘threatened ecological communities’ (EPBC, 1999). The latter is
composed of finely defined ecosystem types—such as the Aquatic
Root-Mat Communities of the Leeuwin Naturaliste Ridge, or Eastern Suburbs Banksia Scrub of the Sydney Region—that often have
1477
very small geographic ranges and are already considered critically
threatened.
Similarly, in our analysis we considered and rejected a number
of broader ecosystem types, such as the Brigalow Belt, Avon
Wheatbelt of Western Australia, and Grassy Box Woodlands, because we believe these ecosystems have ‘already tipped’—they
are so drastically diminished or have experienced such profound
degradation and regime changes that their ecology is fundamentally altered. Our emphasis, then, is on ecosystems that currently
retain largely natural characteristics across substantial parts of
their geographic range but are at risk of changing dramatically in
the near future.
4.2. Predisposing factors
Why are certain Australian ecosystems particularly susceptible
to tipping points? We can draw some tentative conclusions by
evaluating the most important features (those ranked 1–3 by our
panel of experts) across our 10 vulnerable ecosystem types (Table
1). The most frequently cited feature of vulnerable ecosystems is a
restricted geographic range, which limits their capacity to withstand anthropogenic pressures simply by persisting in places
where such pressures are absent. Elevationally limited mountain
ecosystems, coastal wetlands, drier rainforests, Mediterranean
habitats of southwestern Australia, islands, and estuarine ecosystems are all considered vulnerable for this reason. The second most
frequently cited feature, a narrow environmental envelope, is related partially to the first. This feature characterizes mountain ecosystems, coral reefs, drier rainforests, islands, and estuarine
habitats. Such ecosystems appear sensitive to even relatively modest changes in environmental conditions.
Four other features were also considered relatively important,
being cited among the most important predisposing features for
3–4 ecosystems each (Table 1). Ecosystems that have suffered substantial anthropogenic fragmentation, that rely on critical ‘framework’ species (such as one or a few species of canopy trees, or
coral-building organisms), that are constrained by close proximity
to humans or human activities, or that already live close to an environmental threshold, also appear particularly vulnerable to tipping
points. These associations generally seem logical. For instance,
fragmented ecosystems are unusually vulnerable to climatic and
other environmental vicissitudes (Laurance, 2002). Ecosystems
near their limits of environmental tolerance, or that rely on one
or a few types of critical framework species, appear similarly
vulnerable.
4.3. Key drivers
We now identify the most pervasive environmental drivers that
predispose Australian ecosystems to tipping points. Our analysis is
based on ranking the relative importance of 13 environmental
drivers for each of our 10 vulnerable ecosystems (Table 2). As before, our focus is on the drivers that we regarded as most important
(those ranked 1–3 for each ecosystem). Notably, the anthropogenic
threats identified here may well differ from those that have altered
Australian ecosystems in the past (see Flannery, 1994; Johnson,
2006).
The two most important of the top-ranked drivers, extreme
weather events and changes in water balance and hydrology, were
each considered important for seven of the 10 ecosystems. Extreme weather events include severe, short-term phenomena such
as heat waves, droughts, and intense storms. We speculate that the
Australian continent, whose precipitation and hydrology are
strongly influenced by the El Niño-Southern Oscillation (Nicholls
et al., 1997; Chiew et al., 1998), whose ancient, relatively flat land
surface is poor at capturing rainfall, and which is dominated by
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W.F. Laurance et al. / Biological Conservation 144 (2011) 1472–1480
strongly seasonal environments at tropical and subtropical latitudes, may be particularly susceptible to such events. Changes in
water balance and hydrology usually arise from water overharvesting, such as is occurring in the Murray-Darling Basin, or from
changes in moisture inputs, a phenomenon that under plausible
scenarios of future climate change could imperil montane ecosystems that rely on orographic rainfall and/or cloud-stripping (Still
et al., 1999; Bradley et al., 2006).
Many ecosystems are also vulnerable to rising temperatures or
rising sea levels (Table 2), both of which relate directly to global
warming. Among the myriad ways in which global change phenomena could affect Australian ecosystems, one of the potentially
most important is by altering fire regimes (Bradstock, 2010). Fire
regimes are largely determined by weather and fuel loads. Increasing atmospheric CO2 could potentially increase fuel loads via enhanced primary productivity (Donohue et al., 2009; Sun et al.,
2010), but this effect could be magnified or diminished by changes
in available moisture, depending on the location. In some ecosystems, serious weed invasions are profoundly altering fire regimes
(Fig. 1). Fire-promoting invaders can dramatically transform ecosystems, usually favoring short-lived annuals and exotics at the expense of long-lived trees.
Although factors relating to climatic change are likely to play a
key role in predisposing Australian ecosystems to tipping points,
we emphasize that most of our vulnerable ecosystems are being
influenced by multiple drivers (Table 2). For us, this reinforces a
general view that synergisms among different environmental drivers can be extremely important, predisposing species and ecosystems to serious environmental changes (Laurance and Cochrane,
2001; Brook et al., 2008; Laurance and Useche, 2009). In our analysis, examples of such synergisms are pervasive—for example, between weed invasions and fire, between land-use change and
climatic change, between anthropogenic activities and introduced
pathogens, and between coastal land-use pressures and rising sea
levels. For the Australian environment, as elsewhere, combinations
of environmental perils may be the death knell for many
ecosystems.
4.4. Conservation actions to avoid tipping points
The threats facing vulnerable ecosystems in Australia are often
multi-faceted and, at least for some perils such as global climate
change, rising ocean acidity, and the continued spread of certain
invasive species and pathogens, largely beyond the control of Australian resource managers. In practical terms, this limits the tools
that can be applied to mitigate these pressures. Rather than
preaching despair, however, we believe much can be done to limit
the further decline of vulnerable Australian ecosystems.
A key priority is to identify likely or imminent changes in vulnerable ecosystems and taxa (e.g. Abbott and Le Maitre, 2010;
Hughes et al., 2010; Woinarski et al., 2010). A full discussion of this
concept is beyond the scope of this paper, but we note two key
points. First, the best approach for judging whether an ecosystem
is approaching a tipping point may be to examine key ecological
processes involved in proper ecosystem functioning and integrity
(Dunning et al., 1992; Didham et al., 1996), rather than biodiversity
indicators (such as species richness) that can have delayed responses to disturbance effects (Loehle and Li, 1996; Vellend
et al., 2006). Second, a key harbinger of tipping points may be a
‘critical slowing’ of ecosystem dynamics. This can include slower
recovery from disturbances, increased variance in ecosystem
dynamics, and increased auto-correlation in ecosystem properties
as the tipping point is approached (see van Nes and Scheffer
(2007), Biggs et al. (2009), Scheffer et al. (2009), Drake and Griffen
(2010), Scheffer (2010) for discussion). Further, phenomena such
as an increased variance and spatial auto-correlation might be
detectable from spatial patterns in vegetation (Bailey, in press),
potentially allowing ecosystem vulnerability to be evaluated via
remote sensing, rather than requiring detailed field studies. Such
approaches might provide important insights into the status and
vulnerability of particular ecosystems.
In addition, on-the-ground conservation and management actions can often have a profound impact on ecosystem resilience.
In broad terms, concrete steps such as increasing the size and number of protected areas, limiting external disturbances such as habitat conversion and new roads (Goosem, 2007; Laurance et al.,
2009), creating buffer zones and wildlife corridors, restoring key
habitats and landscape linkages (Shoo et al., 2010), and designing
and locating nature reserves to maximize their resilience to climate change (Hannah et al., 2007; Loarie et al., 2009; Shoo et al.,
2010) can play vital roles in maintaining ecosystem viability. Key
phenomena such as fire regimes can often be managed via steps
such as prescriptive burning, silviculture, livestock grazing, fire
suppression, and controlling human ignition sources (Yibarbuk
et al., 2001; Murphy et al., 2009; Russell-Smith et al., 2010).
Managing natural and semi-natural ecosystems in a world that
is continually in flux is a great challenge, but societies are adapting
to these realities. Environmental regulations and policies are
changing profoundly in an effort to address complex and multi-faceted environmental challenges (Lockwood et al., 2010). Conservation efforts are increasingly being integrated across institutions
and among public, private, and civil sectors to address uncertainty
and ‘wicked’ environmental problems (Holling, 1978; Robinson
et al., 2009) in an adaptive and flexible manner (Dietz et al.,
2003; Armitage et al., 2009). Environmental ‘horizon scanning’ is
being used to anticipate new threats (Laurance and Peres, 2006;
Sutherland and Woodroof, 2009). Great challenges lie ahead for
Australian ecosystems, as elsewhere, but much can still be done
to address them.
Acknowledgements
We thank S.G. Laurance, G.R. Clements, and R.K. Didham for
comments on the manuscript and C. Gemellaro, K. Milena, and P.
Byrnes for logistical assistance. The raw data for this study, including a list of all nominated vulnerable ecosystems, are available
upon request. This paper results from a collaborative investigation
among the Innovative Research Universities of Australia
(www.iru.edu.au).
References
Abbott, I., Le Maitre, D., 2010. Monitoring the impact of climate change on
biodiversity: the challenge of megadiverse Mediterranean climate ecosystems.
Austral Ecology 35, 406–422.
Adam, P., 1992. Wetlands and wetland boundaries: problems, expectations,
perceptions and reality. Wetlands 10, 60–67.
Armitage, D., Plummer, R., Berkes, F., Arthur, R., Charles, A., Davidson-Hunt, I.,
Diduck, A., Doubleday, N., Johnson, D., Marschke, M., McConney, P., Pinkerton,
E., Wollenberg, E., 2009. Adaptive co-management for social–ecological
complexity. Frontiers in Ecology and the Environment 7, 95–102.
AWC, 2010. Where Have All the Mammals Gone? Australian Wildlife Conservancy.
<http://www.australianwildlife.org/images/file/Northern_Mammal_WM_
Winter_2010_-lowres.pdf>.
Bailey, R.M., in press. Spatial and temporal signatures of fragility and threshold
proximity in modelled semi-arid vegetation. Proceedings of the Royal Society B.
doi:10.1098/rspb.2010.1750.
Beck, M.W., Heck, K.L., Able, K.W., Childers, D.L., Eggleston, D.B., Gillanders, B.M.,
Halpern, B., Hays, C.G., Hoshino, K., Minello, T.J., Orth, R.J., Sheridan, P.F.,
Weinstein, M.P., 2009. The identification, conservation, and management of
estuarine and marine nurseries for fish and invertebrates. BioScience 51, 633–
641.
Beeton, R.J.S., Buckley, K.I., Jones, G.J., Morgan, D., Reichelt, R.E., Trewin, D., 2006.
Australia State of the Environment 2006. Department of Environment and
Heritage, Canberra, Australia.
Biggs, R., Carpenter, S.R., Brock, W.A., 2009. Turning back from the brink: detecting
an impending regime shift in time to avert it. Proceedings of the National
Academy of Sciences United States of America 106, 826–831.
W.F. Laurance et al. / Biological Conservation 144 (2011) 1472–1480
Bowman, D.M.J.S., 2000. Australian Rainforest: Island of Green in a Land of Fire.
Cambridge University Press, Cambridge, UK.
Bowman, D.M.J.S., Woinarski, J.C.Z., 1994. Biogeography of Australian monsoon
rainforest mammals: implications for the conservation of rainforest mammals.
Pacific Conservation Biology 1, 98–106.
Bradley, R.S., Vuille, M., Diaz, H.F., Vergara, W., 2006. Threats to water supplies in
the tropical Andes. Science 312, 1755–1756.
Bradstock, R.A., 2010. A biogeographic model of fire regimes in Australia: current
and future implications. Global Ecology and Biogeography 19, 145–158.
Brook, B.W., Sodhi, N.S., Bradshaw, C.J.A., 2008. Synergisms among extinction
drivers under global change. Trends in Ecology & Evolution 23, 453–460.
Burbidge, A.A., 1999. Conservation values and management of Australian islands for
non-volant mammal conservation. Australian Mammalogy 21, 67–71.
Burbidge, A.A., Manly, B.F.J., 2002. Mammal extinctions on Australian islands:
causes and conservation implications. Journal of Biogeography 29, 465–475.
Burbidge, A.A., McKenzie, N.L., Brennan, K.E.C., Woinarski, J.C.Z., Dickman, C.R.,
Baynes, A., Gordon, G., Menkhorst, P.W., Robinson, A.C., 2009. Conservation
status and biogeography of Australia’s terrestrial mammals. Australian Journal
of Zoology 56, 411–422.
Cahill, D.M., Rookes, J.E., Wilson, B.A., Gibson, L., McDougall, K.L., 2008. Phytophthora
cinnamomi and Australia’s biodiversity: impacts, predictions and progress
towards control. Australian Journal of Botany 56, 279–310.
Cahoon, D.R., Hensel, P., Rybczyk, J., McKee, K.L., Proffitt, C.E., Perez, B.C., 2003. Mass
tree mortality leads to mangrove peat collapse at Bay Islands, Honduras after
Hurricane Mitch. Journal of Ecology 91, 1093–1105.
Chiew, F.H.S., Piechota, T.C., Dracup, J.A., McMahon, T.A., 1998. El Niño/Southern
Oscillation and Australian rainfall, streamflow and drought: links and potential
for forecasting. Journal of Hydrology 204, 138–149.
Colloff, M.J., Baldwin, D.S., 2010. Resilience of floodplain ecosystems in a semi-arid
environment. Rangeland Journal 32, 305–314.
Cowie, I.D., Short, P., Osterkamp Madsen, M., 2000. Floodplain Flora: A Flora of
Coastal Floodplains of the Northern Territory, Australia. Australian Biological
Resources Study, Canberra, Australia.
CSIRO, Australian Bureau of Meteorology, 2007. Climate Change in Australia:
Technical Report 2007. CSIRO, Canberra, Australia.
Davis, J.R., Koop, K., 2006. Eutrophication in Australian rivers, reservoirs and
estuaries – a southern hemisphere perspective on the science and its
implications. Hydrobiologia 559, 23–76.
De’ath, G., Lough, J.M., Fabricius, J.E., 2009. Declining coral calcification on the Great
Barrier Reef. Science 323, 116–119.
Didham, R.K., Ghazoul, J., Stork, N.E., Davis, A.J., 1996. Insects in fragmented forests:
a functional approach. Trends in Ecology and Evolution 11, 255–260.
Dietz, T., Ostrom, E., Stern, P., 2003. The struggle to govern the commons. Science
302, 1907–1912.
Donohue, R.J., McVicar, T.R., Roderick, M.L., 2009. Climate-related trends in
Australian vegetation cover as inferred from satellite observations, 1981–
2006. Global Change Biology 15, 1025–1039.
Drake, J.M., Griffen, B.D., 2010. Early warning signals of extinction in deteriorating
environments. Nature 467, 456–459.
Duke, N.C., Meynecke, J.O., Dittmann, S., Ellison, A.M., Anger, K., Berger, U., Cannicci,
S., Diele, K., Ewel, K.C., Field, C.D., Koedam, N., Lee, S.Y., Marchand, C., Nordhaus,
I., Dahdouh-Guebas, F., 2007. A world without mangroves? Science 317, 41–
42.
Dunning, J.B., Danielson, B.J., Pulliam, H.R., 1992. Ecological processes that affect
populations in complex landscapes. Oikos 65, 169–175.
Ecosure, 2009. Prioritisation of High Conservation Status Offshore Islands.
Department of Environment, Water, Heritage and the Arts, Canberra, Australia.
EPBC, 1999. Environmental Protection and Biodiversity Act (EBPC), List of
Threatened Ecological Communities. Australian Government, Canberra.
<http://www.environment.gov.au/cgi-bin/sprat/public/
publiclookupcommunities.pl>.
Eslami-Andargoli, L., Dale, P.E.R., Sipe, N., Chaseling, J., 2010. Local and landscape
effects on spatial patterns of mangrove forest during wetter and drier periods:
Moreton Bay, Southeast Queensland, Australia. Estuarine and Coastal Shelf
Science 89, 53–61.
Fairfax, R., Fensham, R., Butler, D., Quinn, K., Sigley, B., Holman, J., 2009. Effects of
multiple fires on tree invasion in montane grasslands. Landscape Ecology 24,
1363–1373.
Fairweather, P.G., Lester, R.E., 2010. Predicting future ecological degradation based
on modelled thresholds. Marine Ecology Progress Series 413, 291–304.
Fensham, R.J., 1994. The invasion of Lantana camara L. in Forty Mile Scrub National
park, north Queensland. Australian Journal of Ecology 19, 297–305.
Flannery, T., 1994. The Future Eaters: An Ecological History of the Australasian
Lands and People. Grove Press, New York, USA.
Frazier, P., Page, K., 2006. The effect of river regulation on floodplain wetland
inundation, Murrumbidgee River, Australia. Marine and Freshwater Research
57, 133–141.
Garkaklis, M.J., Calver, M.C., Wilson, B.A., Hardy, G.E.St.J., 2004a. Habitat alteration
caused by an introduced plant disease, Phytophthora cinnamomi: a potential
threat to the conservation of Australian forest fauna. In: Lunney, D. (Ed.),
Conservation of Australia’s Forest Fauna. Royal Zoological Society of New South
Wales, Mosman, Australia., pp. 181–194.
Garkaklis, M.J., Bradley, J.S., Wooller, R.D., 2004b. Digging and soil turnover by a
mycophagous marsupial. Journal of Arid Environments 56, 569–578.
Gell, P., Fluin Tibby, J., Hancock, J., Harrison, G., Zawadzki, J., Haynes, A., Khanum, D.,
Little, S., Walsh, B., 2009. Anthropogenic acceleration of sediment accretion in
1479
lowland floodplain wetlands, Murray-Darling Basin, Australia. Geomorphology
108, 122–126.
Gibbons, P., 2010. Prioritizing conservation in temperate woodlands. In:
Lindenmayer, D., Bennett, A., Hobbs, R. (Eds.), Temperate Woodland
Conservation and Management. CSIRO Publishing, Collingwood, Victoria,
Australia, pp. 15–21.
Goosem, M., 2007. Fragmentation impacts caused by roads through rainforests.
Current Science 93, 1587–1595.
Hall, K., Baldwin, D.S., Rees, G.N., Richardson, A., 2006. Distribution of inland
wetlands with sulfidic sediments in the Murray-Darling Basin, Australia.
Science of the Total Environment 370, 235–244.
Hannah, L., Midgley, G., Andelman, S., Araújo, M., Hughes, G., Martinez-Meyer, E.,
Pearson, R.G., Williams, P., 2007. Protected area needs in a changing climate.
Frontiers in Ecology and the Environment 5, 131–138.
Hennessy, K., Fitzharris, B., Bates, B.C., Harvey, N., Howden, M., Hughes, L., Salinger,
J., Warrick, R., 2007. Australia and New Zealand. In: Parry, M.L., Canziani, O.,
Palutikof, J., van der Linden, P., Hanson, C. (Eds.), Climate Change 2007: Impacts,
Adaptation and Vulnerability. Cambridge University Press, Cambridge, UK., pp.
507–540.
Hero, J.-M., Morrison, C., Gillespie, G., Roberts, J.D., Newell, D., Meyer, E., McDonald,
K., Lemckert, F., Mahony, M., Osborne, W., Hines, H., Richards, S., Hoskin, C.,
Clarke, J., Doak, N., Shoo, L., 2006. Overview of the conservation status of
Australian frogs. Pacific Conservation Biology 12, 313–320.
Holling, C., 1978. Adaptive Environmental Assessment and Management. John
Wiley and Sons, London, UK.
Hoskin, C.J., 2004. Australian microhylid frogs (Cophixalus and Austrochaperina):
phylogeny, taxonomy, calls, distributions and breeding biology. Australian
Journal of Zoology 52, 237–269.
Hughes, L., 2003. Climate change and Australia: trends, projections and impacts.
Austral Ecology 28, 423–443.
Hughes, T.P., Graham, N.A.J., Jackson, J.B.C., Mumby, P.J., Steneck, R.S., 2010. Rising
to the challenge of sustaining coral reef resilience. Trends in Ecology &
Evolution, doi:10.1016/j.tree.2010.07.011.
Humphries, S.E., Groves, R.H., Mitchell, D.S., 1991. Plant Invasions of Australian
Ecosystems: Kowari 2. Australian National Parks and Wildlife Service, Canberra.
Hutley, L.B., Doley, D., Yates, D.J., Boonsaner, A., 1997. Water balance of an
Australian sub-tropical rainforest at altitude: the ecological and physiological
significance of intercepted cloud and fog. Australian Journal of Botany 45, 311–
329.
Johnson, C.N., 2006. Australia’s Mammal Extinctions: A 50,000 Year History.
Cambridge University Press, Melbourne, Australia.
Johnson, J.E., Marshall, P.E. (Eds.), 2007. Climate Change and the Great Barrier Reef:
A Vulnerability Assessment. Great Barrier Reef Marine Park Authority,
Townsville, Australia.
Jones, M., Jarman, P., Lees, C., Hesterman, H., Hamede, R., Mooney, N., Mann, D.,
Pukk, C., Bergfeld, J., McCallum, H., 2007. Conservation management of
Tasmanian devils in the context of an emerging, extinction–threatening
disease: devil Facial Tumor Disease. EcoHealth 4, 326–337.
Kingsford, R.T., 2000. Ecological impacts of dams, water diversions and river
management on floodplain wetlands in Australia. Austral Ecology 25, 109–127.
Kingsford, R.T., Thomas, R., 2004. Destruction of wetlands and waterbird
populations by dams and irrigation on the Murrumbidgee River in arid
Australia. Environmental Management 34, 383–396.
Kingsford, R.T., Brandis, K., Thomas, R.F., Crighton, P., Knowles, E., Gale, E., 2004.
Classifying landform at broad spatial scales: the distribution and
conservation of wetlands in NSW, Australia. Marine and Freshwater
Research 55, 17–31.
Kutt, A., Woinarski, J.C.Z., 2007. The effects of grazing and fire on vegetation and the
vertebrate assemblage in a tropical savanna woodland in north-eastern
Australia. Journal of Tropical Ecology 23, 95–106.
Laurance, W.F., 1991. Ecological correlates of extinction proneness in Australian
tropical rainforest mammals. Conservation Biology 5, 79–89.
Laurance, W.F., 2002. Hyperdynamism in fragmented habitats. Journal of Vegetation
Science 13, 595–602.
Laurance, W.F., Cochrane, M.A., 2001. Synergistic effects in fragmented landscapes.
Conservation Biology 15, 1488–1489.
Laurance, W.F., Peres, C.A. (Eds.), 2006. Emerging Threats to Tropical Forests.
University of Chicago Press, Chicago, USA.
Laurance, W.F., Useche, D.C., 2009. Environmental synergisms and extinctions of
tropical species. Conservation Biology 23, 1427–1437.
Laurance, W.F., McDonald, K.R., Speare, R., 1996. Epidemic disease and the
catastrophic decline of Australian rain forest frogs. Conservation Biology 10,
406–413.
Laurance, W.F., Goosem, M., Laurance, S.G., 2009. Impacts of roads and linear
clearings on tropical forests. Trends in Ecology and Evolution 24, 659–669.
Lindenmayer, D.B., Possingham, H.P., 1996. Modelling the relationships between
habitat connectivity, corridor design and wildlife conservation within
intensively logged wood production forests of south-eastern Australia.
Landscape Ecology 11, 79–105.
Loarie, S.R., Duffy, P.B., Hamilton, H., Asner, G.P., Field, C.B., Ackerly, D.D., 2009. The
velocity of climate change. Nature 462, 1052–1055.
Lockwood, M., Davidson, J., Curtis, A., Stratford, E., Griffith, R., 2010. Governance
principles for natural resource management. Society and Natural Resources 23,
986–1001.
Loehle, C., Li, B.-L., 1996. Habitat destruction and the extinction debt revisited.
Ecological Applications 6, 784–789.
1480
W.F. Laurance et al. / Biological Conservation 144 (2011) 1472–1480
Mackey, B.G., Woinarski, J.C.Z., Nix, H., Trail, B., 2007. The Nature of Northern
Australia: Its Natural Values, Ecology, and Future Prospects. ANU Electronic
Press, Canberra, Australia.
McCarthy, M.A., Gill, A.M., Lindenmayer, D.B., 1999. Fire regimes in mountain ash
forest: evidence from forest age structure, extinction models and wildlife
habitat. Forest Ecology and Management 124, 193–203.
McJannet, D.L., Wallace, J.S., Reddell, P., 2007. Precipitation interception in
Australian tropical rainforests: II. Altitudinal gradient of cloud interception,
stemflow, throughfall and interception. Hydrological Processes 21, 1703–1718.
Meyer, E., Hero, J.-M., Shoo, L., Lewis, B., 2005. Recovery Plan for the Wallum
Sedgefrog and Other Wallum-dependent Frog Species 2005–2009. Report to
Department of Environment and Heritage, Canberra, Australia.
Midgley, J.J., Lawes, M.J., Chamaillé-Jammes, S., 2010. Savanna woody plant
dynamics; the role of fire and herbivory, separately and synergistically.
Australian Journal of Botany 58, 1–11.
Mooney, S.D., Harrison, S.P., Bartlein, P.J., Daniau, A., Stevenson, J., Brownlie, K.,
Buckman, S., Cupper, M., Luly, J., Black, M., Colhoun, E., D’Costa, D., Dodson, J.,
Haberle, S., Hope, G., Kershaw, P., Kenyon, C., McKenzie, M., Williams, N., 2010.
Late Quaternary fire regimes of Australia. Quaternary Science Reviews 30, 28–
46.
Morton, S.R., Short, J., Barker, R.D., 1995. Refugia for Biological Diversity in Arid and
Semi-arid Australia. Biodiversity Series Paper 4, Department of the
Environment, Sport and Territories, Canberra, Australia.
Murphy, B.P., Russell-Smith, J., Watt, F.A., Cook, G.D., 2009. Fire management and
woody biomass carbon stocks in mesic savannas. In: Russell-Smith, J.,
Whitehead, P.J., Cooke, P. (Eds.), Culture, Ecology and Economy of Fire
Management in North Australian Savannas: Rekindling the Wurrk Tradition.
CSIRO Publishing, Collingwood, Victoria, Australia, pp. 361–387.
Murphy, B.P., Russell-Smith, J., Prior, L.D., 2010. Frequent fires reduce tree growth in
northern Australian savannas: implications for tree demography and carbon
sequestration. Global Change Biology 16, 331–343.
Myers, N., Mittermeir, R.A., Mittermeier, C.G., Fonseca, G.A.B., Kent, J., 2000.
Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
Nicholls, N., Drosdowsky, W., Lavery, B., 1997. Australian rainfall variability and
change. Weather 52, 66–71.
Nielsen, D.L., Brock, M.A., Rees, G.N., Baldwin, D., 2003. Effects of increasing salinity
on freshwater ecosystems in Australia. Australian Journal of Botany 51, 655–
665.
Pickering, C., Good, R.B., Green, K., 2003. The Ecological Impacts of Global Warming
– Potential Impacts on the Biota of the Australian Alps. Report for the Australian
Greenhouse Office, Canberra, Australia.
Pitman, A.J., Narisma, G., Pielke, R.A., Holbrook, N., 2004. Impact of land cover
change on the climate of southwest Western Australia. Journal of Geophysical
Research 109, D18109. doi:10.1029/2003JD004347.
Pounds, J.A., Fogden, M., Campbell, J., 1999. Biological response to climate change on
a tropical mountain. Nature 398, 611–615.
Price, O.F., Woinarski, J.C.Z., Robinson, D., 1999. Very large area requirements for
frugivorous birds in monsoon rainforests of the Northern Territory, Australia.
Biological Conservation 91, 169–180.
Prior, L.D., Williams, R.J., Bowman, D.M.J.S., 2010. Experimental evidence that fire
causes a tree recruitment bottleneck in an Australian tropical savanna. Journal
of Tropical Ecology 26, 595–603.
Rea, N., Storrs, M.J., 1999. Weed invasions in wetlands of Australia’s Top End:
reasons and solutions. Wetlands Ecology & Management 7, 47–62.
Robinson, C.J., Eberhard, R., Wallington, T., Lane, M., 2009. Institutional
Collaboration for Effective Environmental Governance in Australia’s Great
Barrier Reef. CSIRO Water for Healthy Country and MTSRF Technical Report,
Brisbane, Australia.
Rossiter-Rachor, N.A., Setterfield, S.A., Douglas, M.M., Hutley, L.B., Cook, G.D.,
Schmidt, S., 2009. Invasive Andropogon gayanus (gamba grass) is an ecosystem
transformer of nitrogen relations in Australian savanna. Ecological Applications
19, 1546–1560.
Russell-Smith, J., 1991. Classification, species richness, and environmental relations
of monsoon rain forest in northern Australia. Journal of Vegetation Science 2,
259–278.
Russell-Smith, J., Bowman, D.M.J.S., 1992. Conservation of monsoon rainforest
isolates in the Northern Territory, Australia. Biological Conservation 59, 51–63.
Russell-Smith, J., Ryan, P.G., Cheal, D., 2001. Fire regimes and the conservation of
sandstone heath in monsoonal northern Australia: frequency, interval,
patchiness. Biological Conservation 104, 91–106.
Russell-Smith, J., Price, O.F., Murphy, B.P., 2010. Managing the matrix: decadal
responses of eucalypt-dominated mesic savanna to ambient fire regimes in
three north Australian conservation reserves. Ecological Applications 20, 1615–
1632.
Scheffer, M., 2010. Complex systems: foreseeing tipping points. Nature 467, 411–
412.
Scheffer, M., Bascompte, J., Brock, W.A., Brovkin, V., Carpenter, S.R., Dakos, V., Held,
H., van Nes, E.H., Rietkerk, M., Sugihara, G., 2009. Early-warning signals for
critical transitions. Nature 461, 53–59.
Setterfield, S.A., Rossiter-Rachor, N.A., Hutley, L.B., Douglas, M.M., Williams, R.J.,
2010. Turning up the heat: the impacts of Andropogon gayanus (gamba grass)
invasion on fire behaviour in northern Australian savannas. Diversity and
Distributions 16, 854–861.
Sharp, B.R., Bowman, D., 2004. Patterns of long-term woody vegetation change in a
sandstone-plateau savanna woodland, Northern Territory, Australia. Journal of
Tropical Ecology 20, 259–270.
Sheaves, M., 2009. Consequences of ecological connectivity: the coastal ecosystem
mosaic. Marine Ecology Progress Series 391, 107–115.
Sheaves, M., Johnston, R., 2008. Influence of marine and freshwater connectivity on
the dynamics of subtropical estuarine wetland fish metapopulations. Marine
Ecology Progress Series 357, 225–243.
Shoo, L.P., Storlie, C., Vanderwal, J., Little, J., Williams. S.E., 2010. Targeted protection
and restoration to conserve tropical biodiversity in a warming world. Global
Change Biology, doi:10.1111/j.1365-2486.2010.02218.x.
Skerratt, L.F., Berger, L., Speare, R., Cashins, S., McDonald, K., Phillott, A., Hines, H.,
Kenyon, N., 2007. Spread of chytridiomycosis has caused the rapid global
decline and extinction of frogs. EcoHealth 4, 125–134.
Steffen, W., Burbidge, A.A., Hughes, L., Kitching, R., Lindenmayer, D., Musgrave, W.,
Stafford Smith, M., Werner, P.A., 2009. Australia’s Biodiversity and Climate
Change. Natural Resource Management Ministerial Council, Canberra, Australia.
Still, C.J., Foster, P.N., Schneider, S.H., 1999. Simulating the effects of climate change
on tropical montane cloud forests. Nature 398, 608–610.
Sun, F.F., Kuang, Y.W., Wen, D.Z., Xu, Z.H., Li, J.L., Zuo, W.D., Hou, E.Q., 2010. Longterm tree growth rate, water use efficiency, and tree ring nitrogen isotope
composition of Pinus massoniana L. in response to global climate change and
local nitrogen deposition in southern China. Journal of Soils and Sediments 10,
1453–1465.
Sutherland, W.J., Woodroof, H.J., 2009. The need for environmental horizon
scanning. Trends in Ecology and Evolution 24, 523–527.
Tebaldi, C., Hayhoe, K., Arblaster, J.M., Meehl, G.A., 2006. Going to extremes: an
intercomparison of model-simulated historical and future changes in extreme
events. Climatic Change 79, 185–211.
Thoms, M.C., Southwell, M., McGinness, H.M., 2005. Floodplain-river ecosystems:
fragmentation and water resources development. Geomorphology 71, 126–138.
Underwood, J.N., 2009. Genetic diversity and divergence among coastal and
offshore reefs in a hard coral depend on geographic discontinuity and oceanic
currents. Evolutionary Applications 2, 222–233.
Valentine, L.E., Roberts, B., Schwarzkopf, L., 2007. Mechanisms driving avoidance of
non-native plants by native lizards. Journal of Applied Ecology 44, 228–237.
van Nes, E.H., Scheffer, M., 2007. Slow recovery from perturbations as a
generic indicator of a nearby catastrophic shift. American Naturalist 169,
738–747.
Vellend, M., Verheyen, K., Jacquemyn, H., Kolb, A., van Calster, H., Peterken, G.,
Hermy, M., 2006. Extinction debt of forest plants persists for more than a
century following habitat fragmentation. Ecology 87, 542–548.
Wahren, C.-H., Papst, W.A., Williams, R.J., 1999. Post-fire regeneration in Victorian
alpine and subalpine vegetation. In: Conference Proceedings – Australian
Bushfire Conference. Albury, Victoria, Australia.
Ward, D.J., Lamont, B.B., Burrows, C.L., 2001. Grasstrees reveal contrasting fire
regimes in eucalypt forest before and after European settlement of
southwestern Australia. Forest Ecology and Management 150, 323–329.
Washington-Allen, R.A., Briske, D.D., Shugart, H.H., Salo, L.F., 2009. Introduction to
special feature on catastrophic thresholds, perspectives, definitions, and
applications. Ecology and Society 15, 38. <http://www.ecologyandsociety.org/
vol15/iss3/art38/>.
Watson, J.E.M., Evans, M.C., Carwardine, J., Fuller, R.A., Joseph, L.N., Segan, D.B.,
Taylor, M.F.J., Fensham, R.J., Possingham, H.P., 2010. The capacity of Australia’s
protected-area system to represent threatened species. Conservation Biology,
doi:10.1111/j.1523-1739.2010.01587.x.
Wedderburn, S.D., Walker, K.F., Zampatti, B.P., 2008. Salinity may cause
fragmentation of hardyhead (Teleostei: Atherinidae) populations in the River
Murray, Australia. Marine and Freshwater Research 59, 254–258.
Weste, G., Marks, G.C., 1987. The biology of Phythophora cinnamomi in Australasian
forests. Annual Review of Phytopathology 25, 207–229.
Williams, S.E., Pearson, R.G., Walsh, P.J., 1996. Distributions and biodiversity of the
terrestrial vertebrates of Australia’s Wet Tropics: a review of current
knowledge. Pacific Conservation Biology 2, 327–362.
Williams, S.E., Bolitho, E.E., Fox, S., 2003. Climate change in Australian tropical
rainforests: an impending environmental catastrophe. Proceedings of the Royal
Society B 270, 1887–1892.
Woinarski, J.C.Z., Hempel, C., Cowie, I., Brennan, K., Kerrigan, R., Leach, G., RussellSmith, J., 2006. Distributional pattern of plant species endemic to the Northern
Territory, Australia. Australian Journal of Botany 54, 627–640.
Woinarski, J.C.Z., Armstrong, M., Brennan, K., Fisher, A., Griffiths, A.D., Hill, B., Milne,
D.J., Palmer, C., Ward, S., Watson, M., Winderlich, S., Young, S., 2010. Monitoring
indicates rapid and severe decline of native small mammals in Kakadu National
Park, northern Australia. Wildlife Research, doi:10.1071/WR09125.
Yates, C.J., McNeill, A., Elith, J., Midgley, G.F., 2010. Assessing the impacts of climate
change and land transformation on Banksia in the South West Australian
Floristic Region. Diversity and Distributions 16, 187–201.
Yibarbuk, D., Whitehead, P.J., Russell-Smith, J., Jackson, D., Godjuwa, C., Fisher, A.,
Cooke, P., Choquenot, D., Bowman, D., 2001. Fire ecology and Aboriginal land
management in central Arnhem Land, northern Australia: a tradition of
ecosystem management. Journal of Biogeography 28, 325–343.