Download The red fox in Australia—an exotic predator turned biocontrol agent

Biological Conservation 108 (2002) 335–359
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The red fox in Australia—an exotic predator turned biocontrol
agent
J.E. Kinneara,*, N.R. Sumnerb, M.L. Onusa
a
Department of Conservation and Land Management (CALM), CALMScience Division, Woodvale Research Centre, PO Box 51, Wanneroo, 6065,
Western Australia
b
Western Australian Marine Research Laboratories, Fisheries Department, PO Box 20, North Beach, 6020, Western Australia
Received 5 June 2001; received in revised form 5 February 2002; accepted 15 March 2002
Abstract
The most important problem regarding mammal conservation in mainland Australia is the low abundance and limited distributions of many species, a legacy of an unprecedented collapse of the mammal fauna on a continental scale that unfolded following
European colonisation. Two major hypotheses (not necessarily always mutually exclusive) have been proposed to account for the
collapse (1) niche loss–damage due to a variety of causes and (2) predation by exotics, in particular by the red fox. This paper
provides evidence the supporting the latter cause as a major factor.
Five case studies in Western Australia demonstrate that the fox is an efficient predator that restricts medium-sized marsupials to
refugia at low densities. Removal of the fox by baiting typically produces two prey responses (1) significant population recoveries
and (2) the colonisation and exploitation of habitats outside of refugia. To date, 11 medium-sized marsupial species, representing
seven families, have responded in a like manner. The impact of the fox on its known marsupial prey mimics a biocontrol agent as it
severely limits prey distribution and abundance. Niche denial and population suppression characterise it’s actions on a suite of
vulnerable species not yet fully documented. # 2002 Elsevier Science Ltd. All rights reserved.
Keywords: Marsupial conservation; Fox (Vulpes vulpes); Predation; Predator removal; Biocontrol; Meta-analyses
1. Introduction
Essentially, after an invading species becomes
established the ecological ‘rules’ or processes which
operated in a given system change. . . . the ‘rules’ or
processes permitting the coexistence of a species
complex are drastically altered leading to extinction
of native species’ (Mooney and Drake, 1989, p. 492).
During the two centuries that followed the European
invasion of Australia, something happened to the
ecological processes or ‘rules’ governing Australia’s ecosystems. This conclusion became inevitable after the
publication of a paper by Burbidge and McKenzie
(1989) on the current status of a major species complex—the mammals. In their pioneering paper, they
demonstrated that Australia had suffered more mammal
* Corresponding author.
E-mail address: [email protected] (J.E. Kinnear).
extinctions, more range contractions, and more population declines than any other biogeographical realm. In
retrospect therefore, it is difficult to avoid this unfortunate conclusion—the European colonisation of Australia resulted in an unprecedented wildlife catastrophe
on a continental scale.
It is our view that the cause of the mammal decline
will never be universally attributed to any particular
factor as causality in ecology is typically complex (see
Hilborn and Stearns, 1982), but unquestionably, some
factors will be identified as being more significant
(proximate) than others. This of course raises the question: what were/are the major factors that made survival
impossible for so many mammal species over such vast
areas of the Australian landscape?
The ensuing search for answers has failed to achieve a
consensus as two competing views have emerged, one
wide ranging in scope, the other much more specific.
Advocates of the former have focused on a list of
environmental and biotic factors such as climate
changes; habitat loss; habitat damage and fragmentation;
0006-3207/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved.
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J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
the impact of competitors, for example, rabbits, livestock
and feral species; wildfires; disease and predation—the
last has been generally judged to be a secondary factor or
dismissed entirely (Burbidge and McKenzie, 1989;
Johnson et al., 1989; Morton, 1990; Hone, 1999).
Other workers have placed a greater emphasis on
depredations by introduced species, in particular, by the
European red fox (Vulpes vulpes; Hoy, 1923; Wood
Jones, 1923–1925; Finlayson, 1961; Christensen, 1980;
King et al., 1981; Kinnear et al., 1988, 1998; Friend,
1990; Friend and Thomas, 1994; Short et al., 1994,
2002; Augee et al., 1996; Hobbs and Mooney, 1998).
The debate continues (Caughley and Gunn, 1996; Hone,
1999).
As a first step, we propose that the primary causes of
the mammal decline, both past and present, be viewed
within the context of two working hypotheses not
necessarily mutually exclusive in every case. The
hypotheses are:
H1. Niche loss–damage (NLD).
H2. Predation by introduced species in particular, by the
fox.
In terms of niche theory (sensu Hutchinson, 1957), the
focus of the NLD hypothesis is primarily on the fundamental niche, while the predation hypothesis is concerned with the realised niche. These distinctions are
profound, and indeed, in many cases, the fate of the
surviving mammal fauna may be dependent upon their
resolution.
1.1. Fundamental vs. realised niches: implications for
conservation
other species; we show that niche denial exists for a suite
of marsupial species surviving in a variety of habitats
over a wide geographic area.
1.2. A proposed model
We submit that currently, one model broadly applies,
at least for a range of medium-sized marsupial species.
We submit that the European fox in Australia mimics
the role of a multi-specific biocontrol agent affecting a
range of marsupial species. Evidence supporting this
hypothesis is presented in the following sections—
although, we have strong reservations about the longterm stability of many existing relationships.
1.3. Scope of this paper
In the following sections, we describe five case studies,
undertaken over the period 1980–1996, as a result of
a fox control experiment initiated in 1978 on rockwallabies (Kinnear et al., 1988, 1998). The results of this
study motivated us to carry out a series of fox removal
trials on sites supporting populations of other rare and
endangered marsupial species. Each trial is presented as
a separate case history with short sections describing
Methods, Results and Discussion. Meta-analysis was
used to collectively analyse the trials and the paper
concludes with a General Discussion that addresses
many debated issues pertaining to the predation
hypothesis.
2. Methods
2.1. Case studies
Factors affecting the fundamental niche of a species
are commonly associated with habitat change due to
alteration and manipulation of the indigenous landscape, with the result that the landscape may no longer
meet the requirements of affected species. In essence, the
NLD hypothesis asserts that colonisation has produced a
landscape greatly diminished in carrying capacity (zero
in many instances), and thus is no longer capable of
supporting much of its indigenous mammalian wildlife.
The predation hypothesis provides an alternative
explanation—niche denial. It asserts that despite the
changes to the indigenous landscape, a major cause of
the mammal decline has been due to predation. Thus,
for many Australian mammals, niches still exist that are
capable of supporting flourishing populations, but
occupancy has been denied because of depredations by
an exotic predator in particular, the red fox.
Niche denial by the fox, which mimics actual loss of
carrying capacity, first became evident in a study involving rare and endangered rock-wallabies (Kinnear et al.,
1988, 1998). In this paper we extend the concept to
2.1.1. Basic design
Unless otherwise noted later, the basic design of the
case studies consisted of the following procedures.
Abundance indices of medium-sized marsupials were
collected before the implementation of fox control, and
again, after an extended period of fox control. Where
circumstances permitted, an unreplicated control site
(no fox control) was used.
Indices of abundance were obtained by trapping and
by repeated spotlight counts using long range, 100-W
lights along defined routes. Wire cage traps, typically set
at intervals of 100 m, were baited with bread and peanut
paste, or a combination of rolled oats, peanut paste and
sultanas. Traps were set at dusk and cleared each
morning. Trapped animals were fitted with numbered
tags in both ears and released at the capture site.
On smaller experimental sites ( < 12,000 ha) foxes
were controlled by the monthly application of 1080poison meat baits (fresh or dried) or intact fowl eggs
using proven methods (sodium monofluoroacetate, 4.5
J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
mg; Kinnear et al., 1988, 1998; Wong et al., 1995). A
larger mainland site was systematically baited aerially
following the methods devised and evaluated by
Thompson and Algar (2000) and Thompson et al.
(2000). Additional details are described, where relevant,
in the appropriate case study.
2.2. Case 1. The Dampier Archipelago: Rothschild’s
rock-wallaby
The Dampier Archipelago was separated from the
mainland ca. 8000 years ago by rising sea levels. It now
comprises 42 islands of varying sizes lying within a 45
km radius of the town of Dampier on the northwest
coast of Western Australia (Fig. 1). The climate is maritime arid. Rainfall is seasonal (summer), but unreliable
with a mean annual fall of 276 mm, and evaporation
exceeds rainfall by a factor of nine. The mean maximum
temperature is 35 C (Morris, 1990). Rothschild’s rockwallaby (Petrogale rothschildi) is found on three islands,
Rosemary (1062 ha), Enderby (3290 ha) and Dolphin
(3203 ha; Fig. 1).
The first recorded fox bounty payments were paid in
1930 at Roebourne on the nearby mainland (Ride et al.,
1964). Foxes were prevalent on the adjacent mainland
and they were also present on Dolphin, Angel and
337
Gidley Islands when this study was launched. Feral cats
(Felis catus) were present on Dolphin Island and the
nearby mainland; the dingo (Canis dingo) is absent from
archipelago.
2.2.1. Methods
Beginning in 1979–1980, standardised spotlight
counts of rock-wallabies on selected areas of Enderby
Island (fox free) and Dolphin Island (fox infested) were
carried out (Fig. 1). Traverses on foot were made at
using a 100-W long-range spotlight powered by a 12 V
automotive battery mounted on a modified backpack.
Wallabies are readily sighted in these landscapes as the
islands largely consist of low hummock grasslands and
scree. An aerial baiting program for foxes was initiated
(1984) following some exploratory trials (1980–1981) to
determine the level of bait acceptance and the risk
to non-target species (Table 1). The northern region of
Burrup Peninsula was baited to create a buffer zone or
sink for foxes. This step was based on the assumption
that the dispersal rate of foxes to Dolphin Island would
be reduced. Foxes inhabiting the nearby islands, Angel
and Gidley (Fig. 1) were poisoned in order to eliminate
potential immigrants from these sources.
In 1990, the spotlight traverses on Enderby and Dolphin Islands were repeated together with traverses
Fig. 1. The Dampier Archipelago: Rothschilds’ rock-wallaby is found on the mainland (at low densities) and on three islands in the archipelago—
Enderby, Rosemary and Dolphin. Foxes arrived in the region during the 1930s and subsequently colonised Dolphin, Angel and Gidley Islands. The
upward projecting bars next to Enderby (fox free) and Dolphin Islands (fox infested initially, and subsequently, after the implementation of fox
control) represent the number of sightings per three hours of transect (see also, Table 2).
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J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
Table 1
Details of baiting events (1980–1989) carried out in the Dampier Archipelago (see Fig. 1)
Date
Method
Areas baited
Comments
October 1980
Manual
Dolphin I.
38 beach sectors baited
May 1981
Manual
Dolphin I.; Burrup Peninsula
Most southern beaches on Dolphin; north Burrup beaches
September 1984
Aerial
Dolphin, Angel, and Gidley
Islands; Burrup
2530 baits (1.5 mg 1080) dropped in 200 m grid pattern;
1230 baits laid along tracks on Burrup.
October 1987
Aerial
Dolphin, Angel, and Gidley
Islands; Burrup
2010 baits dropped (4.5 mg 1080)
October 1989
Aerial
Dolphin, Angel, and Gidley
Islands; Burrup
1500 baits on beaches, valleys, mangroves and fresh water pools
of selected baited and unbaited areas of the adjacent
Burrup Peninsula.
2.2.2. Results: relative abundance: fox free vs. fox
infested
There were striking differences in rock-wallaby sightings between the fox-free and fox-infested islands
(Table 2; Fig. 1). During the 10+ hours of traverses
made on each island for the period 1979–1980, 195 rockwallabies were sighted (18.7/h 1.73 SE) on Enderby,
while only three wallabies were observed (0.30/h) on
Dolphin Island—an average rock-wallaby sighting ratio
of 62:1 (fox-free/fox-infested).
2.2.3. Relative abundance: under fox control
After a 6-year period of fox control, less intensive (ca.
3 h) spotlight traverses produced these results: on foxfree Enderby, 19.2 1.35 rock-wallaby sightings/h were
recorded while on fox-controlled Dolphin, 8.8 0.84/
h—a sighting ratio of approximately 2:1—nearly a 26
fold sighting increase for Dolphin Island. The 1990
Burrup traverses (8 h) produced one wallaby sighting
(Table 2, Fig. 1).
2.2.4. Discussion
2.2.4.1. Refugia and niche extensions. On fox-free
Enderby and Rosemary Islands, footprints and pads of
rock-wallabies were conspicuous on sand-plain areas
where they prefer to graze. In contrast on Dolphin
Island before fox control, the converse prevailed; signs
were non-existent apart from an occasional sighting on
rock-piles. Under fox control, not only did the sighting
rate increase, but some wallabies were encountered foraging a considerable distance from their rocky shelter.
Kinnear et al. (1988, 1998) observed a similar increase in
foraging range (i.e. realised niche extension) in response
to fox control in the case of the rock-wallaby Petrogale
lateralis, which lives in an agricultural setting.
One could argue that the Dolphin Island rock-wallaby
population was being limited by transient abiotic factors
that ceased to operate during the latter course of the
study. This argument is not supported by the sightings
on nearby Enderby Island, which did not vary. Significantly, there was also no change in rock-wallaby
sightings on the adjacent Burrup peninsula in the
absence of repeated baitings, which has been shown to
be necessary on the mainland in order to sustain the
required level of fox control (Fig. 1; Table 2; Kinnear et
al., 1988; Thompson et al., 2000). Butler (1983) recorded
zero sightings during a comprehensive biological survey
of the Burrup Peninsula.
The long fox-baiting interval (24–36 months) on Dolphin Island was sufficient to produce a rock-wallaby
population recovery because of the presence of a water
barrier that presumably served as a deterrent to potential invaders, and the creation of a buffer zone on the
adjacent Burrup Peninsula. Buffer zones have since been
shown to retard recolonisation by foxes (Thompson et
al., 2000).
2.3. Case 2: Tutanning: a wheatbelt nature reserve
remnant
In the Western Australia (WA) wheatbelt, more than
90% of the original landscape (ca. 15 million ha) has
been cleared for agriculture. The region previously supported a diverse mammal fauna with 46 species occurring in the region (Shortridge, 1909).
During the 1960s six species of medium sized mammals were present in the Tutanning remnant (2200 ha),
and three of these species were shown to be moderately
abundant in a study by Sampson (1971). However,
during the early 1970s all populations crashed, and by
1978 three species—numbat or banded-anteater (Myrmecobius fasciatus), quenda (Isoodon obesulus, southern
brown bandicoot) and western ringtail possum (Pseudocheirus occidentalis)—were no longer resident. Sightings of the woylie (a bettong or rat kangaroo, Bettongia
penicillata) ceased and two other species, the tammar
wallaby (Macropus eugenii) and the brushtail possum
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J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
Table 2
Relative abundance of rock-wallabies on islands in the Dampier Archipelago under the following conditions (1) fox free (2) fox infested (3) fox
control (see Fig. 1)
Date
Traverse time (min)
Dolphin Island (fox infested) 1979–1980 census (no fox control)
6 June 1979
170
5 May 1980
82
6 May 1980
85
7 May 1980
135
9 May 1980
130
Totals
Mean
602
231
Enderby Island (fox free) 1979–1980 census
4 June 1979
103
5 June 1979
70
6 June 1979
60
7 June 1979
70
5 May 1980
50
12 May 1980
85
13 May 1980
90
14 May 1980
100
628
3
9
12
13
7.2
9.2
10.0
34
1
0
<1
0
27
25
27
23
10
19
28
36
15.7
21.4
27.0
19.7
12.0
13.0
18.7
21.6
195
18.61.73
Enderby Island (fox free) 1990 census
6 June 1990
96
7 June 1990
67
8 June 1990
68
Totals
MeanSE
0
0
0.71
0.89
0
8.80.84
Burrup Peninsula (Fox infested) 1990 census
9–11 September 1990
183 (unbaited area)
24–26 October 1990
305 (baited 12 months ago)
Totals
MeanSE
0
0
1
2
0
Number sighted per hour
0.30
Dolphin Island 1990 census (fox control)
23 June 1990
75
24 June 1990
78
25 June 1990
78
Totals
MeanSE
Rock-wallabies sighted
231
(Trichosurus vulpecula) were infrequently sighted. This
was the situation in 1984 when we initiated a fox control
program within Tutanning Nature Reserve.
2.3.1. Methods
Prior to the implementation of fox baiting, two trapping sessions for woylies were carried out. The first session (January 1979) was limited to a southeast area
previously trapped by Sampson (1971). The second session took place in October–November 1984 prior to the
first baiting. On this occasion, we set up trap-lines at
sites over a wider area of the reserve. Linear sets of 10
traps (1 km long) placed along tracks at 100 m intervals
sampled a range of plant associations throughout the
reserve (Fig. 2). Beginning in November 1984 and following the procedures developed by Kinnear et al.
31
24
19
19.4
21.5
16.8
74
19.21.35
(1988, 1998), poison baits were laid monthly at 100 m
intervals along all internal tracks and the boundaries of
the reserve.
In September 1989 after approximately 5 years of
fox baiting, trap lines were set up as previously described.
When it soon became evident that the woylies
had increased substantially, we extended our coverage to other areas of the reserve that we had not previously trapped. The reserve was trapped again in 1992
(Fig. 2).
2.3.2. Results: trapping
A summary of the trapping results for woylies is presented in Table 3. Fig. 2 illustrates the trap success rate
(percentage) for individual trap lines for the years 1984,
1989 and 1992.
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J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
2.3.3. Spotlight counts
Fig. 3 illustrates the trends (1979–1992) and more
recent (1998) increases for tammars are also shown
(from CALM’s Western Shield database, courtesy of P.
Orell). The number of sightings prior to fox control are
similar to those recorded during an extensive series of
spotlight surveys carried out by Arnold and Steven
(1988, personal communication). They recorded all
mammal sightings while spotlighting for kangaroos
along the reserve boundary. During 50 circuits of the
boundary carried out between June 1979 and December
1984, they recorded on average < 2 tammars, and < 1
brushtail possums. Woylies were not recorded.
2.3.4. Discussion
The initial trapping effort undertaken in January 1979
covered Sampson’s study area. During his study (1967–
1970), he achieved trap success rates ranging from 10 to
21% for woylie, quenda and brushtail possum. Our
effort in 1979 (380 trap nights) yielded a single male
woylie, a success rate of 0.26% (Table 3).
The period, 1950s–early 1970s, during which a suite of
medium-sized marsupials was moderately abundant
within Tutanning was a local phenomenon, and moreover, it occurred in the absence of overt fox control. One
would be hard pressed therefore, to interpret Sampson’s
data as evidence that the fox might be a biocontrol
Fig. 2. Trap success rates obtained for woylies at different sites within Tutanning Nature Reserve before the implementation of fox control (1984),
and after 5 and 8 years of control. Prior to fox control, woylies were captured at only two sites that were largely comprised of dense thickets of
Gastrolobium spp., which served as predation refugia. Trap success rate averaged 4.5% within the two refuges and zero for all other trap lines
(overall average 2.17%). During subsequent trapping periods (1989 and 1992), woylies were captured over a very much wider area of the reserve.
Table 3
A summary of trapping results (excluding repeats) for Tutanning woylies before fox control, and after the implementation of controla
Year
Total trap nights
No fox control
January 1979
October–November 1984
380
322
1
7
0.26
2.17
Fox control commenced November 1984
September 1989
July–August 1992
320
266
64
76
20.00
28.57
a
Total captures
Trap success (%)
During January 1979 trapping was limited to Sampson’s (1971) study area. In 1984, a wider area was trapped in particular, Gastrolobium
thickets (see text), which proved to be refuge sites. In 1989 and 1992, an even wider area was sampled (Fig. 2).
J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
341
Fig. 3. Spotlighting counts obtained before and after fox control for three marsupials species persisting in Tutanning Nature reserve. (a) Woylies
sightings, which prior to fox control, were zero because of a restricted distribution within dense cover. (b) Brush-tail possums were sighted mainly in
trees, but following fox control, sightings increased and individuals were frequently sighted on ground with young. (c) Tammar wallaby sightings,
which gradually increased from <2 to 40 h1. (The 1998 data courtesy of P. Orell, Wildlife Branch.)
agent. However in retrospect, there are some compelling
reasons to believe that his study may have been confounded; four reasons are discussed as follows.
1. During the 1950s, a fox bounty payment system
was in force (Whitehouse, 1976). Apart from
the financial incentive to control foxes, foxes
were actively hunted for recreation, and because
they were perceived to be a menace to young
lambs.
2. The period of fauna abundance coincided with a
fire succession stage when the cover was dense,
and thus provided some protection from predators (A.R. Main, personal communication).
3. Tutanning carries extensive stands of toxic plants
(Gastrolobium spp.). This genus is noted for its
ability to synthesise monofluoroacetate (1080).
Woylies and brushtail possums are strikingly
tolerant to 1080 (King et al., 1981; Twigg and
King, 1991) and by inference, this suggests that
they consume 1080 plant materials. Indeed,
woylies are known to cache toxic seeds of Gastrolobium, and there are anecdotal accounts from
early settlers of domestic pigs dying through secondary poisoning after being fed woylies. Thus it
is possible that depredations by foxes on toxic
victims were contributing to their control.
4. Christensen (1980) has linked certain instances of
mammal abundance with broad-scale rabbit
control by the WA Agriculture Protection Board
(APB). The toxin 1080 was used and it is noted
for its impact on non-target species higher in the
food chain (secondary poisoning). Algar and
Kinnear (1996) described an incident when
radio-collared foxes died following rabbit control by the ABP on nearby farmland. McIlroy
and Gifford (1991) have also recorded similar
findings. During the 1960s, the use of 1080 for
rabbit control peaked and fox numbers were low
(King et al., 1981). An APB policy change in the
early 1970s led to the abandonment of broadscale rabbit control.
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J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
It is likely therefore that the earlier circumstances
negated to some extent the impact of the fox within
Tutanning. Whatever the cause, this period of abundance was a local, transient phenomenon. By the mid1970s, all species were in decline with three species
declining to extinction and moreover, the decline coincided with the cessation of broad-scale rabbit control.
This situation has since been reversed by the implementation of fox control; the survivors—woylies, tammars and brushtail possums—have recovered and are
now common. The quenda and the numbat have been
successfully re-introduced (Friend and Thomas, 1994;
personal communication).
2.3.5. The Tutanning Annex
The Annex (114 ha) is a remnant block that is separated from the SE sector of the main Tutanning reserve
by a farm paddock. Its vegetation is dominated by
Allocasuarina spp. commonly known by early settlers as
‘tamma or tammar bush’.
2.3.6. Methods
A spotlight survey was carried out in December 1987.
Fox baiting was extended to the Annex in November
1989. Follow-up spotlight surveys were made in
November 1992 and May 1998 (the latter by P. Orell,
Wildlife Branch).
2.3.7. Results and discussion
The results (Fig. 4) illustrate a 12–20 fold increase in
tammar sightings, most of which were observed feeding
nearby in adjacent paddocks. Brushtail possums, previously unsighted, were recorded in significant numbers
(Fig. 4).
In summary, the Annex results, except for the absence
of the woylie, mirrored the results obtained from the
nearby main reserve. Tammars were conspicuously
more abundant when compared to the main reserve. A
public road bisects the main reserve and poaching has
been noted. This may have accounted for the difference,
as the Annex has no public access. After steps were
taken to curtail poaching (L. Silvester, District Wildlife
Officer, personal communication), recent (1998) surveys
of tammars (by P. Orell, personal communication) have
recorded a large increase for the main reserve (Fig. 3).
2.4. Case 3: Boyagin Nature Reserve
The 4780 ha Boyagin Nature Reserve (ca. 24 km NW
of Pingelly WA) is comprised of two parts (west and
east) separated by farmland. Unlike Tutanning’s recent
history, there are no records, official or otherwise, indicating that Boyagin enjoyed a flourishing period of
mammal abundance. Naturalist H. Butler surveyed the
area in 1972 and sighted one tammar; 10 years
later, Reserves officer D. Hart trapped intensively and
Fig. 4. The Tutanning Annex remnant is separated from the main
reserve by a farm paddock. (a) The large increase by tammars following fox control has elevated the species from rarity to pest status
locally, as most were observed grazing on farmland. Data for 1998 (P.
Orell) were collected at seeding time and hence sightings were largely
restricted to the annex where tammars were less visible. (b) Brushtail
possum sightings.
captured one brushtail possum (CALM Departmental
records).
In 1985, numbats were released into East Boyagin
without fox control, but the translocation failed. However under fox control, a second translocation was successful (Friend, 1990). We initiated a monitoring
program on both sections for other medium-sized
mammals in 1989 for the purpose of comparing their
abundance. When this objective was achieved, baiting
was extended to W. Boyagin in late 1989 and we continued to monitor abundance on both sides.
2.4.1. Methods
Trapping and spotlight methodology were as described
previously. Despite an intensive trapping effort, and
after 7 years of fox control on E. Boyagin, and 3 years
on W. Boyagin, no woylies were captured. We therefore
concluded that woylies were no longer resident on Boyagin. In 1992, 40 woylies, sourced from Dryandra
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Woodland, were released on East and West Boyagin (14
females, six males per side).
2.4.2. Results and discussion
2.4.2.1. Trapping results: possums. Fig. 5 displays the
trapping results for both East and West Boyagin. There
is a marked difference in capture rates between E. Boyagin (baited from 1985) and W. Boyagin (not baited
until November 1989). West Boyagin essentially served
as a control population for four years (no fox control,
1985–1989). When the trapping results for both sides
are compared for this period, the benefits conferred by
baiting are clearly evident, as there was a nine-fold difference by 1989 (Fig. 5).
2.4.2.2. Trapping results: woylies. Woylies, which were
re-introduced to Boyagin in 1992, were firmly established by 1996 on both sides, but at substantially different
densities and this possibly confounded the trapping
results for both woylies and possums species (Table 4).
Woylie captures predominated on W. Boyagin and
possum captures were relatively few, but this was
reversed for E. Boyagin. On W. Boyagin 88 woylies
were captured over 150 trap nights (59% success rate)
while on E. Boyagin 11 woylies and 52 possums were
captured. To allow for this competition for traps, we
have also elected to calculate the trap success rate for
possums by subtracting the woylie captures from the
total number of traps set (Table 4). We cannot account
for these differences; it could be due to the baiting history, differences in carrying capacity, competition for
traps or a combination of these factors.
Spotlighting results (1989–1992) for possums and
tammars are shown in Fig. 6. With fox control, an
increasing trend is evident for possums, as is the case for
tammars although the sighting rate is lower. Visibility
affects spotlight counts and generally, it is the density of
cover that is the major determinant, but other factors
may be important.
2.5. Case 4: Dryandra Woodland
Dryandra Woodland is a collection of 17 remnants
comprising a total area of ca. 28,000 ha (Friend et al.,
1995). The main block (ca. 12,000 ha—the largest remnant) was selected as the study site.
In 1970–1971, A.A. Burbidge (unpublished report)
carried out an intensive trapping and spotlight fauna
survey in the main block over a 12 month period.
His survey coincided with Sampson’s study at Tutanning, but unlike Sampson’s results, Burbidge’s trapsuccess rates for medium-sized mammals were low
namely, brushtail possum 4.0%; woylie 2.7%; quenda
0.35%—the latter not having been trapped since then.
Table 4
Woylie trapping data (1996) 4 years after translocation to Boyagin
under fox control. Brushtail possum data also listed
Trap
nights
Woylie
including
repeats
Woylie
no repeats
Possum
including
repeats
Possum
no repeats
East Boyagin
50
5
50
1
50
3
5
0
3
13
22
17
13
22
14
Totals
9
8
52
49
West Boyagin
50
30
50
29
50
29
30
17
12
6
6
6
6
3
2
Totals
59
18
11
88
Fig. 5. A comparison of trap success rates for brushtail possums on East and West Boyagin under differing fox control regimes. Data for 1996*
corrected to allow for trap interference by woylies (see text).
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J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
Fig. 6. Spotlight counts for Boyagin Nature Reserve. (a) Brushtail
possums. (b) Tammar wallaby.
The next trapping exercise made in 1975 failed to capture a single specimen of any of the above species
(Christensen, unpublished, departmental files).
In September 1982, J.A. Friend commenced a fox
baiting trial on a section of the main block of Dryandra
(Fig. 7). The purpose of the program was to test the
response of the numbat population to fox control
(Friend, 1990; Friend and Thomas, 1994).
Friend’s baited area encompassed some sites previously trapped by Burbidge and Christensen. This area
was trapped again in 1984 along with additional trap
lines that were established outside of Friend’s baited
area (Fig. 7, Departmental files). At this stage, after 2
years of fox control, it was evident that woylie trap
success rate were substantially greater in Friend’s baited
area compared to outside of the baited area. We trapped the same areas again in 1989 and shortly afterwards, the whole of the main Dryandra block was
baited. Three years later (1992) we carried out a trapping census that sampled the entire main block.
2.5.1. Results and discussion
2.5.1.1. Trapping results: woylies. Fig. 8 illustrates the
results for 1984 and 1989, after 2 and 7 years, respectively
of localised fox control (trap-lines 1–4, within Friend’s
baited area, trap-lines 5–13, outside of the baited area,
Fig. 7), and for 1992, after 3 years fox control throughout the entire main block.
Woylies responded to fox control in a manner comparable to Boyagin and Tutanning. In the absence of
fox control, it was necessary to trap intensively for
extended periods in order to detect their presence, and
in many areas none were captured. For example, within
the area that became Friend’s baiting area, Burbidge
captured 21 woylies during 822 trap-nights of effort
(2.55% success), while Christensen captured zero woylies during 158 trap-nights. By 1984 after 2 years of fox
control, a 50% increase in effort by Christensen produced 36 woylies (15.3% success). In 1989, we caught 75
woylies in Friend’s baited area at a rate comparable
with the 1984 effort.
Judging from 1989 results, it would appear from our
trapping effort that woylie densities had stabilised
within Friend’s baited area (ca. 16% in 1984 and 1989).
However, by 1992, after the whole of the main block
had been baited for 3 years, the trap success rate (Fig. 8)
increased to 56%—presumably due to a higher level of
fox control achieved by the baiting of the entire main
block. Kinnear et al. (1988) found that foxes rapidly reinvaded small baited areas.
The results from trap-lines 5–13 (area not baited until
1989; Figs. 7 and 8) situated at varying distances from
the perimeter of the baited zone, indicates a zero to low
survival rate for woylies not directly afforded the protection provided by baiting. Some protection was indirectly provided for woylies living adjacent to the
southern boundary of Friend’s baited area (trap-lines 5–
8, Figs. 7 and 8). In general, the trap success rate for
woylies varied inversely with distance from the baited
area (exception, trap line 11, Figs. 7 and 8).
After 3 years of fox control throughout the main
block, woylies extended their realised niche to SE sections of Dryandra where none had been trapped or
sighted previously (Fig. 8). The SE section yielded trap
success rates in excess of 70% for some trap lines. In
1987, a spotlight traverse through this area (Coelac
Road, Fig. 7) produced zero sightings for all species.
2.5.1.2. Spotlighting results: no fox control. During
1971–1972 in addition to trapping, A.A. Burbidge carried out an extensive series of spotlight transects (19
random and 20 fixed routes). An inspection of Burbidge’s random and standardised spotlight data does
not reveal any major differences for all species. Thus, a
traverse along any route only produced < 1 sighting on
average (Table 5).
In 1987, our results for unbaited areas of Dryandra
were similar (Table 6). Woylie and possum sightings
were typically low prior to the baiting of the entire
block, but they both increased sharply after baiting of
J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
345
Fig. 7. The main block of Dryandra Woodlands is a large (ca. 12,000 ha) wheatbelt native remnant. This figure displays the location of 13 woylie
trap-lines, and ‘Friend’s baited area’ (the enclosed area; Friend, 1990), which represents an area selectively baited from 1982 to 1989. The whole of
Dryandra has been baited from 1989 onwards.
the entire block (Table 6). Tammar sightings were
infrequent and variable and to date have remained so
(P. Mawson, personal communication).
2.6. Case 5: Fitzgerald River National Park
Fitzgerald River National Park (FRNP) is located on
the south coast of WA between Bremer Bay and Hopetoun (Fig. 9). The park (329,000 ha) is approximately 27
times larger than Dryandra’s main block (Chapman and
Newbey, 1995). Apart from wildfires, it has a history
that has been relatively free of disturbance.
Chapman and Newbey (1995, p. 93) list 26 mammal
species that were known to be present in the Fitzgerald
area prior to European settlement. Many of these species were also part of a now greatly fragmented wheatbelt fauna, and both regions have experienced a similar
level of extinctions (> 40%). Survival of medium sized
mammals has been typically poor, as only four spp of a
known 11 spp (> 150 g) were recently recorded by
Chapman and Newbey. Moreover, the surviving species
were not recorded as being abundant or widely distributed. For example, Chapman and Newbey trapped
only one quenda, sighted only two tammars and eleven
brush wallabies (Macropus irma; uncommon and
restricted). Brushtail possums were recorded as being
present along watercourses (numbers not stated).
2.6.1. Objectives
The objectives of the FRNP study were threefold:
1. To extend fox control to a much larger unfragmented area in a more mesic biogeographical
region of the state.
2. To determine if two aerial baitings per year were
sufficient to significantly lower and maintain fox
numbers over a large unfragmented area of conservation estate.
3. To assess if this level of baiting produced a positive population response by resident mediumsized mammals.
2.6.2. Methods
Trap lines extending for 4 km (40 traps set at 100-m
intervals) were set out along vehicle tracks so as to
sample the range of plant associations namely heath,
woodland, riparian and mallee within the study areas.
Spotlight traverses likewise sampled the earlier associations but covered a larger area.
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J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
Fig. 8. Dryandra Woodlands showing the trapping results for woylies obtained for the years 1984, 1989, and 1992. Initially, woylie increases were
largely confined to Friend’s baited area (baited from 1982) and some nearby trap sites (Fig. 7). Trap success rates declined to zero at the more distant
sites. The whole of Dryandra was baited in 1989 and by 1992, woylies had colonised most of the reserve at high densities.
Table 5
Counts (numbers h1) of marsupial species observed along fixed spotlight transects before fox control, within Friend’s baited area (Fig. 7), and after
fox control throughout the main block
Possum sightings (h1)
Tammar sightings (h1)
1.68
2.32
2.0
0.57
0.50
0.54
Localized fox control from 1982 (Friend’s baited area)
December 1987 (5.03)
2.58
December 1989 (8.12)
13.3
1.19
2.71
0
0.37
Fox control (1989) extended to whole of Dryandra main block
September 1990 (4.5)
15.7
November 1992 (5.74)
23
6.67
9.9
4.67
1.23
Year (total hours)
No fox controla
1970 Random routes (31.6)
1971 Fixed routes (43.8)
Means/h
a
Woylie sightings (h1)
0.60
0.27
0.41
Data provided by A.A. Burbidge.
2.6.2.1. Baiting protocol. The FRNP was partitioned on
a north–south axis into approximately two equal parts
(Fig. 9). Beginning in February 1991 and ending September 1995, the western part was aerially baited twice
yearly during spring and autumn. Baits consisted of
dried meat containing 4.5 mg, 1080 and were distributed
at a density of approximately six baits per km2. This
protocol has been shown to be effective method for
reducing fox densities (Thompson and Algar, 2000;
Thompson et al., 2000).
The timing of the baitings was designed to minimise
recruitment by exposing foxes to poison baits during the
reproductive and dispersal phases of their life cycle
(spring/autumn, respectively). Supplementary baitings
J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
(December 1995 and February–March 1996) were made
from a vehicle at the study sites on the western side after
aerial baitings ceased in September 1995.
2.6.2.2. Assessing the level of fox control. We used
the cyanide technique to estimate the effectiveness
of the baiting regime (Algar and Kinnear, 1992). This
Table 6
Counts (numbers h1) of marsupial species observed along fixed spotlight transects excluding Friend’s baited area (Fig. 7)
Year (total hours)
Possum
Tammar
Woylie
(numbers h1) (numbers h1) (numbers h1)
No fox control except for Friend’s baited area
December 1987 (2.43 h) 1.65
2.88
December 1987 (1.88 h) 0.53
2.66
Mean
1.16
2.78
0.00
0.00
0.00
Whole of Dryandra main block baited 1989
September 1989 (2.55 h) 5.49
3.92
September 1990 (1.10 h) 2.73
6.36
September 1990 (1.08 h) 2.78
6.48
September 1990 (1.02 h) 4.72
5.88
0.00
0.00
0.00
0.00
After 3 years of fox control of entire main block
November 1992 (2.42 h) 27.69
22.31
0.00
347
technique generates an abundance index—the number
of foxes sampled per 20 km transects. During the first
year of fox control, cyanide transects were carried out
on both the baited and unbaited sides of the park 2–4
weeks after each baiting (February 1991, November
1991). Cyanide transects were repeated on both sides 5–
6 months after the March 1993 baiting, but just prior to
the next baiting (September).
2.6.3. Results and discussion
2.6.3.1. Effectiveness of the baiting protocol. The relative
impact of the aerial baitings on fox numbers is indicated
in the sample sizes of the cyanide transects for the
unbaited and baited areas (Fig. 10). On the baited side,
the cyanide index declined by an average of 80% for the
1991 trials, and by 75% for the 1993 trial. The latter
outcome signified that recruitment by foxes was negligible between spring and autumn baiting events. These
results are comparable with more comprehensive studies
on bait uptake and fox mortality (Thompson and Algar,
2000; Thompson et al., 2000). In a trial involving 45
radio-tagged foxes, Thompson et al. (2000; Fig. 2)
showed that following an aerial baiting, more than 70%
of the tagged foxes were dead within 10–15 days and all
were dead after 44 days.
Fig. 9. Fitzgerald River National Park: The park (ca. 329,000 ha) was divided approximately into two parts and the western side was aerially baited
twice yearly beginning in February 1991. Two similar study sites were selected on each side of the park, and medium-sized mammals were monitored
until 1996.
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J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
Fig. 10. The western side of the park (Fig. 9) was baited at approximately 6-month intervals. The effectiveness of the baitings was assessed by cyanide baitings (Algar and Kinnear, 1992), a sampling
technique that generates an index of fox abundance—number of foxes
sampled by cyanide baits/20 km. In 1991, we sampled the fox populations on both sides 2–4 weeks after each baiting. Fig. 10 indicates that
the baitings reduced the fox population by approximately 75–80%. In
1993, we carried out an autumn baiting, and we sampled the fox
populations again approximately 6 months later, just prior to the next
(spring) baiting. The purpose of this sampling was to determine if the
fox population had recovered during the 6-month interval between
baitings. The results indicate that there was no net recruitment,
whereas on the unbaited side, foxes had recovered to their original
density.
2.6.3.2. Possum population responses: trapping. Possums
were present on the unbaited eastern side, but 604 trap
nights over a 2-year period yielded only a single possum
in woodland habitat. In contrast, 600 trap nights yielded
48 possums on the baited side, and significantly, the
capture rate increased exponentially (Fig. 11; 1998 data
courtesy P. Collins).
2.6.3.3. Spotlighting. Spotlighting produced 123 possum
sightings within the baited area, but only 12 sightings
within the unbaited area (Table 7). An upward trend
in tammar sightings from the baited study sites is also
evident (Table 7). No tammars were sighted in the
unbaited area.
2.6.4. Postscript: an update
Since the conclusion of this study in 1996, fox control
has continued at a higher level (4 times year1) under
the auspices of Western Shield a statewide exotic predator control program (Bailey, 1996). CALM regional
staff have continued to monitor mammals within our
western study area. A brief summary of their trapping
results follows (information provided by P. Collins).
Possums have continued to increase (Fig. 11) to the
extent that they are considered to be a hindrance as they
dominate the capture statistics to the exclusion of other
potential subjects. Quenda (bandicoots) are being captured routinely. Brush wallabies are now commonly
Fig. 11. A comparison of brushtail possum trap success rates in Fitzgerald River National Park—unbaited versus baited (see text for more
recent results).
sighted over wide areas. The carnivorous marsupial,
Dasyurus geoffroii, (a quoll) has been captured for the
first time, and there has been a spate of captures of
the very rare and endangered Dibbler (Parantechinus
apicalis).
3. Statistical methodology: meta-analysis
Meta-analysis was first used for studies in the social
sciences (see Hedges and Olkin, 1985; Cooper and
Hedges, 1994, among others). It has also been applied in
ecology (Gurevitch and Hedges, 1993; Gurevitch et al.,
1992). This type of analysis is suited to a situation where
a researcher(s) wishes to combine the results of several,
possibly contradicting, separate studies in order to reach
a general overall conclusion or summarise the results of
past research.
The data from the foregoing trapping and spotlight
trials will be analysed separately using meta-analysis to
test whether fox control, as achieved by using poison
baits, increases the abundance of medium sized native
marsupials. It maybe one of the first times this technique has been used on wildlife survey data. Additionally, bootstrapping will be used to determine the
distribution of the effect sizes from different studies.
3.1. Methods
Small numbers of observations from separate studies
were combined to enable a meaningful analysis. The
data for each study consisted of one or more measures
directly related to the abundance of medium-sized
native marsupials both before and after the commencement of a fox control program. For each study all survey data before fox control commenced were combined
to obtain the best indicator of abundance. However,
after the commencement of the fox control program at a
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J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
site a gradual increase in abundance was expected. For
this reason only data from surveys conducted more than
2 years after baiting commenced were combined to
allow time for a response to occur.
All studied sites in Western Australia where adequate
data for both with and without fox control (treatment
and control) was available were used for the analysis.
However, two species of native marsupials had become
locally extinct at certain sites: the tammar at Dryandra
(along the selected spotlight routes) and woylie at Boyagin. Since no response was possible, these species at
these sites were excluded from the analysis.
3.1.2. Spotlight surveys
For the spotlight transects (Table 9), the number of
animals spotted per hour was used. When data from
two or more surveys for a treatment were available, they
were combined by adding the counts from each survey
and re-computing the rate of sightings (equivalent to the
mean weighted by the duration of the survey in hours).
The standardised difference (di) was used to represent
the effect size
3.1.1. Trapping surveys
For the trapping surveys (Table 8), the proportion of
successes expressed as the number of animals caught
divided by the number of traps set was used. When data
from two or more surveys were available, the total
number of animals trapped divided by the total number
of traps set (trap nights) was used. For these data the
variance was estimated from the binomial distribution.
where X ti is the weighted mean of the treatment group
(with fox control) for the ith study, X ci is the weighted
mean of the control group (prior to fox control) and si is
the pooled standard deviation for the two groups. The
conditional variance of di was estimated as
di ¼
vi ¼
X ti X ci
si
ð1Þ
nti þ nci
di2
þ
t
c
t
n i ni
2 ni þ nci
ð2Þ
where nti is the within-study sample size in the treatment
group (survey duration in hours) and nci the withinstudy sample size in the control group of the ith study.
Table 7
Fitzgerald River National Park: a comparison of spotlight counts
(numbers h1) of brush-tail possums and tammars along fixed routes
in the unbaited eastern section and the baited western section
Year (total hours)
Eastern section—no fox control
December 1994 (2.9)
November 1995 (6.5)
Possums
sightings (h1)
Tammars
sightings (h1)
1.72
1.08
0.00
0.00
Western section—fox control from 1991
April–November 1993 (5.2)
2.13
December 1994 (6.1)
4.41
November 1995 (2.38)
19.3
February–May 1996 (3.4)
11.5
1.37
1.63
5.47
10.6
3.2. Meta-analysis
A homogeneity test statistic (Shadish and Haddock,
1994) was used to test whether the studies shared a
common population effect size. If test statistic Q exceeds
the upper-tail critical value of the chi-square distribution at k1 degrees of freedom, where k is the number
of studies, the observed variance in the effect sizes is
significantly greater than expected for studies that share
a common effect size. When Q is rejected the heterogeneity may be accounted for by using a random
effects model rather than fixed effects model. Under a
random effects model the effect size is random with its
own distribution.
Table 8
Meta-analysis trapping data: random effects models—proportions
Site
Dryandra 1971–1972
Dryandra Trapline 7
Dryandra Trapline 8
Dryandra Trapline 9
Dryandra Trapline 10
Dryandra Trapline 11
Dryandra Trapline 12
Dryandra Trapline 13
Tutanning
Boyagin
FRNP
Species
Woylie
Woylie
Woylie
Woylie
Woylie
Woylie
Woylie
Woylie
Woylie
Possum
Possum
No fox control
Fox control
Nights1
Captures1
Nights2
Captures2
980
120
40
39
40
40
40
40
702
696
604
21
10
3
2
1
0
0
0
8
4
1
772
16
20
20
20
24
16
16
586
844
600
146
4
6
7
9
6
4
3
140
149
48
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J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
Table 9
Meta-analysis spotlight data: random effects models—mean differences
Site
Dryandra Route 2
Dryandra Route 2
Tutanning
Tutanning
Tutanning
Tutanning Annex
Tutanning Annex
Boyagin
Boyagin
Dolphin Island
FRNP
FRNP
Species
Woylie
Possum
Woylie
Possum
Tammar
Possum
Tammar
Possum
Tammar
Rock-wallaby
Possum
Tammar
Control
Treatment
Si
Hours1
Rate1
Hours2
Rate2
4.98
4.98
23.34
23.34
23.34
1.38
1.38
11.18
11.18
10.02
9.37
9.37
3.61
3.41
0
0.39
0.47
0
5.07
0.27
0.09
0.33
1.28
0
2.42
2.42
34.94
34.94
34.94
2.91
2.91
19.00
19.00
3.85
7.41
7.41
27.69
22.31
1.00
4.75
5.01
7.90
77.66
5.95
1.32
8.83
5.05
2.66
The variance component for the random effects model
was estimated in two ways (Shadish and Haddock,
1994). Firstly, the ordinary (unweighted) sample estimate of the variance of the effect sizes was used to
estimate the variance component. Secondly, the weighted
sample estimate of the variance of the effect sizes was
used to estimate the variance component.
The remaining calculations for both the trapping and
spotlight surveys follow those described by Shadish and
Haddock (1994). A Mathcad worksheet (Mathsoft,
1995), available from the authors, was set up to perform
the computations.
A one-tailed t-test was used to test the null hypothesis
that the population effect size is zero (i.e. fox control
does not increase the abundance of medium sized native
marsupials) against the alternative hypothesis that, the
mean effect size is greater than zero (fox control increases
the abundance of medium sized native marsupials). The
test statistic was calculated using both the ordinary
(unweighted) sample estimate of the variance of the effect
sizes, and the weighted sample estimate of the variance of
the effect sizes to estimate the variance component.
3.3. Bootstrapping
The weighted effect sizes were bootstrapped to test the
same null hypothesis against the alternative hypothesis.
The bootstrapping approach does not require the same
assumptions of normality as the t-test and will perform
better when the data are skewed. When plotted, the
bootstrapped values provide valuable information on
the distribution of the effect sizes.
3.4. Results
3.4.1. Trapping surveys
The homogeneity test statistic for the fixed effects
model Q=73.3 exceeded the upper tail critical value of
chi-square at 10 degrees of freedom (P< 0.001) indicating
2.15
0.58
0.21
1.43
2.18
2.54
25.74
2.06
0.33
0.86
1.52
1.73
the heterogeneity could not be explained by sampling
error alone, if studies all shared a common population
effect size. A random effects model was required to take
proper account of the heterogeneity between studies.
Both test statistics calculated using the ordinary
(unweighted) sample estimate of the variance of the effect
sizes and the weighted sample estimate of the variance
of the effect sizes to estimate the variance component
were highly significant (P < 0.001).
The bootstrapping result was also highly significant
since the bootstrapped values did not include zero. The
null hypothesis was rejected in favour of the alternative
hypothesis: fox control increases the abundance of
medium-sized native marsupials.
3.4.2. Spotlight surveys
The homogeneity test statistic for the fixed effects
model Q=60.0 exceeded the upper tail critical value of
chi-square at 11 degrees of freedom (P < 0.001) indicating the heterogeneity could not be explained by sampling error alone if studies all shared a common
population effect size. A random effects model was
required to take proper account of the heterogeneity
between studies.
The test statistic calculated using the ordinary
(unweighted) sample estimate of the variance of the
effect sizes was significant (P < 0.05), whereas, the test
statistic calculated using the weighted sample estimate
of the variance was highly significant (P < 0.001).
The bootstrapping result was also highly significant
since the bootstrapped values did not include zero. The
null hypothesis was rejected in favour of the alternative
hypothesis: fox control increases the abundance of
medium sized native marsupials.
3.5. Discussion
It was not surprising that random effects models were
required to take proper account of the heterogeneity
J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
between studies. The variation in the response between
studies was large due to different species, sites and differing number of years between the commencement of
fox control and when the surveys were conducted.
Random effects models were required to properly
account for this variation.
For many of the spotlight surveys there was barely
sufficient observations to estimate the pooled standard
deviation, at least two observations both before and
after fox control were needed. However, for Dryandra it
was only possible to estimate the standard deviation
before fox control commenced since there was only one
subsequent observation. It is likely that the standard
deviation for this site was underestimated, and in turn
responsible for a large value for the standardised mean
difference. The standard deviation for Tutanning Annex
could only be estimated for the observations after fox
control commenced for the same reason.
351
4. In the absence of fox control, prey species persist
at low densities within sites that serve as predation refugia. However, because the population
densities are very low within refugia, it is unlikely
that such populations will be stable over the
long-term (see later).
5. Removal of foxes from refuge sites not only
increases native prey populations, but also
enables prey species to occupy and utilise habitats not exploited in the presence of foxes—an
example of niche denial followed by niche
expansion.
6. In general, at sites still carrying multiple species
of medium-sized mammals, fox control produced
a positive population response by all species.
7. To date, the suppression of prey species by the
fox has not yet affected reproductive fitness (due
to bottlenecking) as indicated by the positive
population responses of endangered prey.
3.6. Conclusions
When all studies are considered together, baiting to
control foxes has a large positive effect on the abundance of medium sized native marsupials. For the spotlight studies the effect sizes ranged from 1.5 to 32.6,
these are considered to be very large (Cohen, 1969)
indicating a dramatic response in the abundance of
native marsupials to fox control.
The tammar population within Dryandra Woodland
and Boyagin Nature Reserve did not respond positively
to fox control. Possible reasons are: visibility restrictions due to dense cover; carrying capacity intrinsically
low for tammar; NLD; and poaching. Tammars have
responded positively elsewhere (i.e. Tutanning and
FRNP; see also Tables 10 and 11) and in some cases,
this species has locally achieved ‘pest’ status.
4.1. An update from Western Shield
4. General discussion
To have generality, results should be consistent
under a wide variety of circumstances (Johnson,
1999).
The rationale for the case studies described in this
paper originated from fox removal experiments from
sites that were replicated along with controls (Kinnear
et al., 1988, 1998)—a hypothetical-deductive (H-D)
design (Beck, 1997). It is significant that all of the
case studies produced results similar to the rock-wallaby
study, i.e. fox control produces significant population
increases of rare and endangered marsupials. Additionally, these outcomes have extended our understanding
of the impact of fox predation in the following ways:
1. The fox is a very efficient predator of mediumsized marsupials (see later for further discussion
regarding predator efficiency).
2. Suppression of marsupial populations by the fox
affects an array of species over a wide geographic
range and in a variety of habitats.
3. Suppression of native prey by foxes was common
to both small (2200 ha) and large areas (329,000
ha) of conservation estate.
Under Western Shield, a wide area management
response to the fox threat, the number of sites subject
fox control has increased, and likewise for species
translocations. A central database exists and is being
maintained under the auspices of CALM’s Wildlife
Branch (P. Orell, personal communication).
Some results as of 1999 are as follows: baiting has
produced positive population responses at 25 sites
comprising a total of 11 species and representing
seven marsupial families. In addition, seven species
belonging to six families have been successfully translocated to 15 sites where they formerly occurred
(Tables 10 and 11).
Clearly, these data indicate that the spectrum of
Western Australian marsupial prey species suppressed
by the fox is broad, and on this basis we make this following generalisation namely that: the European fox
should be recognised as a multi-species biological control
agent affecting a subset of Australian mammals—the full
range yet to be documented.
This generalisation is based on an initial H-D experiment and a series of case histories (this paper and other
cases; see Table 10), the latter methodology being
one that has been championed by Shrader-Frechette
and McCoy (1993). In their critique of ecological
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Table 10
A list of marsupial species that have persisted in predation refuges at low densities, and have since increased and expanded their use of the habitat
following ongoing fox baiting programs
Species
Number of sites
Reference source
Notes and comments
Family Macropodidae—Wallabies
Black-flanked rock-wallaby
(Petrogale lateralis)
Six sites
Kinnear et al. (1998)
and unpublished works
Population increases at five wheatbelt
sites. Population increase within Cape
Range National Park (Kinnear, 1995)
Rothschild’s rock-wallaby
(Petrogale rothschildi)
One site
This paper
Dolphin Island, Dampier Archipelago
(See text)
Yellow-footed rock-wallaby
(Petrogale xanthopus)
Numerous sites
P. Alexander, and P. Copley,
Dept. Environ . . . S. Australia
Operation ‘‘Bounceback’’—a wide-area
feral animal control program in the
Flinders and Olary Ranges involving
fox control
Tammar wallaby (Macropus eugenii)
Five sites
This paper; WSa database
Tutanning NR; Tutanning annex; FRNP;
Perup and Kingston forest (near Manjimup)
This paper
Wheatbelt remnants: Dryandra and
Tutanning; Perup and Kingston forests
(Manjimup)
Sinclair et al. (1996)
Last recorded in the 1870s and believed to
be extinct. Nil captures during survey of
Two Peoples Bay Nature Reserve in 1970s;
rediscovered in 1994 after the
implementation of fox control program
Family Pseudocheiridae—Ringtail Possums
Western ringtail possum
Two sites
(Pseudocheirus occidentalis)
WS database
Perup and Kingston forests (near
Manjimup)
Family Phalangeraidae—Brushtail Possums
Western brushtail possum
Seven sites
(Trichosurus vulpecula)
This paper; WS database
Wheatbelt remnants: Tutanning, Boyagin,
Lake Magenta; FRNP, South Coast;
Batalling (near Collie), Perup and Kingston
forests; (Manjimup)
Family Perameloidae—Bandicoots and Bilbies
Quenda or Southern brown
Six sites
bandicoot (Isoodon obesulus)
C. Pentland (Hon. Thesis);
WS database
Twin Swamps and Ellenbrook (Perth
suburb); L. Magenta (wheatbelt); Perup
and Kingston (Manjimup); Waychinnicup
NR (near Albany)
Family Myrmecobiidae—The numbat or banded ant-eater
Numbat (Myrmecobius fasciatus)
Two sites
Friend (1990)
Wheatbelt; Dryandra; Perup (Manjimup
forest site)
Family Potoroidae—Potoroos and Bettongs (Rat Kangaroos)
Woylie or Brush-tail bettong,
Four sites
or rat kangaroo
(Bettongia penicillata)
Gilberts’ potoroo (Potorous gilbertii)
One site. Two peoples
Bay, south coast of WA
Family Dasyuridae—Quolls or native cats and other carnivorous marsupials
Red-tail phascogale (Phascogale calura) Three sites
Friend (unpublished)
Chuditch or Western quoll
(Dasyurus geoffroii)
a
Four sites
Morris et al. (1995)
‘Western Shield’ database (courtesy of P. Orell, Wildlife Branch).
Wheatbelt remnants. Fox removal
produced increases on baited sites, but not
on unbaited sites
Batalling forrest; Hills forest; Noggerup;
St. John forest
J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
353
Table 11
A list of marsupial species that have been successfully translocated to sites where the species formerly occurreda
Species
Number of sites
Notes and comments
Family Macropodidae—Wallabies
Black-flanked rock-wallaby (Petrogale lateralis)
One site
Querekin rock population extinction occurred in late 1980s
in the absence of fox control (Kinnear et al., 1998). Five
animals sourced from Nangeen Hill translocated to Querekin
in 1990 after implementation of fox control. In 1998, 45
individuals trapped
Tammar wallaby (Macropus eugenii)
One site
Batalling forest. Translocations to five other sites, but too
early to make an assessment
Family Potoroidae—Potoroos and Bettongs (Rat Kangaroos)
Woylie or Brush-tail rat kangaroo (Bettongia penicillata)
Seven sites
Most sites within Jarrah forest: Batalling, St. John forest,
Hills Forest, Julimar. Wheatbelt: Boyagin. Recently to the
semi-arid sites Lake Magenta and Francois Peron National
Park; and both appear to be successful. Source populations;
Dryandra, Perup
Boodie (Bettongia lesueur)
One site
Heirisson Prong (Shark Bay, a CSIRO Project, Short, 1999).
Animals sourced from fox-free island
Family Pseudocheiridae—Ringtail Possums
Western ringtail possum (Pseudocheirus occidentalis)
One site
Leschenault Peninsula: animals sourced from Busselton area
either from wildlife carers or rescued from residential
development sites
Family Perameloidae—Bandicoots and Bilbies
Western Barred Bandicoot (Perameles bougainville)
One site
Heirisson Prong (Shark Bay, a CSIRO Project) animals from
fox-free island source
Quenda or Southern brown bandicoot (Isoodon obesulus)
Four sites
Tutanning, Dongolocking, Boyagin Nature Reserves and
Mt. Barker. Animals sourced mainly from sites due for
development
Family Myrmecobiidae—The numbat or banded ant-eater
Numbat (Myrmecobius fasciatus)
Three sites
Dragon Rocks, Boyagin and Tutanning Nature Reserves.
Population recoveries of numbats, a diurnally active species,
can be limited by feral cats and native predators eg, Chuditch
(a quoll or native cat) and raptors as is the case in Batalling
forest and Karroun Hill
Family Dasyuridae—Quolls or native cats and other carnivorous marsupials
Chuditch or Western quoll (Dasyurus geoffroii)
Four sites
a
Julimar forest; L. Magenta; Cape Arid; Mt Lindesay. An
initial translocation to a forest site (Lane Poole, 1987) failed
in the absence of fox control
All sites subject to ongoing fox baiting programs. Data from Western Shield database (courtesy of P. Orell, Wildlife Branch).
methodology, they argue for a case history approach, as
they believe that an excessive reliance on H-D experimentation is responsible for the dearth of valid generalisations in ecology.
4.2. Biological control agents: essential propertiesattributes
In theory, the ideal biocontrol system (as envisaged
for economic pests) is a system where (1) the pest
population is driven to extinction or if not, it is maintained at below threshold densities at which damage is
tolerable (2) the controlling agent is host specific (3) the
agent can increase rapidly in response to host increases
and (4) the controlling agent persists even though prey
densities are maintained at low densities (Murdoch,
1990, 1992, 1994; Murdoch and Briggs, 1996).
Parasitoids tend to meet these specifications. Generalist predators can be very effective, but they have
undesirable properties, as they are typically not targetspecific—a caveat confirmed by the list of marsupial
victims suppressed by the fox (Table 10). Indeed, the fox
would be an example of biological control gone utterly
wrong, a disastrous worst-case scenario.
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4.2.1. The fox as a biocontrol agent
As a biocontrol agent, the fox is not lacking in
appropriate attributes: it has a high searching ability; it
is a mobile, broad-niche species as indicated by its rapid
spread and current distribution (King and Smith, 1985;
Coman, 1995; Saunders et al., 1995). Furthermore, it is
not tightly coupled to any particular prey, as it is a
dietary generalist par excellence because of its carnivore–omnivore–scavenger tendencies—the latter making it vulnerable to control by baiting.
It is a highly skilled predator and indeed, it is even
claimed to be capable of regulating rabbit populations
(Newsome et al., 1989; Pech et al., 1992), but see Boutin
(1995). It has been documented as a surplus killer of
marsupials (Kinnear et al., 1998; Short et al. 2002). In
drought affected habitats it may become locally extinct,
but because of its mobility it can readily re-invade. All of
these characteristics make the fox an effective biocontrol
agent that affords little respite to vulnerable fauna lacking a history of co-evolution (Short et al., 2002).
4.2.2. Models and biocontrol agents
In a series of papers modelling predator–prey systems,
Sinclair, Pech and colleagues (1998 and references
therein) have produced a number of models describing a
range of possible outcomes. A predator cum biocontrol
agent would fall within the ambit of their models. We
suggest that two models would apply namely: (1) the
predator limits prey populations to low densities and
maintains them as such in refuges, and (2) the predator
drives prey populations to extinction. Model 1 fits the
observed refuge populations described in this paper, but
in our view, the question of stability would remain suspect as the system may well revert to a model 2 in the
long term (see Sections 4.9, 4.10 for examples). Translocations of prey to non-refuge sites without fox control
would fit model 2; such outcomes have occurred (e.g.
numbats at Boyagin; woylies within the jarrah forest,
Christensen, unpublished).
4.2.3. Missing Australian marsupial pests
Environmental disturbances can affect different species in different ways; some species may decline as a
result whereas others may prosper because of new
favourable circumstances and thus achieve pest status.
In parts of Australia, kangaroos have become so, but
medium-sized marsupial pests are practically unknown
over wide areas of mainland Australia. Currently, in
Australia, one has to look to fox-free Tasmania and
Kangaroo Island to find examples. Both of these habitats have historically experienced an environmental
impact comparable to the mainland following settlement. On Kangaroo island tammars are culled by
shooting; in fox-free Tasmania, 1080 is used to control
medium-sized marsupials. In contrast, on mainland WA,
apart from kangaroos, one needs to use 1080 to control
foxes in order to produce a marsupial pest. Tutanning
tammar wallabies and wheatbelt rock-wallabies are
examples (P. Orell, personal communication). This outcome is consistent with the view that the fox is acting as
a biocontrol agent.
4.3. Possible confounding of the results due to feral cats
and the dingo
The impact of the dingo can be discounted because it
was absent from all of the study sites (see also Short et
al., 2002 for more detailed discussion regarding the
dingo).
The feral cat was present at all sites. Its predation
ecology has been reviewed by Dickman (1996a, b), but
the available evidence about its impact on medium-sized
mammals presents a confusing picture. Christensen and
Burrows (1994) failed in an attempt to re-introduce two
marsupials species at a desert site because of cat predation. The fox and the dingo were effectively controlled,
but control of the feral cat was not successful. Conversely, feral cats are present in fox/dingo-free Tasmania yet the fauna, including the barred bandicoot
(Perameles gunnii), is largely intact. This species, a likely
prey item, is still relatively widespread and abundant in
Tasmania (Mallick et al., 1997, 1998), but critically
endangered on the Australian mainland (Seebeck,
1995). Cats have been present on Garden and Rottnest—two small islands near Perth, WA—dating from
the colonial period, but despite this long association,
two wallabies, the tammar and the quokka (Setonix
brachyurus), continue to thrive despite their presence.
However this pattern does not hold for other island
situations, as the cat is linked to the extinction of a hare
wallaby, a bettong and a bandicoot (Burbidge, 1971).
It can be argued that, given the results of the case
studies, the data may have been confounded by the
removal of feral cats as well as foxes. However this is
highly unlikely, as numerous trials have revealed that
meat baits are ineffective in controlling feral cats
(Christensen and Burrows, 1994; unpublished trials).
Thus we can reasonably conclude that the treatment
was selective for foxes.
4.4. Other possible limiting factors
The five case studies consistently produced results (as
has CALM’s Western Shield) that conformed to the
following pattern namely: fox control, as achieved by
baiting, typically results in significant population
increases and niche expansions by medium-sized marsupials (see Section 3.2). These results eliminate NLD as
a factor—that is, lack of carrying capacity—and likewise, reproductive fitness.
Alternative explanations and interpretations are
nonetheless possible. Any other explanation needs to
J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
satisfy these questions. (1) Given the low population
densities of every experimental population prior to fox
control, why so few marsupials? (2) Why did they all
increase after the implementation of baiting programs?
Some possible biotic factors previously listed will be
considered (see Section 1). These include factors such as
pathogens (including parasites) and competitors, for
example, rabbits, domestic stock and feral species.
Pathogens will be considered first.
On considering the diversity of sites, the diversity of
species, and the geographic scale of the experiments,
then on epidemiological grounds it seems improbable
that every species, at every site, were limited by a
pathogen(s). If pathogens were involved, then it seems
equally as improbable that all pathogens abruptly
ceased to be limiting following baiting. Nor it is likely
that the applied treatment (meat baits) provided a cure.
None of the sites carried domestic stock or alien feral
species. All sites carried rabbits apart from the Dampier
Archipelago sites, which are rabbit-free. No attempts
were made to control rabbits at any site. Given that
foxes are alleged to limit rabbit populations (Pech et al.,
1992), then it is possible that baiting could have enabled
rabbits to increase. No pattern is discernable, as marsupials increased in the presence of rabbits and also,
when they were absent.
Abiotic environmental factors include climatic factors
such as drought, extreme temperatures or events that
adversely affect survival and reproduction. Again, given
the geographic scale of this study, it also seems unlikely
that, prior to fox control, these limiting factors were
operative in every case over such a wide geographic
range—such is the nature of the WA climate. It also
seems improbable that a simultaneous relaxation of
these factors, leading to conditions favouring population growth, would have coincided with the commencement of baiting at every site.
Furthermore, four of the five sites—Dryandra, Boyagin, Tutanning and the FRNP—are situated in a productive agricultural region, which does not experience
extended periods of adverse climatic conditions. Population crashes of prey species can occur in this environment, but the environmental stress would be of short
duration, hence population recoveries would follow
relatively quickly. This was not the case, because all of
these sites had a long history of low abundance preceding the trials—apart from Tutanning, which has been
already discussed (see descriptions of these sites and
their historical backgrounds).
Finally, purists of the H-D school will object to the
experimental design (Beck, 1997, but see critique of HD by Shrader-Frechette and McCoy, 1993). Nevertheless, it should be recalled that the baiting trials were
not devoid of control sites. With the exception of
Tutanning, every site had some areas that served as
untreated controls—i.e. no baiting. It is noteworthy
355
that, no population recoveries occurred at any of these
untreated sites.
In summary, when the evidence is considered in its
entirety, the weight of the evidence consistently supports
a strong case for excluding many other potentially limiting factors.
4.5. The fox as an efficient predator of marsupials
Biocontrol agents/predators will extinguish their prey
when the predation rate exceeds the prey growth rate
over all prey densities. This outcome may be avoided if
prey have access to a refuge (Rosenzweig and MacArthur, 1963), or if the predator switches to an alternative
prey when prey become rare. Significantly however,
Short et al. (2002) found that the expected switch did
not occur in a case involving predation by foxes on a
population of rat-kangaroos (Bettongia lesueur). After
reducing the bettong population to a low density, foxes
continued to depredate bettongs in the presence a very
high density rabbit population (Oryctolagus cuniculus).
A predator or biocontrol agent is judged to be efficient (and therefore, its prey vulnerable) if it is capable
of limiting its prey populations to low densities
(Rosenzweig and MacArthur, 1963; Rosenzweig, 1969).
Predator efficiency and prey vulnerability are therefore,
relative attributes. A predator may be efficient in relation to a particular prey species but not so in relation to
other species. As prey species, many Western Australian
marsupials are vulnerable (e.g. in WA to date, 11 spp),
partly because they are not particularly adapted to cope
with high depredation rates due to (1) their intrinsically
low fecundity (especially macropodines e.g. wallabies)
(2) low population growth rates, and (3) inappropriate
anti-predator defenses and life histories (relative to the
fox) due to their Gondwana heritage.
4.6. Gondawana anti-predator defenses: transferable and
sufficient?
Co-evolved anti-predator defenses (and lifestyles) by
indigenous prey in response to their native predators do
not necessarily protect prey from the depredations of a
recently introduced exotic species. Hanski et al. (2001)
argue that the impact of predators has been under-rated
because of a failure to acknowledge ecological differences amongst predators. Krefft’s (1866, p. 20) description’s of a hare-wallaby’s shelter (Lagochestes sp., prior
to the colonisation by the fox) is indicative. It reads as
follows to quote . . . ‘‘(It) is generally found asleep under
some saltbush or any other sheltered locality.’’ Apparently, most any shady site would do even in the presence
of its native predators, which is in sharp contrast to
existing habitats—for example, rock piles, dense cover,
trees and burrows—in which surviving marsupial species are found today.
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Hare-wallabies like most medium-sized marsupials
are now either extinct or rare over much of their
former ranges, as are most of the arid zone mediumsized marsupials.
Rock-wallabies are another case. Numerous species
have managed to thrive in fragmented rocky outcrops in
the presence of their natural predators for thousands of
years—a fragmented lifestyle that allegedly, is suppose
to make them more vulnerable to predators (see Section
4.7). However, following the arrival of the fox in WA,
widespread extinctions have occurred, and extinctions
are still being recorded (Pearson, 1992; Kinnear et al.,
1998). From these observations, two inferences emerge
concerning fragmentation (1) a fragmented lifestyle did
not prevent rock-wallabies from establishing thriving
populations in the presence of their natural predators,
and more significantly (2) their anti-predator defences,
while sufficient to cope with native predators, have since
proven to be hopelessly inadequate in relation to the fox
(Pearson, 1992; Kinnear et al., 1998). A review of the
evidence regarding the vulnerability of marsupials to
fox depredations can be found in Short et al. (2002).
4.7. Predation and habitat fragmentation
It is generally believed that populations surviving in
small remnants (high perimeter-to-area ratio) are more
vulnerable to predation than those persisting in large
tracts of suitable habitat. The evidence supporting this
argument is largely based on studies of avian nest
predation (Reese and Ratti, 1988). Brown and Litvaitis
(1995) failed to demonstrate increases in foraging efficiencies by foxes and coyotes on cottontail rabbits
(Sylvilagus transitionalis) in a fragmented landscape.
Reese and Ratti (1988) concluded that the evidence is
limited, and that the situation is more complex than a
simple area effect. It is also noteworthy that the mammals in the large Fitzgerald River National Park
(329,000 ha) fared no better than those in the extensively fragmented areas of the WA wheatbelt (Chapman
and Newbey, 1995).
4.8. Habitat disturbance and predation
The argument linking of enhanced prey vulnerability
with habitat fragmentation has a parallel in regards to
habitat disturbance. It has been argued that closed forest habitats in their relatively undisturbed state exclude
foxes (Jarman, 1986). Road and track construction are
alleged to diminish the effectiveness of such habitats as
these constructs are suppose to facilitate access by foxes
thus making native species more vulnerable. Meek and
Saunders (2000) believe this perception needs to reassessed, because they radio-tracked foxes living and
foraging within dense forest and heaths in the absence
of roads. Using radio-tagged foxes, Algar (unpublished)
recorded a similar finding in Kalbarri National Park in
WA where the loss of medium-sized mammals has been
almost total. Dolphin Island has remained essentially
‘‘pristine’’ (no history of permanent human settlement,
agriculture, mining etc.); the FRNP has a similar history, yet medium-sized mammals of these sites have
been impacted just as severely as highly disturbed areas.
Clearly these perceptions need to be re-assessed. As
shown in the case studies, the fox appears to be a very
efficient predator of many medium-sized marsupials
under a wide variety of environmental circumstances.
4.9. NLD and the significance of translocations
More evidence about the efficiency of the fox and
NLD can be deduced from successful translocation
experiments. The woylie translocation to Boyagin was
successful as was the Numbat translocation (Friend,
1990; see list in Table 11). Kinnear et al. (1998) recorded
the extinction of a small rock-wallaby population at a
site not subject to fox control (Querekin). Subsequently
five wallabies were translocated to the site from a
nearby colony, and the founders under fox control have
since increased to 45 (Eldridge et al., 2001). Four points
arise from these translocation examples: (1) existing
former habitats still retain the capacity to meet the
requirements of the earlier species (niches intact, little or
no NLD) (2) in the absence of fox control, the sites were
unable to maintain populations of the earlier species
(carrying capacity zero in the presence of the fox) (3) the
founding populations were not lacking in reproductive
fitness despite a history of bootlenecks and (4) one
should not assume that sites serving as refugia are
secure (Pearson, 1992; Kinnear et al., 1998).
4.10. Marsupial refugia: are they safe havens?
Rock-piles, trees, and dense vegetative cover (often
containing 1080 poison plants in WA; Christensen,
1980; King et al., 1981) are associated with marsupial
survival and thus, serve as predation refugia. Refugia
become evident whenever remnant populations expand
and establish viable populations in the surrounding
habitat following the implementation of fox control.
The observed habitat colonisations outside of refugia
(realised niche expansions) by the woylie in Tutanning
and Dryandra illustrate this point (Figs. 2 and 8; see
also Kinnear et al., 1998).
In WA, there are reasons to suspect that, in the
absence of fox control, the available refugia are not
particularly secure principally because prey densities are
so low. Furthermore, Pearson (1992) has provided evidence of instability in the case of rock-wallaby populations living on arid zone refuge sites. During 1988–1990,
he visited 80 sites historically known to have carried
wallabies (as recently as 1940), and he found that 83%
J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
of these populations were now extinct. Kinnear et al.
(1998) recorded a rock-wallaby population extinction in
a more mesic environment. These findings are not
encouraging for it is evidence that refugia are not necessarily a guarantee of population stability. Wildlife
agencies should take note; a risk-averse policy is advisable, for it seems unwise to assume that known refuge
populations are secure.
4.11. Relevance of predation models
The utility of predation models is limited because of
the difficulties encountered in testing them. In the cases
involving cryptic predator–prey relationships, as for
example, secretive nocturnal species (the Australian
situation), the testing of would be a formidable task
fraught with difficulties. In essence, the task consists of
determining who is killing whom at any given prey
density. One needs to be able to record every individual
predation event (who and whom) over a range of prey
densities. Technological advances are needed.
One model, of considerable interest, involves multiple
prey population states. The model predicts that under
predation, prey may exist in either of two stable states, a
low density (predator pit) state or a higher density state.
The predator is supposed to regulate its prey at low
densities, but at high densities it becomes inefficient. The
latter high density state is of interest, because fox control would be not required if prey were sufficiently
numerous (see also, Pech et al., 1992).
This model could be crudely tested by creating a high
density prey population followed by the withdrawal of
fox control. It would be a test of the efficiency of the fox
as a predator over a range of marsupial prey densities.
We suspect that the prey would crash for reasons
described in Short et al. (2002). The Tutanning history
is an example. Nevertheless, it should be done because
of the implications for fox management, and also
because it would advance our understanding of the
ecology of the fox in Australia.
5. Concluding remarks
The most important problem regarding mammal conservation in Australia is the low abundance and limited
distributions of many species (Burbidge and McKenzie,
1989; Smith and Quin, 1996). Advocates of the nicheloss-damage hypothesis have compiled a list of abiotic
and biotic interactions allegedly responsible for the presumed loss of carrying capacity of the landscape.
Accordingly therefore, the restoration of the landscape
to a more pristine state is one of the keys to mammal
conservation.
As advocates of the view that predation by the fox is
also a major threatening process, we do not dispute the
357
fact that the carrying capacity of the Australian landscape in relation to mammals (and other spp) has been
affected in an absolute sense. What we seek to emphasise is that predation by the fox can mimic loss of carrying capacity through niche denial. When a species is
classified as rare and endangered, then the task facing
conservation biologists is to identify the limiting factors
(sensu Krebs, 1995) affecting such populations. Predation in WA is such a factor, and we see no reason why
the fox factor should not be widespread. It does raise a
matter that may also be commonplace, but has not yet
been investigated. NLD and fox predation may be
jointly proximate—that is, both habitat restoration and
predator control (including feral cats in some circumstances), may be needed to produce a positive population response by an endangered species.
In some situations niche denial may well confound
and distort perceptions about species habitats, as it
confines surviving species to refugia, a situation that can
create the belief that refugia represent preferred or
essential habitats, when in fact, they are survival niches.
It seems likely that these ecological distortions caused
by exotic predators have confounded attempts to
achieve an understanding of the factors threatening
survival of endangered species. Moreover, it is also
likely that, this confusion has influenced research, policy-making, and wildlife management.
In view of these conclusions, how this invader is perceived is vitally important—indeed, critical for the survival and future of many threatened species. To argue
that the fox in Australia is a typical predator coexisting
with its prey in a dynamic equilibrium is to belie its
impact (Hone, 1999). One might reasonably classify it as
a keystone species that qualifies as a ‘diversity-reducing’
predator (sensu Schoener and Spiller, 1996), which it
certainly appears to be. It is our proposition that the
impact of the fox would be more fully appreciated, if it
were recognised for what it really is—an exotic predator,
pre-adapted to assume the role of a biocontrol agent.
Both of these interpretations emphasise the need to
identify and to the assess risk to all species of wildlife
posed by the fox. Additionally, there is an urgent need
to devise a long-term method of fox control that ideally,
would be self-sustaining, because 1080-baiting, effective
as it is, is at best an essential holding action. The current
search for a biocontrol method (Tyndale-Biscoe, 1994)
must be supported and maintained. In the meantime the
use of 1080 must be safeguarded until a biological solution is found.
Acknowledgements
We are especially grateful to P. Orell and P. Mawson
of CALM’s Wildlife Branch, for their assistance in
compiling Tables 10 and 11. P. Orell and P. Collins
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J.E. Kinnear et al. / Biological Conservation 108 (2002) 335–359
kindly provided recent census data that enabled us to
update the situation in Tutanning Nature Reserve and
FRNP respectively. A.A. Burbidge and P. Christensen
generously provided important historical data for
Dryandra Woodland. I. Abbott reviewed an earlier
draft and made numerous helpful comments and suggestions. Professors A.R. Main and A. Kinnear provided
much thoughtful advice and encouragement. An anonymous referee provided much constructive criticism.
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