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Multi-scale patterns of habitat use by re-introducedmammals: A case study using medium-sized marsupials

Graeme R. Finlaysona,*, Emerson M. Vieirab, David Priddelc, Robert Wheelerc,Joss Bentleyd, Chris R. Dickmana

aInstitute of Wildlife Research, School of Biological Sciences, University of Sydney, Sydney, NSW 2006, AustraliabLaboratorio do Ecologia de Mamiferos, Centro 2, Universidade do Vale do Rio dos Sinos, UNISINOS,

CP 275 Sao Leopoldo, RS 93022-000, BrazilcDepartment of Environment and Climate Change (NSW), P.O. Box 1967, Hurstville, NSW 2220, AustraliadAustralian Wildlife Conservancy, Scotia Sanctuary, via Wentworth, NSW 2648, Australia

A R T I C L E I N F O

Article history:

Received 14 May 2007

Received in revised form

10 October 2007

Accepted 14 October 2007

Available online 26 November 2007

Keywords:

Habitat use

Re-introduction

Conservation

Endangered

Marsupial

0006-3207/$ - see front matter � 2007 Elsevidoi:10.1016/j.biocon.2007.10.008

* Corresponding author: Tel.: +61 (0)2 9351 86E-mail address: graeme.finlayson@bio.usy

A B S T R A C T

Knowledge of the habitat requirements of threatened species at both local and landscape

scales is crucial for maintaining viable populations and for making conservation and man-

agement decisions. Here, we use live trapping and radio-tracking to investigate habitat use

by four species of threatened marsupials – burrowing bettongs (Bettongia lesueur), brush-

tailed bettongs (B. penicillata), greater bilbies (Macrotis lagotis), and bridled nailtail wallabies

(Onychogalea fraenata). The study populations had been re-introduced to Scotia Sanctuary in

western New South Wales, Australia, within a predator-proof area. All showed preferences

for particular macrohabitats while resting by day, with M. lagotis and B. penicillata selecting

Eucalyptus woodland with Triodia understorey and B. lesueur and O. fraenata selecting Euca-

lyptus woodland with shrubs. However, they showed no such partiality at night. Bettongia

penicillata used areas with Triodia and litter but few herbs for shelter, while burrows of M.

lagotis avoided shrubs. Habitat components that influenced trap captures were: crust cover

and herb layer cover (negative) for B. penicillata, trees <5 m in height and number of shrubs

(both negative) for B. lesueur, crust cover for M. lagotis, and crust cover and trees <5 m high

for O. fraenata (both negative). There was also a negative association at this scale between B.

penicillata and both B. lesueur and M. lagotis, suggesting the possibility of competition. Our

results support the idea that studies at multiple spatial scales are crucial to understand

the habitat use and requirements of threatened fauna, and should therefore be incorpo-

rated into future re-introduction programs.

� 2007 Elsevier Ltd. All rights reserved.

1. Introduction

Habitat can be defined as the physical space required by an

organism to gain essential resources for survival and repro-

duction (Partridge, 1978). Patterns of habitat use are not ran-

dom, with animals generally using certain habitats in

er Ltd. All rights reserved

83; fax: +61 (0)2 9351 411d.edu.au (G.R. Finlayson

preference to others. Such preferences might be influenced

by both abiotic and biotic factors, with the latter including

availability of feeding resources, risk of predation, and intra-

and interspecific competition (Falkenberg and Clarke, 1998).

The scale on which animals respond to habitat differences

can also vary, with some showing distinct responses to differ-

.

9.).

B I O L O G I C A L C O N S E R V A T I O N 1 4 1 ( 2 0 0 8 ) 3 2 0 – 3 3 1 321

ences both between habitats and between patches within

habitats (i.e. microhabitats) (Torres-Contreras et al., 1997; Kelt

et al., 1999; Moura et al., 2005).

Understanding habitat preferences and patterns of habitat

utilization by threatened fauna can be critical for informing

management and conservation decisions. For example, key

microhabitats that protect remaining breeding populations

of the midwife toad (Alytes muletensis) from the impacts of

introduced species are now used to determine possible

re-introduction sites for this species (Moore et al., 2004).

Knowing species’ habitat requirements is important also for

conservation planning in relation to reserve size and location

(Noss et al., 2002) and for incorporation into models that pre-

dict locations of suitable habitat patches (Metzger et al., in

press; Smith et al., in press). Moreover, assessment of the

habitats used by threatened species can be at the forefront

of conservation efforts for those species (Cahill and Matthy-

sen, in press).

Since European settlement of Australia, the decline in the

mammalian fauna has been severe (Burbidge and McKenzie,

1989; Dickman, 1994a, b; Short and Smith, 1994; Short, 1998;

Burbidge and Manly, 2002). This decline has been attributed

to many factors including predation by the introduced red

fox (Vulpes vulpes) and cat (Felis catus), and competition with

introduced herbivores such as the European rabbit (Oryctola-

gus cuniculus) (Morton, 1990). In an attempt to restore ele-

ments of Australia’s biodiversity, re-introductions into large

fenced areas, where the aforementioned threats have been

removed, provide opportunities for creating large, secure

self-sustaining populations of threatened species and also

for studying aspects of their biology to assist future conserva-

tion and management. As part of the management of these

populations, post-release studies into aspects of the species’

behaviour and ecology are essential (IUCN, 2006). Information

on the local abundance and success of re-introduced popula-

tions is also of utmost importance (Lindenmayer, 1994).

Furthermore, multiple-species re-introduction programs pro-

vide unique opportunities to gain insights about former inter-

species interactions which no longer occur elsewhere.

One such re-introduction program is at Scotia Sanctuary in

western New South Wales, where 4000 ha of relatively intact

old-growth low-growing, multi-stemmed eucalypt woodland

have been fenced and all introduced large and medium-sized

mammals (foxes, cats, goats (Capra hircus) and rabbits) eradi-

cated. Since November 2004 a series of re-introductions has

been carried out, with burrowing bettongs (Bettongia lesueur),

brush-tailed bettongs (B. penicillata), greater bilbies (Macrotis

lagotis) and bridled nailtail wallabies (Onychogalea fraenata)

being experimentally released into the fenced area. At the time

of European settlement, all four species were widespread

across much of arid and semi-arid Australia (Dickman et al.,

1993; Strahan, 1995). In particular, bettongs were reported to

have some of the most extensive ranges of anyof the Australian

marsupials (Troughton, 1957; Finlayson, 1958) and were likely

to have occupied a wide range of vegetation communities

across their range. Bilbies also ranged over much of mainland

Australia, but are now restricted to just 20 per cent of their for-

mer distribution in parts of the Tanami Desert (Northern Terri-

tory), Pilbara and southern Kimberley (Western Australia), and

as an isolated population in south-western Queensland

(Southgate, 1990). The bridled nailtail wallaby suffered such a

severe range reduction and population decline in the early

20th century that it was presumed extinct (Maxwell et al.,

1996). A single population was rediscovered in central Queens-

land in 1973 (Gordon and Lawrie, 1980).

These species, along with many other native species that

once dominated the semi-arid regions of Australia, probably

played a pivotal role in landscape functioning. For example,

bettongs disperse fungal spores (Claridge and May, 1994), in-

crease productivity of herbs (Noble et al., 2007), disperse seeds

(Murphy et al., 2005) and create nutrient patchiness by their

extensive digging (Garkaklis et al., 2003; James and Eldridge,

2007). There is also evidence that selective browsing by these

species assisted with the regulation of fire-promoting popula-

tions of native shrubs (Noble and Grice, 2002). Insights into

patterns of habitat use should help wildlife managers to

understand and address the loss of such ecological processes.

The future success of re-introductions of species back into

parts of their original ranges also relies on the understanding

of the interaction between these species and their

environment.

The re-introduction of the four species at Scotia Sanctuary

was part of a large-scale multi-species biodiversity restora-

tion project undertaken by the Australian Wildlife Conser-

vancy in collaboration with the New South Wales

Department of Environment and Climate Change and the

University of Sydney. This initiative was the first re-introduc-

tion involving two species of bettongs, and the first in New

South Wales involving all four species. It provided a unique

opportunity to study patterns of habitat use by these species.

Neither the broad vegetation formations (macrohabitats) nor

the finer-scale habitat components used by these species

are known for the habitats studied here, although they cover

much of the former ranges of each species. We aimed to eval-

uate habitat use at these different scales and to quantify pat-

terns of habitat selection and partitioning during diurnal

(resting) and nocturnal (active) periods. Partly because of

the species’ high population densities, we also investigated

whether competition for resources might potentially play a

role in shaping patterns of space use among species. Specifi-

cally, we predicted that any habitat partitioning would be

most pronounced between the two bettong species, as would

be expected from competitive avoidance. Both species histor-

ically co-occurred within the region and, although their diets

probably differ, increased dietary overlap could be expected

within an enclosed area (Sampson, 1971; Christensen, 1980;

Robley et al., 2001; Murphy et al., 2005). We expected our re-

sults to provide insight into the habitat requirements of all

species, hence informing management decisions in both this

and other multi-species re-introductions.

2. Study site

The study was carried out at Scotia Sanctuary (64,000 ha;

141�10 0E, 33�10 0S), 150 km south of Broken Hill, on the bound-

ary of the arid and semi-arid climatic zones (Fig. 1). Rainfall

averages 257 mm a year and is highly irregular. The region en-

dures hot summers with mean daily temperatures of 17–33 �Cand cool winters with mean daily temperatures of 5–17 �C.

Evaporation rates are high, with evaporation rates that are

Fig. 1 – Scotia Sanctuary, New South Wales, showing the location of the sanctuary and surrounding reserves. The top inset

shows the area in relation to Australia and the bottom inset shows the release site in relation to the entire sanctuary.

322 B I O L O G I C A L C O N S E R V A T I O N 1 4 1 ( 2 0 0 8 ) 3 2 0 – 3 3 1

six times higher than the average annual rainfall (Westbrooke

et al., 1998). The sanctuary lies within a region of sedimentary

rocks of Cainozoic age, with red earthy sands and sandy sol-

onized brown soils overlying sandy clays, generally of aeolian

origin (Westbrooke et al., 1998). The dominant landforms in-

clude east–west parallel sand dunes with narrow sandy

swales and open calcareous swales of varying width.

Four dominant vegetation communities, or macrohabitats,

occur within the 4000-ha fenced site used for animal releases:

Eucalyptus woodland with an understorey of Triodia scariosa;

Eucalyptus woodland over shrubs; Casuarina pauper woodland;

and shrubland (previously cleared woodland undergoing

regeneration) (Fig. 2). Dominant Eucalyptus species are E. ole-

osa, E. costata, E. dumosa, and E. socialis. Frequently occurring

grasses and herbs in these communities include Austrostipa

spp., Vittadinia cuneata complex, Dissocarpus paradoxus, Cheno-

podium cristatum and Podolepis capillaries (Westbrooke et al.,

1998; J. Bentley, pers. obs). Despite previous disturbance, Sco-

tia Sanctuary supports some of the most intact Eucalyptus and

Casuarina woodland in the region. The sanctuary has a short

grazing history, and only small areas of woodland have burnt

in the release site since 1975 (Fig. 2).

3. Methods

3.1. Re-introduction background

Releases occurred within the fenced site between November

2004 and September 2005, with 172 brush-tailed bettongs,

118 burrowing bettongs, 40 greater bilbies, and 161 bridled

nailtail wallabies released there from on-site captive breeding

colonies. During the period of the current study there were

two releases, in June 2005 and September 2005. Numbats

(Myrmecobius fasciatus) had been released into the fenced site

Fig. 2 – The 4000 ha release site within Scotia Sanctuary showing the main vegetation communities within the reserve;

Eucalyptus with a Triodia scariosa understorey ( ), Eucalyptus with an understorey of mixed shrubland (h), Casuarina pauper

woodland ( ), and mixed shrubland ( ). Some areas of Eucalyptus woodland have been burnt since 1975 (j). Trap sites and

tracks are also indicated.

B I O L O G I C A L C O N S E R V A T I O N 1 4 1 ( 2 0 0 8 ) 3 2 0 – 3 3 1 323

in 1999 and greater stick-nest rats (Leporillus conditor) were re-

leased in 2006.

3.2. Post-release radio-tracking

As part of the re-introduction program, ten individuals of

each species were radio-tracked for periods of two weeks (1)

immediately following release and (2) six weeks after release.

Bettongs and wallabies were fitted with collar-mounted VHF

transmitters (25 g and 31 g respectively) and bilbies with a

9 g tail-mounted VHF transmitter (SirTrack Wildlife Tracking

Solutions, New Zealand). All transmitters were less than 2%

of body weight. Animals were radio-tracked daily during each

two-week period to their diurnal resting place (burrow, den, or

shelter; hereafter referred to as shelter site). A description of

each shelter site was recorded and the location determined

using a GPS unit (Garmin� 12X). Only those shelter sites lo-

cated 6–8 weeks after release were used to describe habitat

use because sites used during the first two weeks were con-

sidered likely to be temporary (i.e. prior to the establishment

of a stable home range).

3.3. Animal trapping

Trapping sessions were conducted every three months be-

tween June 2005 and June 2006. A trapping network of 114 trap

sites was established along an extensive system of tracks

which covered the entire study site (Fig. 2). Each trap site con-

tained three wire cage traps (small: 57 · 23 · 23 cm; medium:

62 · 25 · 25 cm; and large: 76 · 33 · 32 cm), and was about

500 m from its nearest neighbour. Traps were set at dusk, cov-

ered in hessian sacks to protect animals from the elements,

324 B I O L O G I C A L C O N S E R V A T I O N 1 4 1 ( 2 0 0 8 ) 3 2 0 – 3 3 1

and baited with a mixture of rolled oats, peanut butter, honey

and vanilla essence. Trap sites were grouped into two series,

or runs, of approximately equal size. Each series was trapped

for three nights, with all trapping taking place over six consec-

utive nights. In an attempt to limit possible sampling bias, the

direction of travel along a particular series was reversed on

alternate nights, that is, for example, the starting point on

night 1 was the finishing point on night 2. We started to check

and close traps 2–3 h after sunset, and finished before sunrise.

Bettongs and wallabies were identified using individually num-

bered passive integrated transponder tags (AVID�, supplied by

Austock Rural Services Pty Ltd.), with new animals being tagged

at first capture. To identify bilbies recaptured during each trip

we marked the ear of each bilby with ink. We recorded the date,

site of capture, passive integrated transponder tag number,

species and sex of each animal trapped.

3.4. Habitat variables

Since the trapping grid covered the entire study site (Fig. 2),

macrohabitat availability was calculated as the sum of trap sta-

tions within each of the four major vegetation communities

present. We also measured 10 fine-scale habitat variables that

could potentially influence the distribution of the four species

within the study site. We considered each trap station to be a

sampling point, and measured variables along three 20-m tran-

sect lines, the starting point of each being selected randomly

within a 20-m radius of the trap or shelter site. We estimated

the following variables: crust cover (% cover of hardened soil

surface); number of Triodia hummocks; trees at two different

heights (<5 m and >5 m); herb cover (plants <0.5 m in height);

litter cover; amount of bare ground; the number of shrubs;

the area covered by logs (>10 cm diameter); and the area cov-

ered by vegetative debris (uprooted trees or shrubs, usually

associated with roads). Crust cover, litter cover, bare ground

cover and herb cover were calculated using a step-point meth-

od (Evans and Love, 1957; Etchberger and Krausman, 1997) as

the proportion of total footsteps along each line that fell within

each of these categories. Proportions were transformed using

arcsine prior to analysis (Zar, 1996). We recorded all other hab-

itat variables 2-m either side of the transect line. Trees with

trunks outside the transect, but with overhanging branches,

were counted as being within the transect. All variables were

measured once around each trap site during March 2006. We

considered the arithmetic mean of the total of each habitat var-

iable recorded on the three transects as the value for that par-

ticular variable at each trap site.

The same 10 habitat variables were also measured at 30

shelter sites (10 each for B. lesueur, B. penicillata and M. lagotis)

that had been found by radio-telemetry. We did not include

O. fraenata as this species is substantially larger than the other

three and individuals generally rest above ground in the

shade of trees or shrubs. We did not wish to disturb and scat-

ter resting animals at their shelters by our sampling protocol.

3.5. Data analysis

3.5.1. Diurnal habitat useTo detect patterns of diurnal habitat use at the macrohabitat

scale we used chi-squared contingency tests to determine

whether the distributions of shelter sites of the four species

showed any association with the distributions of available

macrohabitats within the study site.

To analyze patterns of diurnal habitat use at a finer scale

and detect differences among species we used a multi-re-

sponse permutation procedure within the program PC-ORD

4.20 (McCune and Mefford, 1999). The multi-response permu-

tation test statistic is based on the within-group average of

pairwise distance measures between object response values

in Euclidian data space (Zimmerman et al., 1985). It is a

non-parametric procedure for testing the hypothesis of no

difference between two or more groups of entities and is anal-

ogous to a t-test or a one-way F-test, but is not constrained by

the assumptions required by these tests (Biondini et al., 1988).

We compared differences among four groups: three spe-

cies (B. lesueur, B. penicillata and M. lagotis) and the available

habitat (i.e. measured at all trap sites). Although adequate

for comparing groups with different sample sizes, as in this

study, the multi-response permutation analysis only indi-

cates differences among groups; it does not identify which

variables drive the differences. Consequently, when this anal-

ysis indicated a significant difference among the four groups,

we compared each of the 10 original variables among these

groups using a Kruskal–Wallis test to indicate which variables

contributed to the observed inter-group differences. For these

analyses we used SigmaStat (version 2.03; SPSS Inc., Rich-

mond, California).

3.5.2. Nocturnal habitat useTo detect patterns of nocturnal habitat use at the macrohab-

itat scale we again used chi-squared tests to determine

whether the distributions of trapping locations were associ-

ated with those of the macrohabitats within the study site.

For each individual, we used only the first capture at least

six months after release and the first capture in each subse-

quent trapping session. Multiple trap encounters of the same

individual within a single trapping session were not used as

they were considered to be non-independent.

To analyze habitat utilization at a finer-scale during noc-

turnal periods we used data on species occurrences at trap

sites and habitat variables recorded at each trap site to run

a canonical correspondence analysis. Data were again re-

stricted to the first capture at least six months after release

and the first capture in any subsequent trapping session.

The canonical correspondence analysis, performed using

PC-ORD 4.20, provides an explanatory analysis of potential

relationships between two or more sets of variables (McGari-

gal et al., 2000), in this case, the association between species

occurrences (captures at trap sites) and habitat variables. We

also used the Monte Carlo permutation procedure within PC-

ORD to test the significance of relationships between habitat

variables and species occurrences. This results in a species-

environment correlation coefficient (ter Braak, 1995).

We used multiple regression analysis to determine the ef-

fect of the finer-scale habitat variables, as well as the presence

of the other species, on the occurrence of each re-introduced

species during periods of nocturnal habitat use. This analysis

yields a more specific prediction of the interaction between

each species and the measured habitat variables and can be ap-

plied after the use of an exploratory analysis, such as canonical

B I O L O G I C A L C O N S E R V A T I O N 1 4 1 ( 2 0 0 8 ) 3 2 0 – 3 3 1 325

correspondence analysis, to accurately confirm its results (ter

Braak, 1995; Dalmagro and Vieira, 2005). The technique is also

useful as it provides insight into the potential for competition

between species and describes community patterns of multi-

ple species associated with particular habitat variables (Fox

and Luo, 1996; Luo et al., 1998). Following Dalmagro and Vieira

(2005), we considered the number of captures of each species as

the dependent variable and the finer-scale habitat variables as

the independent variables. We standardized the species vari-

ables by dividing each value by the standard deviation, thus

equalling thevariance to 1 to provide a more accurate represen-

tation of possible competitive effects (Fox and Luo, 1996; Luo

et al., 1998). We ran a backward stepwise multiple regression

analysis (a-to-enter = 0.15, a-to-remove = 0.15) with each spe-

cies as the dependent variable and the fine-scale habitat vari-

ables and occurrences of the other three species as the

independent variables. Variables were checked for inter-corre-

lation and three (Triodia cover, % bare soil and % litter cover)

were removed from the final regression analysis to reduce

any autocorrelation problems (Philippi, 1993). Analyses were

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

Casuarina pauper Eucalyptus & Triod

Prop

ortio

n

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

Casuarina pauper Eucalyptus & Triodia

Prop

ortio

n

Fig. 3 – (a) The proportion of available habitat types (j) and the p

each habitat type for four re-introduced species: B. lesueur ( ), B

Sanctuary. (b) The proportion of available habitat types (j) and

habitat type for four re-introduced species: B. lesueur ( ), B. penic

period at Scotia Sanctuary.

performed using Systat Software Inc. v. 11.0 (Richmond, Cali-

fornia, USA).

4. Results

4.1. Animal trapping

In total, we captured the four study species 2564 times in 3420

trap nights between June 2005 and June 2006. This comprised

836 captures of 162 individual B. lesueur, 1485 captures of 195

B. penicillata, 107 captures of 94 M. lagotis and 136 captures of

83 O. fraenata.

4.2. Habitat use

4.2.1. Diurnal habitat useIn all, 1023 diurnal locations were obtained for all species.

Pair-wise comparisons between macrohabitats that were

available and those used for diurnal resting indicated habitat

selection by each of the four species (Fig. 3a). The frequency of

ia Eucalyptus & shrubs Shrubland

Eucalyptus & shrubs Shrubland

roportion of daytime shelter or burrow sites recorded within

. penicillata (h), M. lagotis ( ) and O. fraenata ( ) at Scotia

the proportion of nocturnal captures recorded within each

illata (h), M. lagotis ( ) and O. fraenata ( ) within a 12-month

326 B I O L O G I C A L C O N S E R V A T I O N 1 4 1 ( 2 0 0 8 ) 3 2 0 – 3 3 1

burrow sites used by B. lesueur differed among the available

macrohabitats (Fig. 3a; v2 = 190.74, df = 3, p < 0.001), with more

burrows than expected located within Eucalyptus woodland

with a shrubby understorey. The frequency of shelter sites

used by B. penicillata also differed from that available

(Fig. 3a; v2 = 297.27, df = 3, p < 0.001), with disproportionately

more shelters located in Eucalyptus woodland over Triodia. A

similar pattern was found for burrows of M. lagotis (Fig. 3a;

v2 = 264.38, df = 3, p < 0.001). The frequency of diurnal shelter

Table 1 – Median values (25–75% percentiles) of the ten habitare-introduced to Scotia Sanctuary

Available Bettongia penicilla

Trees < 5 m (80 m2) 0.3 (0–1.00)a 3.8 (1.3–4.7)b

Trees > 5 m (80 m2) 0.3 (0–1.00)a 1.8 (1.50–3.33)b

Shrubs > 0.5 m (80 m2) 7.3 (3.7–10.3)a 3.8 (1.00–5.67)a,b

Log length (m) 0 (0–1.0) 0 (0–0)

Debris area (m2) 0 (0–2.7) 0 (0–0)

Crust cover (%) 17.4 (10.3–29.3) 13.5 (12.3–19.0)

Herb layer cover (%) 17.7 (5.7–34.8)a 3.8 (0.0–4.3)b

Triodia (80 m2) 0 (0–5.0)a 26.3 (24.0–26.9)b

Bare soil (%) 30.1 (16.7–42.9) 23.9 (17.5–28.0)

Litter (%) 22.2 (6.2–39.4)a 57.1 (53.8–67.2)b

Data for available habitat were collected at trapping sites (see text). P va

variable and were less than 0.05 where indicated. Pairwise a posteriori

lowercase letters.

M.lagotis

B.penicillata

Debris area

Loglength

Shrubs

Trees>5m

Trees<5m

Crust cover

Fig. 4 – Ordination diagram from canonical correspondence analy

trapping locations at least six months after release at Scotia Sanc

arrows.

sites used by O. fraenata indicated selection for Eucalyptus

woodland with a shrubby understorey and shrubland, and

avoidance of Eucalyptus woodland with Triodia understorey

(Fig. 3a; v2 = 80.89, df = 3, p < 0.001).

When comparing the association of shelter sites and fine-

scale habitat variables, we found a marked difference between

the four groups (three species and available habitat) based on

the multi-response permutation procedure (p < 0.0001).

Kruskal–Wallis tests revealed significant differences for six of

t variables measured at shelter sites of three species

ta Bettongia lesueur Macrotis lagotis P

1.2 (0.3–2.0)a,b 0.8 (0.2–1.8)a,b <0.001

0.8 (0.33–1.67)a,b 1.3 (0.7–2.0)a,b <0.001

5.5 (3.7–0.7)a,b 3.2 (1.3–5.0)b 0.008

0 (0–3.7) 0 (0–1.2) 0.25

0 (0–0.3) 1.0 (0–2.7) 0.20

10.6 (5.3–24.3) 23.5 (15.7–28.0) 0.36

4.0 (1.7–12.9)a,b 8.4 (5.9–13.5)a,b <0.001

3.5 (0–10.9)a 11.33 (0.17–33.9)a,b <0.0001

41.6 (29.2–46.6) 29.8 (9.6–41.6) 0.21

36.4 (30.6–46.6)a,b 37.9 (31.1–43.2)a,b <0.001

lues are for Kruskal–Wallis tests comparing the four groups for each

significant differences (Dunn–Sidak test; P < 0.05) are indicated with

B.lesueur

O.fraenata

Herb layercover

sis of the distribution of four re-introduced species based on

tuary. Species are indicated by a (j) and habitat variables by

Table 2 – Habitat and species associations for trapping captures of four mammal species re-introduced to Scotia Sanctuary

Environmental variables Target species

Bettongia lesueur Bettongia penicillata Macrotis lagotis Onychogalea fraenata

Habitat

Crust 2.214b 1.216a �1.298a

<5 m trees �0.175a �0.253a

Herb �0.626a

Shrubs �0.019a

Logs

Debris

>5 m trees

Species

B. lesueur �0.196a

B. penicillata �0.264 �0.254a

M. lagotis �0.205a

O. fraenata

Data are based on regression coefficients of the fine scale habitat variables using backwards stepwise analysis. Only the significant partial

regression coefficients of variables that remained in the final model are shown.

a (p < 0.05).

b (p < 0.01).

B I O L O G I C A L C O N S E R V A T I O N 1 4 1 ( 2 0 0 8 ) 3 2 0 – 3 3 1 327

the habitat variables (Table 1). Pair-wise comparisons indi-

cated a difference between the location of B. penicillata shelter

sites and trees less than 5 m in height, trees greater than 5 m in

height, % herb layer cover, Triodia cover and % litter cover. The

shelter sites of B. lesueur differed from those of B. penicillata

with respect to spinifex cover, but were not significantly differ-

ent to the available habitat. The shelter sites of M. lagotis were

associated with fewer shrubs than in the available habitat

(Table 1).

4.2.2. Nocturnal habitat useA total of 991 captures of the four study species was used to

determine whether the nocturnal use of macrohabitats was

random compared to the distribution of habitats within the

study area. No difference was detected among any of the four

species (Fig. 3b; v2 < 3.1; df = 3, p > 0.20, for all species).

At the finer scale, the Monte Carlo permutation showed a

significant species-environment interaction (correlation coef-

ficient = 0.494, p = 0.005), with canonical correspondence

analysis revealing that different habitat variables were associ-

ated with each species (Fig. 4). The occurrence of B. penicillata

was related to crust cover and trees less than 5 m high, whilst

that of B. lesueur was associated with an increased cover of

herbs. There was also a distinct separation between these

two species along the first axis of the ordination, suggesting

a marked negative association in their occurrence (Fig. 4).

Associations were less obvious for either M. lagotis or

O. fraenata.

The multiple regression revealed similar patterns to those

of the canonical correspondence analysis, with significant

associations between species and particular habitat variables

for the four species (Table 2). There was a negative correlation

between the occurrence of B. lesueur and trees less than 5 m, a

strong positive correlation between the occurrence of B. peni-

cillata and crust cover, and negative correlations between the

occurrence of O. fraenata with crust and trees less than 5 m in

height (Table 2). The values obtained for the multiple regres-

sion were: M. lagotis, R2 = 0.117, p = 0.027; B. penicillata,

R2 = 0.287, p < 0.001; B. lesueur, R2 = 0.155, p = 0.002; and for O.

fraenata, R2 = 0.134, p = 0.007. Competition coefficients were

significant between both species of Bettongia and between B.

penicillata and M. lagotis (Table 2).

5. Discussion

The four study species showed some similarities and differ-

ences in their patterns of habitat use at the two scales evalu-

ated, and also between day and night. All showed selection

for diurnal resting locations but appeared to be less selective,

or were randomly distributed, during nocturnal foraging peri-

ods. Our results highlight the need for evaluating patterns of

habitat use not only for activity periods but also during rest-

ing. The resting period is often neglected in habitat-use stud-

ies as data collection is often based primarily on captures

(Vernes, 2003). However, as each of the species in this study

probably faces higher risks of predation by day, it is also dur-

ing this period that they might be more selective in terms of

habitat use.

A lack of preference for any particular macrohabitat dur-

ing foraging was also observed in the same study area for

numbats (Vieira et al., 2007). Although there is little informa-

tion on population densities for numbats or for any of our

study species in western New South Wales prior to European

settlement, our results may indicate that sufficient food and

other resources were available across all habitats and that

selection for any particular habitat conferred no net benefit.

Also, these species are highly mobile; for example, both

B. penicillata and B. lesueur often move more than a kilometre

in a single night (Christensen, 1980; Christensen and Burrows,

1995). Consequently, there is a chance that traps separated by

500 m caught animals passing on their way to preferred forag-

ing sites. Alternatively, within the fenced area where long-

distance dispersal is limited, foraging in unsuitable areas

may be forced upon individuals once the carrying capacity

within each favoured habitat is reached and territories are

established. In the latter situation, assessment of the impact

328 B I O L O G I C A L C O N S E R V A T I O N 1 4 1 ( 2 0 0 8 ) 3 2 0 – 3 3 1

of these animals on the overall health of the environment

should be a priority. Trends in body condition over a longer

period of time should assist in determining which hypothesis

holds true.

At a finer scale we recorded differences among species in

habitat utilization for both diurnal resting and nocturnal forag-

ing. However, all specieswere more selective for diurnal resting

sites than for nocturnal foraging habitats, as indicated by the

generally lower values of the regressions. Differences in fine-

scale habitat selection were particularly evident for the two

species of Bettongia, leading to a negative relationship between

the numbers of captures of each of these two species.

Since release, the population of B. penicillata has increased

and then declined whereas the population of B. lesueur has in-

creased steadily (G. Finlayson, unpublished data). The differ-

ence in population trends between the two species may be

due to differences in habitat use during a prolonged drought

that extended through the current study. By burrowing, B.

lesueur may be better able to cope with drought than its con-

gener, which does not generally use burrows but prefers to

construct elaborate nests above ground (Christensen, 1995).

A burrowing lifestyle can be expected to be advantageous in

this semi-arid environment, especially during extended dry

periods. Burrows provide shelter from environmental ex-

tremes (Ancel et al., 1998) and so reduce water loss and

expenditure of energy (Darden, 1972; Hansell, 1993; Shimmin

et al., 2002). There is evidence that throughout the more arid

expanses of their historical range, populations of B. lesueur

vastly outnumbered those of B. penicillata, a trend that was re-

versed in the higher rainfall areas of south-western Australia

(Finlayson, 1958). Despite some fine-scale habitat partition-

ing, the negative association between the two bettong species

revealed by the regression analysis may be suggestive of com-

petition. The continued monitoring of these bettong popula-

tions is thus of utmost importance, particularly as both

translocated and naturally occurring populations of B. penicil-

lata elsewhere have declined significantly in recent years

(A. Wayne, pers. comm.). Regression analysis also indicated

potential competitive effects between B. penicillata and M. lag-

otis. More detailed studies of the fine-scale movements, diets

and interactions between B. lesueur, B. penicillata and M. lagotis

may be useful to balance the long term management of these

species at Scotia Sanctuary.

The species most selective for diurnal shelter was B. peni-

cillata. At the macrohabitat scale this species favoured areas

of Eucalyptus woodland with a Triodia understorey, with a high

proportion of shelters occurring at the base of Triodia hum-

mocks. This pattern was confirmed at a finer scale using

habitat variables measured at shelter sites. Interestingly, in

contrast to previous observations of this species (Christensen,

1980; 1995; Christensen and Leftwich, 1980), only a few B. pen-

icillata used burrows or piles of debris for shelter, and this

generally occurred within the first two weeks after release,

prior to the establishment of stable home ranges.

The results of the canonical correspondence analysis and

the higher regression coefficient for B. penicillata suggest fur-

ther that this species is more highly associated with certain

habitat variables during nocturnal foraging than are the other

species. The association between this species and crust cover

can be attributed to the species’ association with spinifex, as

crust cover and spinifex cover were strongly correlated. It

seems that B. penicillata favours areas of increased spinifex,

which provide cover for both diurnal shelter and protection

during nocturnal foraging. In a population of B. penicillata in

Western Australia, scrub density and bare ground were iden-

tified as important characteristics of the preferred habitat for

this species, with animals absent from open areas and areas

with extremely dense ground cover (Christensen, 1980). The

Kruskal–Wallis tests revealed that the shelter sites of B. peni-

cillata were also associated with sites with more trees less

than 5 m high.

Cover can have strong effects on the use of habitat by

small mammals (Dickman, 1992; Hughes and Ward, 1993). In

a concurrent study examining the use of microhabitats by

the re-introduced bettongs at Scotia, Pizzuto et al. (2007)

found that nocturnal foraging movements and activity points

of both B. penicillata and B. lesueur were associated with high

levels of ground cover. In our study, we found B. lesueur to

be positively, but not significantly, correlated with herb layer

and negatively correlated with trees less than 5 m high. This

may be a product of them preferring disturbed habitat where

trees have been removed and where drainage lines and soil

disturbance favour the construction of large warrens and

the growth of species in the herb layer. It is also possible that

favoured food resources such as chenopod forbs, which dom-

inate the herb layer and are more abundant in these open

areas, are the driving force behind some of the observed dis-

tribution patterns observed. After re-introduction on the

north-west coast of Western Australia, B. lesueur favoured

feeding sites in regenerating vegetation that had been re-

cently burnt (Christensen and Burrows, 1995).

We found no evidence of habitat partitioning between the

two semi-fossorial species, B. lesueur and M. lagotis. Both spe-

cies were trapped in similar ratios across all macrohabitats.

They both constructed their burrows in three of the four mac-

rohabitats, but overlapped only in two. Macrotis lagotis fa-

voured areas of Eucalyptus woodland with a Triodia

understorey whereas B. lesueur tended to construct burrows

in Eucalyptus woodland with a shrubby understorey. At the

Arid Recovery Reserve in South Australia, where both species

have been successfully re-introduced, also into a fenced area,

both species tended to construct their burrows in dune habi-

tat (most similar to the Eucalyptus woodland with a Triodia

understorey on Scotia Sanctuary) (Moseby and O’Donnell,

2003; Finlayson and Moseby, 2004). In the current study, con-

trasting rates of capture between species make it difficult to

draw more definitive conclusions.

At two sites in Queensland, O. fraenata has been shown to se-

lect shrubs, hollow logs, fallen timber and dense grass tussocks

for diurnal shelter, and is generally solitary (Fisher, 2000). At

Scotia Sanctuary, this species generally rested at the base of

shrubs in shallow depressions termed hip-holes (Eldridge and

Rath, 2002) within areas of Eucalyptus woodland with a shrubby

understorey. Animals also used fallen logs, piles of debris and

large burrows for shelter. Debris is common on Scotia Sanctu-

ary where trees have been felled for the construction of fences

and roads. This characteristic may explain the negative corre-

lation we observed between captures of O. fraenata and small

trees. After the first release, in December 2004, O. fraenata

favoured the shelter of shrubs at the interface of Eucalyptus

B I O L O G I C A L C O N S E R V A T I O N 1 4 1 ( 2 0 0 8 ) 3 2 0 – 3 3 1 329

woodland with a shrubby understorey and more open and pre-

viously cleared shrubland, which supports favourable pasture

for foraging with a dense herb layer of grasses and forbs. Patchy

clearing of regrowth to create edges near pasture has been pre-

viously noted as an appropriate management strategy for this

species (Fisher, 2000). For many other Australian vertebrates,

particularly macropods, the creation of habitat mosaics is re-

garded as an appropriate management objective (Law and

Dickman, 1998).

In conclusion, our results indicate that, at a macrohabitat

scale, the four species do not select habitat types for foraging

but select specific habitats for diurnal resting, with M. lagotis

and B. penicillata preferring areas of Eucalyptus woodland with

Triodia understorey and B. lesueur and O. fraenata seeming to

select areas of Eucalyptus woodland with a shrubby understo-

rey. At a finer scale, both species of Bettongia showed distinct

patterns of habitat use, with B. penicillata being the most

selective in terms of the habitat variables we measured. As

this is also the species whose population has been declining

in the study area, this may imply a competitive effect of

B. lesueur on B. penicillata; this interpretation is supported by

the negative relationship between both species that we

detected at a fine habitat scale. However, these results must

be approached with caution, as competition may be a func-

tion of the state of the habitat at the time of the study, which

is likely to vary in association with climatic conditions or

wildfire in the region. Seasonally fluctuating exploitative

competition has been hypothesised between B. lesueur and

O. cuniculus in semi-arid coastal Western Australia where die-

tary overlap was higher during the summer months when for-

age was less available (Robley et al., 2001). There could also be

a change in the behaviour of all species once second and third

generation individuals establish in their populations. Previ-

ous experimental studies in other taxa have demonstrated

that captive-bred individuals can behave differently in re-

introduced populations (Kelley et al., 2006), and therefore

potentially drive ‘unnatural’ behaviour patterns. We also

found that distinct differences between species in their habi-

tat use emerged at different spatial scales. The apparent

superiority of B. lesueur is possibly more related to habitat

use at the micro-habitat scale or may vary in relation to cli-

matic conditions which fluctuate dramatically in arid sys-

tems. Our results reinforce the view that multi-species

studies at multiple spatial scales are crucial to understand

the habitat use of threatened fauna and should be incorpo-

rated into species recovery efforts by conservation agencies.

This is particularly important for re-introductions of multi-

species populations into parts of their former range in Austra-

lia, where land-use practices have dramatically altered the

landscape, and should remain a priority in recovery planning.

Acknowledgements

This project was completed in accordance with approval from

the University of Sydney’s Animal Ethics Committee. Project

title: ‘Scotia endangered mammal recovery project’, project

approval number L04/12-2004/2/4010. All field work was con-

ducted under scientific permit number S10614 Department

of Environment and Climate Change (New South Wales). We

thank the Australian Wildlife Conservancy for providing field

equipment, on-site accommodation and other facilities. We

also thank numerous volunteers who provided assistance

with fieldwork. Funding was provided by an Australian Wild-

life Conservancy postgraduate award (to Graeme Finlayson)

and by a Postdoctoral Grant to Emerson Vieira from the Brazil-

ian Government (CAPES – Fundacao Coordenacao de Aper-

feicoamento de Pessoal de Nıvel Superior). We are grateful

to the editor and two anonymous referees for helpful reviews

and comments.

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