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Foraging activity by the southern brown bandicoot (Isoodon obesulus) as a mechanism for soil turnover

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Abstract

Mammals that forage for food by biopedturbation can alter the biotic and abiotic characteristics of their habitat, influencing ecosystem structure and function. Bandicoots, bilbies, bettongs and potoroos are the primary digging marsupials in Australia, although most of these species have declined throughout their range. This study used a snapshot approach to estimate the soil turnover capacity of the southern brown bandicoot (Isoodon obesulus, Shaw 1797), a persisting digging Australian marsupial, at Yalgorup National Park, Western Australia. The number of southern brown bandicoots was estimated using mark-recapture techniques. To provide an index of digging activity per animal, we quantified the number of new foraging pits and bandicoot nose pokes across 18 plots within the same area. The amount of soil displaced and physical structure of foraging pits were examined from moulds of 47 fresh foraging pits. We estimated that an individual southern brown bandicoot could create similar to 45 foraging pits per day, displacing similar to 10.74 kg of soil, which extrapolates to similar to 3.9 tonnes of soil each year. The digging activities of the southern brown bandicoots are likely to be a critical component of soil ecosystem processes.
Foraging activity by the southern brown bandicoot
(Isoodon obesulus) as a mechanism for soil turnover
Leonie E. Valentine
A,B,C
, Hannah Anderson
A
, Giles E. StJ. Hardy
A
and Patricia A. Fleming
A
A
Western Australia Centre of Excellence for Climate Change, Woodland and Forest Health,
School of Veterinary and Life Sciences, Murdoch University, Perth, WA 6150, Australia.
B
Present address: ARC Centre of Excellence for Environmental Decisions, School of Plant Biology,
University of Western Australia, Crawley, WA 6009, Australia.
C
Corresponding author. Email: leonie.valentine@uwa.edu.au
Abstract. Mammals that forage for food by biopedturbation can alter the biotic and abiotic characteristics of their habitat,
inuencing ecosystem structure and function. Bandicoots, bilbies, bettongs and potoroos are the primary digging marsupials
in Australia, although most of these species have declined throughout their range. This study used a snapshot approach to
estimate the soil turnover capacity of the southern brown bandicoot (Isoodon obesulus, Shaw 1797), a persisting digging
Australian marsupial, at Yalgorup National Park, Western Australia. The number of southern brown bandicoots was
estimated using markrecapture techniques. To provide an index of digging activity per animal, we quantied the number of
new foraging pits and bandicoot nose pokes across 18 plots within the same area. The amount of soil displaced and physical
structure of foraging pits were examined from moulds of 47 fresh foraging pits. We estimated that an individual southern
brown bandicoot could create ~45 foraging pits per day, displacing ~10.74 kg of soil, which extrapolates to ~3.9 tonnes of soil
each year. The digging activities of the southern brown bandicoots are likely to be a critical component of soil ecosystem
processes.
Additional keywords: biopedturbation, ecosystem engineering, soil movement.
Received 8 October 2012, accepted 7 May 2013, published online 22 May 2013
Introduction
Mammals that move or manipulate soil for food or to create shelter
(biopedturbation) can act as ecosystem engineers (Whitford
1999), creating disturbances that may be essential for maintaining
ecosystem health (Eldridge and James 2009; Eldridge et al.2009).
Mammalian biopedturbation creates small-scale disturbances via
soil turnover (Whitford 1999; Eldridge et al.2012) and can
subsequently alter the physical properties of soil, including soil
compaction and water inltration (Garkaklis et al.1998,2000,
2003). Several Australian marsupials dig, though the bettongs
(Bettongia spp., Aepyrymnus rufescens), potoroos (Potorous
spp.), bilbies (Macrotis spp.) and bandicoots (Perameles spp.,
Isoodon spp. and Echymipera rufescens) are the main marsupials
in Australia responsible for creating foraging pits (Martin 2003).
These marsupials are adapted to digging in soil, and use their
strong forefeet and claws to create foraging pits while searching
for food, such as invertebrates, tubers, seeds and fungi. The soil-
turnover capacity of these digging marsupials is impressive, with
individual woylies (Bettongia penicillata) estimated to displace
~4.8 tonnes of soil each year (Garkaklis et al.2004).
Australian digging marsupials (here dened as bettongs,
potoroos, bilbies and bandicoots) are all within the critical weight
range and considered most at risk from introduced predators
(Johnson and Isaac 2009), and most of these species have suffered
drastic declines in mainland populations and substantial range
contractions (Van Dyck and Strahan 2008). Of the 16 extant
digging marsupial species, 11 are considered to be of
conservation concern, while a third (5 species) are considered
critically endangered or endangered (Environment Protection
and Biodiversity Conservation Act 1999). Despite the grim
conservation status of most Australian digging marsupials,
several species (e.g. Isoodon macrourus,I. obesulus and
Perameles nasuta) persist within parts of their former range on
mainland Australia, sometimes in highly modied environments
(e.g. Hughes and Banks 2010). However, the potential ecosystem
role of these species has not been investigated.
The southern brown bandicoot (I. obesulus, Shaw 1797) is a
medium-sized omnivorous marsupial that occurs in scattered
areas across parts of eastern, southern and south-western
Australia (Van Dyck and Strahan 2008). Home-range estimates
for the southern brown bandicoot vary from 0.5 to 6.0 ha (Lobert
1990), with males typically having larger home ranges than
females (Heinsohn 1966), and in areas of high density (and
correspondingly high food supply) home ranges are likely to
Journal compilation ÓCSIRO 2012 www.publish.csiro.au/journals/ajz
CSIRO PUBLISHING
Australian Journal of Zoology, 2012, 60, 419423 Short communication
http://dx.doi.org/10.1071/ZO13030
overlap (Broughton and Dickman 1991). Although the eastern
subspecies (I. obesulus obesulus) is listed as endangered
(Environment Protection and Biodiversity Conservation Act
1999), in south-western Australia the southern brown bandicoot
(I. obesulus fusciventer) is the only persisting commonly
occurring digging marsupial, especially within the
urbanwildland interface. Foraging pits are created by
bandicoots when digging with their strong forefeet for fungal
fruiting bodies, invertebrates and subterranean plant material
(Van Dyck and Strahan 2008). Previous observations have
indicated that southern brown bandicoots may be prolic
diggers(Heinsohn 1966; Quin 1985).
The southern brown bandicoot occur in two distinct habitats in
south-western Australia open forest, and dense vegetation
around swamps and watercourses (Cooper 2000a,2000b)and
this mammal has consequently been identied as susceptible to
declining groundwater and rainfall (Wilson et al.2012). In the
urbanwildland interface surrounding Perth, populations of the
southern brown bandicoot persist in the bush fragments and
conservation reserves, often without predator control. In this
study, we quantied the physical structure of southern brown
bandicoot foraging pits and estimated soil turnover in a small area,
to compare with other digging marsupial species and to assist in
determining the potential role of the southern brown bandicoot in
maintaining ecosystem processes.
Materials and methods
Study site
This study was conducted at Martins Tank at the edge of Martins
Lake, Yalgorup National Park on the Swan Coastal Plain IBRA
region (Thackway and Cresswell 1995) in south-western
Australia (3250054.5200S, 1154008.7200 E). Yalgorup National
Park (~12 888 ha) has high regional biodiversity values based
around the chain of 10 coastal lakes, swamps and tuart
(Eucalyptus gomphocephala) forests (Portlock et al.1993).
Although sections of the national park are baited with 1080
(sodium uoroacetate) to assist in the control of the introduced red
fox (Vulpes vulpes), the area surrounding Martins Lake is not
currently baited. The region has a Mediterranean-type climate
with hot dry summers and mild wet winters and an average annual
rainfall of 864 mm (Bureau of Meteorology, Lake Preston Lodge
2 Comp., #009679). Yalgorup National Park contains three major
dune systems: the Quindalup, Spearwood and Bassendean Dunes
(Portlock et al.1993). Our research focussed on foraging activity
and soil turnover of bandicoots within a small section of the
National Park, consisting of a 2-ha area (200 m 100 m) in the
vegetation running parallel to Martins Lake. Our study site was
located on Spearwood Dunes, where soils were predominantly
yellow-phase Karrakatta sands. Vegetation in the study area
included lake-fringing vegetation dominated by Melaleuca
preissiana and M. rhaphiophylla and interspersed with tuarts,
with a dense understorey of sedges (mostly Gahnia trida)
transitioning to a combination of tuart trees, peppermint (Agonis
exuosa) and paperbark (M. rhaphiophylla), and a tuart, jarrah
(E. marginata) and marri (Corymbia calophylla) overstorey with
a mid-storey layer of scattered Banksia grandis,B. attenuata and
grasstrees (Xanthorrhoea spp.), and an open understorey of
zamia palms (Zamia spp.) and various herbaceous species (e.g.
Jacksonia sternbergiana,Hibbertia hypericoides) (Portlock
et al.1993).
Estimating soil turnover by the southern brown bandicoot
Bandicoot foraging activity was assessed for 18 plots (each
10 m 10 m), with plots haphazardly stratied along the
vegetation gradient described above, with each plot separated
from each other by a minimum of 30 m. We counted the number of
new foraging pits and nose pokes created within each plot during a
24-h period in June and in August 2011. A bandicoot foraging
pitwas dened as having a clear point at the bottom of the pit and
a spoil heap adjacent to the pit (where displaced soil was
accumulated via the digging activities of the bandicoots). A nose
pokewas dened as an obvious movement of the ground debris
and soil but without a dened point or adjacent spoil heap. Due to
rain occurring in the days before examining foraging activity (but
not during the sample period), new foraging pits and nose pokes
were easily identied during both sampling sessions (as rain in the
previous day had left impressions in the spoil of existing foraging
pits).
After counting foraging pits (described above), we used
markrecapture trapping (three nights in June and August 2011)
to estimate the number of southern brown bandicoots potentially
responsible for creating the foraging pits in the 2-ha study area. A
transect of 10 cage traps (Shefelds: 20 cm 20 cm 56 cm)
were spread evenly across the study area. All traps were baited
with universal bait (a combination of peanut butter, rolled oats,
sardines and trufe oil). Hessian bags and pieces of tarpaulin were
placed over all cage traps to provide shelter and to prevent rain
entering the cage. The traps were open in the afternoon each day
and checked within 3 h of sunrise the following morning. All
animals captured were weighed, measured (head length and
long pes), sexed and individually marked using ISO FDX-B
microchips (OzMicrochips, NSW) inserted subcutaneously on
the nape of the neck. Retrapped animals were detected using the
RT100 ISO Scanner (Real Trace, NSW). In this study we have not
assessed home-range sizes for the southern brown bandicoot,
although previous work in south-western Australia indicates that
home ranges are ~2.3 ha for males and ~1.8 ha for females, but
they may overlap (Broughton and Dickman 1991). As we did not
estimate the spatial range of the animals at Martins Tank, we used
the total number of animals captured (both trapping sessions
combined) as our estimate of the number of bandicoots creating
foraging pits within the 2-ha area.
The number of foraging pits was quantied by averaging the
number of new foraging pits per plot counted in June and August
2011 and extrapolating this value to a per-hectare estimate. Plaster
of Paris (Diggers Plaster of Paris, South Australia) was poured
into 47 fresh bandicoot diggings that were representative of the
range of foraging pit sizes observed in plots. We measured the
width (at soil surface) and depth of the plaster moulds, and the
volume of each mould (in millilitres) was estimated by water
displacement (1200 mL graduated cylinder). Measurements
reported are the average standard error. Soil density
(1.25 g cm
3
) was estimated as the average density obtained from
four soil core samples of known volume (~1021 cm
3
) that were
420 Australian Journal of Zoology L. E. Valentine et al.
oven-dried for 72 h (K. Ruthrof, unpubl. data). The amount of soil
displaced by one bandicoot in a night was calculated as:
Soil displaced ðg individual1ð24-h periodÞ1Þ
¼ðno:of new foraging pits bandicoot1ð24-h periodÞ1Þ
ðforaging pit volumeÞðsoil densityÞ
This gure was also then expressed as tonnes
individual
1
year
1
.
Limitations to this study
Our study provides a snapshot approach at estimating the soil-
turnover capacity of the southern brown bandicoot, and has
several limitations that should be considered. First, we used a
single location, Martins Tank, to obtain our estimates of foraging
activity and foraging pit dimensions for the southern brown
bandicoot. These values may vary depending on location, habitat,
soil type and bandicoot density. Second, to estimate the number of
bandicoots creating the foraging pits, we have used the total
number of bandicoots captured within the 2-ha area. Given our
uncertainty of the spatial range of foraging bandicoots, the
foraging pits within our study area may have been created by one
or several bandicoots. Using the total number of captured
bandicoots may overestimate the number of bandicoots creating
the foraging pits and thus could represent a conservative estimate
of the soil-turnover capacity of this species. Third, our estimates
of foraging activity are based on two nightsdata collection and
the extrapolation to an annual estimate of soil turnover does not
reect seasonal differences in foraging behaviour and intensity.
Results
In total, eight bandicoot individuals were captured in the 2-ha area
over 60 trap-nights (June and August sessions combined). Six
bandicoots (two female, four male) were captured in June and
recaptured in August, along with an additional two individuals
(one male, one escaped before it was sexed). Males were typically
larger and heavier (n= 5, mean s.e.: body mass = 1724 107 g;
head length = 93.2 2.1 mm, pes length = 65.0 1.3 mm) than
females (n= 2, mean s.e.: body mass = 1165 15 g; head
length = 85.1 6.0 mm; pes length = 60.6 2.0 mm). The eight
individuals were all in visibly good condition, with no fur loss,
scratches or other signs of ghting.
Across the 18 survey plots there were 36 new foraging pits and
88 new nose pokes in June and 32 new foraging pits and 122 new
nose pokes in August, with a range of 06 foraging pits and 021
nose pokes observed per plot in both sampling periods. The mean
number of new foraging pits day
1
averaged 1.8 plot
1
(10 10 m), which extrapolated to 180 new foraging pits ha
1
in a
24-h period. For the purposes of this study, we have assumed that
all eight individual southern brown bandicoots created the
foraging pits (i.e. 4 individual bandicoots ha
1
), which equates to
45 foraging pits day
1
(individual bandicoot)
1
.
Moulds of 47 fresh foraging pits indicated that foraging pits
were fairly consistent in their physical size. Foraging pits were
conical in shape, measuring 100.9 3.9 mm across at the soil
surface with a mean depth of 69.6 3.2 mm (depth range
35135 mm). The mean volume of these foraging pits was
191 15 mL. In a single night of our study, the soil displaced
by one bandicoot at Martins Tank was therefore estimated
as 8595 cm
3
or 10.74 kg (calculated as follows: 10 743.75 g
soil displaced individual
1
(24-h period)
1
= 45 foraging
pits bandicoot
1
(24-h period)
1
191 mL soil displaced
1.25 g cm
3
soil density). Assuming no seasonal differences in
foraging activity, this value can then be extrapolated to an annual
turnover of 3.14 m
3
or 3.92 tonnes for each individual.
Discussion
Southern brown bandicoots are opportunistic omnivores that
forage for a variety of food, consuming invertebrates, fungi, plant
material and occasionally small vertebrates, with diets reecting
seasonally and locally abundant food items (Heinsohn 1966;
Quin 1988; Van Dyck and Strahan 2008). Foraging of bandicoots
via nose pokes may assist bandicoots in detecting subterranean
prey items (Quin 1992) and/or target invertebrates (e.g.
cockroaches, crickets, spiders) that commonly occur in the leaf
litter layer (Hattenschwiler et al.2005). In Tasmania, a single wild
bandicoot was observed digging 21 foraging pits within 36 min
(Heinsohn 1966), while bandicoots in captivity have been
observed digging up to 32 foraging pits in an evening (Quin
1985). In our study, we estimated that a single bandicoot dug ~45
foraging pits each day, representing a considerable impact in
terms of soil turnover.
Bettongs and potoroos forage principally on fruiting bodies of
underground fungi (Van Dyck and Strahan 2008) and may create
higher numbers of foraging pits while searching for food (e.g.
woylie: 38114 foraging pits individual
1
(Garkaklis et al.2004);
southern brown bandicoot: ~45 foraging pits individual
1
).
Although we did not examine the density of foraging pits
throughout seasons, previous research has indicated that the
densities of foraging pits of digging marsupials may vary
throughout the year, potentially in relation to the availability of
hypogeal fungal fruiting bodies (Claridge et al.1993). As the diet
of the southern brown bandicoot varies seasonally (Quin 1988),
the number of foraging pits created by this species is also likely to
vary seasonally. Foraging pits created by the greater bilby and
burrowing bettong are ~80 mm deep (James and Eldridge 2007),
similar in size to those of the southern brown bandicoot (~70 mm).
The long-nosed potoroo (P. tridactylus) creates foraging pits that
vary in depth from 56 to 120 mm (Claridge et al.1993), while the
woylie creates deeper foraging pits (100115 mm: Garkaklis et al.
2004).
Although our study is restricted to a small area and represents a
snapshotof foraging activities of the southern brown bandicoot,
it is the rst to estimate soil turnover rates of the southern brown
bandicoot, with an individual bandicoot (average body mass
1.6 kg) turning over ~10.74 kg day
1
. This equates to ~3.9 tonnes
of soil bandicoot
1
year
1
and falls within the range of soil
displaced (2.79.7 tonnes year
1
) by the similar-sized woylie
(body mass: 1.01.5 kg) (Garkaklis et al.2004). Marsupials that
burrow for food and live underground produce even greater soil
turnover. For example, in predator-free enclosures in arid zones,
where bilbies and burrowing bettongs are held together (therefore
values are for both species combined), these animals excavate
~30 tonnes of soil individual
1
year
1
(Newell 2008).
Soil turnover by the southern brown bandicoot Australian Journal of Zoology 421
The loss of once widespread digging mammals in Australia is
likely to have major ramications for ecosystem processes.
Further research on the foraging activities of the southern brown
bandicoot, preferably over a longer time frame and across several
sites, is necessary to elucidate the soil-turnover capacity of this
digging marsupial. Although the range and population of the
southern brown bandicoot has declined since European
settlement (Abbott 2008), these animals persist in urban,
periurban and rural regions of south-western Australia, where
they are likely to be playing an important role in ecosystem
processes, contributing to the health and function of the
woodlands and forests. Understanding the role of these animals
may therefore contribute towards conservation management
decisions. Since the southern brown bandicoot appears to be more
resilient to human-mediated disturbances compared with other
digging marsupials (e.g. woylie), they provide us with an ideal
opportunity to reintroduce them into landscapes where soil
turnover is required for ecosystem health and function.
Acknowledgements
We gratefully thank the Department of Environment and Conservation Swan
Coastal District for their support with this project, especially Craig Olejnik,
Paul Tholen and Alan Wright. We also thank three anonymous reviewers for
substantially improving this manuscript. Our work was funded by the WA
State Centre of Excellence for Climate Change, Woodland and Forest
Health and the ARC Centre of Excellence for Environmental Decisions, and
was carried out with a Murdoch University Animal Ethics Committee permit
(W2341/10) and a WA Department of Environment and Conservation permit
(Regulation 17: SF001280).
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Handling Editor: Steven Cooper
Soil turnover by the southern brown bandicoot Australian Journal of Zoology 423
www.publish.csiro.au/journals/ajz
... The digging activities of animals excavating hypogeous fungi contribute to bioturbation (soil disturbance) and provide important soil aeration for water penetration and organic matter decomposition (Lamont 1995, Garkaklis et al. 1998, Newell 2008, James et al. 2009, Valentine et al. 2013 122 perform bioturbation to varying degrees, and the relative importance of animal-mediated soil turnover is also dependant on the region and soil type. In Australia, the role of mycophagous vertebrates in soil turnover has been relatively well studied in some regions. ...
... In a healthy system, a multitude of vertebrates forage in the litter and dig down into the mineral soil in search of truffles and other subterranean foods. These activities contribute to the breaking up of the hydrophobic layer at the soil surface and create micro catchments, thus improving water penetration and assisting with organic matter decomposition (Lamont 1995, Garkaklis et al. 1998, Newell 2008, James et al. 2009, Valentine et al. 2013, Davies et al. 2018, Palmer et al. 2020, Maisey et al. 2021. ...
... The brush-tailed bettong digs between 38 and 114 excavations per night, and each individual is estimated to displace an average of 4.8 tonnes of soil per year (Garkaklis et al. 2004). The southern brown bandicoot (Isoodon obesulus) has been estimated to dig about 45 foraging excavations per day and in the process displace about 10.74 kg of soil, resulting in a soil turnover of approximately 3.9 tonnes per year per individual (Valentine et al. 2013). Some of the larger desert species such as the greater bilby (Macrotis lagotis) and the burrowing bettong (Bettongia lesueur) are estimated to turn over approximately 30 tonnes of soil per year per individual (Newell 2008). ...
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The consumption of fungi by animals is a significant trophic interaction in most terrestrial ecosystems, yet the role mammals play in these associations has been incompletely studied. In this review, we compile 1 154 references published over the last 146 years and provide the first comprehensive global review of mammal species known to eat fungi (508 species in 15 orders). We review experimental studies that found viable fungal inoculum in the scats of at least 40 mammal species, including spores from at least 58 mycorrhizal fungal species that remained viable after ingestion by mammals. We provide a summary of mammal behaviours relating to the consumption of fungi, the nutritional importance of fungi for mammals, and the role of mammals in fungal spore dispersal. We also provide evidence to suggest that the morphological evolution of sequestrate fungal sporocarps (fruiting bodies) has likely been driven in part by the dispersal advantages provided by mammals. Finally, we demonstrate how these interconnected associations are widespread globally and have far-reaching ecological implications for mammals, fungi and associated plants in most terrestrial ecosystems. Citation: Elliott TF, Truong C, Jackson S, Zúñiga CL, Trappe JM, Vernes K (2022). Mammalian mycophagy: a global review of ecosystem interactions between mammals and fungi. Fungal Systematics and Evolution 9: 99–159. doi: 10.3114/fuse.2022.09.07
... To successfully find fungal fruiting bodies, many animals will disturb the leaf litter and sometimes dig down into the mineral soil, creating substantial disturbance to the soil. These areas of disturbance promote the decomposition of organic material and improve water penetration and soil hydration (Garkaklis et al. 2004;Newell 2008;Valentine et al. 2013;Elliott and Vernes 2019;Palmer et al. 2020). The health and resilience of both the plant and fungal communities depend in part on animals for these ecosystem services. ...
... In the process of foraging for fungi, the bandicoots also cause bioturbation (soil disturbance) that reduces the oil build-up from Eucalyptus oils and improves water penetration into the soil (Garkaklis et al. 2000). It has been estimated that a Quenda (Isoodon fusciventer) makes approximately 45 digs each night while foraging, resulting in the displacement of about 10.74 kg of soil; this translates into roughly 3.9 tonnes of soil turnover per individual per year (Valentine et al. 2013). Although there have not been similar studies on the soil disturbance produced by eastern barred or southern brown bandicoots, their similar size and foraging habits suggest that they are similarly important bioturbators. ...
Article
Mycophagous mammals perform important ecosystem services through their dispersal of mycorrhizal fungi (particularly truffles). In order to better understand the role of Tasmanian bandicoots in these associations, we examined the stomach and scat contents of specimens of southern brown bandicoots (Isoodon obesulus) and eastern barred bandicoots (Perameles gunnii) preserved in the mammal collections of the Queen Victoria Museum and Art Gallery. Our study shows that fungi are consumed by both species and that these mammals likely play a key role in ecosystem function through their dispersal of mycorrhizal fungal spores.
... This was not an exception. Another study from Yalgorup National Park in Western Australia found that southern brown bandicoots turned over an average of 10.74kg of soil per day, per individual, translating to 3.9 tonnes per year (Valentine et al., 2013). Bandicoots' diggings also have profound, measurable effects on biotic and abiotic communities. ...
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I employ a conceptual synthesis that bridges Western and First Nations sciences in pursuit of a broader understanding of cultural burning as a multispecies practice in Australia. The concept of ‘re-storying’ diminishes nature/culture dualisms and creates space for the role of culture in understanding and shaping ecologies; the concept of ‘niche construction’ fosters attention to the ways in which humans co-construct landscapes with other organisms in ways that affect the communities doing the co-constructing. With this conceptual toolkit, I draw attention to the species that play important roles in cultural burning practices through story, ceremony, and their actions upon the landscape. Animals such as bandicoots, brush turkeys, and raptors have pronounced effects on landscapes, and these in turn alter and affect the ways in which First Nations peoples apply fire. These stories demonstrate the complex, relational, and multispecies nature of cultural burning and the need for broader, more nuanced approaches that allow people to burn for, and with, animals.
... The reserves differed in both biotic and abiotic attributes; for details see Supporting Information S1: Table S1. Native digging mammal species were largely locally extinct from the reintroduction sites and surroundings before the reintroductions However, echidnas (Tachyglossus aculeatus) occur throughout Australia at varying densities (Griffiths 2012) and quenda (Isoodon fusciventer) persisted outside the fence at Karakamia (Western Australia) in low densities (Valentine et al. 2012). ...
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Introduction In Australia, the historical loss of native digging mammals has profoundly changed ecosystems and their functioning. However, little is known about how the decline in digging mammal presence alters microbes and their functional potential and how aridity affects these relationships. Materials and Methods We used metagenomic sequencing to explore changes in genes encoding enzymes for carbon cycling (CAZymes) in five sites along a continent‐wide aridity gradient, with and without digging mammals. Results The diversity of CAZy genes was reduced with increases in aridity, which also affected their structure and reduced the abundance of genes involved in both plant (cellulose and starch) and microbial (glucans, peptidoglycan and chitin) biomass degradation. Conversely, digging mammals had a limited effect on the structure and diversity of CAZy genes, indicating an overall resistance of the microbial carbon cycling potential to mammal disturbance at the whole community level. However, when considering individual functional groups, digging activity increased the abundance of genes involved in microbial biomass decomposition (i.e., glucanases), while reducing the abundance of genes associated with recalcitrant plant biomass degradation (i.e., cellulases). Notably, these effects were observed only in the most arid sites and was mostly mediated by increases in SOM content linked to mammal activity. Conclusions Overall, our study shows that aridity shapes the diversity and structure of CAZy genes, while also modulating the effect of mammal bioturbation on the microbial potential for carbon cycling. This suggests that the loss of digging mammals throughout much of Australia's arid zone, in particular, is likely to have important repercussions on the microbial capacity to carry decomposition processes and the turnover of organic matter in soils.
... The spatial autocorrelation analysis indicated a positive relationship between feeding pit size and clustering. This could be driven by differences in prey depths, where larger rays are able to access deeper, more rewarding prey than smaller rays (Ebert & Cowley, 2003;Tillett et al., 2008). Future studies should aim to determine whether prey depth affects bioturbation depth, and how that relates to foraging ray size. ...
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Bioturbation of sediments is a key ecosystem service in estuarine and marine ecosystems, and rays (superorder Batoidea: skates, stingrays, electric rays and shovelnose rays) are among the largest bioturbators, modifying their habitat through foraging and predation. Ray activities cycle nutrients, increase oxygen penetration and re‐stratify sediments. However, given rays are globally threatened, it is unclear to what extent the loss of rays, and the ecosystem services they provide, would affect ecosystem processes. This study assessed the likely amount of sediment displaced annually by rays during foraging activities at an estuary scale. To achieve this, an aerial drone was used to map daily ray bioturbation activity, as evident from the presence of feeding pits. High‐resolution, 2.6 cm px⁻¹, Digital Elevation Models (DEM) were created and used to measure the volume of sediment displaced by feeding pits. We found rays within the Brisbane Water estuary in NSW, Australia excavated 1.20 (±0.68) tonnes of sediment per day within this 1443 m² intertidal area, or a rate of 575.2 cm³ m⁻² per day. This bioturbation rate is relatively high compared to bioturbation rates documented in other ray species. Spatial autocorrelation analysis indicated that the ray feeding pits were significantly clustered by location as well as size (P < 0.01), suggesting size segregation of ray foraging. When bioturbation rates were conservatively extrapolated across measured feeding area in the estuary, we calculated rays displace 57.6 (±32.4) tonnes of sediment per day, or 21.0 (±11.4) kilotonnes per year. This underlines how ray bioturbation likely shape estuary processes, and how the loss of rays and their ecosystem services would likely have considerable impacts on estuarine sedimentary ecosystems. These findings emphasize the ecological importance of rays in an ecosystem and a need to better understand the consequences of anthropogenic pressures to these services.
... This contrasts with the digs of scratch-digging marsupials that are two-to six-times deeper (e.g. woylies: 100-150 mm in depth: Garkaklis et al. 2003; or quenda: average depth 69.6 ± 3.2 mm: Valentine et al. 2012). Consequently, echidnas displace substantially less soil than quenda and woylies (Table 2). ...
Article
Bioturbation by digging animals is important for key forest ecosystem processes such as soil turnover, decomposition, nutrient cycling, water infiltration, seedling recruitment, and fungal dispersal. Despite their widespread geographic range, little is known about the role of the short-beaked echidna (Tachyglossus aculeatus) in forest ecosystems. We measured the density and size of echidna diggings in the Northern Jarrah Forest, south-western Australia, to quantify the contribution echidna make to soil turnover. We recorded an overall density of 298 echidna diggings per hectare, 21% of which were estimated to be less than 1 month old. The average size of digs was 50 ± 25 mm in depth and 160 ± 61 mm in length. After taking into account seasonal digging rates, we estimated that echidnas turn over 1.23 tonnes of soil ha−1 year−1 in this forest, representing an important role in ecosystem dynamics. Our work contributes to the growing body of evidence quantifying the role of these digging animals as critical ecosystem engineers. Given that the echidna is the only Australian digging mammal not severely impacted by population decline or range reduction, its functional contribution to health and resilience of forest ecosystems is increasingly important due to the functional loss of most Australian digging mammals.
... Soil displacement alters the chemical and structural properties of soils, increases water infiltration (Garkaklis et al., 1998), run-off and erosion (Eldridge & Myers, 2001), and moderates the availability of soil nutrients such as labile carbon, nitrogen, and sulfur (Eldridge & Mensinga, 2007). Conditions within foraging pits can provide a microclimate conducive to plant germination (Eldridge & Koen, 2021;Louw et al., 2021;Martin, 2003) while burying and mixing of litter and soil allows greater assimilation by macro-and micro-invertebrates, thus fuelling high rates of nutrient cycling (Mallen-Cooper et al., 2019;Valentine et al., 2013) and improving plant growth (Fleming et al., 2014;Valentine et al., 2018). ...
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Abstract Ecosystem engineers that modify the soil and ground‐layer properties exert a strong influence on vegetation communities in ecosystems worldwide. Understanding the interactions between animal engineers and vegetation is challenging when in the presence of large herbivores, as many vegetation communities are simultaneously affected by both engineering and herbivory. The superb lyrebird Menura novaehollandiae, an ecosystem engineer in wet forests of south‐eastern Australia, extensively modifies litter and soil on the forest floor. The aim of this study was to disentangle the impacts of engineering by lyrebirds and herbivory by large mammals on the composition and structure of ground‐layer vegetation. We carried out a 2‐year, manipulative exclusion experiment in the Central Highlands of Victoria, Australia. We compared three treatments: fenced plots with simulated lyrebird foraging; fenced plots excluding herbivores and lyrebirds; and open controls. This design allowed assessment of the relative impacts of engineering and herbivory on germination rates, seedling density, vegetation cover and structure, and community composition. Engineering by lyrebirds enhanced the germination of seeds in the litter layer. After 2 years, more than double the number of germinants were present in “engineered” than “non‐engineered” plots. Engineering did not affect the density of seedlings, but herbivory had strong detrimental effects. Herbivory also reduced the floristic richness and structural complexity (
... Bandicoots are a family of marsupials (Peramelidae) found across Australia and New Guinea (Warburton and Travouillon, 2016). They have specialist digging traits (Martin et al., 2019a;Martin et al.,2019b;Warburton et al., 2015) that reflect their adaptation to turning over a vast volume of soil (Valentine et al., 2013) while digging in search of foodbulbs, insects, and hypogeous fungi fruiting bodies (truffles). This digging has several benefits for ecosystem health (Mallen-Cooper et al., 2019), including improved soil moisture and microbial communities (Eldridge and Mensinga, 2007;Valentine et al., 2017), enhanced seedling recruitment and growth (Valentine et al., 2017;Valentine et al., 2018), and increased dispersal of mycorrhizal fungi (Dundas et al., 2018;Hopkins et al., 2021;Tay et al., 2018). ...
Article
Residential gardens can provide essential opportunities for native wildlife and represent a valuable way of creating new habitats. Bandicoots (marsupial family Peramelidae) are medium-sized digging mammals that play a valuable role in maintaining ecosystem health; retaining these important ecosystem engineers across urban landscapes, including in private gardens, can have enormous conservation benefits. Urbanisation is a significant threat for some bandicoot species, and therefore understanding the factors associated with their activity can help guide urban landscape and garden design. To identify key features associated with the activity of a local endemic bandicoot species, the quenda (Isoodon fusciventer), we carried out a camera trap survey of front and back yards for 65 residential properties in the City of Mandurah, Western Australia. We compared quenda activity with biotic and abiotic factors that could indicate potential predation risk (activity of domestic dogs Canis familiaris and cats Felis catus, and the presence of artificial or natural protective cover), food availability (including deliberate or inadvertent supplementary feeding, provision of water, and diggable surfaces) and garden accessibility (distance to bushland, permeability of boundary fencing, and garden position). Supplementary feeding was strongly associated with quenda activity. Quenda were also more active in back yards, and in gardens where there was greater vegetation cover. Of concern, quenda activity was positively associated with cat activity, which could reflect that straying pet cats are attracted to gardens that harbour wildlife populations, including quenda. Furthermore, almost half of the gardens showed cat activity despite only a small sample of the surveyed residents owning a pet cat. Results of this study can help guide the design of residential gardens to increase useful habitat for these important digging mammals. Vegetation, wood mulch and semi-permeable fencing can provide valuable resources needed to support the persistence of quendas across the rapidly changing urban landscape mosaic, where natural and managed (e.g., gardens and parks) green spaces are becoming less common and more isolated.
Article
The excavation of Chinese pangolin ( Manis pentadactyla ) is expected to alter habitat heterogeneity and thus affect the functioning and structure of forest ecosystems. In this study, the bioturbation of Chinese pangolin on forest soils in three regions (Heping, Tianjingshan, and Wuqinzhang) across Guangdong province was quantified. Overall, a mean of 2.66 m ³ ·ha ⁻¹ and 83.1 m ² ·ha ⁻¹ of burrows and bare mounds, respectively, was excavated by Chinese pangolin; the disturbed soils had significantly lower water content and P, C, available N concentrations, but higher bulk density, pH, and microbial abundance than those undisturbed soils. The unevenness of habitat heterogeneity improvement was mainly ascribed to the stronger soil disturbance caused in resting burrows by pangolins. Patterns of altering habitat heterogeneity were site‐specific, with high‐intensity soil disturbance occurring most in shrubs, meadows, steep habitats at high elevations, and mountain tops in Heping, while in broad‐leaved, coniferous and mixed coniferous and broad‐leaved forests away from human settlements in Tianjingshan and upper mountains at high elevations far away from roads and human settlements in Wuqinzhang. Road networks are the main interference for the burrow distribution in Heping and Wuqinzhang and should be programmed.
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Arid Recovery, a fenced reserve free of feral predators in arid South Australia, has successfully reintroduced two critical weight range (CWR) mammals, greater bilbies (Macrotis lagotis) and burrowing bettongs (Bettongia lesueur) to facilitate the restoration of arid Australian ecosystems. This thesis evaluates the ecological roles of these reintroduced species and their relationship to ecosystem functioning and the restoration of these ecosystems. Surveys of foraging diggings and soil seed banks, and dietary analysis were used to measure impacts of these species on three main habitats within the Reserve. The results showed that bilbies and bettongs have three major roles in ecosystem functioning: consumers, ecosystem engineers, and dispersers of seeds and fungi. Both bilbies and bettongs were omnivorous, though their diets were distinctly different, with the bilbies focused more on invertebrates and seeds, while the bettongs consumed a greater proportion of coarser plant materials. The seed portion of the diets of both species during 2003-04 differed from a similar study three years previously, shortly after the animals had been reintroduced to Arid Recovery in 2000- 01. During 2003-04, the bilbies consumed a lower proportion of seeds of species of grasses and more of forbs, while seed consumption by bettongs narrowed to be almost exclusively the seeds of shrubs. The number of bilby and bettong diggings varied significantly both spatially and temporally, with averages of 7,530 ± 820 diggings ha-1 in Dunes, 10,560 ± 980 diggings ha-1 in Mulga, and 7,120 ± 610 diggings ha-1 in Swale. This resulted in an average of 2 to 3% disturbance of soil surface area, which is similar to or higher than reported for other Australian or overseas semi-fossorial species. The temporal variation in rates of digging was correlated with minimum daily temperatures and rainfall but not moonlight. This variation was also correlated with counts of bilby but not bettong tracks, suggesting that the temporal variability of diggings was related to levels of bilby activity. The persistence of bilby and bettong diggings differed between the three habitat types, with the majority of the diggings in the Mulga (94%) and Swale (87%) persisting for over 12 months, while Dune diggings filled much faster, with only 15% persisting over 12 months. These diggings were shown to accumulate and bury seeds and litter, and, under some conditions, enhance germination. The seeds of two plant species, the annual grass, Dactyloctenium radulans, and the shrub, Enchylaena tomentosa, germinated from bilby faecal pellets, and over a third of bilby faecal pellets contained fungal spores. Therefore bilbies have the potential to be dispersers of both seeds and fungi. All three major roles of the bilbies and bettongs in ecosystem functioning (consumers, ecosystem engineers, and dispersers of seeds and fungi) have the potential to affect the flows of organic, soil and water resources, and therefore vegetation structure and overall productivity. Soil seed bank densities differed between areas with and without bilbies and bettongs. However, the heterogeneity of the system made it difficult to confidently relate these differences to any particular effects of the bilbies and bettongs. Both bilbies and bettongs were able to locate and dig seeds buried 20 cm deep, and the caches of seed-harvester ants. Experiments showed that in areas of high digging density, 71 to 94% of seed rain accumulated and became buried in diggings. Since bilbies and bettongs have the potential to use buried seed resources, they have the potential to significantly affect soil seed banks through their consumption of seeds, redistribution of seeds through their digging activities and their interactions with other granivorous species. This study is a first step towards understanding the roles of reintroducing CWR mammals to arid ecosystems. Possible longer term effects of these reintroductions will depend on suitable regulation of animal numbers, and climatic patterns, as restorative effects of diggings would be greatest during periods of good rainfall, whereas droughts would slow restorative processes. Although the results of this research are unique for Arid Recovery, the principles of evaluating all major ecological roles of reintroduced species and their interactions with their environment could provide guidance for other reintroductions. These interactions are complex and would require longer-term studies over a range of conditions and locations to further understand the role of reintroducing CWR mammals to ecological restoration.
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Over the last 30 years declining rainfall and increased aquifer abstraction have heavily impacted water availability and ecosystems on the Gnangara Groundwater System (GGS). The mammal fauna of the area is considered to have been rich, with up to 28 terrestrial and 5 volant native species recorded since European settlement. This study investigated previous and current distribution of mammals on the GGS, and assessed potential impacts of predicted rainfall and groundwater declines on mammals. A general survey was conducted at 40 sites, and targeted trapping was undertaken for Hydromys chrysogaster and Isoodon obesulus fusciventer at wetlands. Nine native and seven introduced terrestrial mammal species were recorded during the general survey and capture rates were very low (1.05%). The most commonly captured native species was Tarsipes rostratus. There is evidence that only 11 (9 recorded and 2 considered to be extant) of the 28 historically recorded terrestrial native mammals still persist in the area. The species predicted to be most susceptible to rainfall and groundwater level declines include H. chrysogaster, I. obesulus fusciventer, and T. rostratus. Management and recovery actions required to protect mammals under predicted climatic changes include identification and maintenance of refugia and ecological linkages, supplementation of lakes, development of ecologically appropriate fire regimes, and control of predators.
Article
Analysis of 48 faecal samples of lsoodon obesulus, collected over three seasons from Huonville in southern Tasmania, revealed prey representing 36 plant and invertebrate taxa. I. obesulus appears to be a qualitatively opportunistic omnivore feeding on a wide range of invertebrate and plant material. Quantitatively, in terms of type of prey, a large number of disparities exist between arthropod prey items in the diet and in pitfall traps and soil samples. Principal invertebrate items comprised Formicidae, Scarabaeidae larvae, Staphylinidae beetles, Calliphoridae larvae and Araneae. Major plant items were grasses, seeds, clover root nodules, Gasteromycete and Zygomycete fungi. The diet appeared to reflect seasonally and locall y abundant food items.
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This paper, an integration of history, ecology and zoogeography, is based on a comprehensive search for firsthand (eyewitness) information from navigators' and explorers' journals (1658-1875), colonists' accounts (1829-1889) and later settlers' records and oldtimers' recollections (1890-2006). Pertinent data for 37 conspicuous vertebrate species (10 bird, 26 mammal and 1 snake species) were collated, analysed, and integrated with more recent scientific information. Much of the information discovered in colonial records and obtained from interviews with oldtimers has been neglected by zoologists and ecologists. The original distributional limits of many of the species studied were thus clarified and redetermined. Detailed information is also provided on the history of the introduction of 14 mammal species into south-west WA, in order to assess their potential contribution to the extinction of native vertebrate species. The introduction, spread and density in bushland of commensal and livestock species does not correlate with the chronology of declines of native species. Changes in geographical distrbution of species were assessed against an interpretive framework of 29 factors, and based on this analysis, a conceptual model (termed the 'fusion' model) of mammal declines and extinctions in south-west and adjacent parts of WA since European settlement is proposed. The reconstructed sequence of events commenced in the 1880s, with declines being caused by disease (10 species estimated to have become totally extinct in WA and 8 species abruptly reduced in abundance and distribution). Another 12 species subsequently reached near-extinction status, following establishment of the fox in the 1920s. Trapping of some species for their fur and accidental poisoning by rabbit baits contributed to local extinctions but were not finally decisive factors. The conceptual framework adopted, based on detailed examination of the information discovered, recognizes three tiers of relevant factors. Only one or two main factors operate at one time, with some of the remaining factors acting in a subsidiary way, and sometimes concurrently or sequentially. Dominant factors are not necessarily the same for each species. Factors usually affected species adversely. South-west WA, despite being settled by Europeans earlier than most other parts of Australia, experienced a stagnant economy, slow population growth and hence minimal clearance of the original vegetation until the 1890s. The anthropogenic factors identified as significant in the decline and depletion of the native fauna, together with an understanding of their correct sequence of operation, provide a historically appropriate conceptual model that may be applicable elsewhere in Australia. The baseline data and historical accounts provide a resource for specialists working on particular species, and include much new material relating to the pelt industry and pest control activities.
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Trap-derived data are not suitable for home range studies in heathland and results of habitat selection studies of this species using trapping data need cautious interpretation. Isoodon obesulus inhabiting the heathland were not territorial and some individuals had ≥1 nest. Location of the nest(s) appeared to influence the level of selection exhibited by an individual for different vegetation types. In this heathland I. obesulus was predominantly diurnal. -from Author
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The impact of urbanisation is delayed for many species, as populations that manage to survive the initial loss of habitat gradually decline throughout the urban–bushland mosaic. Yet many species’ chances of persistence within urban areas can be increased through relatively simple management techniques, and an understanding of how remnant populations use the interface between urban and natural landscapes is therefore crucial to their long-term management. Here we examine the habitat preferences of a semi-urban population of long-nosed bandicoots (Perameles nasuta) that inhabits a matrix of urban open lawn and dense native heath macrohabitats. We radio-tracked animals in these two distinct macrohabitats and compared the microhabitat features between core and peripheral areas of home ranges. Core and peripheral areas did not differ in their characteristics for either macrohabitat; however, individuals showed a high level of fidelity to distinct foraging patches. We then related microhabitat features to an index of foraging activity using generalised linear modelling and found that diggings were more abundant in areas with moist, soft soils close to cover. Soil softness and moisture were experimentally increased via artificial watering on selected sites. After only 10 days there were significantly more diggings on watered than non-watered sites. Thus, bandicoots appear to be a matrix-sensitive species, using some open grass areas of the matrix but requiring the vegetation cover of remnant bush. We suggest, however, that artificial watering and additional cover may be one way to increase foraging opportunities to make this, and other semi-urban, populations matrix-occupying, and thus facilitate bandicoot persistence in the urban mosaic.
Article
An emerging area of interest in geomorphology over the past two decades has been the effects of biota on ecosystem processes. We examined the roles of a range of vertebrates on soil disturbance in two markedly different environments, the semi-arid woodland of eastern Australia and a Chihuahuan Desert grassland–shrubland in the south-western United States. Foraging pits of soil-disturbing vertebrates varied markedly from small scratchings of heteromyid (mainly Dipodomys spp.) rodents (1.8×10−4m3) to deep (1.0×10−2m3) excavations of the burrowing bettong (Bettongia leuseur) and greater bilby (Macrotis lagotis). Vertebrates moved substantial volumes of soil in both environments, and activity was highly temporally and spatially variable. At large spatial scales, soil disturbance by echidnas (Tachyglossus aculeatus) and Gould's sand goannas (Varanus gouldii) was substantially greater in communities dominated by shrubs, and where domestic livestock had been excluded. Heteromyid rodents tended to excavate more foraging pits in coarse-textured vegetation communities (both grasslands and shrublands). In both environments, foraging was concentrated close to perennial plants such as grass tussocks and tree canopies rather than in the interspaces. Foraging pits of Chihuahuan desert animals tended to be higher in labile carbon and support greater levels of infiltration, though this was plant community-dependent. Overall our results indicate that animal foraging is an important geomorphic mechanism capable of mobilizing substantial volumes of soil in arid and semi-arid environments and with potential effects on soil function.
Article
Isoodon obesulus exhibits geographic variation in body size and shape, which appears to be adaptive. The geographic range of this species is declining, so the presence of adaptive divergence is of concern for the conservation of this species, both in the long term (loss of diversity decreasing evolutionary potential) and short term (choice of source populations for translocations). In this study, skulls of I. obesulus, both recent (animals alive within the last 100 years) and fossil (a few thousand years old), were examined and a range of measurements obtained. Comparisons were made between the two data sets to see whether skull morphology has changed over this relatively short period. Such a change may indicate rapid evolution of these characters and therefore the potential for fast regeneration of any lost geographic variation. Fossil skulls were smaller than their recent counterparts, had shorter ‘snouts’ relative to skull width and depth, and displayed no geographic variation in size and shape, whereas recent skulls were geographically differentiated. Because of the apparent rapid evolution in these characters, the implications of adaptive variation in size and shape inI. obesulus with regard to its conservation may be strictly short term, since any geographic variation lost may be quickly recovered if suitable conditions exist.
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The woylie (Bettongia penicillata) was once common and abundant over the southern third of the Australian continent. Since European settlement the range of this rat-kangaroo has become reduced by more than 97%, and until the early 1990s, only 3 small natural populations remained, all in south-western Australia. These medium-sized (c. 1 kg) marsupials create a large number of diggings as they forage for the hypogeous fruiting bodies of ectomycorrhizal fungi upon which they feed. The effect of such foraging activity on the availability of plant nutrients in the vicinity of such diggings was evaluated in simulated digging experiments. Available nitrate, ammonium, and sulfur decreased significantly 3 years after diggings were constructed and had filled in, whereas phosphorus, potassium, iron, and organic carbon remained unchanged. The results suggest that preferential water infiltration via woylie diggings leads to a decrease in those soil nutrients that are susceptible to leaching and indicates that digging vertebrates may influence the distribution of surface soil nutrients.