Digging and Soil Turnover by a Mycophagous Marsupial

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Journal of Arid Environments Journal of Arid Environments 56 (2004) 569–578 www.elsevier.com/locate/jnlabr/yjare

Digging and soil turnover bya mycophagous marsupial

Mark J. Garkaklis*, J.S. Bradley, R.D. Wooller Biological Sciences and Biotechnology, Murdoch University, Western Australia 6150, Australia

Received 21 October 2002; received in revised form 17 March 2003; accepted 7 April 2003

Abstract

The woylie Bettongia penicillata is a small (1 kg) kangaroo-like marsupial that digs to obtain the fruiting bodies of fungi. The number of woylies in a 60 ha area of sclerophyll woodland in south-western Australia was estimated using mark-recapture at 3 month intervals over 3 successive years. The number of new diggings by woylies, determined at the same intervals, allowed an assessment of the rate of digging per individual. This varied three-fold from 38 to 114 diggings per individual per night, with no consistent seasonality. On average, each woylie displaced 4.8 tonnes of soil annually. r 2003 Elsevier Science Ltd. All rights reserved.

Keywords: Population size; Bettongia penicillata; Sclerophyll woodland; Biopedturbation

1. Introduction

Digging and burrowing are behaviours common to manymammals, particularly in arid and semi-arid ecosystems (Kinlaw, 1999; Whitford and Kay, 1999). For example, the heteromyid rodents, gophers and prairie dogs of North America (Steinberger and Whitford, 1983; Heske et al., 1993; Mooneyand Hobbs, 1994, pp. 73–81; Guo, 1996) porcupines and ibex in Israel (Gutterman and Herr, 1981; Yair and Rutin, 1981; Gutterman, 1997; Alkon, 1999) badgers in Europe (Neal and Roper, 1991, pp. 89–106) aardvark and porcupine in southern Africa (Dean and Milton, 1991; Devilliers and van Aarde, 1994) and the potoroid rat-kangaroos in Australia (Claridge and May, 1994; Garkaklis et al., 1998, 2000) all dig or burrow.

*Corresponding author. Tel.: +618-9360-2400; fax: +618-9360-6303. E-mail address: [email protected] (M.J. Garkaklis).

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Whilst burrowing is a behaviour that mayprovide an animal with shelter or a refuge, digging is primarilya foraging activity.For instance, animals dig the soil when caching or accessing hypogeous fungi, bulbs and insects (Whitford and Kay, 1999). Diggings themselves could be considered a disturbance event, since the energy expended bythe animal results in a turnover of the soil at the point of the digging and leaves a number of small holes over the soil surface. Digging byvertebrates, referred to as pedturbation or biopedturbation ( Whitford and Kay, 1999), is now considered to be an important variable in ecosystem function (Dickman, 1999, pp. 113–133; Kinlaw, 1999; see also Jones et al., 1994, 1997; Wright et al., 2002). Biopedturbation is common among manytaxa and ecological communities worldwide and affects geomorphology, soil characteristics, hydrology, vegetation communities and animal diversityat scales from the microsite to the landscape (Kinlaw, 1999; Smith and Foggin, 1999; Whitford and Kay, 1999). Its impact is likelyto be a function of the amount of digging and the distribution of diggings across the landscape. The foraging activityof digging mammals has been measured as the number of disturbances or diggings per unit area (Whitford and Kay, 1999). However, this does not allow an assessment of the overall rate of digging, nor the digging activityper individual. Information on the population dynamics of organisms in relation to their digging regime requires a population estimate for the digging species. This studyquantiﬁed the rate and distribution of digging bythe brush-tailed bettong or woylie (Bettongia penicillata) in a woodland ecosystem in south-western Australia. Woylies are a small (ca. 1 kg) kangaroo-like marsupials which feed extensivelyon the hypogeous fruiting bodies of ectomycorrhizal fungi (Christensen, 1980; Lamont et al., 1985; Claridge and May, 1994; Johnson, 1994a; Claridge and Barry, 2000). In so doing, theymake a number of small, easily recognizable holes to a depth of approximately15 cm ( Garkaklis et al., 1998). Previous studies of the diggings of this mammal have shown that theyalter soil characteristics and water inﬁltration within their habitat (Garkaklis et al., 1998) and mayredistribute nutrient resources between trophic levels within ecosystems (Garkaklis et al., 2000; Garkaklis et al., in press). Once common and abundant across the southern third of Australia, woylies are now reduced to three small natural populations in the south-west of Western Australia (Start et al., 1995). An increase in their numbers in recent years provided an opportunity to study the digging behaviour of a small marsupial that was, until recently, threatened with extinction.

2. Methods

The studywas in Dryandra Woodland (32 480S, 116540E), a low, open eucalypt woodland, 210 km south-east of Perth, Western Australia. This region experiences a mediterranean climate with cool, wet winters and hot, drysummers. Mean annual rainfall is approximately580 mm, most of which falls during winter, but unpredictable summer rainfall associated with thunderstorms can also occur ARTICLE IN PRESS

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(Coates, 1993). Descriptions of the soil and vegetation are found in McArthur et al. (1977), Coates (1993) and Garkaklis et al. (1998, 2000). The size of a small open population of woylies was estimated over 11 trapping sessions, each four nights long, apart from sessions in April 1995 and May1997 which were reduced to three nights due to inclement weather, at approximately3 month intervals from January1995 to August 1997. Four Tomahawk cage traps, baited with a mixture of rolled oats, peanut butter and molasses, were set at 100 m intervals along each of six transects spaced 250 m apart. A boundary strip of half the distance between traps was included to give an effective trapping grid of 60 ha. All animals captured were marked with numbered ear tags and released at their point of capture. The individual numbers of recaptured animals were recorded. Population estimates were made with the JollySeber stochastic model for open populations (Seber, 1982, 1986; Pollock et al., 1990), using a FORTRAN program adapted from Krebs (1989). Confidence intervals for these estimates were calculated using the method of Manly(1984) . It was not assumed that natural mortalitywas absent from the population. However, recruitment within a single trapping session was considered low since each session was short in comparison to the dispersal of young (see Sampson, 1971; Lee and Ward, 1989, pp. 105–115), and the number migrating into the surveyarea is limited bythe territorial behaviour of individuals alreadywithin the studysite ( Christensen, 1980). Most foraging digs at Dryandra are made by woylies (Garkaklis et al. 2000). The number of diggings was estimated using a modified method of Christensen (1980). All the diggings in eight permanentlymarked 10 m Â 10 m quadrats were filled-in. The quadrats occurred within the trapping grid and were distributed at random. The number of new diggings that appeared were counted and filled at intervals that coincided with each trapping session. This provided an estimate of the number of new diggings as a function of time. The amount of soil excavated was estimated using the dryweight of soil from the average size of the diggings ( n ¼ 15) on each sampling occasion. A Kruskal–Wallis test was used to determine if significant differences in the number of diggings occurred between each three monthlysample (Zar, 1984). Non-parametric Tukey-type multiple comparisons (Zar, 1984), using the calculated mean ranks were used in a posteriori analyses. Statistical analyses of the digging data were performed using the appropriate modules of the STATISTICA data analysis package (StatSoft, 1995). The spatial distribution of diggings was determined from the T-square distribution index (Besag and Gleaves, 1973). The hypothesis of a random spatial pattern of diggings was tested using Hines’ test statistic (Hines and Hines, 1979). Each digging measured was selected using a table of random numbers to determine both distance and direction to the random point within the animal trapping grid. Diggings were onlyselected if their spoil appeared to be fresh, their edges were sharp and theywere relativelyfree of plant litter and debris. The distributions of diggings were examined during each trapping session in 1995 in order to determine anychanges in the pattern of diggings as a function of season. Digging distributions were onlyexamined twice yearly in 1996 and 1997. ARTICLE IN PRESS

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3. Results

The estimate of the size of the woylie population in the survey area ranged from 20 individuals in July1995 to 49 in October 1996 ( Fig. 1). Overlap of 95% confidence intervals occurred for manyof the trapping estimates, although population estimates for Julyand October 1995 were significantlylower than January1995 and April, July and October 1996 (Fig. 1). This indicates that the number of woylies in the survey area changed over time. The effective trapping grid covered an area of 60 ha, which was equivalent to an area of 1.2–3.0 ha per individual if occupied singlyand exclusively. The total number of new diggings ranged from 1272 S.E. per 100 m2, for the 3 month period up to April 1995, to 3978 per 100 m2 for the 3 months up to April 1996 (Fig. 2). These values equate to a total new digging rate of 5000–16,000 new diggings ha1 year1. There was a significant difference in the mean total diggings as a function of sampling period (p ¼ 0:0003), indicating that digging activityin the woodland was not constant over time (Fig. 2). However, non-parametric a posteriori analysis found that a significant difference occurred only between the April 1995 value and all other sampling periods after July1995 ( Fig. 2). Distributions of all categories of woylie diggings in all determinations in 1995, 1996 and 1997 were clumped. The aggregate associations determined were highlysignificant in all cases (Hines statistic 1.352–1.436, po0:005). The digging rate for woylies in the survey area varied three-fold from 14,047 diggings per individual per year in April 1995 to 41,812 in October 1995 (Fig. 3). This corresponds to a digging rate of 38–114 diggings per individual per night (Table 1),

Estimated population size 10

0 Jan. Apr. Jul. Oct. Jan. Apr. Jul. Oct. Jan. May Aug. 1995 1996 1997 Trapping Date Fig. 1. Jolly Seber population estimates for woylies as a function of trapping period in Dryandra, Western Australia. Bars show 95% intervals based on the method of Manly(1984) , which generates uneven conﬁdence limits around each estimate. ARTICLE IN PRESS

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Total new digs 20

0 Jan. Apr. Jul. Oct. Jan. Apr. Jul. Oct. Jan. May Aug. 1995 1996 1997 Survey date Fig. 2. Average number of woylie diggings counted per quadrat. Bars represent standard errors.

45000

40000

35000

30000

25000

20000

15000

Annual digging rate (digs/individual/year) 10000 Jan.Apr. Jul. Oct. Jan. Apr. Jul. Oct. Jan.May Aug. 1995 1996 1997 Survey date Fig. 3. Annual digging rate for woylies estimated at each trapping period, Dryandra, Western Australia. Bars represent standard errors.

equivalent to 4–11 diggings per hour over an average 10-h foraging period. Soil turnover over the 3-year period ranged from 2.7 tonnes woylie1 year1 in January 1997 to 9.7 tonnes woylie1 year1 in October 1995 (Table 1). The average annual soil turnover was 4.8 tonnes woylie1 year1. ARTICLE IN PRESS

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Table 1 Digging rates and soil turnover

Sample period Mean7S.E. mass (g dry Digging rate (digs Soil turnover weight) per digging individual1 night1) (tonnes.individual1 year1)

April 1995 243777 38 3.4 July1995 164 737 61 3.6 October 1995 2327108 114 9.7 January1996 181 740 101 6.7 April 1996 203748 68 5.1 July1996 220 7118 51 4.1 October 1996 246770 39 3.5 January1997 194 775 47 2.7 May1997 156 730 67 3.8 August 1997 198758 71 5.2

4. Discussion

The densityof woyliesdetermined in this studywas 4–10 times greater than the 0.07 woylies ha1 recorded for the same woodland by Sampson (1971), but differences in methodologyand changes to woylie conservation practices make direct comparisons difﬁcult. A large increase in densitywas expected due to the feral predator management programs that were introduced in 1981. Christensen (1980) estimated a value of 0.45 woylies ha1 in their favoured habitat in the Perup Fauna PriorityArea, near Manjimup in Western Australia, prior to extensive feral predator management in the area. Once again, the sampling methodologyused in the Perup studydid not allow for an estimation of the population size using the models employed in the current study (Christensen, 1980). Intriguingly, an increase in the rate of digging per animal appeared to precede an increase in the size of the woylie population. Further information is currentlybeing collected to conﬁrm if resource- rich periods, with a higher digging rate, are followed bya population increase. Indeed the opposite scenario maybe true. Woyliesat low population densities may need to dig much more during periods of low resources, and dig less when food is more abundant and easyto obtain. Comparative data for the individual digging rates of other Australian mammals are limited. Mallick et al. (1997) used the number of diggings of the Eastern-barred Bandicoot Perameles gunnii as an index for the overall population size. Theyshowed a positive relationship between the total number of animals trapped over a 5-day period and the number of new diggings estimated using line transect methods. No data on the digging rate per individual were located for comparison with the present study, which coupled population estimates with digging rates to allow an estimate of the averaging digging rate per individual. However, the densities of diggings recorded for several other mammal species (Whitford and Kay, 1999) are summarized in Table 2. ARTICLE IN PRESS

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Table 2 Densityof foraging digs bymammals

Species Diggings produced Region Reference (No. ha1)

B. penicillata Woylie 5000–16,000 per year Western Australia This study B. gaimardi Tasmanian est. 3000 maximuma Tasmania Johnson (1994c) bettong P. tridactylus long-nosed est. 2250 per yearb Southeastern Claridge et al. (1993) potoroo Australia Heteromyid rodents 37,200 per 0.3 year Chihuahuan Desert, Steinberger and USA Whitford (1983) Hystrix indica Indian 100–1000 Negev Desert, Israel Alkon and Olsvig- porcupine Whittaker (1989) H. indica Indian 100–1700 Negev Desert, Israel Yair and Rutin (1981) porcupine H. africaeaustralis Cape 19–52.7 South Africa Devilliers and Van Aarde porcupine (1994) Cyanomys ludovicianus 37,000–65,000 Prairie, USA Whitford and Kay(1999) Prairie dog Otocyon megalotis bat- 94 South Africa Dean and Milton (1991) eared fox and Orycteropus afer aardvark

The data are number of diggings per unit area or digging rate per unit area. Woylie data are from this study, other data from Whitford and Kay(1999) . a Tasmanian bettong digging densities have been estimated from data in Johnson (1994c). b Long-nosed potoroo digging densities have been estimated from data in Claridge et al. (1993).

The number of foraging digs per unit area has been determined for two other potoroids, the Tasmanian bettong B. gaimardi,andPotorous tridactylus the long- nosed potoroo. Digging densities in the preferred habitat of the Tasmanian bettong ranged from approximately500 ha 1 to about 3000 ha1 (Johnson, 1994b, c), whilst the maximum digging rate for the long-nosed potoroo was 2250 ha1 year1 (Claridge et al., 1993). The data for the Tasmanian bettong were recorded over a 1-month period and the rate of digging was not calculated (Johnson, 1994c), whilst the digging densities of the long-nosed potoroo were estimated over a 2-year period (Claridge and Cunningham, 1993; Claridge et al., 1993). Woylie foraging activity, based on the number of digs per unit area, appeared intermediate between these other potoroids and the heteromyid rodents and prairie dogs of North America, but greater than porcupines (Table 2). However, heteromyid rodent digging activityis highlyseasonal, with most diggings appearing over a 3.5- month period (Steinberger and Whitford, 1983). It is unclear if prairie dog digging is also seasonal. If this were true, then the number of foraging digs per unit time would be much greater for both heteromyid rodents and prairie dogs than for woylies during the period of maximum digging activity. Woylies showed no consistent seasonalityin digging activitythat might be related to seasonal breeding or ARTICLE IN PRESS

576 M.J. Garkaklis et al. / Journal of Arid Environments 56 (2004) 569–578 availabilityof hypogeous fruits. For instance, although the highest rate of digging occurred in October 1995, the rate in the following October was verylow. The clumped distribution of woylie diggings identified in this study is similar to the distribution of diggings bythe Tasmanian bettong ( Johnson, 1994c). ‘‘Fine scale’’ measurements of Tasmanian bettong diggings indicated that theywere associated with the stems of Eucalyptus tenuiramus and Acacia dealbata trees, with the densityof diggings directlyrelated to the densityof stems ( Johnson, 1994c). Both Johnson (1994c) and Taylor (1993) suggest that the biomass of ectomycorrhizal roots, and hence the density of hypogeous fruits, is directly related to stem density. The similar fine scale pattern of woylie diggings may also result from a direct relationship between tree stems and hypogeous fruits. However, this could not be confirmed due to difficultyin finding fruits, which appeared to be verypatchy.

Acknowledgements

We thank the Western Australian Department of Conservation and Land Management for access to Dryandra Woodland. This study was supported by a Murdoch UniversityResearch Scholarship.

References

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