Intersite Differences in Population Demography of Mountain

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Biological Conservation 102 (2001) 309–323 www.elsevier.com/locate/biocon

Intersite diﬀerences in population demography of Mountain Pygmy-possums Burramys parvus Broom (1986–1998): implications for metapopulation conservation and ski resorts in Koskiuszko National Park, Australia

Linda S. Broome* NSW National Parks and Wildlife Service, PO Box 2115 Queanbeyan, NSW, 2620, Australia

Received 23 March 1999; received in revised form 23 February 2001; accepted 16 March 2001

Abstract Small, local populations of the endangered Mountain Pygmy-possum Burramys parvus occur on the Koskiuszko Plateau, in south-eastern Australia, including within ski resort lease areas. Between 1986 and 1998 four populations, two within and two outside ski areas, were studied to assess their dynamics and to determine if ski resort management was likely to impact on the conservation of the species. One of the resorts, at Mount Blue Cow, was constructed as the study commenced. Analysis of the 11–12 year data sets showed strong site differences in sex ratios, annual and winter survival rates, site persistence, recruitment and spring weights. Regional trends, attributed to exogenous climatic factors, were evident but population fluctuations were generally uncorrelated and strong site by year interactions occurred for most demographic parameters. Despite this, strong density dependence on all sites in recruitment and to a lesser extent annual survival suggest B. parvus is habitat limited and that social factors drive demographics in these populations. There was no evidence that the ski resort at Mount Blue Cow had any significant impacts above natural yearly variation in demographics in the first 11 years of its operation. However, the highest quality sites, in terms of population size and stability, were those within the two ski resort lease areas. Further, the asynchronous population dynamics, a small amount of migration between habitat patches, differences in site quality and heterogeneity in site structure and aspect, which may contribute to population persistence, indicates that a metapopulation approach to conservation of B. parvus on the Kosciuszko plateau is warranted. This has important implications for long-term conservation of B. parvus in the ski resort areas. These sites will require careful monitoring and management to ensure the continued viability of the resident and surrounding B. parvus populations. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: Alpine; Metapopulation; Burramys parvus; Demography; Small mammal; Ski resort

1. Introduction undergoing deep, seasonal hibernation for up to 7 months for adults and 5 months for juveniles (Geiser The Mountain Pygmy-possum B. parvus (Burramyi- and Broome, 1991; Broome and Geiser, 1995; Ko¨ rtner dae:Marsupialia; 40 g) is endemic to alpine and sub- and Geiser, 1998; Walter and Broome, 1998). Small, alpine areas of south-eastern Australia (Happold, 1989). local populations inhabit patches of periglacial block- All populations occur above the winter snowline, streams, blockfields and other boulder formations approximately 1500 m elevation on the Kosciuszko (Rosengren and Peterson, 1989). These rocky sites plateau of New South Wales (NSW), and in the adja- (herein collectively termed boulderfields) frequently cent high country of Victoria. (Caughley, 1986; Broome have associated with them a shrubby heathland, char- and Mansergh, 1989; Mansergh and Broome, 1994; acterised by an endemic, fruit-bearing conifer, the Heinze and Williams, 1998; Osborne et al., 2000). It mountain plum pine Podocarpus lawrencei. Dry and wet survives the extended period of winter snow cover by heathlands, fens, bogs and snow grass swards (Costin et al., 1979) surround and separate boulderfield patches. * Corresponding author. Fax:+61-2-62994281. Some of the patches at the lowest elevations or on E-mail address: [email protected] (L.S. Broome). northerly aspects on the Kosciuszko plateau extend into

0006-3207/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved. PII:S0006-3207(01)00105-7 310 L.S. Broome / Biological Conservation 102 (2001) 309–323 the Eucalyptus pauciflora treeline, while others are maturity (1 year) and birth rate (four young per litter) entirely above the treeline including near the summit of are constant and even during recruitment peaks the the tallest peak on the Australian mainland, Mount majority of females carry pouch young. A usual litter Kosciuszko (2228 m). size of four results from production of supernumary The seeds and fruit of P. lawrencei, along with those neonates, although there is some evidence that litter size of Leucopogon spp. (NSW) and Rubus spp. (Victoria) may be less than four in adverse conditions (Mansergh provides a substantial part of the autumn diet of B. and Scotts, 1990; Broome et al. unpubl. data). Never- parvus. The principle spring and summer diet is pro- theless, the demographic responses which promote vided by the migratory bogong moth Agrotis infusa population change in B. parvus are likely to be strongly (Mansergh et al., 1990; Smith and Broome, 1992; D. dependent on survival and annual recruitment rates. Heinze, pers. comm. March, 2000). These moths (approximately 25 mm head–body length) arrive in the 2.2. Study sites and trapping high country often in huge numbers in early spring to aestivate in cool crevices among the boulders and depart Study sites were located within the Mount Blue Cow for their low-elevation, winter breeding grounds in and Charlotte Pass ski resort lease areas and at the autumn (Common, 1954). Paralyser and Summit Road (Fig. 1). At Mount Blue The B. parvus population on the Kosciuszko plateau is Cow, boulderfields on the south-east face of the moun- entirely within Kosciuszko National Park. However, tain contain most of the high quality B. parvus habitat populations occur within ski resort lease areas which are and breeding females in the area (Broome, 1992, 2001). heavily used for winter snow sports. When this study These boulderfield patches total approximately 5.0 ha began, little was known of the population ecology of B. and extend from ca. 1800 m to near the peak of Mount parvus or of the relative value of the habitats within ski Blue Cow (1985 m). The Charlotte Pass monitoring site resort lease areas. was a single, large 3.4 ha blockfield situated on the The aim of this study was to investigate the population dynamics and structure of four local populations of B. parvus, two within and two outside ski resort lease areas, to determine if ski resort activities were likely to impact on the conservation of the species in Kosciuszko National Park. The impetus for the research was provided by construction of one of the ski resorts, at Mount Blue Cow, as the study began in 1986.

2. Methods

2.1. Reproductive cycle of B. parvus

B. parvus have an annual reproductive cycle. Mating occurs following snow melt in the Austral spring (October–November in the Kosciuszko area). Females produce a single litter of four pouch young in late November–early December, carry them in the pouch for around 35 days and suckle them at a nursery nest site for a further 30–45 days. Young become trappable from mid-January and both sexes are able to attain sexual maturity at 1 year of age (Kerle, 1984; Mansergh and Scotts, 1990; Broome 1992). Females are relatively sedentary, especially in high quality habitats. More than 75% of adult and subadult male B. parvus migrate from breeding areas by late summer (January) and juvenile males and some juvenile females disperse after weaning (February–April) to over-winter at sites which are at lower elevations or on more westerly or northerly aspects (Mansergh and Scotts, 1989, 1990; Broome, 1992; Walter, 1996; Ko¨ rtner and Geiser, 1998; Broome, Fig. 1. The distribution of B. parvus habitat and locations of study 2001). Generations per year (one), age at sexual populations in Kosciuszko National Park. L.S. Broome / Biological Conservation 102 (2001) 309–323 311 north side of the valley (south-easterly aspect) at Char- referred to collectively as adults/subadults. Record was lotte Pass Village (1740–1765 m). A series of three also taken of the sex, reproductive condition, weight, smaller boulderfields at the same elevation 500 m across presence of parasites and any signs of wounding or dis- the valley on the south side (Fig. 1), the Charlotte Pass ease, and the animals were released at their sites of ‘male site’, was trapped at irregular intervals to detect capture. movements but was not included in the monitoring An access road to Mt. Blue Cow was constructed regime. The Summit Road site (1870–1920 m) consisted before the study began. Major construction work on the of four blockstreams, spaced at 100–500 m apart with resort infrastructure began during November 1986. The intervening shrubby heath along a 1 km section of the resort was partially opened for skiing during winter Koscuiszko summit road (Fig. 1). The total area of 1987 and became fully operational during winter 1988. boulderfields at the site was approximately 2 ha and the site had a north-westerly aspect. The Paralyser site con- 2.3. Data and statistical analysis sisted of one blockstream (0.7 ha) with a southerly aspect below the trig of The Paralyser (Paralyser 1) Data presented here are December (early breeding (1810–1850 m) and a series of blockfields and block- season) estimates. Population sizes with 95% confidence streams 800 m away in the next valley, on the lower intervals were estimated using the heterogeneity model slopes of Mount Perisher (Paralyser 2; 1790–1840 m). (Mh) in program CAPTURE (White et al., 1978), which This sub-site had a boulderfield area of approximately is relatively robust to small sample sizes, especially when 1.7 ha and a south-westerly aspect. capture probabilities are high (White et al., 1982). Trapping was carried out annually during early Numbers trapped were sufficient to derive population December from 1986 (Mount Blue Cow) and 1987 size estimates separately for females and males on Blue (other sites) until 1998. To mark juveniles and assess Cow and Charlotte Pass, but only for sexes combined winter survival, trapping was also conducted during on Summit Road and Paralyser, for which the minimum March–April from 1986 until 1990, and from 1996– numbers of each sex known to be alive (KTBA) are also 1998. Traplines were placed within the boundaries of presented. KTBA’s are ‘filled’ data (i.e. an animal trap- boulderfields, which radiotracking at Mount Blue Cow ped in period 1 and 3 is assumed to be in the population showed effectively represented the habitat area. Traps in period 2, Petrusewicz and Andrezejewski, 1962). Such (Elliott Scientific Equipment, Upwey, Vic Australia methods of direct enumeration are reliable as long as aluminium live-capture traps) were spaced at 5–10 m capture probabilities are high (Hilborn et al., 1976). In intervals, sufficient to ensure that at least 10 traps were this study, KTBA’s differed little from the numbers present in each B. parvus home range (Broome, 1992, trapped (N) or the population size estimates Nˆ (see 2001). One hundred and ninety traps were located at Section 3). However, KTBA’s were necessary for calcu- Mount Blue Cow, 100 at Charlotte Pass and at Summit lating annual and winter survival rates, whereby indivi- Road; and 90 at Paralyser (45 at Paralyser 1, 50 at duals were tracked through years, and are therefore Paralyser 2). Traps were baited with walnuts (or on the used for all demographic analyses. Statistical analyses first day chocolate if collecting scats for dietary analysis, of demographic parameters were carried out by the Smith and Broome, 1992), insulated with Dacron bat- Statistical Consulting Unit, Australian National Uni- ting, covered with plastic bags and checked each morn- versity using GENSTAT 5 (Payne et al., 1987). Data ing for 3 or 4 (if baiting with chocolate) consecutive from 1986 to 1997 were used in most demographic ana- days. All trapped B. parvus were individually marked lyses. Data from 1998, obtained after these were com- with small, ‘‘fish fingerling’’ (Utah Stamp Co.) alumi- pleted, were included in estimates of population size and nium ear tags. At each capture, the number on the ear- for density dependence models. tag of the individual was recorded (recapture), or an Demographics were analysed using regression models eartag was fitted if no tag present (new capture). Each for sites separately to examine year, sex or age effects animal was classified as either:juvenile (young-of-the- and on combined sites to examine site and site by year year), subadult (1-year-old) or adult (2 or more years effects. Sex ratios (the proportion of females) were old). Juveniles (trapped between February and May) modelled using logit regression assuming a binomial were easily distinguished by their small size, grey pelage distribution. Differences in cumulative site persistence and undeveloped pouch or scrotum. One-year-old B. (i.e. minimum age structure) profiles of females and parvus are generally smaller, lighter and more grey in males were examined using an ordinal (proportional colour than adults and do not reach adult size until their hazards) model. Survival estimates were based on second year (Broome, 1992). However, age definition of annual and winter recapture rates. Annual survival was new individuals was not always reliable, especially for the proportion of individuals trapped in December, and males and in years when trapping was not carried out winter survival the proportion trapped in autumn and juveniles tagged in the previous autumn. Therefore, (March–April), which were present the following in most analyses non-juvenile animals are grouped and December (survival =m1/m0, with constant intervals 312 L.S. Broome / Biological Conservation 102 (2001) 309–323 between captures, Caughley, 1977). Recapture rates of tuations in population sizes (Fig. 2a–c). Some regional females are more likely to reflect survival than those of trends in population sizes were evident, with popula- males which may include an element of emigration. This tions generally low in 1992 and on all sites except is particularly likely for winter survival of juveniles, Charlotte Pass in 1994, but these fluctuations were because although most adults and subadults migrate by uncorrelated between sites (Table 1), and on all sites February and therefore winter survival is the survival of except Blue Cow, between sexes. Overall, despite annual individuals which do not migrate, juveniles may con- fluctuations, average population sizes and densities tinue to disperse until April (Broome, 1992). Survival (KTBA/ha) also differed between sites, as did the varia- was analysed using logit regression and a binomial dis- tion about the mean (co-efficient of variation of KTBA; tribution. It was assumed that unmarked B. parvus were Table 2). new recruits in each population. Annual recruitment was the number of new captures expressed as a propor- 3.2. Sex ratios tion of the total number of females in the previous year. The natural log (ln) of recruitment was modelled using As suggested by the population sizes of each sex analysis of variance. (Fig. 2a, b, d, e) the proportion of females differed 2 Body weights were modelled using REML (restricted strongly between sites (X4=25.46, P=0.000). Sex ratios maximum likelihood) variance components analysis. were biased towards females on Blue Cow, Charlotte Year 3 (1988) was omitted from the model and analysed Pass and Paralyser 2 (0.62), but were not significantly separately to obtain mean weights, because trapping different to parity (P<0.05) on Summit Road and that year was carried out over a 3 week time span, with Paralyser 1 (0.44). Some movement of individuals, pre- Summit Road trapped earlier than the other sites. This dominantly males and juveniles, occurred between P1 would have made a large difference to the size of pouch and P2 and when analysed as one habitat unit, the sex young and hence female weights (Broome, unpubl. ratios averaged close to parity (Fig. 3). There was little data). The extent of density dependent relationships evidence of yearly variation in sex ratios within any of between population sizes and annual survival and the sites between 1986 and 1997, although at Blue Cow 2 recruitment were investigated by regressing the annual (X11=13.4, P=0.268) there were very low numbers of survival or recruitment in year t+1 against the numbers males in 1986, Fig. 2a, and at Charlotte Pass 2 of B. parvus KTBA in year t, where the numbers on (X11=9.744, P=0.463) sex ratios were male biased in each site were standardised by the site average. 1997, Fig. 2b. Yearly variation between 1986–1997 was 2 slight at Summit Road (X11=4.31, P=0.932) and at 2 Paralyser (X10=5.962, P=0.818). 3. Results 3.3. Site persistence, longevity and age structure 3.1. Population size For both females (Fig. 4a) and males (Fig. 4b), the Annual population size estimates with confidence majority of individuals (60–80%) were trapped in 1 year intervals are shown on Fig. 2a–c. Differences between only. A high proportion of these individuals were sub- population size estimates and KTBAs were slight, aver- adults (see Fig. 5). However, up to 20% of individuals aging 1.32Æ2.9 individuals and ranging from 0.3 (Blue were trapped in 2 years and 10% over a period of 3 or Cow females) to 3.1 (Summit Road). This indicates that the KTBAs closely approximated total population sizes. B. parvus were easily trapped, with average capture Table 1 Correlation matrix for the population size estimates shown on Figs. 2a, probabilities of 0.58–0.68 across the four sites, and were b, d, e 1987–1997a (F=female; M=male; BC=blue cow; CP=Charlotte attracted by traps as shown by initial capture prob- Pass; SR=Summit road; PA=paralyser) abilities of 0.42–0.58 and recapture probabilities of 0.78–0.92. Results from program CAPTURE usually BC-F BC-M CP-F CP-M SR-F SR-M PA-F indicated population closure, and frequently indicated BC-F 1 for Charlotte Pass and Blue Cow that ‘most of the BC-M 0.66* 1 population has been seen’. Reliability of the estimates CP-F À0.23 À0.30 1 CP-M 0.20 À0.16 0.22 1 was sometimes lower on the other two sites. For exam- SR-F À0.02 À0.04 À0.21 0.50 1 ple, a high population estimate and high variance at SR-M 0.42 0.35 À0.44 0.22 0.39 1 Summit Road in 1997 was caused by an influx of 10 new PA-F 0.42 0.02 À0.18 0.42 0.19 0.55 1 animals (including a male recapture from a previous PA-M À0.02 À0.18 0.56 À0.07 À0.22 À0.46 0.13 trapping session) on the last day of trapping, but the a (n=12, critical value of the correlation coefficient r10 0.05=0.58, number trapped (27) was the same as in 1987 and 1991. r10 0.01=0.71). However, on all sites there were significant yearly fluc- *Significant at P<0.05. L.S. Broome / Biological Conservation 102 (2001) 309–323 313 more years. Females were more likely to remain longer old when last trapped in December 1999, the only year in the population than males (sex adjusted for site, that she did not breed. The oldest male, from Blue Cow, 2 X1=16.84, P=0.000). Site persistence also varied was 5 years old. 2 between sites (site adjusted for sex, X3=14.91, A breakdown of population sizes (KTBA) by age and P=0.002), with individuals of both sexes persisting recapture indicated that much of the variation shown in longer at Charlotte Pass than at the other sites (t=3.04). Fig. 2 was due to fluctuations in the numbers of new Females generally remained over the shortest time per- animals (recruits) trapped each year. Variation in the iod at Paralyser (Fig. 4a), and in contrast to the other proportion of new captures between years was extreme 2 sites, were more likely than males (Fig. 4b) to be caught on Blue Cow (Fig. 5a; X10=16.49, P=0.086). This site only once (Binomial test, P<0.05). However, the oldest was characterised by recruitment pulses of pre- female (shown as 8 years on Fig. 4a), was first trapped dominantly subadult individuals in some years, and a as a subadult on Paralyser 1 in 1989 and was 11 years relatively stable number of recaptured adults (all

Fig. 2. Population sizes in early December on the four study sites, 1986–1998. Population size estimates (CAPTURE model h) with 95% conﬁdence intervals (Æ 2 S.E.):sexes separately for (a) Mount Blue Cow and (b) Charlotte Pass; sexes combined for (c) Summit Road and Paralyser. KTBA’s (sexes separately) for (d) Summit Road and (e) Paralyser. Peaks (above graphs) and lows (below graphs) in (A) annual survival, (W) winter survival and (R) recruitment rates are shown on a, b, d, e (1987–1997). Non-bracketed >2 S.E. above the mean, bracketed >1 S.E. above the mean. Sym- bols are for combined sex and age classes unless indicated otherwise, where f=female only, m=male only, j=juvenile only. Lines under years on the X-axis indicate the years during which winter survival was measured. 314 L.S. Broome / Biological Conservation 102 (2001) 309–323

Table 2 Site and sex means for demographic parameters on the four study sites

Nˆ a KTBAb CV of Density Prop Adult Winter survival Annual Recruitment KTBAc (ktba/ha) newd Wts (1986–1990,1996–1997) survival

Juvenile Ad/Sade Ad/Sade Ad/Sade

Females Blue Cow 28.7 28.5 23.3 5.7 0.56 47.0 0.47 0.65 0.44 0.60 Charlotte Pass 25.9 23.7 19.4 7.0 0.53 46.1 0.31 0.56 0.50 0.57 Summit Road 10.5 35.9 5.2 0.66 48.1 0.39 0.66 0.36 0.62 Paralyser 10.5 36.4 4.5 0.73 45.4 0.27 0.42 0.33 0.79 All sites 0.38 0.58 0.43 0.68 Males Blue Cow 15.7 13.8 36.4 2.6 0.78 40.5 0.17 0.54 0.24 0.47 Charlotte Pass 17.6 16.5 31.0 4.8 0.63 41.0 0.16 0.56 0.35 0.64 Summit Road 11.0 25.7 5.5 0.72 42.3 0.34 0.39 0.27 1.70 Paralyser 8.5 30.3 3.6 0.71 42.9 0.15 0.39 0.26 0.90 All sites 0.19 0.49 0.28 0.66

a Nˆ , estimated population size. b KTBA, number known to be alive. c CV of KTBA, coeﬃcient of variation of KTBA. d Prop new, proportion of new captures. e Ad/Sad, adult/subadult.

December–December recaptures are adults by deﬁni- ber of new animals were assigned to the adult category tion). Recruitment pulses of females were also evident each year, averaging 1–3 individuals on each site for on Summit Road and Paralyser (Fig. 5c, d), and for both males and females (average numbers of new adult males on all sites. Charlotte Pass by contrast, had an females shown on Fig. 5). extremely stable population size of females (Fig. 5b), with little variation in the proportion of new captures 2 between years (X9=8.806, P=0.455). The proportion of 2 new captures varied between sites (X3=12.57, P=0.006), with a lower proportion of new captures at Charlotte Pass compared with the other sites (Table 2). Assignment of ages to new captures was not always reliable (and errors would be more evident in the smaller populations) but most new females on Blue Cow (87%) and Charlotte Pass (75%) appeared to be subadults. This was strongly evident during the years 1987– 1990 when trapping occurred throughout the season and age estimation was most reliable (annual captures of new adults are shown for Blue Cow and Charlotte Pass on Fig. 5a, b). However, on all sites a small num-

Fig. 4. Cumulative site persistence (1987–1997) on the four sites for (a) females and (b) males. Each histogram represents the total number Fig. 3. The proportion of females (mean Æ 2 S.E.) on the study sites of individuals of each sex KTBA for the designated number of years as in early December. The horizontal line represents an even sex ratio. a proportion of all captures. L.S. Broome / Biological Conservation 102 (2001) 309–323 315

Fig. 5. The numbers of female B. parvus KTBA subdivided as newly caught or recaptured on each study site. All December–December recaptures were adults by deﬁnition. Total new individuals include adults and subadults. The mean numbers of new adults caught per year is provided for all sites but is illustrated as yearly captures only on Blue Cow and Charlotte Pass, where age deﬁnition was most accurate.

3.4. Survival and recruitment Winter survival was compared between adult/subadults and juveniles. Winter survival was higher for Annual survival rates were compared between adults females than for males of both age groups only at Blue 2 and subadults over the first 5 years of the study, when Cow (sex, adjusted for age, year X1=17.55, P=0.000), age identification was most reliable. There was no evi- but there was no evidence to suggest an overall sex dif- 2 dence that annual survival differed between adults and ference in winter survival at Charlotte Pass (X1=0.826, 2 subadults on any of the sites except at Blue Cow, where P>0.05), Summit Road (X1=2.82, P>0.05) or Paraly- 2 2 there was a sex by age effect (X3=3.99, P=0.04). Adult ser (X1=2.02, P>0.05). At Charlotte Pass there was a 2 females had higher survival rates than subadult females, year by sex interaction (X5=11.42, P=0.04; due to low while subadult males were more likely to survive than survival of females and high survival of males in 1987). adult males (no adult males were recaptured during the Winter survival was higher for adults/subadults than first five years on Mount Blue Cow; Table 3). The juveniles on all sites. The age effect was strongest at overall trend was similar on Paralyser to Blue Cow, and Charlotte Pass (age adjusted for year and sex for males on all sites (Table 3). Annual survival (combined adult/subadult over all Table 3 Annual survival rates of adult and subadult B. parvus (cumulative over years) was higher for females than males at Blue Cow a 2 years 1986–1990) and Charlotte Pass (sex adjusted for year X1=15.27, 2 P=0.000; X1=6.49, P=0.011), and to a lesser extent at Site Adult F Adult M Subadult F Subadult M 2 Summit Road (X1=3.88, P=0.05), but there was no Blue Cow 0.49 0 0.37 0.26 evidence that annual survival varied between sexes at CPass 0.45 0.11 0.52 0.27 2 Paralyser (X1=1.58, P=0.21), Table 2. Annual survival SRoad 0.37 0 0.38 0.27 2 Paralyser 0.40 0 0.29 0.36 differed strongly between sites (X3=23.44, P=0.000; with no site by sex interaction). Annual survival was Total 0.44 0.02 0.40 0.28 highest at Charlotte Pass and lowest at Summit Road and Paralyser (Table 2). a F, female, M, male. 316 L.S. Broome / Biological Conservation 102 (2001) 309–323

2 X1=22.75, P=0.000) due to relatively low survival of Recruitment rates differed between sites for males juvenile females (Table 2), and was also strong at Blue (F3,27=5.13, P=0.006), but not significantly so for 2 Cow (X1=19.36, P<0.001). The difference between females (F3,27=1.27, P=0.304), although they mirrored 2 ages was less extreme at Summit Road (X1=5.28, annual survival rates (highest at Paralyser and lowest at P=0.022) because of low survival of adult males and Charlotte Pass, Table 2). Recruitment of males was high survival of juvenile males compared with Blue Cow highest at Summit Road and Paralyser and lowest at and Charlotte Pass (Table 2), and at Paralyser Charlotte Pass and Blue Cow (Table 2). Recruitment 2 (X1=5.66, P<0.05), where there was also an age by varied strongly by year for females (F10,27=2.40, 2 year interaction (X5=12.32, P=0.03) due to a higher P=0.034) and males (F10,27=2.87, P=0.014). However, survival of juvenile females than adult females in 1997. site by year interactions in recruitment were strongly 2 Site differences (X3=12.44, P<0.01) were due to low evident (F27,27=4.48, P<0.001, Fig. 7), with extremes in winter survival at Paralyser (mean over sex and age= recruitment often occurring in different years on each 0.32), with little difference between the other sites (0.46 site (summarised on Fig. 2a, b, d, e). on Blue Cow and Summit Road, 0.42 on Charlotte Pass). Annual and winter survival varied strongly by year on 3.5. Body weights 2 Mount Blue Cow (year adjusted for sex X10=24.0, 2 P=0.008; year adjusted for sex, age X6=21.80, Body weights in December also differed strongly 2 2 P=0.001 respectively) and Charlotte Pass (X9=26.26, between sites (X3=29.6, P<0.001) and years 2 2 P=0.002; X5=33.71, P=0.000). The evidence was (X9=238.8, P=0.000), with strong site by year 2 weaker but still significant for winter survival at (X24=62.8, P<0.001) interactions (Fig. 8). Sex differ- 2 2 2 Paralyser (X9=13.11, P=0.16; X5=15.96, P<0.01) and ences (X1=97.1, P=0.000) were due to females carrying year was not significant at Summit Road (year adjusted pouch young. In most years, female weights on Summit 2 2 for sex X9=10.30, P=0.33; X5=3.57, P>0.05). How- Road and frequently at Charlotte Pass tended to be ever, sample sizes were smaller at the latter sites and a greater than those on Blue Cow and Paralyser (Fig. 8a). similar range in annual and winter survival rates occur- Heavier weights at Charlotte Pass would have been red relative to Blue Cow and Charlotte Pass (Fig. 6). influenced by a higher proportion of adults and inter- Extremes in annual and winter survival (one or two actions may have been influenced by differing propor- standard errors difference from the mean) are illustrated tions of subadults or of females carrying young. on Fig. 2a, b, d, e. Annual and winter survival rates However, analysis of a subset of the data using only were strongly correlated for adult/subadult females on recaptures (i.e. known adults and omitting those few all sites (P<0.01) except Summit Road (P< 0.10). females which had already left young in nests and were Comparison of sites indicated an overall year effect on lactating) still revealed strong site differences for females 2 2 annual (X9=27.64, P<0.01) and winter survival rates (X3=13.7, P<0.005; Table 2) and site by year interac- 2 2 (X4=27.74, P<0.001) but with very strong site by year tions (X29=45.7, P<0.05). There were no significant 2 2 interactions (site by year adjusted for sex X24=54.95, site (X3=2.4, P>0.05) or site by year interactions 2 2 P=0.000; X12=25.36, P<0.05; Fig. 6). A site by sex by (X29=34.2, P>0.05) for the very small data subset of year interaction occurred in winter survival (P=0.01) male recaptures. However, males were often heaviest at due to the sex by year interaction at Charlotte Pass; and Summit Road or Paralyser and lightest at Blue Cow site by age by year (P=0.02) due to the age by year (Fig. 8b, Table 2). interaction at Paralyser.

Fig. 7. Yearly recruitment (in December) of females on each study site Fig. 6. Annual survival (December–December) of females on each (ln numbers of new individuals in year t+1/ numbers of individuals study site (predicted probability from GENSTAT regression models). KTBA in the previous year). L.S. Broome / Biological Conservation 102 (2001) 309–323 317

Cow. Females from lower elevations moved up to 1 km during summer to access bogong moths which became concentrated on the peak, but remained at lower elevations at other times of year. Nightly and seasonal movements of up to 1.5 km from the study area to other boulderﬁeld patches on Mount Blue Cow were typical for males, with an occasional return in the same night (a 3 km minimum nightly movement, Broome 1992, 2001). Movements of a similar scale occurred between trap sites in the other study areas, with most movement undertaken by males and juveniles Males moved between Charlotte Pass and Summit Road, a distance of 2 km. One adult moved from the Charlotte Pass breeding site to Summit Road and back again during the same trapping session, and another did so between years. Others were recorded moving from the Charlotte Pass male site to Summit Road in the same season (2) and vice versa (1) and between years (1). Movements frequently occurred between the north and south side of the valley at Charlotte Pass (500–800 m). A juvenile male dispersed from Charlotte Pass in February to Summit Road in December, and one from Summit Road was retrapped 2 years later as a breeding adult at Etheridge Ridge, 2 km away on the western side of the Snowy River (Fig. 1). To avoid the river he would have had to travel around 6 km. Fig. 8. Mean weights in early December (predictions from GENSTAT Movements also occurred in both directions between regression models) on each study site for (a) females, (b) males. Lsd Paralyser 1 and Paralyser 2, a distance of 1 km. Two isÆ2 S.E. adult males were trapped on Paralyser 2 and then subsequently on Paralyser 1 within the same trapping ses- 3.6. Intersite movements sion. Four other males and juveniles of both sexes (three females, two males) moved between trapping sessions Radiotracking at Mount Blue Cow showed that adult (ﬁve from P2 to P1, four from P1 to P2). One movement and subadult female B. parvus were typically sedentary of an adult/subadult female was recorded (going from within high quality habitat near the peak of Mount Blue P2 to P1). No inter-site movement was recorded

Table 4 Correlations between annual survival, recruitment and recruitment residuals for females on the four study sitesa

BCansurvb BCrecc BCrecresd CPansurv CPrec CPrecres SRansurv SRrec SRrecres PAansurv PArec PArecres

BCansurv 1 BCrec 0.47 1 BCrecres 0.09 0.67 1 CPansurv 0.27 0.11 0.15 1 CPrec À0.04 0.24 0.19 0.71 1 CPrecres 0.33 0.23 À0.00 0.61 0.72 1 SRansurv 0.02 À0.75 À0.58 0.01 À0.16 À0.08 1 SRrec 0.21 À0.035 À0.11 0.29 0.21 0.21 0.33 1 SRrecres À0.09 0.093 À0.02 0.01 0.14 À0.16 0.14 0.77 1 PAansurv 0.31 À0.01 0.34 0.28 À0.04 0.00 0.01 0.03 À0.25 1 PArec 0.37 0.45 0.40 0.47 0.63 0.53 À0.29 0.27 0.05 0.57 1 PArecres 0.07 0.20 0.35 0.24 0.57 0.26 À0.04 0.24 0.11 0.26 0.74 1

a (n=11, critical values for correlation coeﬃcients r9 0.05=0.60, r9 0.01=0.73). b ansurv, annual survival. c rec, recruitment. d recres, recruitment residual. 318 L.S. Broome / Biological Conservation 102 (2001) 309–323

Fig. 9. Observed annual survival in year t+1 as a function of the Fig. 10. Observed recruitment in year t+1 as a function of the num- numbers of individuals KTBA in year t. Yearly KTBA’s for each site bers of individuals KTBA in year t. Yearly KTBA’s for each site are are standardised by the 11-year site mean for site comparisons. (a) standardised by the 11-year site mean for site comparisons. Equations Females; the equation is the combined sites regression, (b) males; the are the combined sites regressions (a) females, (b) males. P-values for equation is the regression for Blue Cow only. P-values for the x coef- the x coefficient <0 from the individual site regressions are provided. ficient <0 from the individual site regressions are provided. 4. Discussion between the Blue Cow, Paralyser and Charlotte Pass study sites. 4.1. Density dependence, sex and site differences

3.7. Population fluctuations and density dependence The demographics of animal populations may be influenced primarily by climatic factors, by biotic inter- Correlations of annual survival and recruitment resi- actions or by a combination of both (Krebs, 1995; Lima duals between sites showed few and inconsistent pat- and Jaksic, 1999; Madsen and Shine, 1999). Over much terns (Table 4), indicating that unexplained variance of the Australian continent, climatic extremes and was not strongly related to regional trends. The only unpredictability of rainfall cause many small mammal significant correlation between annual survival and populations to undergo irregular and variable irruptions recruitment was at Charlotte Pass (Table 4), influenced (Madsen and Shine, 1999). The Australian alpine area by a sharp, simultaneous decline in annual survival and in contrast, has a relatively stable, predictable climate recruitment in 1992 and recovery in 1993. However, on with a regular annual cycle. It is therefore likely that B. all sites recruitment and to a lesser extent annual survi- parvus populations will be more subject to density val showed direct density dependence with population dependent factors. In this study, regional influences sizes in the previous year (Figs. 9, 10). Annual survival (year effects) in population size and demographics were of females was density dependent overall, although not evident and these were likely to be climatic in origin. strongly so on Summit Road and Charlotte Pass They corresponded with climatic extremes e.g. late snow (Fig. 9a). The relationship for males was significant only melt in 1992 and June temperature extremes in 1994 on Blue Cow (Fig. 9b). By contrast, recruitment was (Broome, unpubl. data), and there was no evidence of strongly density dependent on all sites for females and regional biotic influences, e.g. disease or predator most sites for males, but weaker at Paralyser (Fig. 10a, b). irruptions. However, the highly stable populations of B. L.S. Broome / Biological Conservation 102 (2001) 309–323 319 parvus for small mammal populations (Cockburn, juveniles from feral cats Felis catus and European foxes 1988), and density dependence in recruitment of both Vulpes vulpes, which are particularly abundant around sexes and survival of females shown in this study indi- the ski resorts and suffer food shortage when B. parvus cate B. parvus are habitat limited, and likely to be are breeding in early spring (Bubela, 1995). A large strongly self-regulating. A density dependent equili- degree of emigration of adults is less likely because the brium view of B. parvus population dynamics (Krebs, breeding sites that were trapped were the most extensive 1995) therefore seems reasonable. That is not to say ones in the region. Juveniles continued to migrate and that the carrying capacity is not subject to change due disperse after trapping in March, contributing to their to changes in food supply or that the relative importance low winter recapture rates, but juveniles of both sexes of biotic interactions as opposed to the exogenous are also less likely to survive hibernation than heavier effects of climate does not vary between sites or years. animals because of their smaller body mass (Geiser and Density dependence in the highest quality habitats Broome, 1991). where bogong moths and seeds are abundant, is likely Site differences in demographics may occur because of to result from the limited availability of suitable sites for differences in habitat structure, quality and aspect. The nesting and hibernating (Ko¨ rtner and Geiser, 1998; habitat characteristics of a site can influence the extent Broome, 2001). Older, heavy individuals of both sexes, of biotic interactions, including social regulation, that which occupy these habitats (Broome, 2001) are likely occur there, as well as the effects of climate (Ims, 1987; to regulate recruitment, particularly of subadults which Ostfeld, 1990; Weiss et al., 1993; Hanski et al., 1995; are smaller and lighter (Broome, 1992). Aggression is Nelson, 1995). Site differences can also lead to asyn- shown by females at nest sites, and kin clusters chrony in local population dynamics (Sutcliffe et al., (Mansergh and Scotts, 1990; Broome, 2001) and 1996). Charlotte Pass appeared to have the highest extremely long lifespans for small mammals (Cockburn quality of the four sites in this study, as suggested by the et al., 1990) may facilitate social regulation. Males can highest density, annual survival and longest site persis- be aggressive to other males when breeding and their tence of females. The relatively stable population size social status may determine selection of hibernation and low recruitment suggests strong social regulation. sites during winter (Kerle, 1984; Broome, 2001). Adult High annual survival of males may have been influenced males possibly leave the habitat of females because of by the close proximity of the relatively large male win- intersexual dimorphism in hibernation strategies (Ko¨ rt- tering site on the south side of the valley. Mount Blue ner and Geiser, 1998; Broome, 2001), but aggression Cow had similar numbers and stability of adults, but from females may encourage adult as well as juvenile the total population size was more variable due to males to leave high quality habitats in late summer recruitment peaks of subadults, which all occurred in (Mansergh and Scotts 1989, 1990; Broome, 2001). Tail years of low snow cover (Broome, unpubl. data). This bites were observed on both sexes, mainly on adults and may have been facilitated by a steep elevational gra- subadults but occasionally on juveniles, on all sites dient, and the presence of boulderfield patches with tall, throughout the snow-free months in this study. Gen- dense shrub cover at lower elevations, which were not eralised aggressive interactions are indicated and the present at the other sites. In the laboratory not all juve- results suggest a high level of social regulation in the niles hibernated (Geiser and Broome, 1991) so it is pos- habitats studied. sible during mild winters where there are shrubs to Survival was generally lower and density dependence provide cover or a subnivean space in which to forage, in annual survival was less prevalent among males than some juveniles may remain active and survive on seeds, females. However, on most sites the few males that did fruits and any available insects. High winter survival of not migrate by March survived winter as well as juvenile females but low annual survival of subadults on females, suggesting that migratory males suffered high- Mount Blue Cow suggests these females were not able est rates of mortality. Winter mortality is generally to subsequently establish nesting sites in the principle likely to be higher for males than females because they boulderfields. hibernate at a higher minimum Tb during torpor and More variable population sizes of females at Summit undergo more frequent arousals, which has an energetic Road and Paralyser may have been influenced by cost (Ko¨ rtner and Geiser, 1998). Additionally, males greater demographic stochasticity within small popula- may be impacted by climate more than females because tions (Shaffer, 1981). However, climate is likely to have they hibernate in warmer microsites less insulated by a greater influence on these populations because the deep snow cover (Walter and Broome, 1998). They may habitat structure offered less buffering from climatic also suffer food shortage and more predation and com- extremes. At Summit Road, the relatively high winter petition from other species in these sites, which are often survival of females and heavy spring weights were asso- at lower elevations or more westerly aspects and have ciated with early snow melt and breeding on the north- few bogong moths (Broome, 2001). High predation westerly aspect. However, boulder depths were shallow rates may also occur on migratory males and dispersing and this population appeared to be adversely affected in 320 L.S. Broome / Biological Conservation 102 (2001) 309–323 years of very low snow cover (Broome, unpubl. data). Higher predation rates may occur in this region, where At Paralyser, low habitat quality may have been due to there is less shrub cover between habitat patches than in the large size of boulders and shallow depth of the main Kosciuszko National Park. Less reliable snow cover and boulderfields at Paralyser 2 (Broome et al., unpubl. more intense interspecific competition in the habitats data). These provided few sheltered spaces for B. parvus used by males may contribute. and bogong moths in summer, a paucity of insulated hibernation sites and a requirement for deep snow cover 4.2. Ski resorts and metapopulation conservation to prevent cold air drainage in winter (Walter and Broome, 1998). Females as well as males hibernated There is no evidence over the first 11 years of the outside the principle boulderfields at this site (Walter, Mount Blue Cow ski resort operating of a declining 1996), perhaps contributing to their low survival. Short trend in population size or any changes in demographics site persistence resulted in the highest proportion of new which cannot be attributed to natural demographic females, mostly subadults. Light-weight individuals are variability. This is with a caveat that few data were less likely to survive hibernation in adverse years (Gei- gathered before the resort was constructed and none ser and Broome, 1991) and this may contribute to low before the access road to the site was built. The Char- population stability. By itself, the Paralyser 1 site lotte Pass resort was established in the 1930s, prior to appeared to be a small patch of higher quality habitat. the discovery in 1970 of B. parvus in the Kosciuszko However, the patch was small and the female which region (Mansergh and Broome, 1994), so there are no occupied this site for 11 years was often the only female pre-development data. It has been operating at its cur- present, and the only recapture in 4 of the 10 years she rent capacity since the mid to late 1970s (Freeman, was captured. 1997). Because of the extent and quality of habitat Female biased sex ratios in small mammal popula- within their boundaries, the resort areas support two of tions can result from differential mortality. However, in the largest B. parvus populations on the Kosciuszko situations where females are defendable, male social plateau. Under current estimates (fewer than 200 dominance may contribute (Ostfeld et al., 1985). The breeding females) they carry around 30% of the entire low recruitment of males at Mount Blue Cow, and population (Broome et al., unpubl. data). Two other, strong density dependence of male annual survival as relatively large populations occur on the western slopes well as recruitment, suggests that male social dominance of Mount Kosciuszko and Townsend. Their dynamics could have influenced female biased sex ratios on this are unknown but because of the aspect they are likely to site, where females were concentrated in high densities experience higher variability due to less reliable snow on the peak of the mountain (Broome, 2001). Densities cover. Populations at these high-elevation sites which of females were higher overall at Charlotte Pass but lack shrub cover, are also vulnerable because they they were uniformly distributed across the site, and at appear to be dependent on migratory bogong moths as Summit Road and Paralyser they were dispersed among their principle food source. Elsewhere, boulderfield pat- scattered boulderfields or in lower densities. Although ches are generally smaller or of lower quality than those annual survival of males (i.e. adult survival) was lower studied at Summit Road and Paralyser. Many support than that of females at Summit Road, sex ratios were less than 10 breeding females and frequently small pat- not biased because of high winter survival and compen- ches of less than half a hectare support no more than satory recruitment of juvenile males. Early snow melt one female (Broome et al., unpubl. data). on this site would increase the chance of juveniles sur- The asynchrony in local population dynamics viving hibernation (Geiser and Broome, 1991). At demonstrated among the four study sites, a small Paralyser, low survival rates of both sexes resulted in amount of dispersal between patches and density unbiased sex ratios. Lack of sex ratio bias on Paralyser dependence at the local population level suggests that 1 and on Summit Road may also have been influenced the scattered B. parvus populations on the Kosciuszko by high mobility of males contributing to more male plateau may function as a metapopulation (Hanski, captures, a trapping bias effect which is exacerbated on 1990, 1991; Hanski and Simberloff, 1997). Most female small study sites (Broome, 1988). In populations of B. parvus were recruited from within each local popula- Rock wallabies, sex ratios changed from female biased tion during this study, but genetic analysis and move- to male biased when foxes were controlled (Kinnear and ment data suggest re-population is possible between all Onus, 1998). At Charlotte Pass in December 1997 sex habitat patches. Two major haplotypes have been iden- ratios were biased towards males for the first time in the tified, with some interchange between them. Mount 11 years of trapping. This coincided with and may have Blue Cow and Charlotte Pass support the largest local been influenced by an intensive fox control program at populations of each haplotype (Osborne et al., 1999). Charlotte Pass during winter 1997. In Victoria, sex This has significant implications for the long-term ratios are extremely female biased at most sites (Man- management of the ski resort areas. Theoretically, and sergh et al., 1989; D. Heinze, pers. comm., March 2000). as this study suggests, variance in patch and population L.S. Broome / Biological Conservation 102 (2001) 309–323 321 size within metapopulations means that local extinc- Although the B. parvus populations in the ski resorts tions are least likely to occur in large, stable, demo- appear healthy so far, impacts may accrue if margin- graphically productive populations (where emigration alisation or loss of habitat occurs in the longterm. exceeds immigration). Additionally, they have the most Damage to vegetation in the habitat, which has occur- impact on metapopulation persistence and are most red in the past, is likely to be cumulative because of slow likely to act as source populations for surrounding, recovery rates. This applies particularly to P. lawrencei lower quality or smaller habitat patches (Pulliam, 1988; which attains ages of several hundred years (Bell and Hanski et al., 1995). Small or lower quality patches are Bliss, 1973; Costin et al., 1979). The effects of snow more likely to be affected by demographic and environ- compression from resort activities on insulation over mental stochasticity and are likely to be non-sustaining in hibernacula, and on the health of the underlying vege- the long-term without immigration from associated source tation, may take increasing effect under diminished patches (Hanski, 1991; Howe et al., 1991; Foley, 1997). snow cover conditions expected with global warming Charlotte Pass and Blue Cow are most likely to act as (Fuller et al., 1969; Baiderin, 1983; Walter and Broome, source populations, but heterogeneity in site structure 1998; Whetton, 1998). and aspect between sites may contribute to metapopu- This study suggests that a metapopulation approach lation persistence (Harrison and Taylor, 1997). Popula- is required, and careful management within ski resort tions on westerly aspects or at low elevations where lease areas will be necessary to maximise the long-term snow melts early, may survive better in years of long stability and persistence of B. parvus on the Kosciuszko snow cover duration. For example, populations on Plateau. It is likely that a similar situation occurs within Summit Road appeared less affected in 1992, the year of the populations in Victoria. On Mount Bogong, the deepest snow cover, when the largest decline occurred at Bogong High Plains and Mount Loch–Mount Higgin- Charlotte Pass. Charlotte Pass was unaffected by an botham, local populations are genetically similar but otherwise regional decline in 1994, which coincided with distinct from those in the Kosciuszko region. Mount extreme temperatures in June before insulating snow Higginbotham contains the largest likely source popu- cover formed, perhaps because the deep boulderfield lation and warm climate refugium, and is also within a provided insulated hibernation sites. Source populations major ski resort, as is the population at Falls Creek on may therefore vary with yearly environmental conditions. the Bogong High Plains. A third, genetically-distict The likely metapopulation structure and limited population occurs within the Mount Buller ski resort, availability of suitable habitat means that retaining all with a possible metapopulation structure occurring on a current areas of habitat is critical for the persistence of local scale over 4–5 km (Heinz and Williams, 1998; B. parvus (McCarthy and Broome, 2000). Loss of habi- Osborne et al., 2000; D. F. Heinze, pers. comm., March tat, reduction in carrying capacity or decreasing con- 2000). However, further detailed study is needed to nectivity between patches in small populations is likely confirm these predictions (Harrison and Taylor, 1997). to decrease metapopulation viability and may lead to Further research is needed on sources of recolonisation, population instability and system collapse (Den Boer, rates of extinction and recolonisation of patches. Future 1968; Lindenmayer and Possingham, 1994; Foley 1997). monitoring should include likely ‘sink’ populations Even apparent ‘sink’ patches may contribute to meta- where populations are smaller, and snow cover and population size and stability (Howe et al., 1991) or act duration are currently more marginal than at those so as dispersal stepping stones (Burgman et al., 1993) and far studied. Monitoring of more marginal sites is more must not be ‘sacrificed.’ In practise, the effects of these likely to detect population extinctions and responses to processes are often difficult to verify (Hanski and Sim- regional climatic influences, like global warming (Howe berloff, 1997). However, reconnection of movement et al., 1991; Harrison, 1994; Hanski and Simberloff, corridors at the Mount Hotham ski resort was shown to 1997). Due to their large size and stability, likely func- increase winter survival of mature female B. parvus in tion as genetically distinct source populations and their disturbed patches by around 40% (Mansergh and additional value as likely warm climate refugia, protec- Scotts, 1989). Even without direct local impacts, habitat tion of the B. parvus populations in the ski resorts is loss and degradation are likely to escalate under the paramount. Careful snowgrooming practices and pro- predicted effects of global warming. Populations which tection of habitat needs to be followed to prevent habi- are small, at low elevations or on westerly aspects are tat degradation in these areas. expected to be impacted first from increased climatic variability and reduced snow cover duration (Busby, 1988; Brereton et al., 1995; Whetton et al., 1996; Whet- Acknowledgements ton, 1998). The few sites with south and south-easterly aspects (which include Mount Blue Cow, Charlotte Pass Thanks to the many volunteers and occasional formal and Paralyser 1) are therefore likely to become increas- assistants who helped with field work and made this ingly important as warm climate refugia. study possible. Particular mention to Ian Pulsford who 322 L.S. Broome / Biological Conservation 102 (2001) 309–323 initiated the study in 1986, Marien Davey and Jan reference to its behaviour during migration and aestivation. Martin for data entry, Ross Cunningham and Christine Australian Journal of Zoology 2, 223–263. 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