P u b l i s h i n g
Wildlife Research Volume 28, 2001 © CSIRO 2001
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Wildlife Research, 2001, 28, 493–506
Population dynamics of three species of dasyurid marsupials in arid central Australia: a 10-year study Christopher R. DickmanA, Adele S. HaythornthwaiteA, Gayle H. McNaughtA, Paul S. MahonAB, Bobby TamayoA and Mike LetnicA A
School of Biological Sciences and Institute of Wildlife Research, University of Sydney, NSW 2006, Australia. B New South Wales National Parks and Wildlife Service, PO Box 1967, Hurstville, NSW 2220, Australia.
Abstract. This study investigated the population dynamics of three species of dasyurid marsupials in sand ridge habitat of the Simpson Desert, western Queensland, over a 10-year period between March 1990 and December 1999. The lesser hairy-footed dunnart (Sminthopsis youngsoni), was captured most consistently over the period of study, followed by the wongai ningaui (Ningaui ridei), and the mulgara (Dasycercus cristicauda). Rates of recapture were low (4.5–22.2%), probably because individuals of each species are very mobile. All species bred in late winter or early spring when animals were aged at least 8–10 months, and independent juveniles first appeared usually in summer. S. youngsoni reared a second litter in late spring or early summer in 3 of the 10 years studied, when the availability of food was likely to have been high; neither N. ridei nor D. cristicauda were known to attempt a second litter within a season. To explore factors that might influence population dynamics, we compared capture rates of each species with measures of rainfall, temperature, vegetation cover, abundance of predators [feral cats (Felis catus), red foxes (Vulpes vulpes), and goannas (Varanus spp.)], dragons, other dasyurids and indices of food abundance. The abundance of S. youngsoni appeared to depend primarily on the cover of spinifex 7–9 months earlier, that of D. cristicauda was related most strongly to rainfall 7–9 months earlier, while that of N. ridei was related to minimum temperature lagged by 1–3 months. While the dynamics of other arid-zone mammals are driven demonstrably by interactions between rainfall, resource availability and predation, our findings suggest that dasyurids have limited flexibility in their life histories and are influenced more subtly and by factors such as facilitation that are just beginning to become apparent. eDCty. anRl.mDicskomfarnid-zonedasyurids
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Introduction Mammals that inhabit arid environments often fluctuate greatly in abundance. In some species, populations are virtually absent from local areas for long periods, and erupt only briefly when conditions are favourable (Finlayson 1939; Carstairs 1976; Predavec and Dickman 1994). In other species, populations may show more regular fluctuations, achieving peaks in abundance in spring and summer and troughs in winter (Friend et al. 1997). The major factor driving population changes in arid-zone mammals is usually considered to be rainfall. Rain provides free water, but perhaps more importantly stimulates primary production that, in turn, increases the food resources available to foragers (Rosenzweig 1968; Stafford Smith and Morton 1990; see also Kotler et al. 1998). Increased resources facilitate reproduction and © CSIRO 2001
enhanced survival of young, allowing population increases weeks or months after rain has fallen (Meserve et al. 1996; Southgate and Masters 1996). Immigration also may contribute to population increases, particularly if rainfall has occurred locally in a drought-struck area (Dickman et al. 1995). Other factors such as competition and predation have also been shown to influence mammalian abundance in deserts (e.g. Heske et al. 1994; Meserve et al. 1996; Mahon 1999), but their effects appear less pervasive than those attributable to rainfall. In arid Australia, dasyurid marsupials are conspicuous and often dominant members of small mammal communities, but the effects of rainfall and other factors on their abundance remain little studied (Morton et al. 1989). Population increases have been noted in some species after periods of high rainfall (Finlayson 1933; Denny 1975), but 10.1071/WR00023
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decreases have been recorded in others (Woolley 1984), perhaps following drowning of animals in burrows (Dickman and Read 1992). In a four-year field study, Morton (1978a) captured most fat-tailed dunnarts (Sminthopsis crassicaudata) from April to July, prior to breeding, although juveniles entered the population progressively through spring and summer. Breeding appeared to be timed so that juveniles were weaned when invertebrate food resources were maximal, but there was little evidence of a correlation between rainfall and abundance of either S. crassicaudata or its food supply (Morton 1978a, 1978b). Similarly, Read (1984a) found no apparent relationship between the abundance of S. crassicaudata and rainfall, or vegetation cover, but noted a decline in abundance of two species of Planigale with the onset of drier conditions. In a further field study, Masters (1993) related changes in abundance of four species of dasyurids to changes in vegetation cover, especially cover of spinifex (Triodia basedowii), to temperature and, in the lesser hairy-footed dunnart (S. youngsoni) only, to rainfall. Morton (1982) concluded that variability in the availability of food (invertebrates) was the dominant selection pressure affecting arid-zone dasyurids, but the relationship between rainfall, food and the dynamics of dasyurid populations remains unclear. The life-history strategies of arid-zone dasyurids differ from those of other small mammals, such as rodents, in being relatively fixed, and this may constrain immediate responses to temporarily improved conditions. Reproduction in all species appears confined to the period from winter to late summer, with a hiatus in autumn (Lee et al. 1982). Although some species show potential to breed in the season of birth, this potential is seldom realised, and individuals in all species studied appear to be at least six months or older at first reproduction (Lee et al. 1982; Morton et al. 1989). Most species of arid-dwelling dasyurids are probably polyoestrous and produce up to two litters in a season (Morton 1982) but, intriguingly, some are monoestrous with short and relatively invariant periods of rut (Lee et al. 1982; Woolley 1991). Monoestry has been explained traditionally as being advantageous in environments where resources are seasonally restricted but reliably timed (Lee et al. 1982; Morton et al. 1989; Dickman 1993). However, because resource flushes in arid environments are usually not predictable, monoestry in desert species remains difficult to interpret. Studies that simultaneously document resource fluctuations and population dynamics over long periods may help to clarify such difficulties, although relatively few have been carried out (Cody and Smallwood 1996). The present paper draws on data from a 10-year study of dasyurids in the Simpson Desert, western Queensland. Our aims were to: (1) describe population fluctuations in three species of dasyurids, (2) describe population processes in each species, and
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(3) relate the population dynamics of each species to rainfall, vegetation cover and other factors that might influence demography. Our study species were the mulgara (Dasycercus cristicauda), the wongai ningaui (Ningaui ridei), and the lesser hairy-footed dunnart (S. youngsoni). Methods Study area The study was carried out on Ethabuka Station, on the north-eastern edge of the Simpson Desert, western Queensland (23°46′S, 138°28′E). The area is characterised by parallel red sand dunes, 8–10 m high and 0.5–1.0 km apart, that run in a NNW–SSE direction in line with prevailing south-south-easterly winds (Purdie 1984; Twidale and Wopfner 1990). Inter-dune valleys, or swales, have clay soils that often pond after rain. Vegetation on the swales is dominated by gidgee (Acacia georginae), forbs and short grasses; this gives way on the dune slopes to spinifex (Triodia basedowii) and patches of perennial shrubs including Acacia ligulata, Dodonaea angustissima, Eremophila spp. and Eucalyptus spp. The dune crests have a sparse cover of shrubs including Grevillea stenobotrya, Tephrosia rosea, Crotalaria spp. and Sida spp. (Dickman et al. 1993); forbs, ephemeral herbs and grasses are abundant after rain. Average annual rainfalls for the three weather stations closest to the study area are 172 mm (Sandringham, n = 40 years of records), 196 mm (Marion Downs, n = 84 years) and 203 mm (Glenormiston, n = 95 years). There is a pronounced wet season, with >50% of rain falling between December and March; however, the annual occurrence and intensity of rainfall is unpredictable (Morton 1982). Summer maximum temperatures reach 46–49°C, while winter minima fall to –6°C (Purdie 1984). Animal trapping Animals were trapped on 60 occasions at the study area between March 1990 and December 1999, at sampling intervals of usually 2–3 months. Animals were live-trapped using pitfall traps. These were constructed from PVC pipe (16 cm diameter, 60 cm deep) buried flush with the ground, and were overlain with drift-fences (5 m long, 30 cm high) of aluminium flywire. Flywire was placed underneath the traps to prevent escape of captured animals. Traps were capped with metal lids when not in use. Pitfall traps were arrayed in grid formation. Each grid comprised six lines of six pitfall traps spaced 20 m apart to cover 1 ha. The top line of traps was positioned along the dune crest, the bottom line ran parallel 100 m away in the swale. Grids were 0.5–2 km apart. Grids arranged in this manner were expected to act as loci within the broader landscape that would intercept animals for capture, and were not expected to contain the ranges of any individuals. Six grids were operated in 1990, and 12 for the remainder of the study. However, in 1999, data were not used from three grids that had been fenced as part of other research. Traps were opened for 2–4 nights per grid on each sampling occasion, and checked in the mornings and sometimes also in the afternoons. Captured animals were identified, weighed and marked uniquely by toe-clipping (until 1993) or by ear-notching (1994 onward). Maximum width of the tail was measured using calipers for all individual D. cristicauda and S. youngsoni to provide a crude index of condition (Morton 1980). In males, reproductive condition was assessed indirectly by measuring the maximum width of the scrotum using calipers. In females, the condition of the pouch was inspected and individuals scored as nulliparous, pouch developing (pouch area becoming depilated, with surrounding growth of long, white hairs), lactating with pouch young present, lactating but pouch young not present, or parous but with no current pouch development.
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Crown–rump lengths of 1–2 pouch young were measured using calipers. Sex of the pouch young was determined for young aged about 10 days or more. Several litters of young of each species were also toe-clipped while in the pouch to investigate spatial relationships among mothers and young following weaning (cf. Cockburn et al. 1985). Five other species of dasyurids were captured and processed in the same way during the study, but captures were too infrequent to analyse. These were the dunnarts Sminthopsis crassicaudata, S. hirtipes and S. macroura, and the planigales Planigale gilesi and P. tenuirostris. The population dynamics of other species of small vertebrates captured during the study have been described elsewhere (Predavec and Dickman 1993, 1994; Dickman et al. 1995, 1999a, 1999b; Mahon 1999). Climate and environmental measurements The long-term monthly rainfall records from the Sandringham, Marion Downs and Glenormiston weather stations, above, were correlated positively (r = 0.72–0.85), and were used to calculate monthly rainfall averages for the study area. Daily temperature data during trapping periods were obtained on-site using a maximum–minimum thermometer from 1990 to March 1995, and an automatic weather station (model: Environdata, Warwick, Queensland) from May 1995 onward. Average minimum and maximum temperatures were calculated for the duration of each trapping period. Vegetation cover was assessed in two ways. First, one pitfall trap station was selected at random from each line of traps from the dune crest to the swale on each grid. A visual estimate was then made of the percentage total cover of live vegetation in a 2.5-m radius centred on each station. Second, using the same procedure, the percentage cover of T. basedowii alone was estimated. Cover assessments were made on five grids from 1990 to October 1993, and on all 12 grids thereafter. Preliminary analyses of growth in T. basedowii at Ethabuka have been presented by Dickman et al. (1999a). Other factors considered likely to influence dasyurid populations were predators, food and shelter resources. Foxes (Vulpes vulpes) and feral cats (Felis catus) are important predators in the study area (Dickman 1996a; Mahon 1999), and were censused by spotlighting along tracks from a slowly moving vehicle. The spotlight run was ~15 km, and was traversed 2–3 times each sampling period. The effectiveness of spotlighting probably declined during the study due to increased cover of vegetation (Mahon et al. 1998). Other terrestrial predators included the goannas Varanus gouldii and V. eremius (CRD, unpublished data). Indices of abundance of these predators were derived from captures of both species combined in the pitfall traps on each sampling occasion. No formal census was made of potential avian predators. However, owls were observed rarely throughout the study, while a specialist rat-predator, the letter-winged kite (Elanus scriptus), was present primarily in 1991 and 1992 during an eruption of long-haired rats (Rattus villosissimus) (Predavec and Dickman 1994). Food resources were assessed in two ways. Firstly, assuming that rodents form part of the diet of dasyurids, we enumerated populations of the two dominant species, the sandy inland mouse (Pseudomys hermannsburgensis) and the spinifex hopping-mouse (Notomys alexis), captured in pitfall traps throughout the study period (see Dickman et al. 1999b for details). The assumption that rodents form part of the diet of dasyurids is reasonable for D. cristicauda (Chen et al. 1998; Masters 1998), but not for N. ridei or S. youngsoni (Fisher and Dickman 1993). Secondly, assuming that well fed animals have relatively fat tails (Morton 1980), we derived an index of condition for individuals by computing the regression between weight (x) and tail width (y). Females and males were analysed separately. The condition index was estimated as the deviation of observed tail width from the tail width predicted from the regression, using the procedures of Krebs and Singleton
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(1993). This indirect method of evaluating available food could be used only on D. cristicauda and S. youngsoni, which have incrassated tails. Only adults were used; for D. cristicauda these were taken to be females ≥50 g and males ≥67.5 g, and for S. youngsoni females ≥7.0 g and males ≥7.5 g. We could not assess food resources or condition for the thin-tailed N. ridei. The shelter resources required by the three study species are poorly known, but most likely include ground-level vegetation and burrows. Dasycercus cristicauda digs its own burrows on the lower slopes of dunes (Woolley 1990), but the other dasyurids use burrows made by other species, including large invertebrates, rodents and, especially, lizards (Dickman 1996b). Radio-tracked N. ridei and S. youngsoni have been found to make extensive use of the burrows of central netted dragons (Ctenophorus nuchalis) (CRD and ASH, unpublished data). Because of the difficulty in counting suitable burrows for the dasyurids, we used the numbers of C. nuchalis on the study grids (Dickman et al. 1999a) as a surrogate measure of the availability of burrow shelters. Statistical analyses Population dynamics were evaluated using catch-per-unit-effort methods (Caughley 1977) rather than with capture–mark–recapture or matrix models (cf. Lima et al. 2001) due to the very low rates of recapture of each species (90% (Beale et al. 1967; Kendall 1980). This procedure simplified the set of independent environmental variables available for each species, and substantially reduced multicollinearity. Stepwise multiple linear regressions were
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Fig. 1. Capture rate of Sminthopsis youngsoni at Ethabuka, south-western Queensland, expressed as captures per 100 trap-nights (mean + s.e.).
run separately using the capture rates for each species as the dependent variable, with environmental variables entered into the models if individually significant at P < 0.05. We considered that capture rates would be unlikely to depend on condition indices, and hence omitted this variable in regression analyses. Instead, we correlated mean condition indices for each sex separately with the capture rate for that sex and with the total capture rate for the species over all sampling occasions when individuals were captured. All computations were carried out using Sigmastat. In using correlation and regression analyses to investigate associations between variables, it is important to acknowledge the problem of lack of temporal independence. Temporal autocorrelation can bias model predictions of population growth (Foley 1994), point erroneously to delayed density dependence (Williams and Liebhold 1995), and also invalidate tests of hypotheses that require independent data. In the present study, we follow other workers (e.g. Predavec 1994; Holbrook et al. 1997) in using correlation and regression analyses descriptively to explore patterns in time-series data, so that the problem of autocorrelation is reduced. Although alternative methods of time-series analysis are available, most use only one data point per year or require long periods (>>10 years) for reliable interpretation (Bjornstad et al. 1995; Swanson 1998). Our data were not sufficient for analysis by these methods.
Results Population dynamics A total of 946 captures was made of the three study species between March 1990 and December 1999 in 64 300 trap-nights. The overall capture rate was 1.47 animals per 100 trap-nights. Sminthopsis youngsoni Over the course of the study, 555 S. youngsoni were captured 713 times, giving a recapture success of 22.2%. More males (412) were captured than females (297); the sex of 4 individuals was not determined. Peak capture rates of 6–8 animals per 100 trap-nights occurred in 1990 and 1998, while a prolonged trough was observed during 1991–94 (Fig.1). There was much variation in capture rates between grids, with standard errors often exceeding means.
Within years, capture rates were usually highest (mean = 1.31–1.33 per 100 trap-nights) in autumn (March–May) and winter (June–August) and least (mean = 0.64 per 100 trap-nights) in spring (September–November). Capture rates of both sexes were equal in autumn, spring and summer (December–February), but in winter males were captured at a higher rate (mean = 0.87 per 100 trap-nights) than females (mean = 0.46 per 100 trap-nights) (χ2 = 28.46, P < 0.001). Reproduction was strongly seasonal, and confined largely to spring and summer. Except for a single female that was recorded lactating in early August 1991, pouch development usually began in August each year, females with pouch young were recorded in September and October (n = 20), and lactating females with vacant pouches in October and November (n = 27) (Fig. 2). In most years lactation ceased by December; however, two lactating females were captured in each of March 1990, February 1998 and March 1999 (Fig. 2). Two of these late-breeding females had been recorded with pouch young in spring the previous year, indicating that they were raising their second litters for the season. No females were known to breed in the season of their birth; all matured at ≥8 months of age with a body weight of ≥7.0 g. One of 20 females with pouch young and one of 27 recorded lactating but with no young in the pouch had bred the previous season, and were thus aged ≥20 months and breeding for at least the second time. All females examined had six nipples (n = 48), except for one with five. Sixteen of 20 females with pouch young had a full complement of six, two had five, one had four and one had three. The sex ratio of pouch young in six litters did not deviate from parity (17 female:19 male, χ2 = 0.11, n.s.). Young in five litters were toe-clipped while in the pouch (14 female:16 male); one juvenile female was recorded subsequently on the grid where her mother had been captured, while a juvenile male was recorded on an adjacent grid ~600 m distant.
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Fig. 2. Number of lactating Sminthopsis youngsoni (n = 43) at Ethabuka, south-western Queensland, expressed as a percentage of all females captured per sampling occasion (n = 297). Lactating females had attached pouch young or vacant pouches. They were captured each year between September and November and, in 1990, 1998 and 1999, in February or March also. No lactating females were recorded between April and July, and one only in August 1991.
Fig. 3. Scrotal width of Sminthopsis youngsoni (n = 412) at Ethabuka, south-western Queensland (mean + s.e.).
The timing of reproductive activity in males paralleled that of females. Males began to exhibit swollen cloacae and increased sternal gland activity in August each year, and also everted the penis during handling. Mean scrotal width increased from autumn through winter, peaked in September, and then usually declined (Fig. 3). Males probably achieved reproductive age at ≥8 months with a body weight of ≥7.5 g and a scrotal width of ≥6.0 mm. Potentially reproductive males fulfilling these minimal criteria were present in most months of the study. However, only 2 of 114 males that were reproductively mature in one season were known to have survived to the next, and were aged ≥21 months at the time of last capture. Pulses of newly-weaned S. youngsoni, weighing as little as 2.2 g, entered traps from November to December each year. In each of February or March of 1990, 1998 and 1999 a second cohort of weanlings also occurred, presumably the result of repeated breeding in those years. Except in years when the breeding season was extended, all individuals captured from March onward weighed ≥4.0 g and overwintered with body weights of 6–13 g prior to breeding (Fig. 4). Young animals were predominant in autumn
populations and primarily responsible for elevated capture rates in this season. Body weight and tail width were related weakly in both sexes: Females: tail width = 3.28 + 0.078 weight (R2 = 0.02, P = 0.13) Males: tail width = 3.86 + 0.047 weight (R2 = 0.01, P = 0.25) For females, condition indices derived from the regression varied considerably among individuals over time (Fig. 5). Indices were generally low between spring 1992 and autumn 1995, when capture rates were also low; however, the mean condition index for females was not correlated with either total capture rate (r = 0.12, n.s.) or the capture rate of females only (r = 0.18, n.s.) over the study period. Seasonally, condition indices were usually highest in winter and least in summer, with this trend being most evident in the second half of the study (Fig. 5). For males, within- and between-year trends in the condition index strongly paralleled those for females (Fig. 5). Mean condition index for males was not correlated with the total capture rate
Fig. 4. Overall capture rate of Sminthopsis youngsoni by body weight at Ethabuka, south-western Queensland, in four months in each of 1990, 1996 and 1998. Overall capture rate is expressed as captures per 100 trap-nights summed over all trapping grids. (a) February and March, (b) May and June, (c) August, (d) October.
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Fig. 5. Condition index for Sminthopsis youngsoni at Ethabuka, south-western Queensland, expressed as the deviation of observed tail width from that predicted in a body weight–tail width regression. Symbols represent mean values per trapping session (+s.e.).
(r = 0.19, n.s.) or with that of males only (r = 0.23, n.s.) over the study period. Dasycercus cristicauda In all, 31 female, 45 male and 6 unsexed D. cristicauda were captured 99 times over the study, yielding an overall capture rate of 0.15 per 100 trap-nights and recapture success of 17.2%. Peak capture rates of 1.4 per 100 trap-nights were recorded in November 1992 and November 1997; capture rates of
