In terms of population dynamics, \boom-and-bust\ cycling is a situation in which

Journal Article

Kerrie Bennison,

Parks Australia, Department of Environment and Energy, Canberra, Australian Capital Territory, Australia

Desert Ecology Research Group, School of Life and Environmental Sciences, The University of Sydney, New South Wales, Australia

Search for other works by this author on:

Published:

20 September 2018

• 
  PDF
• Split View
• • Article contents
  • Figures & tables
  • Video
  • Audio
  • Supplementary Data

• Cite

  Cite

  Kerrie Bennison, Robert Godfree, Christopher R Dickman, Synchronous boom–bust cycles in central Australian rodents and marsupials in response to rainfall and fire, Journal of Mammalogy, Volume 99, Issue 5, 10 October 2018, Pages 1137–1148, https://doi.org/10.1093/jmammal/gyy105

  Close

• • Email
  • Twitter
  • Facebook
  • More

Close

Navbar Search Filter Microsite Search Term Search

Abstract

Mammals in arid environments often show pronounced fluctuations in population size, oscillating from being almost absent to being ubiquitous and present at very high density. The low, or “bust,” phases of populations usually occur during prolonged periods when the environmental carrying capacity is low (Yang et al. 2010) and resources are depressed (Letnic et al. 2005). Large or mobile mammals may respond to such conditions by dispersing to areas where resources can be accessed more readily (e.g., Fennessy 2009), but terrestrial small mammals are usually constrained in mobility and have to deal with resource shortages in situ (Degen 1997; Fox 2011). Some species can make directed movements of several kilometers to access fresh resources (Dickman et al. 1995; Letnic 2002) or retreat to refuge habitats (Milstead et al. 2007; Pavey et al. 2014, 2017). Others persist by exploiting cached food resources (Kelt 2011), foraging selectively in the highest-quality food patches (Bleicher and Dickman 2016), or reducing their needs for energy and water via physiological mechanisms such as nest sharing or torpor (Morton 1978; Geiser 2004). When conditions improve, desert mammals often respond via elevated reproduction, survival, and immigration to achieve, within a few months, populations that may be 2–3 orders of magnitude greater than those present during the bust phase (D’Souza et al. 2013; Greenville et al. 2013). Population peaks, or “booms,” are often ephemeral, and may last less than a year if conditions deteriorate rapidly (Dickman et al. 2010).

Improved conditions in most arid regions are brought about by heavy rains that stimulate pulses of productivity (Whitford 2002), although floods from rains that have fallen elsewhere can have similar effects (Letnic and Dickman 2010). These pulses produce food for primary consumers and shelter in the form of increased vegetation cover, and are the most reliable predictors of rodent irruptions in arid regions (e.g., Newsome and Corbett 1975); links between rainfall and rodent booms have been traced over periods exceeding 100 years (Plomley 1972; Greenville et al. 2012). Ensuing bust phases result from declines in productivity as conditions dry, but can be hastened and prolonged by events such as wildfire (Letnic et al. 2005). Wildfires remove vegetation cover and food resources, and also create open habitats that increase the hunting efficiency of predators on small mammals (McGregor et al. 2015). Although boom and bust dynamics have been described for many species of desert-dwelling mammals (e.g., Whitford 2002; Fox 2011; Ojeda et al. 2011), they appear to be most pronounced in rodents that occupy regions with unpredictable rainfall regimes (e.g., Australia—Dickman et al. 1999, 2010; Namibia—Griffin 1990). Rodents in these regions often exhibit opportunistic breeding in response to rainfall events (Breed and Ford 2007). They also show greater flexibility in diet and social behavior than do their counterparts in deserts where rainfall is low but seasonably reliable (Murray et al. 1999; Lima et al. 2008; Fox 2011; Shenbrot 2014), perhaps increasing the efficiency with which temporary resource pulses can be exploited (Letnic and Dickman 2010).

Despite the apparent ubiquity of the rainfall–rodent association in arid environments and our mechanistic understanding of how it works, neither rodents nor other small mammals always increase after rainfall. Long-term field programs are increasingly uncovering circumstances where study species show inconsistent responses to rainfall events, and even negative effects of rainfall on population size. In Chile, for example, Meserve et al. (2011) showed that caviomorph rodents sustain larger populations than sigmodontine rodents if there are moderate rainfall events between years of high rainfall, whereas the latter rodents dominate if rainfall pulses are widely separated. The difference may be explained by differences in life history traits between the 2 groups of rodents, with fast-breeding sigmodontines better able to exploit ephemeral resource pulses and slower-breeding, longer-lived caviomorphs better able to maintain their populations if conditions during bust periods allow persistence (Previtali et al. 2009, 2010). In the Negev Desert, negative relationships between rainfall and rodents in dry river bed habitats may arise due to flash floods in some years (Shenbrot et al. 2010), while in the Chihuahuan Desert inconsistent relationships between rainfall and rodent responses over a 28-year period appear to have arisen due to interactions between rainfall and shrub density and other factors (Thibault et al. 2010).

Insectivorous small mammals might be expected to show smaller populations and delayed responses to rainfall pulses because of their dependence on secondary productivity (invertebrates). Some species, such as Onychomys spp. (Thibault et al. 2010) and Notiosorex crawfordi (Chung-MacCoubrey et al. 2009), do indeed behave as expected, but others show no evident demographic response to rainfall (Meserve et al. 2011; Greenville et al. 2016) and may even decline after heavy precipitation events (Woolley 1984). These observations suggest that rainfall often triggers irruptions of desert mammals, but also that the relationship is complex, and support the call of Lindenmayer et al. (2012) for more long-term studies to help understand the processes that drive animal populations.

Fire also can affect the composition of communities in fire-prone landscapes. In spinifex-dominated habitats in central Australia, postfire recovery involves a predictable succession of plant species, beginning with forbs and grasses, followed by the dominance of spinifex again 5–10 years later, after sufficient heavy rains have fallen (Latz 1999; Allan and Southgate 2002; Southgate and Carthew 2008; Nguyen et al. 2015). Leonard (1976) found a 50–90% reduction in litter invertebrates following prescribed burns in forests. Fire can affect small mammals by direct mortality or indirectly by removing food and shelter and exposing individuals to increased risk of predation (Sutherland and Dickman 1999; Letnic et al. 2013).

In this paper, we investigate temporal changes in populations of rodents and dasyurid marsupials over a period of 16 years at sites in central Australia. The dominant species of rodents—spinifex hopping mouse (Notomys alexis, average weight 32.1 g, range 26.3–38.7 g), sandy inland mouse (Pseudomys hermannsburgensis, average weight 13.2 g, range 9.3–17.8 g), desert mouse (Pseudomys desertor, average weight 25.1 g, range 14.5–31.5 g), and house mouse (Mus musculus, average weight 12.6 g, range 9–17.5 g)—often respond positively to rainfall elsewhere in Australian desert habitats (e.g., Masters 1993; Pavey et al. 2008; Letnic et al. 2011a), but the responses vary in magnitude and timing (Southgate and Masters 1996), and are sometimes muted even after heavy rainfall events (Dickman et al. 1999). These species are broadly omnivorous, although seeds and green plant material form > 50% of their diets (Murray and Dickman 1994; Murray et al. 1999). The dominant dasyurid species at the study sites, including the brush-tailed mulgara (Dasycercus blythi, ~100 g), wongai ningaui (Ningaui ridei, average weight 8.2 g, range 5–10 g), and lesser hairy-footed dunnart (Sminthopsis youngsoni, average weight 10.4 g, range 6–12.4 g), sometimes increase after rain, but results again are not consistent across studies (Masters 1993; Dickman et al. 2001; Masters and Dickman 2012; Greenville et al. 2016). Invertebrates comprise the bulk of the diet of the dasyurids, although D. blythi also hunts small vertebrates (Fisher and Dickman 1993; Masters 1998). All these small mammals generally decline after wildfire (Letnic et al. 2004; Pastro et al. 2011), although muted responses are sometimes reported (Southgate and Masters 1996; Bennison et al. 2013). Introduced predators such as the European red fox (Vulpes vulpes) and feral cat (Felis catus) may hasten postfire declines, especially of rodents, which are selectively depredated in open habitats compared to dasyurids (Spencer et al. 2014).

We expected that populations of these small mammals generally would respond positively to rainfall and negatively to wildfire, and also that variation in the strength and timing of responses would arise due to differences in life history traits and diets of the study species. We used long-term data (1994–2010) to test the following 3 broad hypotheses:

H1: Dasyurid marsupial populations will exhibit less variability and lower capture rates than sympatric rodents.

H2: Mammals generally will respond positively to rainfall, with rodents responding more quickly and strongly and declining more rapidly during drought than marsupials.

H3: Rodents and dasyurids will decline following wildfire, with rodents showing greater preference for postfire regeneration than marsupials.

For the 3rd hypothesis we assumed that the omnivorous diets of Australian desert rodents (Murray et al. 1999) would allow them to exploit the new plant growth available after a fire more quickly than dasyurids, which need to wait for invertebrates to recolonize postfire. We assumed that during drought, the ability of marsupials to store energy resources in their tails and enter periods of torpor (Geiser 2004) would allow them to persist longer than rodents, which need a more consistent supply of food.

Materials and Methods

Study sites

The study was carried out at Uluṟu-Kata Tjuṯa National Park (UKTNP) in the southwest of the Northern Territory, 320 km southwest of Alice Springs, central Australia (Fig. 1). The park covers 1,325 km2 and is managed jointly by Parks Australia and Aṉangu Traditional Owners (Director of National Parks 2010). The dominant landscape features include Uluṟu, a red sandstone rock formation 9.4 km in circumference and 340 m high, and Kata Tjuṯa, a complex of 36 basalt and granite conglomerate domes that cover 35 km2 and rise to 500 m above the surrounding desert. Sand dunes and plains surround these rocks (Director of National Parks 2010). The climate of the park is semiarid, with annual rainfall averaging 280 mm and temperatures ranging from < 0°C on winter nights to > 40°C in summer (Bureau of Meteorology 2010). Rainfall is extremely variable (< 150 mm to > 800 mm per year), with heaviest rainfalls during summer.

Fig. 1.

The study area at Uluṟu-Kata Tjuṯa National Park in the southwest of the Northern Territory, showing locations of major towns and (inset) location within Australia.

The study sites were originally selected by the Commonwealth Scientific and Industrial Research Organisation’s Division of Wildlife and Ecology between 1987 and 1990 for ecological surveys of the vertebrate fauna of UKTNP (Reid et al. 1993). Site selections were based on having 1 site in each of the park’s 6 major land classes: alluvial fans at Uluṟu, alluvial fans at Kata Tjuṯa, sedimentary foothills at Kata Tjuṯa, mulga shrubland, soft spinifex, and hard spinifex. An additional 2 sites in the soft spinifex land class included the distinctive vegetation types of mallee (Eucalyptus gamophylla, E. mannensis, E. socialis, and E. oxymitra), and Acacia ammobia open woodlands. The closest distance between sites was 5 km. Mammal surveys (see details below) were continued at the same sites for this study and were considered spatially independent with respect to the movements of small mammals, but not temporally independent. Surveys were completed by members of the Muṯitjulu Community, staff from UKTNP, and Steve McAlpin, a consultant ecologist.

Rainfall and fire

Rainfall records were compiled from daily rain gauge data collected near the UKTNP headquarters building from 1968 to the present. Fire histories were obtained for each site and each survey from satellite image-based fire mapping undertaken by the park. Widespread fires occurred frequently (e.g., 2002, 2004, and 2006), the most extreme of which occurred in 2002, affecting > 70% of UKTNP and 6 of the 8 study sites.

Field surveys

Site surveys were conducted in 1994, 1995, 1997, 1999, 2000, 2002, 2004, 2006, 2008, and 2010. With the exception of 1 survey in March 1995, all surveys were carried out in spring (October or November) to maximize the chance of recording mammal breeding activity, to coincide with reptile activity as part of broader survey objectives (not reported), and to minimize animal heat stress associated with trapping during summer.

Trapping effort at each site consisted of 250 aluminum “Elliott” type-A traps (33 × 10 × 10 cm; Elliott Scientific Equipment, Upwey, Victoria, Australia) and 36 pitfall traps (20-liter plastic buckets). Elliott traps were arranged in 10 rows of 25 traps, with each trap separated by 20 m. Pitfall traps were arranged in 4 arrays in a cross formation, with a central pitfall bucket surrounded by 4 “arms” each containing 2 buckets spaced 5 m apart (i.e., 9 buckets per trap array). Pitfall trap lines were placed to sample the environmental or topographical variation within a site. A drift fence of wire mesh, 30 cm high, ran between each bucket to maximize the chance of animals encountering a trap. Elliott traps were baited with a mixture of oats, peanut butter, and water in the late afternoon and checked in the early morning. Pitfall traps were checked 2–3 times daily depending on ambient temperatures. All traps remained open for 3 days at each site on every survey. Prior to 2000, data were available for species identity only; from 2000 onward, animals were weighed, and inspected for sex and reproductive condition. All animals were released at the point of capture. Captured animals were marked using a permanent marker pen to ensure identification of recaptures on subsequent mornings; this involved placing a small mark on the inside of ears. All the methods employed conform to the American Society of Mammalogists’ guidelines for animal research (Sikes et al. 2016). This work was conducted under approval from the Director of National Parks Australia.

Tests of the 3 broad hypotheses

Changes in the total number of individuals captured (C; hereafter, “captures” refers to numbers of individuals, i.e., excluding recaptures) over time formed the basis of tests of the 3 hypotheses (H1–H3 above). Capture success was determined for rodents and dasyurid marsupials (excluding Pseudantechinus macdonnellensis, which was not targeted by pitfall traps, and separately for the larger D. blythi, which is rarely caught in pitfall traps and has a restricted distribution across the park) by dividing the total number of individuals captured (C) by total trap nights for each survey occasion. Variability in the total number of individuals captured across years for the mammal groups and individual species was determined using the coefficient of variation (CVC) expressed as a percentage of the mean. These analyses were used to test our first hypothesis (H1) that dasyurid marsupial populations would exhibit less variability and lower capture rates than rodents.

Hypothesis 2 relates to the speed and magnitude of mammal responses to rainfall. We first explored these relationships using Spearman rank correlation analyses of small dasyurid and rodent captures and cumulative rainfall in the preceding 3, 6, and 12 months leading up to each survey (CR3, CR6, and CR12). We used both aggregated pitfall and Elliott trap captures and pitfall-only captures between 1997 and 2010 as trappability of different mammal groups varied overall and in response to seasonal conditions (Supplementary Data SD1). Therefore, where data were available, we repeated some analyses with pitfall trap data alone to ensure consistency of results given the variation in efficiency and equivalency between the trapping methods. Differences in the temporal responses of dasyurid marsupials and rodents to rainfall were then assessed using estimates of the finite rate of increase (λ) across consecutive surveys (t and t + 1). Since our best estimates of population size were total numbers of individuals captured (C) within each survey, we simply estimated the finite rate of increase as λ = (Ct+1/Ct). Lambda (λ) values of > 1 and < 1 indicate increasing and decreasing populations, respectively.

Our 2nd hypothesis (H2) was that the dasyurid marsupials would respond more slowly (i.e., show delayed responses) and less strongly (i.e., smaller increases in captures across consecutive surveys) to rainfall than rodents. Cross-survey comparisons with different preceding rainfall (CR3, CR6, and CR12) profiles yielded 5 general tests of this hypothesis (full details in Table 1). These tested for: 1) no change in marsupial or rodent captures across surveys (H2a), 2) an increase in rodents but not marsupials (H2b), 3) a decrease in rodents but not marsupials (H2c), 4) a larger increase in rodents than marsupials (H2d), and 5) a larger decrease in rodents than marsupials (H2e). Three cross-survey comparisons were available for H2c and H2d. All comparisons were made using all trap captures and pitfall-only captures (where available; Table 1).

Table 1.

Cross-survey comparisons of responses of rodent and dasyurid marsupial groups to antecedent rainfall in southwest Northern Territory, Australia. CR comp is the period of cumulative rainfall of interest prior to each survey (3, 6, or 12 months). δCR is the difference (mm) in cumulative rainfall between survey 2 (t + 1) and survey 1 (t) for each CR comp (nd = no data).

Table 1.

Cross-survey comparisons of responses of rodent and dasyurid marsupial groups to antecedent rainfall in southwest Northern Territory, Australia. CR comp is the period of cumulative rainfall of interest prior to each survey (3, 6, or 12 months). δCR is the difference (mm) in cumulative rainfall between survey 2 (t + 1) and survey 1 (t) for each CR comp (nd = no data).

Finally, to explore the effect of prescribed burns and the large wildfire of 2002 that affected 6 of the 8 sites on the mammal groups (H3), we first determined the number of captures of dasyurids (excluding D. blythi) and rodents at each site within each survey year. Sites were then classified by habitat type as “burned” (sites containing at least some area burned within the past 5 years) and “unburned” (no burned areas within the past 5 years), and total captures of both mammal groups were determined across all burned and unburned sites within each survey year. Finally, total captures were determined for both habitat types across all survey years. We first tested for a difference in habitat preference (burned versus unburned) within rodent and marsupial groups separately during each survey year using the chi-squared (χ2) goodness of fit test assuming equal expected counts in burned and unburned plots. This tested for evidence of habitat preference within each mammal group. We then tested for differences in habitat preference between the 2 mammal groups (rodents versus marsupials) using the chi-squared (χ2) goodness of fit test with habitat type and mammal group as blocked variables, again separately for each survey year.

Results

Capture rates and variability in dasyurids and rodents (H1)

From 1994 to 2010, the survey amassed 68,640 trap nights (60,000 Elliott and 8,640 pitfall; 1 trap night = 1 trap open for 1 night). This yielded 2,988 individual small mammals captured (2,676 rodents, 267 small dasyurid marsupials, and 45 D. blythi), with an overall trapping success of 4.4%. Total trapping success was highest for rodents (3.9%), followed by small dasyurids (0.4%) and D. blythi (0.07%). Ten mammal species were recorded: 4 rodents (M. musculus, P. hermannsburgensis, P. desertor, N. alexis) and 6 marsupials (P. macdonnellensis, S. ooldea, S. youngsoni, S. hirtipes, D. blythi, N. ridei).

Rodents dominated the mammal assemblage, with P. hermannsburgensis being the most commonly captured species (1,336 total pitfall and Elliott trap captures across 10 surveys), followed by the introduced M. musculus (803 captures) and the native N. alexis (381 captures; 44% of which occurred in 1 year). Small dasyurids were caught far less frequently than rodents, with S. hirtipes and P. macdonnellensis being least often encountered (7 and 12 captures, respectively). Even S. youngsoni, the most abundant marsupial (with 104 captures), was caught less frequently than P. desertor, the least common rodent (143 captures).

Capture rates varied widely across the mammal groups and species throughout the 16-year study period (Figs. 2A–D). Overall, the fewest captures occurred in 2002 and 2008 (57 and 118 captures, respectively), and the most captures occurred in 1999 and 2000 (721 and 690, respectively; Figs. 2A and 2B). Differences in total annual capture rates mainly reflected variation in captures of P. hermannsburgensis, M. musculus, and N. alexis (totals of 649 and 612 individuals captured in 1999 and 2000 versus 50 in 2002; Fig. 2C). This pattern deviated from that of marsupials (Fig. 2D), which had lower capture rates overall and a less pronounced peak in 1999–2000. Captures of marsupials still varied widely across years (from 5 individuals in 2002 to 67 in 2010), and fluctuated in a broadly synchronous way with rodents (Fig. 2B), especially for pitfall-only data (Fig. 2E). Some species also showed order of magnitude or greater population increases across surveys (e.g., N. ridei in 2008–2010 and N. alexis in 1997–1999; Figs. 2C and 2D) that did not occur in other species. Dasycercus blythi was caught in the 4 surveys up to 2000 but not thereafter (Fig. 2A).

Fig. 2.

Captures of small mammals during the 1994–2010 study period. A) Total number of individuals captured of marsupials (small dasyurid marsupials and Dasycercus blythi shown separately) and rodents in each survey year; B) total number of individuals captured of the same species and species groups on log10 scale; C) total number of individuals captured of rodent species; D) total number of individuals captured of marsupial species; E) captures of rodents and marsupials in pitfall traps; F) rainfall in 3-, 6-, and 12-month periods prior to each survey.

Rodents exhibited greater overall variability in capture rates across surveys than marsupials (CVC = 81% versus 64%), a pattern that was stronger if only pitfall data are considered (CVC = 91% versus 64%; Fig. 2E). However, there were large interspecific differences within mammal groups, with annual captures of some dasyurid species being more variable than those of some rodents. For example, the most variable species were the dasyurids N. ridei (CVC = 119%) and D. blythi (CVC = 135%), and the rodent N. alexis (CVC = 135%). Species with lower interannual variability in capture rates included both dasyurids (S. youngsoni, CVC = 65%; S. ooldea, CVC = 90%) and rodents (P. hermannsburgensis, CVC = 77%; P. desertor, CVC = 80%; and M. musculus, CVC = 105%). Due to the higher overall capture rate of rodents versus dasyurids, the range of total rodent captures across years (52 to 670) was greater than that of dasyurids (5 to 71).

Response of dasyurids and rodents to rainfall (H2)

Total rainfall varied widely throughout the 16-year study period (Fig. 2F), with cumulative 12-month preceding rainfall (CR12) ranging from 168 mm (2008) to 709 mm (2000). Rainfall in the 3- and 6-months preceding each survey (CR3 and CR6) was even more variable (CR3 = 0–136 mm and CR6 = 11–168 mm, respectively) and often uncorrelated with CR12.

There were no obvious patterns between the preceding 12-month rainfall and mammal captures. For example, 690 mammals (34 small dasyurids, 8 D. blythi, and 648 rodents) were captured in the wettest survey year (2000; CR12 = 709 mm), fewer than those captured in 1999 (37, 14, and 670, for a total of 721), which was a relatively dry year (CR12 = 224 mm). In the very dry year 2008 (CR12 = 168 mm), 118 mammals were captured (17 dasyurids, 0 D. blythi, and 101 rodents), similar to the number captured in 2010 (169 total), which was much wetter (CR12 = 390 mm). Correlation analysis uncovered no significant relationships between CR12 and total captures of either marsupials (excluding D. blythi) (P > 0.10 for r and ρ; Fig. 3A) or rodents (P > 0.10; Fig. 3B).

Fig. 3.

Relationships between total captures (in pitfall and Elliott traps) of marsupials and rodents with rainfall in the 3, 6, and 12 months preceding each survey over the 1994–2010 study period. A), C), and D) Marsupials and rainfall in previous 12, 6, and 3 months, respectively; B), E), and F) rodents and rainfall in previous 12, 6, and 3 months, respectively.

In contrast, there were significant or marginally significant positive relationships between total captures of marsupials and cumulative rainfall in the previous 6 months (P < 0.1; Fig. 3C) and 3 months (P < 0.1 and P < 0.01; Fig. 3D). Data from pitfall traps only also showed that capture rates of marsupials generally increased with CR6 and CR3 (Figs. 4A and 4B) but not CR12 (ρ = 0.33, P > 0.10).

Fig. 4.

Relationships between pitfall trap captures of dasyurid marsupials and rodents with rainfall in the 3, 6, and 12 months preceding each survey over the 1994–2010 study period. A) Marsupials, 6 months; B) marsupials, 3 months; C) rodents, 6 months; D) rodents, 12 months.

There were no relationships between total captures of rodents and CR6 or CR3 (P > 0.1; Figs. 3E and 3F), although a weak positive relationship existed between rodents captured in pitfall traps and CR6 (ρ = 0.69, P < 0.05; Fig. 4C), and the highest capture rate for rodents occurred following the wettest preceding 12-month period (Fig. 4D).

Table 1 shows the finite rate of population growth (λ) in captures of mammal groups between consecutive surveys. First, we hypothesized (H2a) that capture rates of both rodents and marsupials would be similar in 1997 and 1999 due to similar preceding rainfall conditions in both years. However, total captures of both groups more than doubled in 1999 relative to 1997 (λROD = 3.16 and λMAR = 2.18; Table 1). There was no evidence that rodents or marsupials responded to rainfall within 3 months (H2b), since between 1994 and 1995 marsupials increased (λMAR = 2.31) while rodents decreased (λROD = 0.82). However, we lacked specific pitfall trap data for these years. There was also no consistent evidence that rodents or marsupials declined during short-term 3- to 6-month-long drought (H2c), with capture rates increasing or declining in either or both groups depending on the survey comparison (Table 1).

There was strong independent evidence, based on pitfall trap data only, however, that captures of rodents increased more than captures of marsupials following at least 6 months of favorable rainfall (H2d). Indeed, in all 3 relevant cross-survey comparisons (1999–2000, 2002–2004, and 2008–2010) λROD exceeded that of λMAR, with the greatest difference occurring in the very wet year 2010 (12.25 versus 4.47; Table 1). There was also evidence that rodents declined more severely than marsupials under long-term (12-month) drought conditions (H2e), based both on aggregate captures (λROD = 0.38, λMAR = 0.65; Table 1) and on pitfall-only captures (λROD = 0.25, λMAR = 0.65; Table 1). Collectively, these data suggest that rodents tended to respond more strongly to longer-term (6- to 12-month) but not short-term (3-month) rainfall patterns than marsupials.

Rodent and dasyurid responses to wildfire (H3)

The number of study sites affected by fire in the previous 5 years varied widely across surveys, ranging from 6 (out of 8 sites) in 2002, 2004, and 2006, to none in 2000. At least one-half of all sites had been burned in 7 out of 10 surveys, with only 1999, 2000, and 2008 containing 2 or fewer burned sites. The extensive wildfires of 2002 reduced the capture rate of both mammal groups: in 2000, 648 rodents and 34 marsupials were captured during the survey, this reduced to 34 rodents and 5 marsupials following the fires in 2002.

More marsupials and rodents were captured on burned sites in all years except 1999, 2000, and 2008. However, this does not account for differing numbers of burned versus unburned sites across years. Assuming equal mean capture rates in unburned and burned plots, total captures of rodents were higher than expected in burned plots across all years (χ21 = 95.6; P < 0.001) and within all individual years (P < 0.05 for all) except 2002 (χ21 = 1.64; P > 0.05). Very high relative capture rates (RCR = mean capture rate in burned plots/mean capture rate in unburned plots) were observed in burned plots in 1994 (RCR = 7.6), 1995 (3.6), 1997 (5.4), 2004 (6.5), and 2006 (5.3). Rodents appeared to strongly prefer burned areas about 2 years after the widespread severe fires of 2002 (RCR = 6.5 in 2004), but this preference then declined through 2006, 2008, and 2010 (RCR = 5.3, 2.1, and 1.8, respectively).

Marsupials showed a significant preference for burned plots in 1994, 1995, and 2010 (P < 0.05 for all), but in all other years showed no significant preference. However, all captures (n = 5) in 2002 occurred in burned plots, and the RCR exceeded 1 in 1997 and 2004. As with rodents, the strongest preference for burned plots was observed soon after fire, especially in 1994 (RCR = 6.6), and to a lesser extent in 2010 (RCR = 2.5) and 2004 (RCR = 1.6). Unlike rodents, fewer marsupials were recorded in burned plots in 1999, 2006, and 2008 (RCR < 1), although these differences were not significant (P > 0.05). Consistent with these results, rodents and marsupials showed no difference in preference for burned versus unburned habitats in all years except in 1999 (χ21 = 3.9; P < 0.05), 2006 (χ21 = 30.3; P < 0.001), and marginally so in 2008 (χ21 = 3.2; P < 0.07), when rodents strongly preferred burned plots and marsupials showed no preference.

Discussion

The environmental fluxes associated with rainfall, drought, and fire in central Australian deserts are usually assumed to be responsible for the mammal “boom” and “bust” events that occur in these landscapes. However, these relationships have been little quantified, albeit with some notable exceptions (e.g., Southgate and Masters 1996; Pavey et al. 2008; Greenville et al. 2013, 2016). Over the 16 years of the present study, we tested specific hypotheses about the effects of varying rainfall and fire on desert-dwelling mammals in Australia. Unexpectedly, our initial predictions were supported only in part. Our study varied considerably from others conducted in arid Australia, most notably because the interval between samples was long (usually 2 years) and because we sampled a larger area than most previous studies. Because of these differences in our sampling design, it is possible that the immediate responses of small mammals to fire and rainfall were missed, that ephemeral irruptions could have occurred and subsided without being detected, or that responses differed in strength across the different land systems that we surveyed. We keep these possibilities in mind when discussing the results in terms of our broad hypotheses below.

Capture rates and variability in dasyurids and rodents

Rodents were caught more frequently than dasyurid marsupials, which supported our initial hypothesis, but our supposition that dasyurid populations would exhibit less variability than rodents was not well supported. In the same general study area, Masters (1993) observed a much greater increase in numbers of rodents (P. hermannsburgensis, M. musculus) than dasyurids (D. blythi, N. ridei, and S. youngsoni) following rain, and proposed that the observed stability of dasyurid populations arose from their tendency for reproduction to be locked into seasonal, temperature-driven changes in food availability. In contrast, our study showed broadly synchronous temporal and directional changes in capture rates and a typical boom and bust cycle in both rodents and marsupials, albeit of greater size for rodents.

Generally, this synchronicity may be partly explained by dietary overlap between groups, particularly following rain. Although rodents are omnivorous, some studies have shown a preference by rodents for invertebrates over seed and other food sources (Murray and Dickman 1994; Murray et al. 1999). Simultaneous exploitation of invertebrate resources (e.g., an abundance of termites following rain) by rodents and dasyurids may explain this pattern. The typically greater absolute fluctuation in rodent numbers may reflect their additional capacity to utilize seed resources. For dasyurids, the ability of most to store energy as fat in their tails, reduce energy demands via torpor during resource scarcity (Geiser and Körtner 2010), and selectively exploit high-quality food patches during drought (Bleicher and Dickman 2016) may compensate for their reduced fecundity compared to rodents, resulting in similar overall demography.

The general situation is complicated, however, by differences within both mammal groups. For example, P. hermannsburgensis, N. ridei, and D. blythi underwent massive population fluctuations not seen in other species within their respective groups. Similarly, Letnic (2002) found that population growth of the rodent N. alexis was muted compared to that of other sympatric rodents in the Simpson Desert following rain. Within species, Dickman et al. (1999) found that P. hermannsburgensis irrupted in the absence of rain at 1 study site and responded more slowly than expected to rainfall at another. These results suggest that many factors, perhaps including different habitat requirements, relationships with predators, competition, or breeding patterns, may generate asynchronous population dynamics among some desert mammals (Greenville et al. 2016).

Responses of dasyurids and rodents to rainfall

Capture rates of mammals did not always fluctuate predictably with rainfall. Both rodents and dasyurids appeared to respond positively to accumulated rainfall over the prior 6 months, but only dasyurids responded over the 3-month time frame. There was no evidence of a rapid boom in M. musculus numbers 2 months after rain, as described by Dickman et al. (1999). Rodent numbers tended to decrease more quickly than those of dasyurids during long (12-month), but not short (3- to 6-month) droughts. However, factors other than just rainfall clearly influenced population size. In some surveys, capture rates increased following drought (e.g., 1999), and in others they failed to increase after rain (e.g., 2010).

Three additional factors may have influenced our results. In the Simpson Desert, Dickman et al. (1999) reported peak populations of N. alexis and P. hermannsburgensis between June and August, with numbers declining precipitously by summer. As noted above, most of our surveys were carried out in late spring and 2 years apart, increasing the chance that actual population peaks and troughs were missed. Secondly, population increases during dry periods may reflect the high diversity of habitat and topography of our study sites (Bennison et al. 2013), which could influence food availability. Most previous studies have taken place in relatively uniform spinifex grassland (Masters 1993; Southgate and Masters 1996; Dickman et al. 1999; Greenville et al. 2016) where mammalian dynamics could be expected to be more tightly attuned to the rainfall regime. The drainage lines, waterholes, and varied grassland and wooded habitats of our sites likely provided different levels of food resources at different times for the study species, potentially allowing increases in populations even during periods of low rainfall (Free et al. 2013, 2015). Finally, our results may be due to the timing of the surveys which generally coincided with the main dasyurid breeding season (Aslin 1995; McKenzie and Cole 1995).

Rodent and dasyurid responses to fire

Consistent with our hypothesis, fire appeared to immediately reduce capture rates of both rodents and dasyurids, with both groups declining drastically following the extensive wildfire in 2002 which occurred just prior to the survey. However, following this initial decline rodents and dasyurids rapidly increased in abundance, and by 2 years post-wildfire (e.g., 2004) both groups showed a strong preference for burned habitat. In rodent populations, but not dasyurids, this pattern of preference was sustained for at least 4–6 years after fire, and over the entire study period, which contained both wildfire and prescribed fire, rodents were consistently more numerous in plots that had burned within the past 5 years (“burned” plots). This tendency was weaker, but still present, in marsupials, which showed a preference for burned plots in 4 of the 10 census years, and no preference in other years.

The preference of both rodents and dasyurids for habitat that had burned within the past 5 years, and as soon as 2 years following major wildfire (e.g., 2002), suggests that prescribed burns and occasional severe wildfires in the landscapes of central Australia are not necessarily detrimental to mammal communities, and may be favorable as part of a landscape fire mosaic. This result accords with similar studies conducted in the Chihuahuan Desert of North America (Monasmith 1997) but not with work reported elsewhere in arid Australia (Letnic et al. 2005; Pastro et al. 2011). The latter studies suggest instead that fires create open habitats that increase the hunting success of introduced predators such as European red foxes and feral cats. It is not clear whether introduced predators have similar effects at Uluṟu. Feral cats are subject to intermittent removal by National Park staff, and foxes are sometimes present. Possibly uncontrolled populations of the dingo (Canis dingo) at Uluṟu suppress populations of foxes and feral cats, as they do elsewhere in arid Australia (Letnic et al. 2011b), especially in the wake of fires (Bliege Bird et al. 2018). Although this possibility remains to be tested, dingoes are less likely than cats and foxes to heavily depredate dasyurids and small rodents (Spencer et al. 2014), and may allow these small mammals to exploit burned sites.

The omnivorous diet of Australian desert rodents (Murray et al. 1999) may facilitate the exploitation of the new plant growth and seed resources that are often available in recently burned areas. Captures of rodents surged in plots burned during the extensive 2002 wildfires, and then stayed higher than in unburned plots for at least 6 more years. This pattern of postfire persistence was less pronounced in dasyurids, especially 2 years postburn, perhaps due to the longer period that may be needed for the recovery of insect populations (Leonard 1976) in these habitats.

In summary, this 16-year study of small mammals at UKTNP showed that, contrary to expectation, both rodent and dasyurid marsupial populations fluctuated in a broadly synchronous manner over time. While the larger sizes of the rodent populations resulted in larger absolute changes in population size, boom and bust cycles, driven at least in part by rainfall, were characteristic also of dasyurids. Furthermore, both rodents and dasyurids recovered well from drought and wildfire, and tended to prefer habitats burned 2–6 years previously. Our findings contrast with much previous research (e.g., Letnic et al. 2005; Pastro et al. 2011; Greenville et al. 2016). These differences may reflect, in part, differences in sampling regimes that have been used across studies, but could also reflect differences in other factors such as levels of predator activity. This later possibility invites further research.

Supplementary Data

Supplementary data are available at Journal of Mammalogy online.

Supplementary Data SD1.—Variation in trappability of the study species.

Acknowledgments

We would like to acknowledge the Director of National Parks for supplying all funds and logistics associated with this study. Many members of the Muṯitjulu Community and past and present staff of Uluṟu-Kata Tjuṯa National Park energetically and enthusiastically contributed their expertise and time to complete the surveys. We particularly acknowledge R. Uluṟu, B. Tjikatu, D. Walkabout, S. and H. Wilson, M. Teamay, N. Jingo, E. Richards, R. Kulitja, J. Trigger, Wangin No 1, H. Reid, P. Hookey, M. Starkey, P. Wilson, L. Lester, C. Woods, T. Guest, J. Clayton, S. Steele, M. Wilson, R. Frith, S. Wright, G. Cole, D. Moneymoon, N. Couthard, N. and R. Okai, and many members of the Muṯitjulu Community who have now passed away and should not be named here. We thank S. McAlpin for his commitment, enthusiasm, resilience, and monumental effort in overseeing the surveys and W. Powrie for his help across many years.

Literature Cited

Allan

G. E.

2002

.

Fire regimes in the spinifex landscapes of Australia

. Pp.

145

–

176

in

Flammable Australia: the fire regimes and biodiversity of a continent

(R.A. Bradstock , J. E. Williams , and A. M. Gill , eds.).

Cambridge University Press

,

Cambridge, United Kingdom

.

Aslin

H

1995

.

Ooldea dunnart

. Pp.

152

–

153

in

The mammals of Australia

(R. Strahan , ed.).

Reed New Holland

,

New South Wales, Sydney, Australia

.

Bennison

K.

2013

.

Habitat use and ecological observations of the Ooldea dunnart (Sminthopsis ooldea) at Uluṟu–Kata Tjuṯa National Park, Northern Territory

.

Australian Mammalogy

35

:

175

–

179

.

Bleicher

S. S.

2016

.

Bust economics: foragers choose high quality habitats in lean times

.

PeerJ

4

:

e1609

.

Bliege Bird

R.

2018

.

Aboriginal burning promotes fine-scale pyrodiversity and native predators in Australia’s western desert

.

Biological Conservation

219

:

110

–

118

.

Breed

B.

2007

.

Native mice and rats

.

CSIRO Publishing

,

Collingwood, Victoria, Australia

.

Chung-MacCoubrey

A.

2009

.

Captures of Crawford’s gray shrews (Notiosorex crawfordi) along the Rio Grande in central New Mexico

.

Western North American Naturalist

69

:

260

–

263

.

Degen

A. A

1997

.

Ecophysiology of small desert mammals

.

Springer

,

Berlin, Germany

.

Dickman

C. R.

2010

.

Social organization and movements of desert rodents during population “booms” and “busts” in central Australia

.

Journal of Mammalogy

91

:

798

–

810

.

Dickman

C. R.

2001

.

Population dynamics of three species of dasyurid marsupials in arid central Australia: a 10-year study

.

Wildlife Research

28

:

493

–

506

.

Dickman

C. R.

1999

.

Long-term dynamics of rodent populations in arid Australia: the influence of rainfall

.

Wildlife Research

26

:

389

–

403

.

Dickman

C. R.

1995

.

Long-range movements of small mammals in arid Australia: implications for land management

.

Journal of Arid Environments

31

:

441

–

452

.

Director of National Parks

2010

.

Uluṟu-Kata Tjuṯa National Park Management Plan 2010–2020

.

Australian Government

,

Canberra, Australian Capital Territory, Australia

.

D’Souza

J. B.

2013

.

Perfect storm: demographic responses of an irruptive desert mammal to prescribed burns following flooding rain

.

Austral Ecology

38

:

765

–

776

.

Fennessy

J

2009

.

Home range and seasonal movements of Giraffa camelopardalis angolensis in the northern Namib Desert

.

African Journal of Ecology

47

:

318

–

327

.

Fisher

D. O.

1993

.

Diets of insectivorous marsupials in arid Australia: selection for prey type, size or hardness

?

Journal of Arid Environments

25

:

397

–

410

.

Fox

B. J

2011

.

Review of small mammal trophic structure in drylands: resource availability, use, and disturbance

.

Journal of Mammalogy

92

:

1179

–

1192

.

Free

C. L.

2013

.

Resource pulses in desert river habitats: productivity-biodiversity hotspots, or mirages

?

PLoS One

8

:

e72690

.

Free

C. L.

2015

.

Diversity and community composition of vertebrates in desert river habitats

.

PLoS One

10

:

e144258

.

Geiser

F

2004

.

The role of torpor in the life of Australian arid zone mammals

.

Australian Mammalogy

26

:

125

–

134

.

Geiser

F.

2010

.

Hibernation and daily torpor in Australian mammals

.

Australian Zoologist

35

:

204

–

215

.

Greenville

A. C.

2012

.

Extreme climatic events drive mammal irruptions: regression analysis of 100-year trends in desert rainfall and temperature

.

Ecology and Evolution

2

:

2645

–

2658

.

Greenville

A. C.

2013

.

Extreme rainfall events predict irruptions of rat plagues in central Australia

.

Austral Ecology

38

:

754

–

764

.

Greenville

A. C.

2016

.

Population dynamics of desert mammals: similarities and contrasts within a multispecies assemblage

.

Ecosphere

7

:

e01343

.

Griffin

M

1990

.

A review of taxonomy and ecology of gerbilline rodents of the central Namib Desert, with keys to the species (Rodentia: Muridae)

. Pp.

83

–

98

in

Namib ecology: 25 years of Namib research

(M. K. Seely , ed.).

Transvaal Museum

,

Pretoria, South Africa

.

Kelt

D. A

2011

.

Comparative ecology of desert small mammals: a selective review of the past 30 years

.

Journal of Mammalogy

92

:

1158

–

1178

.

Latz

P

1999

.

Bushfires and bushtucker: aboriginal plant use in central Australia

.

IAD Press

,

Alice Springs, Australia

.

Leonard

B

1976

.

The effect of forest fire on the ecology of leaf litter organisms

.

Victorian Naturalist

94

:

119

–

122

.

Letnic

M

2002

.

Long distance movements and the use of fire mosaics by small mammals in the Simpson Desert, central Australia

.

Australian Mammalogy

23

:

125

–

134

.

Letnic

M.

2010

.

Resource pulses and mammalian dynamics: conceptual models for hummock grasslands and other Australian desert habitats

.

Biological Reviews

85

:

501

–

521

.

Letnic

M.

2004

.

The responses of small mammals and lizards to post-fire succession and rainfall in arid Australia

.

Journal of Arid Environments

59

:

85

–

114

.

Letnic

M.

2011b

.

Does a top predator suppress the abundance of an invasive mesopredator at a continental scale

?

Global Ecology and Biogeography

20

:

343

–

353

.

Letnic

M.

2011a

.

Resource pulses, switching trophic control, and the dynamics of desert small mammal assemblages in arid Australia

.

Journal of Mammalogy

92

:

1210

–

1222

.

Letnic

M.

2005

.

The responses of mammals to La Niña (El Niño Southern Oscillation) - associated rainfall, predation, and wildfire in central Australia

.

Journal of Mammalogy

86

:

689

–

703

.

Letnic

M.

2013

.

Desert small mammal responses to wildfire and predation in the aftermath of a La Niña driven resource pulse

.

Austral Ecology

38

:

841

–

849

.

Lima

M.

2008

.

Chihuahuan Desert kangaroo rats: nonlinear effects of population dynamics, competition, and rainfall

.

Ecology

89

:

2594

–

2603

.

Lindenmayer

D. B.

2012

.

Value of long-term ecological studies

.

Austral Ecology

37

:

745

–

757

.

Masters

P

1993

.

The effects of fire-driven succession and rainfall on small mammals in spinifex grassland at Uluṟu National Park, Northern Territory

.

Wildlife Research

20

:

803

–

813

.

Masters

P

1998

.

The mulgara Dasycercus cristicauda (Marsupialia: Dasyuridae) at Uluṟu National Park, Northern Territory

.

Australian Mammalogy

20

:

403

–

407

.

Masters

P.

2012

.

Population dynamics of Dasycercus blythi (Marsupialia: Dasyuridae) in central Australia: how does the mulgara persist

?

Wildlife Research

39

:

419

–

428

.

McGregor

H.

2015

.

Feral cats are better killers in open habitats, revealed by animal-borne video

.

PLoS One

10

:

e133915

.

McKenzie

N. L.

1995

.

Lesser hairy footed dunnart

. Pp.

152

–

153

in

The mammals of Australia

(R. Strahan , ed.).

Reed New Holland

,

New South Wales, Sydney, Australia

.

Meserve

P. L.

2011

.

Global climate change and small mammal populations in north-central Chile

.

Journal of Mammalogy

92

:

1223

–

1235

.

Milstead

W. B.

2007

.

Spatial ecology of small mammals in north-central Chile: role of precipitation and refuges

.

Journal of Mammalogy

88

:

1532

–

1538

.

Monasmith

T. J

1997

.

Fire effects on small mammals and vegetation of the northern Chihuahuan Desert

.

M.S. thesis

,

Texas Tech University

,

Lubbock

.

Morton

S. R

1978

.

Torpor and nest-sharing in free-living Sminthopsis crassicaudata (Marsupialia) and Mus musculus (Rodentia)

.

Journal of Mammalogy

59

:

569

–

575

.

Murray

B. R.

1994

.

Granivory and microhabitat use in Australian desert rodents: are seeds important

?

Oecologia

99

:

216

–

225

.

Murray

B. R.

1999

.

The dietary ecology of Australian desert rodents

.

Wildlife Research

26

:

421

–

437

.

Newsome

A. E.

1975

.

Outbreaks of rodents in semi-arid and arid Australia: causes, preventions, and evolutionary considerations

. Pp.

117

–

151

in

Rodents in desert environments

(I. Prakash and P. K. Ghosh , eds.).

Dr. W. Junk

,

The Hague, The Netherlands

.

Nguyen

V.

2015

.

On the validity of visual cover estimates for time series analyses: a case study of hummock grasslands

.

Plant Ecology

216

:

975

–

988

.

Ojeda

R. A.

2011

.

Mammals of the Monte Desert: from regional to local assemblages

.

Journal of Mammalogy

92

:

1236

–

1244

.

Pastro

L. A.

2011

.

Burning for biodiversity or burning biodiversity? Prescribed burn vs. wildfire impacts on plants, lizards, and mammals

.

Ecological Applications

21

:

3238

–

3253

.

Pavey

C. R.

2017

.

The role of refuges in the persistence of Australian dryland mammals

.

Biological Reviews

92

:

647

–

664

.

Pavey

C. R.

2014

.

Population dynamics and spatial ecology of a declining desert rodent, Pseudomys australis: the importance of refuges for persistence

.

Journal of Mammalogy

95

:

615

–

625

.

Pavey

C. R.

2008

.

Population dynamics and prey selection of native and introduced predators during a rodent outbreak in arid Australia

.

Journal of Mammalogy

89

:

674

–

683

.

Plomley

N. J. B

1972

.

Some notes on plagues of small mammals in Australia

.

Journal of Natural History

6

:

363

–

384

.

Previtali

M. A.

2009

.

Population dynamics of two sympatric rodents in a highly variable environment: rainfall, resource availability, and predation

.

Ecology

90

:

1996

–

2006

.

Previtali

M. A.

2010

.

Effects of more frequent and prolonged El Niño events on life-history parameters of the degu, a long-lived and slow-reproducing rodent

.

Conservation Biology

24

:

18

–

28

.

Reid

J. R. W.

1993

.

Uluṟu fauna: the distribution and abundance of vertebrate fauna of Uluṟu (Ayers Rock-Mount Olga) National Park, N.T

.

Australian National Parks and Wildlife Service

,

Canberra, Australian Capital Territory, Australia

.

Shenbrot

G

2014

.

Population and community dynamics and habitat selection of rodents in complex desert landscapes

.

Mammalia

78

:

1

–

10

.

Shenbrot

G.

2010

.

Long-term study of population dynamics and habitat selection of rodents in the Negev Desert

.

Journal of Mammalogy

91

:

776

–

786

.

Sikes

R. S.

2016

.

2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education

.

Journal of Mammalogy

97

:

663

–

688

.

Southgate

R.

2008

.

Post-fire ephemerals and spinifex-fuelled fires: a decision model for bilby habitat management in the Tanami Desert, Australia

.

International Journal of Wildland Fire

16

:

741

–

754

.

Southgate

R.

1996

.

Fluctuations of rodent populations in response to rainfall and fire in a central Australian hummock grassland dominated by Plectrachne schinzii

.

Wildlife Research

23

:

289

–

303

.

Spencer

E. E.

2014

.

Diet and prey selectivity of three species of sympatric mammalian predators in central Australia

.

Journal of Mammalogy

95

:

1278

–

1288

.

Sutherland

E. F.

1999

.

Mechanisms of recovery after fire by rodents in the Australian environment: a review

.

Wildlife Research

26

:

405

–

419

.

Thibault

K. M.

2010

.

Long-term insights into the influence of precipitation on community dynamics in desert rodents

.

Journal of Mammalogy

91

:

787

–

797

.

Whitford

W. G

2002

.

Ecology of desert systems

.

Academic Press

,

San Diego, California

.

Woolley

P. A

1984

.

Reproduction in Antechinomys laniger (‘spenceri’ form) (Marsupialia: Dasyuridae): field and laboratory observations

.

Australian Wildlife Research

11

:

481

–

489

.

Yang

L. H.

2010

.

A meta-analysis of resource pulse-consumer interactions

.

Ecological Monographs

80

:

125

–

151

.

© 2018 American Society of Mammalogists, www.mammalogy.org

© 2018 American Society of Mammalogists, www.mammalogy.org

Supplementary data

What kind of curve represents exponential growth?

What are population dynamics quizlet?

Which is an example of a population?

What causes logistic growth?