P u b l i s h i n g
Wildlife Research Volume 29, 2002 © CSIRO 2002
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Wildlife Research, 2002, 29, 423–429
Do European rabbits (Oryctolagus cuniculus) influence the population ecology of the burrowing bettong (Bettongia lesueur)? Alan J. RobleyA,C, Jeff ShortB and Stuart BradleyA A
School of Biological Science and Biochemistry, Murdoch University, Murdoch, WA 6007, Australia. B CSIRO Sustainable Ecosystems, Private Bag 5, Wembley, WA 6913, Australia. C Present address: Arthur Rylah Research Institute, Department of Natural Resources and Environment, PO Box 137, Heidelberg, Vic. 3084, Australia.
Abstract. The influence of the European rabbit (Oryctolagus cuniculus) on the survival of medium-sized native mammals remains unclear despite 60 years of speculation. Most medium-sized native species that might have been affected by the presence of rabbits are extinct, rare, or endangered. This limits the opportunity to study their interaction with introduced herbivores. We studied the effect of changes in rabbit density on aspects of the ecology of burrowing bettongs (Bettongia lesueur) reintroduced to mainland Australia on Heirisson Prong, Shark Bay, Western Australia. The rabbit population at the site grew to a 10-year high concomitant with a dry summer and low and declining pasture cover. Rabbit browsing led to widespread defoliation of, and subsequent death of, many palatable shrubs. Despite these adverse conditions, reproduction, recruitment and rate of increase of bettongs did not vary with changes in rabbit density, nor did the survival of adult males and females. This work casts doubt on the idea that competition with an introduced herbivore, such as the rabbit, was an important factor in the decline of the burrowing bettong. It highlights the need to understand the ecologies and life histories of native and introduced species in order to manage for the long-term persistence of native species. WR010 7 eAEf.teaJRctlo. bflreayb tisonburowingbetongs
Introduction Burrowing bettongs (Bettongia lesueur) once ranged across the southern two-thirds of mainland Australia from Broome in the north-west to the Murray–Darling junction in the south-east (Short and Turner 1993). The last museum record of this species from continental Australia is from 1942 (Kitchener and Vicker 1981). Finlayson (1958) and Burbidge and McKenzie (1989) have attributed its decline on the mainland to exploitative competition for food resources with introduced herbivores, especially the European rabbit (Oryctolagus cuniculus). Finlayson (1961), writing on observations he made in central Australia in 1931–35 and 1950–56, described the effect of rabbits on native species as ‘catastrophic’ due to their competition for food plants. Morton (1990) argued that habitat modification of refuge areas by waves of introduced herbivores, especially the rabbit, during recurrent droughts was a significant factor in the decline of small and medium-sized marsupials, including the burrowing bettong, in arid and semi-arid Australia. The recent reintroduction of the burrowing bettong to mainland Australia at Heirisson Prong, Shark Bay (Short et al. 1994; Short and Turner 2000) presented an opportunity to investigate the interaction between this vulnerable and endangered species (Baillie and Groombridge 1996; © CSIRO 2002
Maxwell et al. 1996) and the introduced European rabbit. In a three-year study of comparative diet (Robley et al. 2001), during which rabbits erupted to high numbers and then declined, we showed that the diets of rabbits and bettong differed statistically but overlapped most during summer when highly nutritious pasture was less abundant. The effect of rabbits on vegetation was obvious and widespread at the time of eruption. Here we describe changes in aspects of the population ecology of both bettongs and rabbits over the same period. If habitat modification or competition for food and shelter were major factors in the historical decline of the burrowing bettong, their effects should have been evident over the period of investigation. Methods Study site Heirisson Prong (26°4′S, 113°8′E) is a peninsula on the southern shores of Shark Bay, Western Australia approximately 900 km north of Perth. The conservation reserve on its northern tip is 12 km long and 2 km across at its widest point and approximately 1200 ha. Its semi-arid coastal environment supports a vegetation complex of low open heath and Acacia shrubs up to 2 m tall. Full descriptions of the reintroduction program and site conditions are given in Short et al. (1994) and Short and Turner (2000). Rabbits colonised the Shark Bay area in c. 1910 (Stodart and Parer 1988). The site is largely free of introduced 10.1071/WR01007
1035-3712/02/050423
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predators, protected by a barrier fence and a 200-km2 buffer zone that is baited regularly with 1080 poison (Short and Turner 2000). Data collection Long-term mean monthly rainfall records from 1893 to 1998 were obtained for Denham, approximately 20 km east of Heirisson Prong, from the Western Australian Bureau of Meteorology. We assessed changes in vegetation cover using a point-sampling technique (Grieg-Smith 1983). Assessments were made each season beginning in winter 1996 and finishing in summer 1998. We sampled vegetation across 18 permanent transects spaced at random intervals across Heirisson Prong. A transect was defined by a 50-m tape stretched across the crowns of plants. At every metre along the tape, a steel rod (2 mm diameter) was dropped to the ground. The number of contacts that non-woody parts of the plants made with the tape was recorded. Percentage foliage cover can exceed 100% due to the additive effect of multiple species. Spotlight counts of rabbits were conducted every three months between January 1995 and February 1998 to assess changes in their relative abundance. Rabbits were counted by two observers from the rear of a 4WD vehicle that traversed a standard route of 20 km, at a speed of 10–15 km h–1. The number of rabbits counted was averaged over the three nights. A measure of changes in absolute density was made to provide an independent estimate of actual numbers of rabbits on Heirisson Prong during this study. Estimates of absolute density of rabbits were made using warren entrance counts (Parer 1982; Parer and Wood 1986) in July 1996, April and November 1997, and May 1998. The number of active entrances per warren were counted along seven east–west transects that crossed Heirisson Prong, over a distance totalling 6.5 km. Each transect was 6 m wide. The number of active entrances was converted to numbers of rabbits using one of two formulae (Parer 1982; Parer and Wood 1986), depending on whether the rabbit population was breeding or not. The formula for a breeding population was applied to counts of warren entrances in July 1996 and May 1998. The formula for a non-breeding rabbit population was applied to counts in April and November 1997. The free-range population of bettongs on Heirisson Prong was monitored to enable estimation of the influence that rabbits may have on various aspects of bettong ecology. Monitoring was undertaken in summer, autumn, winter, and spring each year, from January 1996 to February 1999, by laying out 80 treadle-operated wire cage traps (56 × 22 × 22 cm) spaced at 100-m intervals baited with peanut butter and rolled oats. Traps were set for 2–3 nights over 2–3 sessions, with traps being moved to new locations each session. Individual bettongs were identified by either a numbered ear tag or a unique letter/number code using a Passive Implant Transponder (Central Animals Records Aust. Pty Ltd, Keysborough, Victoria). This allowed calculation of known-to-be-alive estimates. Bettongs that were translocated either from Dorre Island or released from captivity (Short and Turner 2000) were excluded in the calculation of demographic parameters. However, it was not possible to separate offspring born to females that were translocated or released from offspring of females born in situ. At each survey the identity and sex of each bettong was determined and reproductive condition (presence/absence of pouch young and elongated teats) and weight (g) were measured. Pouch young were assigned to broad categories of developmental stage. Only those described as small and unhaired (less than approximately 55 days old: Tyndale-Biscoe 1968) were used in the analysis of reproduction to avoid duplication of measurements of females and pouch young caught in subsequent surveys. Recruitment was calculated as the number of sub-adult bettongs caught in a trapping survey divided by the total number of bettongs caught during that survey. Sub-adults were those animals weighing less than 880 g (Short and Turner 1999).
A. J. Robley et al.
Data analysis It was assumed that changes in the proportion of female bettongs carrying pouch young, and the proportion of recruits entering the population were due to changes in food availability which could be indexed by cumulative rainfall or lagged rainfall. To determine the best rainfall period, r2 values from simple regressions between reproduction and recruitment as dependant variables and rainfall as the independent variable were plotted. Thirteen independent variables were used in the regressions. These were cumulative rainfall over the previous two, three and four months and rainfall over intervals of 2–3 months and lagged by 1–5 months. These periods were selected to coincide with an assumed response time of vegetation to rainfall events and the length of pouch life and post-weaning survival. The percentage of projected foliage cover determined from the vegetation surveys was correlated with rainfall using Spearman rank correlation in Minitab V 10.51 Xtra. The data were examined for homogeneity of variance using Cochran’s C test (Fry 1994) before ANOVAs were performed. Non-replicated two-factor ANOVA was used to examine the changes in the proportion of recruits and the proportion of pouch young per female for the period January 1996 to October 1998 by year and season within year. Both year and season were fixed factors. It was assumed that there was no interaction between the two factors. Normality was checked by plotting cumulative normal probability plots. The relative abundance of rabbits, the number of bettongs known to be alive (excluding reintroduced individuals) and the rate of increase for both species were calculated to the end of February 1999. The observed rates of increase of bettongs were calculated from the change in estimates of bettongs known to be alive, with rate of increase assessed over an 11.5–12.5-month period. The rate of increase of rabbits was estimated from changes in relative abundance from the spotlighting surveys. These estimates were transformed to natural logarithms to calculate estimates of exponential rates of increase. A yearly exponential rate of increase (r) was calculated as the logged estimate of relative abundance in summer of one year minus the logged estimate in the previous summer (Bayliss 1987) The rate at which the populations doubled was calculated as 0.6931/r (Caughley 1977). Annual adult survival in bettongs was estimated using the program MARK (White and Burnham 1999). This program provides estimates of survival and recapture rates from marked animals that are re-encountered after release. Estimates were based on a Cormack–Jolly–Seber model (CJS). Estimates of the survival (∅) and recapture (P) probabilities for adult bettongs were calculated by comparing the global model with two factors (sex, s, and time, t), where both survival and recapture are time dependant (∅s×t, Ps×t; CJS model), to an additive model (∅s+t, and Ps+t). This is equivalent to a two-factor ANOVA testing for the interaction between sex and time for both survival and recapture. These models were tested using a likelihood ratio test (Lebreton et al. 1992).
Results Rainfall and vegetation The study period was characterised by high winter rainfall in 1996 and 1998 and low summer rainfall in 1997/98 (Fig. 1). Winter rainfall in 1996 was 222 mm, double the long-term mean for this three-month period and one of the five wettest winters in the 100-year record. The total rainfall for winter 1997 was 112 mm, typical of the long-term mean for winter. The rainfall for winter in 1998 (179 mm) was 68 mm above the long-term mean. No rainfall was recorded for the five months from November 1997 to March 1998. The long-term mean rainfall for this five-month period is 39 mm, hence the
Effect of rabbits on burrowing bettongs
425
Table 1. The annual exponential rates of increase, and doubling (+) and/or halving (–) time (months) for rabbit and bettong populations at Heirisson Prong during the study Rates of increase are calculated from spotlight indices of rabbits and estimates of bettongs known to be alive by comparing estimates from summer in one year with those of summer in the following year. Note: although reintroduced bettongs were excluded from these calculations, their offspring were included; thus population rates of increase may be overestimated
Rainfall (mm) and percentage plant cover
180
Rainfall Cover
160 140 120 100 80 60 40 20
1997
Nov
Jul
Sep
May
Jan
Mar
Nov
Jul
Sep
May
Jan
Mar
Nov
Jul
1996
Sep
May
Jan
Mar
Nov
Jul
1995
Sep
May
Jan
Mar
0
1998
Fig. 1. The monthly rainfall (mm) recorded at Denham, and the change in the percentage vegetation cover on Heirisson Prong. Percentage plant cover exceeds 100 due to the cumulative effects of multiple layers of vegetation.
1997/98 summer was dry, but typical of the long-term rainfall for this period. Vegetation cover reached a maximum (172.5%) in spring 1996 after the high rainfall in the preceding winter (Fig. 1). Vegetation cover declined to its lowest point (35%) in late autumn 1998. Vegetation cover was correlated with rainfall in the previous three months (r = 0.84, n = 8, P < 0.05). Changes in rabbit population characteristics The relative abundance of the rabbit population increased from five per spotlight kilometre in January 1996 to 18 per kilometre in December 1997. The population then declined sharply to less than 0.4 per spotlight kilometre in October 1998 (Fig. 2). By counting warren entrances, the density of rabbits was estimated at 14 ha–1 in July 1996 and April 1997, rising to 20
280 260 240 220
15
200 180 160
10
140 120 100
Number of bettongs
Rabbits per spotlight kilometre
Rabbit abundance Bettong abundance
80
5
Rabbit population Rate of increase Doubling/halving time (months) Bettong population Rate of increase Doubling time (months)
1996
1997
1998
–0.67 –12.40
0.97 +8.60
–2.07 –4.00
1.020 +8.20
0.79 +9.50
0.88 +10.60
38 ha–1 in November 1997. This latter figure equated to approximately 45600 rabbits in the study area. At this time, there were about 65 bettongs on Heirisson Prong (Short and Turner 2000), hence rabbits outnumbered bettongs by about 700 to one. The rabbit population subsequently crashed to pre-peak levels of 13 ha–1 in May 1998 and remained low. In 1996 the rabbit population, as assessed by spotlight counts, declined at an annual rate of increase of –0.67 (Table 1). In 1997 the annual rate of increase was 0.97 (Table 1), indicating that the rabbit population would double approximately every 8.6 months. The rabbit population then crashed in 1998 at an annual rate of increase of –2.07; the population halved in 4.0 months (Table 1). Thus, the study period was characterised by three periods: a moderately declining rabbit population; a rabbit population that increased rapidly to a high density; and a rabbit population that declined sharply to low density. Changes in bettong population characteristics Reproduction Bettongs are continuous breeders on Heirisson Prong with a mean of 70% of females carrying small pouch young throughout the study period (Appendix 1). The proportion of females carrying pouch young did not significantly differ between years, but differed significantly between seasons (Table 2). The proportion of females with small pouch young declined during summer periods and peaked during winter (Fig. 3). Simple regression showed that there was no significant relationship between the number of females with pouch young and rainfall.
60 40
Recruitment
20
0 Jan Mar May Jul Sep Nov Jan Mar May Jul Sep Nov Jan Mar May Jul Sep Nov Jan Mar May Jul Sep Nov Jan Mar
0
1995
1996
1997
1998
Fig. 2. The change in the relative abundance of rabbits and bettongs on Heirisson Prong, 1995–99.
The proportion of subadult bettongs in the trapped population varied from 0.04 to 0.35, averaging 0.13 over the 13 trapping sessions (Appendix 2). The ratio of males to females was close to parity (1:1.02 M:F). Unreplicated two-factor ANOVA of recruits, with year and season as fixed
426
A. J. Robley et al.
Source of variation
d.f.
s.s.
m.s.
F
P
Year Season Error Total
02 03 06 11
0.08 0.18 0.06 0.32
0.04 0.06 0.01
3.98 6.04
0.08 0.03
1.0
Proportion of young per female
20
15
10
5
0
0.9
0
0.8 0.7
100
150
20
50
Fig. 5. The proportion of recruits and rainfall (3 months lagged by 5 months). Recruits = 5.97 + 0.06(rainfall, mm) (r2 = 0.61, F1,10 = 15.97, P =
