• dispersal;
  • immunocontraception;
  • movement;
  • pest management;
  • ranges;
  • Vulpes vulpes


  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • 1
    This paper reports on the behavioural effects of surgical sterilization when used to simulate immunocontraception in free-ranging female foxes Vulpes vulpes.
  • 2
    During 3 years of trapping, 348 male and female foxes were fitted with transmitters in two treatment (females sterilized) and two untreated areas.
  • 3
    Radio-tracking indicated that sterile and fertile vixens maintained similar-sized territories during the breeding season, but that sterile females were possibly more likely to share their territories with each other.
  • 4
    There were no consistent differences in survival or dispersal between sterile and fertile females.
  • 5
    Outcomes from the study suggest that immunocontraception in free-living foxes is feasible.


  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The introduced European red fox Vulpes vulpes L. has long been recognized as a serious threat to populations of Australian wildlife (Finlayson 1961; Kinnear, Onus & Bromilow 1988; Priddel 1989; Friend 1990; Short & Milkovits 1990). Native fauna did not evolve with the fox and hence have few predation avoidance strategies, a problem further compounded by habitat fragmentation since European settlement. The fox is also increasingly perceived as a significant predator of livestock, although studies to determine the extent of this impact have been highly variable (Saunders et al. 1995; Greentree et al. 2000).

Historically, a variety of management strategies has been employed to try and reduce the impact of foxes. These have included bounty systems, shooting, trapping, den destruction and poisoning. The most common fox control strategy used today is poisoning with 1080 bait, an activity carried out over large tracts of Australia (Saunders et al. 1995). Evaluations of effectiveness for this strategy are limited, although Tyndale-Biscoe (1994) suggested that poisoning is ineffective in the long term because of the intrinsic capacity of foxes to rapidly replace those that are killed. There are additional concerns over the long-term use of lethal control measures, covering issues such as animal welfare, non-target risk and bait shyness. Consequently, it is highly desirable that suitable alternatives or supplements to lethal baiting are made available.

With recent research into the molecular basis of fertilization, immunocontraception (preventing normal recognition between sperm and egg, thus impeding fertilization) has been suggested as a potential strategy for the suppression of reproduction in free-living pest animals (Tyndale-Biscoe 1994). To be effective in reducing breeding success to a level that achieves population control, such a strategy by necessity is targeted at females (Bomford 1990).

Foxes are monoestrus, largely monogamous, mostly live as pairs or sometimes in family groups, and maintain territories (Saunders et al. 1995). The number of non-breeding vixens in any population is variable, being greatest where populations are subject to low levels of control and least where mortality rates are high (Corbet & Harris 1991). Sterilization of dominant females has been shown theoretically to reduce the productivity of a target population (Caughley, Pech & Grice 1992). One of the basic premises of immunocontraception is that, although pregnancy is prevented, normal endocrine function and reproductive behaviour of treated individuals remains unimpaired. For the fox this should result in the retention of the fundamental attributes of sociality, such as territorial integrity and mating systems (Newsome 1995). Without this tactical advantage, compensatory behaviour could render immunocontraception useless as a fox management strategy. Other possible forms of compensation that may occur within a treated population include greater post-natal survival of cubs produced by the remaining fertile females, and in turn a greater contribution by these cubs to the rate of increase in subsequent years. Reduced survivorship of sterile females resulting in their replacement by resident (non-territorial) or dispersing fertile females might also negate any treatment effect.

In this paper, we report on the effects of surgical sterilization on female foxes. This approach has previously been suggested as a viable means of simulating fertility control for pest animals (Kennelly & Converse 1993). Population control through immunocontraception seeks to reduce the average rate of population increase (r) by suppressing the birth rate. To achieve this may require levels of sterility of between 65% and 80% (Pech et al. 1997; Hone 1999), a difficult target to simulate and maintain in free-living fox populations when using such a labour-intensive method as surgical sterilization. Our main objective was therefore to determine if the normal territorial behaviour of these sterilized foxes was maintained and if any other compensatory mechanisms became apparent in the process.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References


Research was conducted at four sites on the Great Dividing Range in central New South Wales, Australia (Fig. 1). Two sites (sites 1 and 2) were situated on the eastern and western foreshores of Lake Burrendong (32°42′ S, 149°10′ E). The third study site (site 3) was situated at Larras Lee (33°17′ S, 149°06′ E) and the fourth site (site 4) at Murringo (34°18′ S, 148°32′ E). The two Burrendong sites were separated by a large enough body of water that we considered them to represent two distinct fox populations (later confirmed by radio-tracking studies).


Figure 1. Location of study sites.

Download figure to PowerPoint

Site topography ranged from hilly to undulating lowland, with elevations from 450 m to 800 m. The climate is typically temperate, with warm to hot summers and cool to cold winters. Temperatures range from a mean maximum of 32 °C in summer to a mean minimum of 0 °C in winter. Rainfall is generally reliable and slightly seasonal, with a winter–spring dominance. Average annual rainfall across the region is within the range of 550–750 mm (Australian Bureau of Meteorology 1988). Rainfall for the period leading up to and during the study for the three site localities is presented as cumulative rainfall deficiency graphs (Foley 1957) in Fig. 2. Cumulative deviation of monthly rainfall from the mean of that month provided a description of rainfall trends at the sites using averaged data from the nearest weather stations (Lake Burrendong, Molong and Young).


Figure 2. Cumulative rainfall deficiency graphs for Burrendong, Molong and Young.

Download figure to PowerPoint

The Burrendong sites on the Macquarie River consisted of dam foreshores that are managed for water catchment. This includes the use of grazing stock. The other sites were purely agricultural enterprises concentrating on the production of merino wool, prime fat lambs, beef cattle and winter cereal crops. Most of the grazing country has been cleared of native vegetation and, at Larras Lee and Murringo, pastures are improved with legume and Phalaris spp. Remnant vegetation consists of dry sclerophyll forest and woodland.

Apart from occasional recreational hunting, no fox control had been undertaken at any of these sites within the 10 years prior to project commencement.


The project involved the study of fox behaviour with and without imposed sterility. Sites 2 and 4 (Burrendong 2 and Murringo) were selected for study of intact populations, while at sites 1 and 3 (Burrendong 1 and Larras Lee) vixens were caught and surgically sterilized by tubal ligation at a nearby veterinary clinic.

Rates of increase

Spotlight counts were conducted at all four sites along set transects (Burrendong 1, 23·8 km; Burrendong 2, 21·5 km; Larras Lee, 19·1 km; Murringo, 18·9 km) for three consecutive nights and at 3-monthly intervals. A four-wheel drive vehicle travelled at 5–10 km h−1 along set tracks at each site. An observer used a 100-W spotlight and counted all foxes seen on both sides of the track. The mean number of foxes per kilometre of transect in each session was then used as a seasonal index of relative fox abundance. Counts were conducted every season between July 1994 and October 1997 (Fig. 3).


Figure 3. Spotlight counts of foxes (mean density per transect kilometre) for the four study sites.

Download figure to PowerPoint

Annual rates of increase were calculated using spotlight counts (foxes seen per transect kilometre) for each session. The log-transformed fox densities (Y) were then modelled using a linear mixed-effects model:

  • Y= mean + season + day + site + treatment × day +site ×season+error

where season, site and treatment (with and without imposed sterility) are factors with four, four and two levels, respectively, and day is a quantitative variable. Terms in italics were fitted as random effects. The error structure was an exponential correlation model (Diggle, Liang & Zeger 1994) fitted separately for each site. The models were fitted using ASREML (Gilmour et al. 1999). The purpose of this analysis was to determine if there was a significant difference in the rates of increase between the treatment sites (females sterilized) and the control sites (females intact).

Live capture and handling

Foxes were caught using Victor Soft-Catch™ traps (Woodstream Corporation, Lititz, PA, USA). These were set just below ground level and tethered to a 50-cm steel retaining peg that was driven 2–5 cm below ground level. The traps were set at irregular intervals along trails, farm roads, fence holes and at locations considered to be in suitable fox-trapping habitat. Single trap sets were baited with meat (rabbit, sheep, kangaroo) or lure (fox urine, fox faeces, synthetic fermented egg) or both. Multiple trap sets of between two and six traps were occasionally established around animal carcasses (sheep or kangaroo). Details of trapping procedures and results are described in Kay et al. (2000).

Trapping was restricted to a period prior to the onset of breeding (January–July) and was conducted in 1994, 1995 and 1996 at the Burrendong sites and in 1995 and 1996 at the Larras Lee and Murringo sites. Upon capture, foxes were anaesthetized with a mixture of ketamine hydrochloride (0·2 ml 5 kg−1) and xylazine hydrochloride (0·1 ml 5 kg−1). Each fox was marked with an individual tag number, and sex, weight and morphometrics were recorded. Foxes were categorized as juvenile or adult using the tooth eruption and wear technique described by Harris (1978). Any severely injured animals or those suffering from mange were killed immediately. At sites 1 and 3, healthy, adult, female foxes were transported to the veterinary clinic for sterilization. Each fox was given an intramuscular injection of penicillin as a post-operative prophylactic. Foxes were released at their point of capture only after recovery from anaesthesia (minimum of 12 h). Males and intact (non-sterilized) females were released sooner.

Sham operations

Early in this experiment it was considered necessary to ensure that the process of surgical sterilization did not have an adverse effect on the survival of study animals. At site 2, where no sterility was imposed, female foxes were trapped, handled and transported as they would have been for the purposes of sterilization. Sham operations were conducted that were identical to the sterilization procedure except that the fallopian tubes were left intact. During 1994 and 1995 we determined the fate of all sham-operated foxes fitted with transmitters. Only those that died of natural causes (excluding those shot, poisoned, killed on roads, etc.) were included in the analysis. Using a GLM procedure in S-Plus 2000 (1999), a logistic model was used to test for differences in the proportions dying. The model included effects for site, male vs. female, intact female vs. sterile female and sham vs. sterile female. This allowed a test of the latter effect after removing the earlier terms in the model.


Trapped foxes were fitted with a transmitter collar (150–151 MHz; Sirtrack™ Ltd, Havelock North, New Zealand) and released at their site of capture. Expected operational life of the collars was 60 months with a pulse rate of 60 beats min−1. The weight of the collar and transmitter was approximately 140 g and only adult animals were fitted with collars. Radio-tracking was conducted from semi-permanent receiving towers located at suitable high points throughout the study sites. Tower locations were positioned accurately from known survey points and differential global positioning systems (GPS). Each receiving tower consisted of a weather-proof shed housing a 6-m high rotating mast fitted with either a single nine-element or twin five-element yagi antennae. Bearings to fox collars were determined using either a null–peak system or single arrays (Amlaner 1980).

Simultaneous radio-tracking was undertaken on an hourly basis for 6 consecutive hours following sunset and for four consecutive nights. These sessions were conducted at least once a month for the 6 months (July–December) incorporating the breeding season. Each fox could potentially be radio-tracked 144 times during this 6-month period. The majority of locations were determined from the triangulation of bearings from the fixed towers. The number of towers at each site depended on the topography, which in turn determined the coverage of foxes. At Burrendong four towers were sufficient to cover both sides of the dam (sites 1 and 2) and ensure that locations on foxes were nearly always determined from a minimum of three towers. Similarly, five towers were necessary at Larras Lee and four at Murringo. Locations were also derived opportunistically from the towers or by walking down foxes during daylight with hand-held antennae and taking locations with a GPS.

The accuracy of the fixed-tower system was determined at each site through the use of ‘dummy’ collars, which were placed at random locations and tracked each session. The locations, as determined by GPS, were regularly changed and were only known by one operator. These collars were fixed to 2-l plastic bottles filled with saline solution to mimic a fox fitted with a collar.

Telemetry data analysis

Bearings from towers were fixed as locations using Locate II© (Nams 1992). As a first step, obviously erroneous locations were discarded from the data set. These were identified from the size of the error ellipse (Nams 1992) and the lack of three or more convergent bearings. All reasonable locations were then entered into Ranges V© (Kenwood & Hodder 1996) for home range analysis. Home range areas were determined using the minimum convex polygon (MCP) method (Mohr 1947; Southwood 1966). This method produces a home range measure that does not explicitly involve the assumption of data independence (Swihart & Slade 1985). It is also a method that has been shown to give a realistic representation of a fox home range (Saunders et al. 1993). In our study it was necessary to understand intraspecific patterns of range use within and between sites. Core areas are more useful for this purpose than ranges represented by peripheral contours (Harris et al. 1990). Consequently, we used 95% and 60% MCP when comparing the home ranges of sterile and intact vixens. A logarithmic transformation was performed on the home range data, which were then analysed using standard linear mixed modelling procedures. The two variables, 60% MCP and 95% MCP, were analysed separately.

The initial model fitted in each case was:

  • Y= mean + site + sex + year + site × sex + site × year + sex × site + site × sex × year + fox +error

where Y denotes the logarithm of the dependent variable (home range), sex denotes the three categories (male, intact female and sterile female).

Fox is included as a random effect associated with each animal and error is assumed to be distributed normally with zero mean and constant variance.

Least-square means for 60% MCP and 95% MCP across significantly different categories were then calculated. These means were obtained using the result that if log(X) is distributed normally with mean µ and variance σ2, then the mean of X equals exp(µ + σ2/2). Standard errors of the estimated means were based on first-order Taylor series approximations.


Collared foxes that had moved off a study site were searched for opportunistically. This was usually done from a vehicle using the network of roads surrounding a study site. Some flights were also conducted for aerial tracking using the methods described in Saunders & Kay (1996). Every trapped fox was fitted with a numbered ear-tag that also included a contact telephone number. This resulted in some hunter returns from foxes collected further away from the study sites. Because the search for dispersing animals was biased, i.e. mostly adjacent to a study site, and with some hunter returns producing exceptionally long distances of travel, measurements of dispersal could only be indicative and not necessarily representative of the population.

The most important differences to be measured related to the probabilities of dispersal for sterile and intact females. Thus, the most consistent effort was concentrated in searching for dispersing animals at Burrendong (site 1) and Larras Lee (site 3). An analysis was performed on the proportions of collared foxes from these sites that were known to have dispersed compared with those that remained on site for sufficient time to presume that they were non-dispersers. Data for the two sites were combined.

The difficulty with this analysis is that a collar can fail or animals can move off site at a rate such that they are never again located. Animals that remained alive on the study site for a minimum of 12 months and were never located off-site (apart from short-term forays) were classed as non-dispersers. Animals that were found alive or dead completely off-site were classed as dispersers. Animals that died within 1 month of release were excluded from the analysis on the basis that their behaviour may have been potentially affected by some post-trapping trauma.


To determine if compensation in survivorship was occurring, we examined, using analysis of variance, the length of time that foxes survived (in days) after being fitted with a transmitter and, in the case of selected females, after they were sterilized. As with analysis of sham operations, we only used animals whose fate was able to be determined and excluded any interventions such as poisoning, shooting and road kills.


  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

During the 3 years of the study at all sites, a total of 348 foxes was trapped from 45 000 trap nights and fitted with radio-transmitters. As a consequence of emigration, death, collar failure or poor data sets, only 45% of foxes originally fitted with collars could be used in subsequent home range analysis.


Sham operations were conducted on 14 females at site 2 in 1994. All mortalities known to be caused by natural factors were recorded at both Burrendong sites (1 and 2) for all categories of fox throughout 1994 and 1995. Details of these foxes are presented in Table 1.

Table 1.  Survivorship of foxes at Burrendong sites (1 and 2) in 1994 and 1995
SiteSex categoryTotalDied
Burrendong (1)Intact female 61 (17%)
Burrendong (1)Sterilized female203 (15%)
Burrendong (1)Male263 (12%)
Burrendong (2)Sham female143 (21%)
Burrendong (2)Male221 (5%)

No site and sex category comparison was significant, including sham vs. sterile (P = 0·43). Consequently, we concluded that surgical sterilization did not have any adverse effects on fox survival and that no further sham comparisons were necessary.


After omitting the non-significant terms treatment × day and site × season, the final model used to examine rates of increase was:

  • Y= mean + season + day + site + error

with Y = log density and the error structure as given in the Methods. Of primary interest is the coefficient of day, as this corresponds to the rate of increase (r) as defined by Caughley (1977). There was a significant (P < 0·05) decline in fox density with day but there was no significant difference in the decline rate between the treatment and control groups. That is, the level of surgical sterilization of trapped females was not sufficient to have a significant effect on rate of increase.


Over all sites and years, the data from 155 foxes were used to determine ranging behaviour during the breeding season (July–December). This involved 15 545 accepted telemetry locations at an average of 100 (± 65 SD) fixes per fox. Details of these foxes are provided in Table 2. Bearing error across all sites (n = 953) was 3·49° (± 2·4° SD).

Table 2.  Foxes used in home range analysis
SiteYearMaleIntact femaleSterile femaleTotal
Burrendong (1)1995 9 5 7 21
 1996 6 810 24
Burrendong (2)199511 8 19
 1996 7 5 12
Larras Lee (3)199510 4 9 23
 1996 3 612 21
Murringo (4)1995 611 17
 1996 711 18
Total 595838155

Omitting terms from the initial model that were not significant at P < 0·05 left the following:

  • log(X60MCP) = mean + site + fox +error
  • log(X95MCP) = mean + year + site × sex + fox +error

That is, for fixed effects, only site was significant for the 60% MCP, while for the 95% MCP there was a significant site × sex interaction as well as a uniform (on the log scale) year effect over all site and sex combinations.

Least-square means across significantly different categories for the two variables, 60% MCP and 95% MCP, averaged over years for the latter variable are presented in Table 3. This table also gives the least significant difference (LSD) rankings. From this table we can see that the sex × site interaction for 95% MCP was mostly due to the low range for intact females at the Murringo site. Without this effect it appears that, biologically, the home ranges of intact females and sterile females were similar. If site is considered as a random effect and site × sex effects, after removing the main effect for sex, are also considered random, then there are no significant differences (at the 0·05 level) between the three categories (males, intact females and sterile females).

Table 3.  Estimated means home ranges (km2) averaged over years (and over sexes for 60% MCP). Also given are standard errors of means in parentheses and LSD ranks for the 60% MCP and 95% MCP means separately. Means differing by more than twice the standard error of their difference are represented by different letters
Site60% MCP95% MCP
MaleSterile femaleIntact female
Murringo0·82 (0·10)a3·64 (0·67)b 1·86 (0·26)a
Larras0·98 (0·11)ab3·09 (0·57)b4·37 (0·63)b5·23 (1·12)bc
Burrendong 11·22 (0·13)b3·97 (0·68)b4·75 (0·75)bc7·23 (1·33)c
Burrendong 21·26 (0·16)b4·28 (0·67)b 4·38 (0·82)bc


Analyses of days of survival (log-transformed) by analysis of variance indicated that the six site × sex combinations (sterile females, intact females and males) did not differ significantly (P = 0·6). The mean numbers of days of survival for the 56 animals was 343 days, with a standard deviation of 273 days.


Hunter returns produced some extreme examples of dispersal from the animal’s point of release. The longest of these was a straight line distance of 300 km south-west of the Murringo site. Another animal was shot 260 km north of the Burrendong site only 1 month after being released. However, these represent outliers, with the majority of animals only moving relatively short distances away from the study sites. Search effort was concentrated around the Burrendong (1) and Larras Lee (3) sites in an attempt to observe any differences in behaviour between intact and sterile females. Details for these sites combined are presented in Table 4.

Table 4.  The number of collared foxes at Larras Lee and Burrendong 1 classified as residents on site or that had dispersed. Mean duration that each fox was tracked after fitting with collars is presented in parentheses (months)
Released with collarStayed on site > 12 monthsDispersedFate not known
Female sterile (n = 54)23 (25) 9 (28)22
Female intact (n = 33) 9 (29)10 (16)14
Male (n = 66)18 (25)18 (13)30

Assuming that the foxes in the category ‘fate not known’ are missing at random, i.e. the proportion of dispersers amongst these is the same as all animals within the corresponding sex category, the estimates of the proportion of dispersers within each sex category are sterile female 28%, intact female 53% and male 73%. These proportions are not significantly different (P > 0·05) based on a binomial model. This analysis could be questioned because animals with an unknown fate are more likely to have dispersed (hence unable to be relocated) than stayed on site. If we now consider the extreme assumption that all animals with an unknown fate had dispersed, estimates of the proportion of dispersers within each sex category would be sterile female 57%, intact female 73% and male 73%. Again, these proportions are not significantly different (P > 0·05) based on a binomial model. The true situation probably lies somewhere between these two assumptions, indicating that sterile females are less likely to disperse than either intact females or males.


  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The use of immunocontraception is highly appealing as a humane alternative to lethal forms of population control (Oogjes 1997). The strategy currently being developed is to target female foxes using a bait-delivered oral vaccine (Bradley, Hinds & Bird 1997), with attenuated Salmonella typhimurium as a candidate vaccine vector (de Jersey et al. 1999). This work remains in the developmental stage and to date the most popular means of predicting the outcomes of fertility control or immunocontraception for the management of foxes and other pest species has been through the use of theoretical models (Caughley, Pech & Grice 1992; Hone 1992; Saunders & Choquenot 1995; Barlow, Kean & Briggs 1997; Pech et al. 1997; Courchamp & Cornell 2000). The main problems with this process are the lack of reliable information on key population parameters and likely compensatory effects (Bomford 1990). Surgical sterilization is an alternative means of testing the concept of immunocontraception and has been used successfully in determining the level of infertility required to cause sustained reduction in the abundance of rabbits Oryctolagus cuniculus (Twigg & Williams 1999). Similarly, Ji, Clout & Sarre (2000) used it to test for behavioural effects of sterilization on possums and it is also the only means available to test for possible effects on the social behaviour of foxes (Robinson & Holland 1995). Newsome (1995) attempted to examine one form of compensatory behaviour (social control of breeding) using pen studies with surgically sterilized female foxes. His studies indicated no loss of dominance with sterilization and no compensatory breeding in their subordinates. In a field study using surgically sterilized foxes, Bubela (1995) found that in the first year sterile females maintained their home ranges and dominance and, when present, subordinate females did not breed. In the second year of the study, one sterilized female may have lost her position in the dominance hierarchy and allowed compensatory breeding in a previously subordinate female. While both of these studies yielded useful observations, throughout the majority of the fox distribution in Australia family groups consist of mated pairs, as dealt with in this study, and not complex hierarchical systems (Birchfield 1980; Saunders et al. 1995; Marlow et al. 2000; McIlroy, Saunders & Hinds 2001). Under these circumstances it is difficult to apply the assumptions of the various territorial hypotheses for foxes based on group living, namely the resource dispersion hypothesis (Macdonald 1983; Carr & Macdonald 1986), the constant territory size hypothesis (von Schantz 1984) and the territory inheritance hypothesis (Lindstrom 1986).

The home range of animals is generally considered to be proportional in area to the resources it contains (Harestad & Bunnell 1979; Lindstedt, Miller & Buskirk 1986), although many other physical and environmental attributes may be equally important (Stamps 1994). Various studies have confirmed that foxes, and other carnivores, living in habitats with abundant resources have relatively small home ranges and that territory size can be determined by metabolic needs (Gittleman & Harvey 1982; Saunders et al. 1993). The overall home range area (MCP) of foxes at all sites in our study was comparable with those observed in the only previous Australian study in temperate farmland habitats (Coman, Robinson & Beaumont 1991) and was also comparable to similar studies in the northern hemisphere (Tullar & Berchielli 1980; Zimen 1984; Cavallini 1992). Given that we concentrated radio-tracking effort mostly during winter and spring seasons, further comparisons with other longer term rural studies are not appropriate as home range size may vary outside these seasons.

The availability of food resources for foxes is likely to be most important during late summer and autumn, when climatically driven fluctuations in prey availability are greatest (Pech et al. 1997) and when female foxes need to accumulate maximum fat reserves in preparation for breeding (Winstanley, Buttemer & Saunders 1999). At all sites in the year prior to the commencement of this study (1994) there was a major drought during this critical period (Fig. 2). In 1995 and 1996, Murringo recovered from this drought while rainfall at Burrendong and Larras Lee continued to be depressed until the beginning of 1996. Between-site comparisons of core (60% MCP) and overall home range (95% MCP) (Table 3) suggest that Murringo foxes had the smaller territories while the remaining sites tended to be similar but larger. In our study, radio-tracking was concentrated on the period of the fox biological year, starting with mating (July) and ending with the independence of cubs from the natal den (December). Saunders et al. (1993) observed an increase in the distance travelled by females as a consequence of foraging for food on behalf of cubs, although this did not affect total home range size. If resources were in any way drought limited at the Burrendong and Larras Lee sites, female foxes may have needed to travel further afield to gather sufficient food to provide for their cubs. Although not significantly different, the predicted home ranges of intact foxes was always greater than those sterilized on the same site, which lends further support to this observation.

The above differences are subtle; however, they do tend to support the notion that the complexities in fox populations will change according to whether drought or plenty prevails (Newsome 1995).

Perhaps more importantly for possible compensatory behaviour under the effects of immunocontraception, there were no significant differences within sites in home range size at either 60% MCP or 95% MCP between sterile or intact females. Although intact female ranges were slightly larger, this was probably only associated with the added burden of provisioning of cubs as discussed above. From this observation we could arrive at the simplistic conclusion that a sterilized population would maintain normal territories but not have the increased demand on resources (and hence impact on prey abundance) associated with cub rearing. Females at all sites and years, regardless of reproductive status, were observed to maintain territories that were generally exclusive. Some exceptions (as observed in similar studies; Harris 1980) were created by mother–daughter relationships, brief forays outside traditional territorial boundaries, and areas of overlap created by possible errors in tracking locations (produced by geographical features, e.g. signal bounce). In 1995 we observed a deviation from this trend at Larras Lee in respect of sterile females where the extent of overlap was marked (Fig. 4). This may have been a manifestation of compensatory behaviour as a consequence of imposed sterility. The extent of territory ‘stacking’ could result in an increased population density of sterile females that may in turn favour reproductive females through greater resource availability in exclusive territories. Stacking may also result in no net change in predation pressure with a greater density of sterile females. That this trend was only apparent at one treatment site and in one year suggests that caution is needed in extrapolating this to a proven compensatory effect.


Figure 4. Home range overlap (95% MCP) of sterilized vixens at Larras Lee in 1995.

Download figure to PowerPoint

One form of compensation that may have a bearing on the use of immunocontraception is survivorship or longevity of treated females. Sterilization may mean that a female is able to survive longer without the stress of reproduction and provisioning of food for cubs. Survivorship of foxes in Australia has been shown to be affected by environmental conditions (Pech et al. 1992). It was fortunate in this study that environmental conditions at the two treatment sites (Burrendong 1 and Larras Lee) were similar so that differences in survivorship between intact and sterile females, for the duration of our study, could be more easily interpreted. What happens towards the end of the expected life span of foxes would require a longer study, although in a parallel demographic study of foxes only 20% of females live past the age of one (Saunders et al., in press). No apparent compensation was occurring in this parameter, i.e. sterile females were not living longer. This was perhaps unexpected given the other observations about female territoriality. Whether or not this is a positive or negative outcome for immunocontraception is unclear. Intuitively, a population with a high proportion of sterile females maintaining stable territories and not producing cubs will have the least impact on prey species (excluding the possibility of territory stacking). The longer these females survive, the more stable will be the spatial organization and the less likely the immigration of new and fertile females into the population. Twigg et al. (2000) found that there was significant increased survivorship in sterilized female rabbits and concluded that this was advantageous as it would lead to a demographic shift towards older, sterile, females that maintain their position in the social hierarchy. Conversely, Jewell (1986) sterilized male Soay lambs Ovis aries and found that this too increased survivorship but also resulted in greater impact through increased grazing pressure. Tuyttens & Macdonald (1998) suggest that reduced mortality of sterilized animals will see the ratio of cubs to adults drop to the point where compensatory increases in fecundity are likely to become significant. However, Saunders & Choquenot (1995), based on a modelled population, estimated that to negate the effects of 75% sterility would require a 100% increase in both adult and juvenile survival and a doubling in the proportion of vixens breeding in their first year. The importance of survivorship in sterilized female foxes and the effect of this at the population level is obviously in need of further clarification. This may not be possible until other factors, such as optimum modes and frequency of delivery of sterility agents, are determined.

Like survivorship, dispersal (and migration) may also exert a significant influence on population parameters and the reduction of impact produced by an immunocontraceptive-treated fox population. In their study of factors affecting the dispersal of foxes, Harris & Trewhella (1988) found that approximately 30% of juvenile and adult female foxes dispersed in any one year. Such a mixing effect would soon negate the efficacy of a sterilizing agent, particularly if it were applied to site-specific fox populations. While not conclusive, the observations in this study suggest that sterile females are more likely to remain resident that intact females. More conclusive was the fact that sterilization did not result in a greater probability of dispersal.

Most of the findings from this study indicate that immunocontraception in free-living fox populations would be ecologically feasible. There are, of course, caveats, such as the absence of longer term effects on behaviour and minimization of recruitment into a treated population. There will also be many logistical considerations that may need to be overcome or at least accommodated. These potentially include integration with conventional (lethal) control operations, levels of bait uptake and rates of sero-conversion, cost-effectiveness, prey response and scale of operation necessary to minimize the effect of recruitment.

The ultimate proof of concept for immunocontraception will only be possible when a viable vaccine and vector are available for field testing. Studies such as the one reported here provide insight into the extent that compensatory behaviour might work against the efficacy of immunocontraception. They also provide the information needed on key parameters that will allow more precise theoretical modelling, the next best way of progressing the current debate on whether or not fertility control is a viable, humane, alternative to the lethal culling of carnivore populations.


  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We thank the many people who helped on all aspects of the project. We are particularly indebted to Garth Dutfield, John Francis, Peter Welsh, Will Lee, Steven Brown, Richard Taubman and Dougald Walker for giving us unhindered access to their properties and facilities. The Department of Land and Water Conservation allowed us access and use of the Burrendong foreshores. Thanks to Geoff Quinn, Rod Edmundson, Rod Thornberry, Roy Winstanley, Darryl Heffernan, Julian Seddon, Sophie Ogborn, Russell Pizel, Lynette McLeod, John Tracey, Adam Eyles and Dannielle Denning for assistance with fox trapping and radio-tracking. Molong, Mudgee and Young Rural Lands Protection Boards gave assistance in locating study sites and obtaining landholder co-operation. Colin Poyner conducted surgical procedures on foxes. Animal ethics approvals for this project were given by CSIRO (permit no. 93/94–06) and NSW Agriculture (permit no. ORA 93/009).


  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • Amlaner, C.J. (1980) The design of antennas for use in radio telemetry. A Handbook on Biotelemetry and Radio Tracking (eds C.J.Amlaner & D.W.Macdonald), pp. 251262. Pergamon Press, Oxford, UK.
  • Australian Bureau of Meteorology (1988) Climatic Averages of Australia. Australian Government Printing Service, Canberra, Australia.
  • Barlow, N.D., Kean, J.M. & Briggs, C.J. (1997) Modelling the relative efficacy of culling and sterilisation for controlling populations. Wildlife Research, 24, 129141.
  • Birchfield, G.L. (1980) The ecology of the red fox in south-western New South Wales. MSc Thesis. University of Sydney, Sydney, Australia.
  • Bomford, M. (1990) A Role for Fertility Control in Wildlife Management. Bulletin No. 7. Bureau of Rural Resources, Australian Government Printing Service, Canberra, Australia.
  • Bradley, M.P., Hinds, L.A. & Bird, P.H. (1997) A bait-delivered immunocontraceptive vaccine for the European red fox (Vulpes vulpes) by the year 2002? Reproduction, Fertility and Development, 9, 111116.
  • Bubela, T. (1995) Social effects of sterilising free-ranging vixens (Vulpes vulpes) in subalpine Australia. PhD Thesis. University of Sydney, Sydney, Australia.
  • Carr, G.M. & Macdonald, D.W. (1986) The sociality of solitary foragers: a model based on resource dispersion. Animal Behaviour, 34, 15401549.
  • Caughley, G.C. (1977) Analysis of Vertebrate Populations. John Wiley & Sons, Chichester, UK.
  • Caughley, G.C., Pech, R. & Grice, D. (1992) Effect of fertility control on a population’s productivity. Wildlife Research, 19, 623627.
  • Cavallini, P. (1992) Ranging behaviour of the red fox (Vulpes vulpes) in rural southern Japan. Journal of Mammalogy, 73, 321325.
  • Coman, B.J., Robinson, J. & Beaumont, C. (1991) Home range, dispersal and density of red fox Vulpes vulpes in central Victoria. Wildlife Research, 18, 215223.
  • Corbet, G.B. & Harris, S. (1991) The Handbook of British Mammals, 3rd edn. Blackwell Scientific Publications, Oxford, UK.
  • Courchamp, F. & Cornell, S.J. (2000) Virus-vectored immunocontraception to control feral cats on islands: a mathematical model. Journal of Applied Ecology, 37, 903913.
  • Diggle, P.J., Liang, K.Y. & Zeger, S.L. (1994) Analysis of Longitudinal Data. Clarendon Press, Oxford, UK.
  • Finlayson, H.H. (1961) On central Australian mammals. IV. The distribution and status of central Australian species. Records of the South Australian Museum, 14, 141191.
  • Foley, J.C. (1957) Droughts in Australia: A Review of Records from the Earliest Days of Settlement to 1955. Bulletin No. 43. Australian Bureau of Meteorology, Melbourne, Australia.
  • Friend, J.A. (1990) The numbat Myrmecobius fasciatus (Myrmecobidae): history of decline and potential for recovery. Proceedings of the Ecological Society of Australia, 16, 369377.
  • Gilmour, A.R., Cullis, B.R., Welham, S.J. & Thompson, R. (1999) ASREML Reference Manual. NSW Agriculture Biometric Bulletin No. 3. NSW Agriculture, Orange, Australia.
  • Gittleman, J.L. & Harvey, P.H. (1982) Carnivore home-range size, metabolic needs and ecology. Behavioural Ecology and Sociobiology, 10, 5763.
  • Greentree, C., Saunders, G.R., McLeod, L. & Hone, J. (2000) Lamb predation and control of foxes in south-eastern Australia. Journal of Applied Ecology, 37, 935943.
  • Harestad, A.S. & Bunnell, F.L. (1979) Home range and body weight – a re-evaluation. Ecology, 60, 389402.
  • Harris, S. (1978) Age determination in the red fox (Vulpes vulpes) – an evaluation of technique efficiency as applied to a sample of suburban foxes. Journal of Zoology, London, 184, 91117.
  • Harris, S. (1980) Home ranges and patterns of distribution of foxes (Vulpes vulpes) in an urban area as revealed by radio-tracking. A Handbook on Biotelemetry and Radio-Tracking (eds C.J.Amlaner & D.W.Macdonald), pp. 685690. Pergamon Press, Oxford, UK.
  • Harris, S. & Trewhella, W.J. (1988) An analysis of some factors affecting dispersal in an urban fox (Vulpes vulpes) population. Journal of Applied Ecology, 25, 409422.
  • Harris, S., Cresswell, W.J., Forde, P.G., Trewhella, W.J., Woollard, T. & Wray, S. (1990) Home-range analysis using radio-tracking data – a review of problems and techniques particularly as applied to the study of mammals. Mammal Review, 20, 97123.
  • Hone, J. (1992) Rate of increase and fertility control. Journal of Applied Ecology, 29, 695698.
  • Hone, J. (1999) On rate of increase (r): patterns of variation in Australian mammals and the implications for wildlife management. Journal of Applied Ecology, 36, 709718.
  • De Jersey, J., Bird, P.H., Verma, N.K. & Bradley, M.P. (1999) Antigen-specific systemic and reproductive tract antibodies in fox immunized with Salmonella typhimurium expressing bacterial and sperm proteins. Reproduction, Fertility and Development, 11, 219228.
  • Jewell, P. (1986) Survival in a feral population of primitive sheep in St Kilda, Outer Hebrides, Scotland. National Geographic Research, 2, 402406.
  • Ji, W., Clout, M.N. & Sarre, S.D. (2000) Responses of male brushtail possums to sterile females: implications for biological control. Journal of Applied Ecology, 37, 926934.
  • Kay, B.J., Gifford, E.J., Perry, R. & Van De Ven, R. (2000) Trapping efficiency for foxes (Vulpes vulpes) in central NSW: age and sex biases and the effects of reduced fox abundance. Wildlife Research, 27, 547552.
  • Kennelly, J.J. & Converse, K.A. (1993) Surgical sterilisation: an underutilized procedure for evaluating the merits of induced sterility. Contraception in Wildlife Management (technical co-ordinator T.J.Kreeger), pp. 2128. Bulletin No. 83. United States Department of Agriculture, Denver, Colorado.
  • Kenwood, R.E. & Hodder, K.H. (1996) Ranges V – An Analysis System for Biological Location Data. Institute of Terrestrial Ecology, Wareham, UK.
  • Kinnear, J.E., Onus, M.L. & Bromilow, R.N. (1988) Fox control and rock-wallaby population dynamics. Australian Wildlife Research, 15, 435450.
  • Lindstedt, S.L., Miller, B.J. & Buskirk, S.W. (1986) Home range, time and body size in mammals. Ecology, 67, 413418.
  • Lindstrom, E. (1986) Territory inheritance and the evolution of group living in carnivores. Animal Behaviour, 34, 18251835.
  • Macdonald, D.W. (1983) The ecology of carnivore social behaviour. Nature, 301, 379384.
  • McIlroy, J.C., Saunders, G.R. & Hinds, L. (2001) The reproductive performance of female red foxes (Vulpes vulpes) in central-western New South Wales during and after a drought. Canadian Journal of Zoology, 79, 545553.
  • Marlow, N.J., Thomson, P.C., Algar, D., Rose, K., Kok, N.E. & Sinagra, J.A. (2000) Demographic characteristics and social organisation of a population of red foxes in a rangeland area in western Australia. Wildlife Research, 27, 457464.
  • Mohr, C.O. (1947) Table of equivalent populations of North American small mammals. American Midland Naturalist, 37, 223249.
  • Nams, V.O. (1992) Locate II Users’ Guide. Pacer Computer Software, Truro, Canada.
  • Newsome, A.E. (1995) Socio-ecological models for red fox populations subject to fertility control in Australia. Annales Zoologica Fennica, 32, 99110.
  • Oogjes, G. (1997) Ethical aspects and dilemmas of fertility control of unwanted wildlife: an animal welfarist’s perspective. Reproduction, Fertility and Development, 9, 163168.
  • Pech, R., Hood, G., McIlroy, J. & Saunders, G.R. (1997) Can foxes be controlled by reducing their fertility? Reproduction, Fertility and Development, 9, 4150.
  • Pech, R.P., Sinclair, A.R.E., Newsome, A.E. & Catling, P.C. (1992) Limits to predator regulation of rabbits in Australia: evidence from predator removal experiments. Oecologia, 89, 102112.
  • Priddel, D. (1989) Conservation of rare fauna: the regent parrot and the malleefowl. Mediterranean Landscapes in Australia – Mallee Ecosystems and Their Management (eds J.C.Noble & R.A.Bradstock), pp. 243249. CSIRO, Melbourne, Australia.
  • Robinson, A.J. & Holland, M.K. (1995) Testing the concept of virally vectored immunosterilisation for the control of wild rabbit and fox populations in Australia. Australian Veterinary Journal, 72, 6568.
  • Saunders, G.R. & Choquenot, D. (1995) The effect of fertility control on fox population dynamics: rate of decline and potential compensatory responses. Proceedings 10th Vertebrate Pest Control Conference (ed. M.Statham), pp. 366371. Department of Primary Industry and Fisheries, Hobart, Australia.
  • Saunders, G.R. & Kay, B. (1996) Movements and home range of feral pigs in Kosciusko National Park, NSW. Wildlife Research, 23, 711719.
  • Saunders, G.R., Coman, B., Kinnear, J. & Braysher, M. (1995) Managing Vertebrate Pests: Foxes. Bureau of Resource Sciences, Australian Government Publishing Service, Canberra, Australia.
  • Saunders, G.R., McIlroy, J.C., Kay, B., Gifford, E., Berghout, M. & Van De Ven, R. (in press) The demography of foxes in central-western New South Wales, Australia. Mammalia, in press.
  • Saunders, G.R., White, P., Harris, S. & Rayner, J. (1993) Urban foxes: food acquisition, time and energy budgeting of a generalised predator. Zoological Society, London, 65, 215234.
  • Von Schantz, T. (1984) Non-breeders in the red fox, Vulpes vulpes. Oikos, 42, 5965.
  • Short, J. & Milkovits, G. (1990) Distribution and status of the brush-tailed rock-wallaby in south-eastern Australia. Australian Wildlife Research, 17, 169179.
  • Southwood, T.R.E. (1966) Ecological Methods. Methuen, London, UK.
  • S-Plus 2000 (1999) Modern Statistics and Applied Graphics. Data Analysis Products Division, Mathsoft Inc., Seattle, WA.
  • Stamps, J. (1994) Territorial behaviour: testing the assumptions. Advances in the Study of Behaviour, 23, 173232.
  • Swihart, R.K. & Slade, N.A. (1985) Testing for independence of observations of animal movements. Ecology, 69, 11761184.
  • Tullar, B.F. & Berchielli, L.T. (1980) Movement of the red fox in central New York. New York Fish and Game Journal, 27, 179204.
  • Tuyttens, F.A.M. & Macdonald, D.W. (1998) Fertility control: an option for non-lethal control of wild carnivores? Animal Welfare, 7, 339364.
  • Twigg, L.E. & Williams, C.K. (1999) Fertility control of an overabundant species: can it work for feral rabbits? Ecology Letters, 2, 281285.
  • Twigg, L.E., Lowe, T.J., Martin, G.M., Wheeler, A.G., Gray, G.S., Griffin, S.L., O’Reilly, C.M., Robinson, D.J. & Hubach, P.H. (2000) Effects of surgically imposed sterility on free-ranging rabbit populations. Journal of Applied Ecology, 37, 1639.
  • Tyndale-Biscoe, C.H. (1994) Virus vectored immunocontraception of feral animals. Reproduction, Fertility and Development, 6, 281287.
  • Winstanley, R., Buttemer, W. & Saunders, G.R. (1999) Fat deposition and seasonal variation in body composition of red fox (Vulpes vulpes) in Australia. Canadian Journal of Zoology, 77, 406412.
  • Zimen, E. (1984) Long range movements of the red fox, Vulpes vulpes L. Acta Zoologica Fennica, 171, 267270.